Osteochondral Tissue Engineering: The Potential of Electrospinning and Additive Manufacturing
Abstract
:1. Introduction
1.1. Osteochondral Damage: Current Challenges
1.2. Aetiology and Epidemiology: Trauma vs. Degenerative Diseases
1.3. Current Therapies: The Pros and Cons
1.4. The Need for Improved Osteochondral Regenerative Solutions
2. Osteochondral Unit: Composition, Structure, and Function
2.1. Articular Cartilage
2.2. Cartilage–Bone Interface: Calcified Cartilage
2.3. Subchondral Bone
3. Osteochondral Tissue Engineering
3.1. The Building Blocks of an Osteochondral Tissue-Engineered Construct
3.1.1. Biomaterials
3.1.2. Incorporation of Biochemical Stimuli
Growth Factor Delivery
Gene Therapy
Small Molecule Delivery
Type of Biochemical Stimulus | Advantages | Disadvantages | Examples | References |
---|---|---|---|---|
Growth factor/chemokine | Specific action and fewer off-target interactions; Efficient mimicking of physiological signalling cascades | Protein instability in non-native conditions; Short half-life times after administration; High cost | bFGF | [150,154] |
BMPs | [145,146,147,148,155,157,158,159] | |||
IGF-1 | [149,158] | |||
TGF-β1 | [141,142,153,154,155,156] | |||
TGF-β3 | [143,144,157,159] | |||
SDF-1α | [151,153] | |||
Protein-coding gene | Specific, long-lasting action and higher stability of DNA compared to protein agents | Immunorecognition of viral vectors; Low efficiency of non-viral vectors; Difficulty in achieving optimal concentrations of target proteins | BMP-2 | [172,173,174] |
TGF-β3 | [172,173,174] | |||
Sox9 | [172,175] | |||
IL-1Ra | [174] | |||
Small molecule | Simple administration; Easy high-throughput screening with low cost; Dose-dependent effects allow for a fine-tuning of the therapeutic concentrations | Off-target systemic interactions may result in adverse side effects | Y27632 | [151] |
Dexamethasone | [188,189] | |||
Alendronate | [183,184] | |||
Berberine | [101] | |||
KGN | [179,180,181,182,183] | |||
BNTA | [186] | |||
DIPQUO | [187] |
3.1.3. Cells
Mimicking the In Vivo Physiological Environment: Dynamic Culture Conditions
3.2. Building Block Assembly: Scaffold Fabrication and Characterisation
3.2.1. Electrospinning
3.2.2. Additive Manufacturing: 3D and 4D Printing
4. From Practice Back to Theory: What Separates the Promise of Tissue-Engineered Strategies from Clinical Success?
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Barbe, M.F.; Driban, J.; Barr, A.E.; Popoff, S.N.; Safadi, F.F. Structure and function of joints. In Bone Pathology; Humana Press: Totowa, NJ, USA, 2009; pp. 51–60. ISBN 9781588297662. [Google Scholar]
- Goldring, S.R.; Goldring, M.B. Changes in the osteochondral unit during osteoarthritis: Structure, function and cartilage–bone crosstalk. Nat. Rev. Rheumatol. 2016, 12, 632–644. [Google Scholar] [CrossRef]
- Tamaddon, M.; Wang, L.; Liu, Z.; Liu, C. Osteochondral tissue repair in osteoarthritic joints: Clinical challenges and opportunities in tissue engineering. Bio-Des. Manuf. 2018, 1, 101–114. [Google Scholar] [CrossRef] [Green Version]
- Sophia Fox, A.J.; Bedi, A.; Rodeo, S.A. The basic science of articular cartilage: Structure, composition, and function. Sports Health 2009, 1, 461–468. [Google Scholar] [CrossRef]
- Oláh, T.; Madry, H. The Osteochondral Unit: The Importance of the Underlying Subchondral Bone. Cartil. Restor. 2018, 13–22. [Google Scholar] [CrossRef]
- Findlay, D.M.; Kuliwaba, J.S. Bone–cartilage crosstalk: A conversation for understanding osteoarthritis. Bone Res. 2016, 4, 16028. [Google Scholar] [CrossRef] [Green Version]
- Houard, X.; Goldring, M.B.; Berenbaum, F. Homeostatic mechanisms in articular cartilage and role of inflammation in osteoarthritis. Curr. Rheumatol. Rep. 2013, 15, 375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lepage, S.I.M.; Robson, N.; Gilmore, H.; Davis, O.; Hooper, A.; John, S.S.; Kamesan, V.; Gelis, P.; Carvajal, D.; Hurtig, M.; et al. Beyond Cartilage Repair: The Role of the Osteochondral Unit in Joint Health and Disease. Tissue Eng. Part B Rev. 2019, 25, 114–125. [Google Scholar] [CrossRef] [Green Version]
- Widuchowski, W.; Widuchowski, J.; Trzaska, T. Articular cartilage defects: Study of 25,124 knee arthroscopies. Knee 2007, 14, 177–182. [Google Scholar] [CrossRef]
- Chu, C.R. Chondral and osteochondral injuries: Mechanisms of injury and repair responses. Oper. Tech. Orthop. 2001, 11, 70–75. [Google Scholar] [CrossRef]
- Gorbachova, T.; Melenevsky, Y.; Cohen, M.; Cerniglia, B.W. Osteochondral Lesions of the Knee: Differentiating the Most Common Entities at MRI. Radiographics 2018, 38, 1478–1495. [Google Scholar] [CrossRef] [Green Version]
- Durur-Subasi, I.; Durur-Karakaya, A.; Yildirim, O.S. Osteochondral Lesions of Major Joints. Eurasian J. Med. 2015, 47, 138–144. [Google Scholar] [CrossRef]
- Looze, C.A.; Capo, J.; Ryan, M.K.; Begly, J.P.; Chapman, C.; Swanson, D.; Singh, B.C.; Strauss, E.J. Evaluation and Management of Osteochondral Lesions of the Talus. Cartilage 2017, 8, 19–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McAdams, T.R.; Mithoefer, K.; Scopp, J.M.; Mandelbaum, B.R. Review: Articular Cartilage Injury in Athletes. Cartilage 2010, 1, 165–179. [Google Scholar] [CrossRef] [Green Version]
- Mithoefer, K.; McAdams, T.; Williams, R.J.; Kreuz, P.C.; Mandelbaum, B.R. Clinical Efficacy of the Microfracture Technique for Articular Cartilage Repair in the Knee. Am. J. Sports Med. 2009, 37, 2053–2063. [Google Scholar] [CrossRef] [PubMed]
- Flanigan, D.C.; Harris, J.D.; Trinh, T.Q.; Siston, R.A.; Brophy, R.H. Prevalence of Chondral Defects in Athletes’ Knees. Med. Sci. Sport. Exerc. 2010, 42, 1795–1801. [Google Scholar] [CrossRef]
- Pereira, H.; Cengiz, I.F.; Vilela, C.; Ripoll, P.L.; Espregueira-Mendes, J.; Miguel Oliveira, J.; Reis, R.L.; Niek van Dijk, C. Emerging Concepts in Treating Cartilage, Osteochondral Defects, and Osteoarthritis of the Knee and Ankle. In Osteochondral Tissue Engineering; Advances in Experimental Medicine and Biology; Springer New York LLC: New York, NY, USA, 2018; Volume 1059, pp. 25–62. [Google Scholar]
- Buckwalter, J.A. Articular Cartilage: Injuries and Potential for Healing. J. Orthop. Sports Phys. Ther. 1998, 28, 192–202. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, I.; Schaefer, D.; Dozin, B. Repair of Osteochondral Lesions. Available online: https://www.ncbi.nlm.nih.gov/books/NBK6458/ (accessed on 30 March 2020).
- O’Driscoll, S.W. The healing and regeneration of articular cartilage. J. Bone Jt. Surg. Am. 1998, 80, 1795–1812. [Google Scholar] [CrossRef]
- Martel-Pelletier, J.; Barr, A.J.; Cicuttini, F.M.; Conaghan, P.G.; Cooper, C.; Goldring, M.B.; Goldring, S.R.; Jones, G.; Teichtahl, A.J.; Pelletier, J.-P. Osteoarthritis. Nat. Rev. Dis. Primers 2016, 2, 16072. [Google Scholar] [CrossRef] [Green Version]
- Loeser, R.F.; Goldring, S.R.; Scanzello, C.R.; Goldring, M.B. Osteoarthritis: A disease of the joint as an organ. Arthritis Rheum. 2012, 64, 1697–1707. [Google Scholar] [CrossRef] [Green Version]
- Nelson, A.E. Osteoarthritis year in review 2017: Clinical. Osteoarthr. Cartil. 2018, 26, 319–325. [Google Scholar] [CrossRef] [Green Version]
- WHO Scientific Group. WHO Chronic Rheumatic Conditions; WHO: Geneva, Switzerland, 2016; Available online: http://www.who.int/chp/topics/rheumatic/en/ (accessed on 6 April 2020).
- Hunter, D.J.; Bierma-Zeinstra, S. Osteoarthritis. Lancet 2019, 393, 1745–1759. [Google Scholar] [CrossRef]
- Farmer, J.M.; Martin, D.F.; Boles, C.A.; Curl, W.W. Chrondral and Osteochondral injuries: Diagnosis and Management. Clin. Sports Med. 2001, 20, 299–320. [Google Scholar] [CrossRef]
- Pontes-Quero, G.M.; García-Fernández, L.; Aguilar, M.R.; San Román, J.; Pérez Cano, J.; Vázquez-Lasa, B. Active viscosupplements for osteoarthritis treatment. Semin. Arthritis Rheum. 2019, 49, 171–183. [Google Scholar] [CrossRef]
- Huang, Y.; Liu, X.; Xu, X.; Liu, J. Intra-articular injections of platelet-rich plasma, hyaluronic acid or corticosteroids for knee osteoarthritis: A prospective randomized controlled study. Orthopade 2019, 48, 239–247. [Google Scholar] [CrossRef] [PubMed]
- Lewis, P.B.; McCarty, L.P.; Kang, R.W.; Cole, B.J. Basic Science and Treatment Options for Articular Cartilage Injuries. J. Orthop. Sports Phys. Ther. 2006, 36, 717–727. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Medvedeva, E.; Grebenik, E.; Gornostaeva, S.; Telpuhov, V.; Lychagin, A.; Timashev, P.; Chagin, A. Repair of Damaged Articular Cartilage: Current Approaches and Future Directions. Int. J. Mol. Sci. 2018, 19, 2366. [Google Scholar] [CrossRef] [Green Version]
- Steadman, J.R.; Rodkey, W.G.; Rodrigo, J.J. Microfracture: Surgical Technique and Rehabilitation to Treat Chondral Defects. Clin. Orthop. Relat. Res. 2001, 391, S362–S369. [Google Scholar] [CrossRef]
- Koh, J. Arthroscopic Microfracture and Chondroplasty. In Techniques in Hip Arthroscopy and Joint Preservation Surgery with Expert Consult Access; Elsevier Inc.: Philadelphia, PA, USA, 2011; pp. 188–194. ISBN 9781416056423. [Google Scholar]
- Steadman, J.R.; Briggs, K.K.; Rodrigo, J.J.; Kocher, M.S.; Gill, T.J.; Rodkey, W.G. Outcomes of microfracture for traumatic chondral defects of the knee: Average 11-year follow-up. Arthrosc. J. Arthrosc. Relat. Surg. 2003, 19, 477–484. [Google Scholar] [CrossRef] [PubMed]
- Harris, J.D.; Brophy, R.H.; Siston, R.A.; Flanigan, D.C. Treatment of Chondral Defects in the Athlete’s Knee. Arthrosc. J. Arthrosc. Relat. Surg. 2010, 26, 841–852. [Google Scholar] [CrossRef]
- Zhang, L.; Hu, J.; Athanasiou, K.A. The role of tissue engineering in articular cartilage repair and regeneration. Crit. Rev. Biomed. Eng. 2009, 37, 1–57. [Google Scholar] [CrossRef] [PubMed]
- Bugbee, W.D.; Pallante-Kichura, A.L.; Görtz, S.; Amiel, D.; Sah, R. Osteochondral allograft transplantation in cartilage repair: Graft storage paradigm, translational models, and clinical applications. J. Orthop. Res. 2016, 34, 31–38. [Google Scholar] [CrossRef] [Green Version]
- Magnussen, R.A.; Dunn, W.R.; Carey, J.L.; Spindler, K.P. Treatment of focal articular cartilage defects in the knee: A systematic review. Clin. Orthop. Relat. Res. 2008, 466, 952–962. [Google Scholar] [CrossRef] [Green Version]
- Nukavarapu, S.P.; Dorcemus, D.L. Osteochondral tissue engineering: Current strategies and challenges. Biotechnol. Adv. 2013, 31, 706–721. [Google Scholar] [CrossRef]
- Ahmad, J.; Jones, K. Comparison of Osteochondral Autografts and Allografts for Treatment of Recurrent or Large Talar Osteochondral Lesions. Foot Ankle Int. 2016, 37, 40–50. [Google Scholar] [CrossRef]
- Demange, M.; Gomoll, A.H. The use of osteochondral allografts in the management of cartilage defects. Curr. Rev. Musculoskelet. Med. 2012, 5, 229–235. [Google Scholar] [CrossRef] [Green Version]
- Stoker, A.; Garrity, J.T.; Hung, C.T.; Stannard, J.P.; Cook, J. Improved preservation of fresh osteochondral allografts for clinical use. J. Knee Surg. 2012, 25, 117–125. [Google Scholar] [CrossRef] [PubMed]
- Pina, S.; Ribeiro, V.; Oliveira, J.M.; Reis, R.L. Pre-clinical and Clinical Management of Osteochondral Lesions. In Regenerative Strategies for the Treatment of Knee Joint Disabilities. Studies in Mechanobiology, Tissue Engineering and Biomaterials; Oliveira, J.M., Reis, R.L., Eds.; Springer: Cham, Switzerland, 2017; pp. 147–161. [Google Scholar]
- Beer, A.J.; Tauro, T.M.; Redondo, M.L.; Christian, D.R.; Cole, B.J.; Frank, R.M. Use of Allografts in Orthopaedic Surgery: Safety, Procurement, Storage, and Outcomes. Orthop. J. Sports Med. 2019, 7. [Google Scholar] [CrossRef] [Green Version]
- Gomoll, A.H. Osteochondral allograft transplantation using the chondrofix implant. Oper. Tech. Sports Med. 2013, 21, 90–94. [Google Scholar] [CrossRef]
- Tompkins, M.; Adkisson, H.D.; Bonner, K.F. DeNovo NT allograft. Oper. Tech. Sports Med. 2013, 21, 82–89. [Google Scholar] [CrossRef] [Green Version]
- Farr, J.; Cole, B.J.; Sherman, S.; Karas, V. Particulated articular cartilage: CAIS and DeNovo NT. J. Knee Surg. 2012, 25, 23–29. [Google Scholar] [CrossRef]
- Gikas, P.D.; Bayliss, L.; Bentley, G.; Briggs, T.W.R. An overview of autologous chondrocyte implantation. J. Bone Jt. Surg. Br. 2009, 91, 997–1006. [Google Scholar] [CrossRef]
- Brittberg, M.; Lindahl, A.; Nilsson, A.; Ohlsson, C.; Isaksson, O.; Peterson, L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N. Engl. J. Med. 1994, 331, 889–895. [Google Scholar] [CrossRef]
- Brittberg, M.; Peterson, L.; Sjogren-Janson, E.; Tallheden, T.; Lindahl, A. Articular Cartilage Engineering with Autologous Chondrocyte Transplantation: A review of recent developments. J. Bone Jt. Surg. Am. Vol. 2003, 85, 109–115. [Google Scholar] [CrossRef]
- Peterson, L.; Brittberg, M.; Kiviranta, I.; Åkerlund, E.L.; Lindahl, A. Autologous chondrocyte transplantation: Biomechanics and long-term durability. Am. J. Sports Med. 2002, 30, 2–12. [Google Scholar] [CrossRef] [PubMed]
- Davies, R.; Kuiper, N. Regenerative Medicine: A Review of the Evolution of Autologous Chondrocyte Implantation (ACI) Therapy. Bioengineering 2019, 6, 22. [Google Scholar] [CrossRef] [Green Version]
- Dewan, A.K.; Gibson, M.A.; Elisseeff, J.H.; Trice, M.E. Evolution of Autologous Chondrocyte Repair and Comparison to Other Cartilage Repair Techniques. Biomed. Res. Int. 2014, 2014, 1–11. [Google Scholar] [CrossRef]
- Kon, E.; Verdonk, P.; Condello, V.; Delcogliano, M.; Dhollander, A.; Filardo, G.; Pignotti, E.; Marcacci, M. Matrix-Assisted Autologous Chondrocyte Transplantation for the Repair of Cartilage Defects of the Knee. Am. J. Sports Med. 2009, 37, 156–166. [Google Scholar] [CrossRef]
- Kon, E.; Filardo, G.; Di Martino, A.; Marcacci, M. ACI and MACI. J. Knee Surg. 2012, 25, 17–22. [Google Scholar] [CrossRef]
- Bartlett, W.; Skinner, J.A.; Gooding, C.R.; Carrington, R.W.J.; Flanagan, A.M.; Briggs, T.W.R.; Bentley, G. Autologous chondrocyte implantation versus matrix-induced autologous chondrocyte implantation for osteochondral defects of the knee. A prospective, randomised study. J. Bone Jt. Surg. Ser. B 2005, 87, 640–645. [Google Scholar] [CrossRef] [Green Version]
- McNickle, A.G.; Provencher, M.T.; Cole, B.J. Overview of Existing Cartilage Repair Technology. Sports Med. Arthrosc. 2008, 16, 196–201. [Google Scholar] [CrossRef] [Green Version]
- Makris, E.A.; Gomoll, A.H.; Malizos, K.N.; Hu, J.C.; Athanasiou, K.A. Repair and tissue engineering techniques for articular cartilage. Nat. Rev. Rheumatol. 2015, 11, 21–34. [Google Scholar] [CrossRef]
- Vilela, C.A.; Correia, C.; Oliveira, J.M.; Sousa, R.A.; Reis, R.L.; Espregueira-Mendes, J. Clinical Management of Articular Cartilage Lesions. In Studies in Mechanobiology, Tissue Engineering and Biomaterials; Springer: Cham, Switzerland, 2017; Volume 21, pp. 29–53. [Google Scholar]
- Camp, C.L.; Stuart, M.J.; Krych, A.J. Current Concepts of Articular Cartilage Restoration Techniques in the Knee. Sports Health Multidiscip. Approach 2014, 6, 265–273. [Google Scholar] [CrossRef] [Green Version]
- Fellows, C.R.; Gauthaman, K.; Pushparaj, P.N.; Abbas, M.; Matta, C.; Lewis, R.; Buhrmann, C.; Shakibaei, M.; Mobasheri, A. Stem Cells in Bone and Articular Cartilage Tissue Regeneration. In Bone and Cartilage Regeneration; Springer: Cham, Switzerland, 2016; pp. 177–204. [Google Scholar] [CrossRef]
- Buckwalter, J.A.; Mankin, H.J. Articular cartilage: Tissue design and chondrocyte-matrix interactions. Instr. Course Lect. 1998, 47, 477–486. [Google Scholar] [PubMed]
- Bhosale, A.M.; Richardson, J.B. Articular cartilage: Structure, injuries and review of management. Br. Med. Bull. 2008, 87, 77–95. [Google Scholar] [CrossRef] [PubMed]
- Hunziker, E.B.; Kapfinger, E.; Geiss, J. The structural architecture of adult mammalian articular cartilage evolves by a synchronized process of tissue resorption and neoformation during postnatal development. Osteoarthr. Cartil. 2007, 15, 403–413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akkiraju, H.; Nohe, A. Role of Chondrocytes in Cartilage Formation, Progression of Osteoarthritis and Cartilage Regeneration. J. Dev. Biol. 2015, 3, 177–192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grodzinsky, A.J.; Levenston, M.E.; Jin, M.; Frank, E.H. Cartilage Tissue Remodeling in Response to Mechanical Forces. Annu. Rev. Biomed. Eng. 2000, 2, 691–713. [Google Scholar] [CrossRef]
- Kiani, C.; Chen, L.; Wu, Y.J.; Yee, A.J.; Yang, B.B. Structure and function of aggrecan. Cell Res. 2002, 12, 19–32. [Google Scholar] [CrossRef] [Green Version]
- Fujioka, R.; Aoyama, T.; Takakuwa, T. The layered structure of the articular surface. Osteoarthr. Cartil. 2013, 21, 1092–1098. [Google Scholar] [CrossRef] [Green Version]
- Buckwalter, J.A.; Mow, V.C.; Ratcliffe, A. Restoration of Injured or Degenerated Articular Cartilage. J. Am. Acad. Orthop. Surg. 1994, 2, 192–201. [Google Scholar] [CrossRef]
- Simkin, P.A. Consider the tidemark. J. Rheumatol. 2012, 39, 890–892. [Google Scholar] [CrossRef] [Green Version]
- Lyons, T.J.; McClure, S.F.; Stoddart, R.W.; McClure, J. The normal human chondro-osseous junctional region: Evidence for contact of uncalcified cartilage with subchondral bone and marrow spaces. BMC Musculoskelet. Disord. 2006, 7, 52. [Google Scholar] [CrossRef] [Green Version]
- Oegema, T.R.; Carpenter, R.J.; Hofmeister, F.; Thompson, R.C. The interaction of the zone of calcified cartilage and subchondral bone in osteoarthritis. Microsc. Res. Tech. 1997, 37, 324–332. [Google Scholar] [CrossRef]
- Arkill, K.P.; Winlove, C.P. Solute transport in the deep and calcified zones of articular cartilage. Osteoarthr. Cartil. 2008, 16, 708–714. [Google Scholar] [CrossRef] [Green Version]
- Hoemann, C.; Lafantaisie-Favreau, C.-H.; Lascau-Coman, V.; Chen, G.; Guzmán-Morales, J. The Cartilage-Bone Interface. J. Knee Surg. 2012, 25, 085–098. [Google Scholar] [CrossRef] [PubMed]
- Clarke, B. Normal Bone Anatomy and Physiology. Clin. J. Am. Soc. Nephrol. 2008, 3, S131–S139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Madry, H.; van Dijk, C.N.; Mueller-Gerbl, M. The basic science of the subchondral bone. Knee Surg. Sports Traumatol. Arthrosc. 2010, 18, 419–433. [Google Scholar] [CrossRef] [PubMed]
- Boskey, A.L. Bone composition: Relationship to bone fragility and antiosteoporotic drug effects. Bonekey Rep. 2013, 2, 447. [Google Scholar] [CrossRef] [Green Version]
- Von Euw, S.; Wang, Y.; Laurent, G.; Drouet, C.; Babonneau, F.; Nassif, N.; Azaïs, T. Bone mineral: New insights into its chemical composition. Sci. Rep. 2019, 9, 8456. [Google Scholar] [CrossRef] [Green Version]
- Franz-Odendaal, T.A.; Hall, B.K.; Witten, P.E. Buried alive: How osteoblasts become osteocytes. Dev. Dyn. 2006, 235, 176–190. [Google Scholar] [CrossRef]
- Mohamed, A.M.F.S. An overview of bone cells and their regulating factors of differentiation. Malays. J. Med. Sci. 2008, 15, 4–12. [Google Scholar]
- Imhof, H.; Sulzbacher, I.; Grampp, S.; Czerny, C.; Youssefzadeh, S.; Kainberger, F. Subchondral Bone and Cartilage Disease. Investig. Radiol. 2000, 35, 581–588. [Google Scholar] [CrossRef]
- Cross, L.M.; Thakur, A.; Jalili, N.A.; Detamore, M.; Gaharwar, A.K. Nanoengineered biomaterials for repair and regeneration of orthopedic tissue interfaces. Acta Biomater. 2016, 42, 2–17. [Google Scholar] [CrossRef] [PubMed]
- Augat, P.; Schorlemmer, S. The role of cortical bone and its microstructure in bone strength. Age Ageing 2006, 35, ii27–ii31. [Google Scholar] [CrossRef] [Green Version]
- Gibson, L.J. The mechanical behaviour of cancellous bone. J. Biomech. 1985, 18, 317–328. [Google Scholar] [CrossRef]
- Getgood, A.; Bhullar, T.P.S.; Rushton, N. Current concepts in articular cartilage repair. Orthop. Trauma 2009, 23, 189–200. [Google Scholar] [CrossRef]
- Di Luca, A.; Van Blitterswijk, C.; Moroni, L. The osteochondral interface as a gradient tissue: From development to the fabrication of gradient scaffolds for regenerative medicine. Birth Defects Res. Part C Embryo Today Rev. 2015, 105, 34–52. [Google Scholar] [CrossRef]
- Oliveira, J.M.; Pina, S.; Reis, R.L.; San, J.R. (Eds.) Osteochondral tissue engineering: Challenges, Current Strategies, and Technological advances, 1st ed.; Springer International Publishing AG: Cham, Switzerland, 2018; Volume 1059, ISBN 9783319767345. [Google Scholar]
- Yang, P.J.; Temenoff, J.S. Engineering Orthopedic Tissue Interfaces. Tissue Eng. Part B Rev. 2009, 15, 127–141. [Google Scholar] [CrossRef] [Green Version]
- O’Brien, F.J. Biomaterials & scaffolds for tissue engineering. Mater. Today 2011, 14, 88–95. [Google Scholar] [CrossRef]
- Howard, D.; Buttery, L.D.; Shakesheff, K.M.; Roberts, S.J. Tissue engineering: Strategies, stem cells and scaffolds. J. Anat. 2008, 213, 66–72. [Google Scholar] [CrossRef] [PubMed]
- Ribeiro, V.; Pina, S.; Oliveira, J.M.; Reis, R.L. Fundamentals on Osteochondral Tissue Engineering. In Regenerative Strategies for the Treatment of Knee Joint Disabilities; Springer: Cham, Switzerland, 2017; pp. 129–146. [Google Scholar] [CrossRef]
- Zhang, B.; Huang, J.; Narayan, R.J. Gradient scaffolds for osteochondral tissue engineering and regeneration. J. Mater. Chem. B 2020, 8, 8149–8170. [Google Scholar] [CrossRef] [PubMed]
- Nooeaid, P.; Salih, V.; Beier, J.P.; Boccaccini, A.R. Osteochondral tissue engineering: Scaffolds, stem cells and applications Scaffolds for osteochondral tissue engineering. J. Cell. Mol. Med. 2012, 16, 2247–2270. [Google Scholar] [CrossRef]
- Nooeaid, P.; Roether, J.A.; Weber, E.; Schubert, D.W.; Boccaccini, A.R. Technologies for multilayered scaffolds suitable for interface tissue engineering. Adv. Eng. Mater. 2014, 16, 319–327. [Google Scholar] [CrossRef]
- Malafaya, P.B.; Silva, G.A.; Reis, R.L. Natural–origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications. Adv. Drug Deliv. Rev. 2007, 59, 207–233. [Google Scholar] [CrossRef] [Green Version]
- Reed, S.; Lau, G.; Delattre, B.; Lopez, D.D.; Tomsia, A.P.; Wu, B.M. Macro- and micro-designed chitosan-alginate scaffold architecture by three-dimensional printing and directional freezing. Biofabrication 2016, 8, 015003. [Google Scholar] [CrossRef] [Green Version]
- Kasoju, N.; Bora, U. Silk fibroin in tissue engineering. Adv. Healthc. Mater. 2012, 1, 393–412. [Google Scholar] [CrossRef] [PubMed]
- Algul, D.; Sipahi, H.; Aydin, A.; Kelleci, F.; Ozdatli, S.; Yener, F.G. Biocompatibility of biomimetic multilayered alginate-chitosan/β-TCP scaffold for osteochondral tissue. Int. J. Biol. Macromol. 2015, 79, 363–369. [Google Scholar] [CrossRef]
- Müller, W.E.G.; Neufurth, M.; Wang, S.; Tolba, E.; Schröder, H.C.; Wang, X. Morphogenetically active scaffold for osteochondral repair (Polyphosphate/alginate/N,O-carboxymethyl chitosan). Eur. Cells Mater. 2016, 31, 174–190. [Google Scholar] [CrossRef] [PubMed]
- Ruan, S.-Q.; Yan, L.; Deng, J.; Huang, W.-L.; Jiang, D.-M. Preparation of a biphase composite scaffold and its application in tissue engineering for femoral osteochondral defects in rabbits. Int. Orthop. 2017, 41, 1899–1908. [Google Scholar] [CrossRef]
- Xiao, H.; Huang, W.; Xiong, K.; Ruan, S.; Yuan, C.; Mo, G.; Tian, R.; Zhou, S.; She, R.; Ye, P.; et al. Osteochondral repair using scaffolds with gradient pore sizes constructed with silk fibroin, chitosan, and nano-hydroxyapatite. Int. J. Nanomed. 2019, 14, 2011–2027. [Google Scholar] [CrossRef] [Green Version]
- Chen, P.; Xia, C.; Mo, J.; Mei, S.; Lin, X.; Fan, S. Interpenetrating polymer network scaffold of sodium hyaluronate and sodium alginate combined with berberine for osteochondral defect regeneration. Mater. Sci. Eng. C 2018, 91, 190–200. [Google Scholar] [CrossRef] [PubMed]
- Filardo, G.; Perdisa, F.; Gelinsky, M.; Despang, F.; Fini, M.; Marcacci, M.; Parrilli, A.P.; Roffi, A.; Salamanna, F.; Sartori, M.; et al. Novel alginate biphasic scaffold for osteochondral regeneration: An in vivo evaluation in rabbit and sheep models. J. Mater. Sci. Mater. Med. 2018, 29. [Google Scholar] [CrossRef] [PubMed]
- Schütz, K.; Despang, F.; Lode, A.; Gelinsky, M. Cell-laden biphasic scaffolds with anisotropic structure for the regeneration of osteochondral tissue. J. Tissue Eng. Regen. Med. 2016, 10, 404–417. [Google Scholar] [CrossRef] [PubMed]
- Bartnikowski, M.; Akkineni, A.R.; Gelinsky, M.; Woodruff, M.A.; Klein, T.J. A hydrogel model incorporating 3D-plotted hydroxyapatite for osteochondral tissue engineering. Materials 2016, 9, 285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhu, Y.; Kong, L.; Farhadi, F.; Xia, W.; Chang, J.; He, Y.; Li, H. An injectable continuous stratified structurally and functionally biomimetic construct for enhancing osteochondral regeneration. Biomaterials 2019, 192, 149–158. [Google Scholar] [CrossRef]
- Hoshiba, T.; Lu, H.; Kawazoe, N.; Chen, G. Decellularized matrices for tissue engineering. Expert Opin. Biol. Ther. 2010, 10, 1717–1728. [Google Scholar] [CrossRef]
- Taylor, D.A.; Sampaio, L.C.; Ferdous, Z.; Gobin, A.S.; Taite, L.J. Decellularized matrices in regenerative medicine. Acta Biomater. 2018, 74, 74–89. [Google Scholar] [CrossRef]
- Kim, Y.S.; Majid, M.; Melchiorri, A.J.; Mikos, A.G. Applications of decellularized extracellular matrix in bone and cartilage tissue engineering. Bioeng. Transl. Med. 2019, 4, 83–95. [Google Scholar] [CrossRef] [Green Version]
- Benders, K.E.M.; van Weeren, P.R.; Badylak, S.F.; Saris, D.B.F.; Dhert, W.J.A.; Malda, J. Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol. 2013, 31, 169–176. [Google Scholar] [CrossRef]
- Sun, X.; Yin, H.; Wang, Y.; Lu, J.; Shen, X.; Lu, C.; Tang, H.; Meng, H.; Yang, S.; Yu, W.; et al. In Situ Articular Cartilage Regeneration through Endogenous Reparative Cell Homing Using a Functional Bone Marrow-Specific Scaffolding System. ACS Appl. Mater. Interfaces 2018, 10, 38715–38728. [Google Scholar] [CrossRef]
- Wang, Z.; Li, Z.; Li, Z.; Wu, B.; Liu, Y.; Wu, W. Cartilaginous extracellular matrix derived from decellularized chondrocyte sheets for the reconstruction of osteochondral defects in rabbits. Acta Biomater. 2018, 81, 129–145. [Google Scholar] [CrossRef]
- Kheir, E.; Stapleton, T.; Shaw, D.; Jin, Z.; Fisher, J.; Ingham, E. Development and characterization of an acellular porcine cartilage bone matrix for use in tissue engineering. J. Biomed. Mater. Res. Part A 2011, 99, 283–294. [Google Scholar] [CrossRef] [PubMed]
- Novak, T.; Fites Gilliland, K.; Xu, X.; Worke, L.; Ciesielski, A.; Breur, G.; Neu, C.P. In Vivo Cellular Infiltration and Remodeling in a Decellularized Ovine Osteochondral Allograft. Tissue Eng. Part A 2016, 22, 1274–1285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elder, S.; Chenault, H.; Gloth, P.; Webb, K.; Recinos, R.; Wright, E.; Moran, D.; Butler, J.; Borazjani, A.; Cooley, A. Effects of antigen removal on a porcine osteochondral xenograft for articular cartilage repair. J. Biomed. Mater. Res. Part A 2018, 106, 2251–2260. [Google Scholar] [CrossRef]
- Li, Y.; Xu, Y.; Liu, Y.; Wang, Z.; Chen, W.; Duan, L.; Gu, D. Decellularized cartilage matrix scaffolds with laser-machined micropores for cartilage regeneration and articular cartilage repair. Mater. Sci. Eng. C 2019, 105, 110139. [Google Scholar] [CrossRef]
- Sutherland, A.J.; Beck, E.C.; Dennis, S.C.; Converse, G.L.; Hopkins, R.A.; Berkland, C.J.; Detamore, M.S. Decellularized Cartilage May Be a Chondroinductive Material for Osteochondral Tissue Engineering. PLoS ONE 2015, 10, e0121966. [Google Scholar] [CrossRef]
- Gentile, P.; Chiono, V.; Carmagnola, I.; Hatton, P. An Overview of Poly(lactic-co-glycolic) Acid (PLGA)-Based Biomaterials for Bone Tissue Engineering. Int. J. Mol. Sci. 2014, 15, 3640–3659. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Yang, F.; Liu, K.; Shen, H.; Zhu, Y.; Zhang, W.; Liu, W.; Wang, S.; Cao, Y.; Zhou, G. The impact of PLGA scaffold orientation on in vitro cartilage regeneration. Biomaterials 2012, 33, 2926–2935. [Google Scholar] [CrossRef]
- Siddiqui, N.; Asawa, S.; Birru, B.; Baadhe, R.; Rao, S. PCL-based composite scaffold matrices for tissue engineering applications. Mol. Biotechnol. 2018, 60, 506–532. [Google Scholar] [CrossRef]
- Wang, S.J.; Zhang, Z.Z.; Jiang, D.; Qi, Y.S.; Wang, H.J.; Zhang, J.Y.; Ding, J.X.; Yu, J.K. Thermogel-coated poly(ε-caprolactone) composite scaffold for enhanced cartilage tissue engineering. Polymers 2016, 8, 200. [Google Scholar] [CrossRef] [Green Version]
- Caetano, G.F.; Wang, W.; Chiang, W.-H.; Cooper, G.; Diver, C.; Blaker, J.J.; Frade, M.A.; Bártolo, P. 3D-printed poly(ɛ-caprolactone)/graphene scaffolds activated with p1-latex protein for bone regeneration. 3D Print. Addit. Manuf. 2018, 5, 127–137. [Google Scholar] [CrossRef] [Green Version]
- Wang, W.; Junior, J.R.P.; Nalesso, P.R.L.; Musson, D.; Cornish, J.; Mendonça, F.; Caetano, G.F.; Bártolo, P. Engineered 3D printed poly(ε-caprolactone)/graphene scaffolds for bone tissue engineering. Mater. Sci. Eng. C 2019, 100, 759–770. [Google Scholar] [CrossRef] [PubMed]
- Du, Y.; Liu, H.; Yang, Q.; Wang, S.; Wang, J.; Ma, J.; Noh, I.; Mikos, A.G.; Zhang, S. Selective laser sintering scaffold with hierarchical architecture and gradient composition for osteochondral repair in rabbits. Biomaterials 2017, 137, 37–48. [Google Scholar] [CrossRef] [PubMed]
- Neumann, A.J.; Quinn, T.; Bryant, S.J. Nondestructive evaluation of a new hydrolytically degradable and photo-clickable PEG hydrogel for cartilage tissue engineering. Acta Biomater. 2016, 39, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Wang, J.; Zhang, F.; Tsang, W.P.; Wan, C.; Wu, C. Fabrication of injectable high strength hydrogel based on 4-arm star PEG for cartilage tissue engineering. Biomaterials 2017, 120, 11–21. [Google Scholar] [CrossRef]
- Papavasiliou, G.; Sokic, S.; Turturro, M. Synthetic PEG Hydrogels as Extracellular Matrix Mimics for Tissue Engineering Applications. In Biotechnology—Molecular Studies and Novel Applications for Improved Quality of Human Life; InTechOpen: London, UK, 2012. [Google Scholar]
- Díaz Lantada, A.; Alarcón Iniesta, H.; García-Ruíz, J.P. Composite scaffolds for osteochondral repair obtained by combination of additive manufacturing, leaching processes and hMSC-CM functionalization. Mater. Sci. Eng. C 2016, 59, 218–227. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Liu, X.; Crook, J.M.; Wallace, G.G. Development of a porous 3D graphene-PDMS scaffold for improved osseointegration. Colloids Surf. B Biointerfaces 2017, 159, 386–393. [Google Scholar] [CrossRef]
- Jiménez, G.; Venkateswaran, S.; López-Ruiz, E.; Perán, M.; Pernagallo, S.; Díaz-Monchón, J.J.; Canadas, R.F.; Antich, C.; Oliveira, J.M.; Callanan, A.; et al. A soft 3D polyacrylate hydrogel recapitulates the cartilage niche and allows growth-factor free tissue engineering of human articular cartilage. Acta Biomater. 2019, 90, 146–156. [Google Scholar] [CrossRef] [PubMed]
- Horkay, F.; Basser, P.J. Composite Hydrogel Model of Cartilage Predicts Its Load-Bearing Ability. Sci. Rep. 2020, 10, 8103. [Google Scholar] [CrossRef]
- Tsai, M.C.; Hung, K.C.; Hung, S.C.; Hsu, S.H. Evaluation of biodegradable elastic scaffolds made of anionic polyurethane for cartilage tissue engineering. Colloids Surf. B Biointerfaces 2015, 125, 34–44. [Google Scholar] [CrossRef] [PubMed]
- Korthagen, N.M.; Brommer, H.; Hermsen, G.; Plomp, S.G.M.; Melsom, G.; Coeleveld, K.; Mastbergen, S.C.; Weinans, H.; van Buul, W.; van Weeren, P.R. A short-term evaluation of a thermoplastic polyurethane implant for osteochondral defect repair in an equine model. Vet. J. 2019, 251, 105340. [Google Scholar] [CrossRef]
- Nair, L.S.; Laurencin, C.T. Biodegradable polymers as biomaterials. Prog. Polym. Sci. 2007, 32, 762–798. [Google Scholar] [CrossRef]
- Freeman, F.E.; Browe, D.C.; Diaz-Payno, P.J.; Nulty, J.; Von Euw, S.; Grayson, W.L.; Kelly, D.J. Biofabrication of multiscale bone extracellular matrix scaffolds for bone tissue engineering. Eur. Cells Mater. 2019, 38, 168–187. [Google Scholar] [CrossRef] [PubMed]
- Mellor, L.F.; Nordberg, R.C.; Huebner, P.; Mohiti-Asli, M.; Taylor, M.A.; Efird, W.; Oxford, J.T.; Spang, J.T.; Shirwaiker, R.A.; Loboa, E.G. Investigation of multiphasic 3D-bioplotted scaffolds for site-specific chondrogenic and osteogenic differentiation of human adipose-derived stem cells for osteochondral tissue engineering applications. J. Biomed. Mater. Res. Part B Appl. Biomater. 2020, 108, 2017–2030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nogami, M.; Kimura, T.; Seki, S.; Matsui, Y.; Yoshida, T.; Koike-Soko, C.; Okabe, M.; Motomura, H.; Gejo, R.; Nikaido, T. A Human Amnion-Derived Extracellular Matrix-Coated Cell-Free Scaffold for Cartilage Repair: In Vitro and in Vivo Studies. Tissue Eng. Part A 2016, 22, 680–688. [Google Scholar] [CrossRef]
- Ingavle, G.C.; Gehrke, S.H.; Detamore, M.S. The bioactivity of agarose-PEGDA interpenetrating network hydrogels with covalently immobilized RGD peptides and physically entrapped aggrecan. Biomaterials 2014, 35, 3558–3570. [Google Scholar] [CrossRef] [Green Version]
- Lam, J.; Lu, S.; Kasper, F.K.; Mikos, A.G. Strategies for controlled delivery of biologics for cartilage repair. Adv. Drug Deliv. Rev. 2015, 84, 123–134. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caballero Aguilar, L.M.; Silva, S.M.; Moulton, S.E. Growth factor delivery: Defining the next generation platforms for tissue engineering. J. Control. Release 2019, 306, 40–58. [Google Scholar] [CrossRef] [PubMed]
- Carragee, E.J.; Chu, G.; Rohatgi, R.; Hurwitz, E.L.; Weiner, B.K.; Yoon, S.T.; Comer, G.; Kopjar, B. Cancer risk after use of recombinant bone morphogenetic protein-2 for spinal arthrodesis. J. Bone Jt. Surg. Ser. A 2013, 95, 1537–1545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levinson, C.; Lee, M.; Applegate, L.A.; Zenobi-Wong, M. An injectable heparin-conjugated hyaluronan scaffold for local delivery of transforming growth factor β1 promotes successful chondrogenesis. Acta Biomater. 2019, 99, 168–180. [Google Scholar] [CrossRef]
- Arora, A.; Mahajan, A.; Katti, D.S. TGF-β1 presenting enzymatically cross-linked injectable hydrogels for improved chondrogenesis. Colloids Surf. B Biointerfaces 2017, 159, 838–848. [Google Scholar] [CrossRef] [PubMed]
- Zhou, M.; Lozano, N.; Wychowaniec, J.K.; Hodgkinson, T.; Richardson, S.M.; Kostarelos, K.; Hoyland, J.A. Graphene oxide: A growth factor delivery carrier to enhance chondrogenic differentiation of human mesenchymal stem cells in 3D hydrogels. Acta Biomater. 2019, 96, 271–280. [Google Scholar] [CrossRef] [PubMed]
- Mahmoudi, Z.; Mohammadnejad, J.; Razavi Bazaz, S.; Abouei Mehrizi, A.; Saidijam, M.; Dinarvand, R.; Ebrahimi Warkiani, M.; Soleimani, M. Promoted chondrogenesis of hMCSs with controlled release of TGF-β3 via microfluidics synthesized alginate nanogels. Carbohydr. Polym. 2020, 229, 115551. [Google Scholar] [CrossRef]
- Taniyama, T.; Masaoka, T.; Yamada, T.; Wei, X.; Yasuda, H.; Yoshii, T.; Kozaka, Y.; Takayama, T.; Hirano, M.; Okawa, A.; et al. Repair of Osteochondral Defects in a Rabbit Model Using a Porous Hydroxyapatite Collagen Composite Impregnated With Bone Morphogenetic Protein-2. Artif. Organs 2015, 39, 529–535. [Google Scholar] [CrossRef]
- Pot, M.; de Kroon, L.; van der Kraan, P.; van Kuppevelt, T.; Daamen, W. Unidirectional BMP2-loaded collagen scaffolds induce chondrogenic differentiation. Biomed. Mater. 2017, 13. [Google Scholar] [CrossRef]
- Mazaki, T.; Shiozaki, Y.; Yamane, K.; Yoshida, A.; Nakamura, M.; Yoshida, Y.; Zhou, D.; Kitajima, T.; Tanaka, M.; Ito, Y.; et al. A novel, visible light-induced, rapidly cross-linkable gelatin scaffold for osteochondral tissue engineering. Sci. Rep. 2014, 4, 4457. [Google Scholar] [CrossRef] [Green Version]
- Wang, Q.; Zhang, H.; Gan, H.; Wang, H.; Li, Q.; Wang, Z. Application of combined porous tantalum scaffolds loaded with bone morphogenetic protein 7 to repair of osteochondral defect in rabbits. Int. Orthop. 2018, 42, 1437–1448. [Google Scholar] [CrossRef] [PubMed]
- Boushell, M.K.; Mosher, C.Z.; Suri, G.K.; Doty, S.B.; Strauss, E.J.; Hunziker, E.B.; Lu, H.H. Polymeric mesh and insulin-like growth factor 1 delivery enhance cell homing and graft-cartilage integration. Ann. N. Y. Acad. Sci. 2019, 1442, 138–152. [Google Scholar] [CrossRef]
- Yang, W.; Cao, Y.; Zhang, Z.; Du, F.; Shi, Y.; Li, X.; Zhang, Q. Targeted delivery of FGF2 to subchondral bone enhanced the repair of articular cartilage defect. Acta Biomater. 2018, 69, 170–182. [Google Scholar] [CrossRef] [PubMed]
- Wen, Y.T.; Dai, N.T.; Hsu, S.H. Biodegradable water-based polyurethane scaffolds with a sequential release function for cell-free cartilage tissue engineering. Acta Biomater. 2019, 88, 301–313. [Google Scholar] [CrossRef]
- Costa, P.F. Bone Tissue Engineering Drug Delivery. Curr. Mol. Biol. Rep. 2015, 1, 87–93. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Wu, T.; Huang, S.; Suen, C.W.W.; Cheng, X.; Li, J.; Hou, H.; She, G.; Zhang, H.; Wang, H.; et al. Sustained Release SDF-1α/TGF-β1-Loaded Silk Fibroin-Porous Gelatin Scaffold Promotes Cartilage Repair. ACS Appl. Mater. Interfaces 2019, 11, 14608–14618. [Google Scholar] [CrossRef] [PubMed]
- Fathi-Achachelouei, M.; Keskin, D.; Bat, E.; Vrana, N.E.; Tezcaner, A. Dual growth factor delivery using PLGA nanoparticles in silk fibroin/PEGDMA hydrogels for articular cartilage tissue engineering. J. Biomed. Mater. Res. Part B Appl. Biomater. 2020, 108, 2041–2062. [Google Scholar] [CrossRef]
- Diaz-Rodriguez, P.; Erndt-Marino, J.D.; Gharat, T.; Munoz Pinto, D.J.; Samavedi, S.; Bearden, R.; Grunlan, M.A.; Saunders, W.B.; Hahn, M.S. Toward zonally tailored scaffolds for osteochondral differentiation of synovial mesenchymal stem cells. J. Biomed. Mater. Res. Part B Appl. Biomater. 2019, 107, 2019–2029. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Yue, H.; Huang, W.; Lin, X.; Xie, X.; He, Z.; He, X.; Liu, S.; Bai, L.; Lu, B.; et al. Cryogenic 3D printing of heterogeneous scaffolds with gradient mechanical strengths and spatial delivery of osteogenic peptide/TGF-β1 for osteochondral tissue regeneration. Biofabrication 2020, 12, 025030. [Google Scholar] [CrossRef]
- Crecente-Campo, J.; Borrajo, E.; Vidal, A.; Garcia-Fuentes, M. New scaffolds encapsulating TGF-β3/BMP-7 combinations driving strong chondrogenic differentiation. Eur. J. Pharm. Biopharm. 2017, 114, 69–78. [Google Scholar] [CrossRef] [Green Version]
- Lu, S.; Lam, J.; Trachtenberg, J.E.; Lee, E.J.; Seyednejad, H.; van den Beucken, J.J.J.P.; Tabata, Y.; Wong, M.E.; Jansen, J.A.; Mikos, A.G.; et al. Dual growth factor delivery from bilayered, biodegradable hydrogel composites for spatially-guided osteochondral tissue repair. Biomaterials 2014, 35, 8829–8839. [Google Scholar] [CrossRef] [Green Version]
- Di Luca, A.; Klein-Gunnewiek, M.; Vancso, J.G.; van Blitterswijk, C.A.; Benetti, E.M.; Moroni, L. Covalent Binding of Bone Morphogenetic Protein-2 and Transforming Growth Factor-β3 to 3D Plotted Scaffolds for Osteochondral Tissue Regeneration. Biotechnol. J. 2017, 12, 1700072. [Google Scholar] [CrossRef]
- Ni, Z.; Zhou, S.; Li, S.; Kuang, L.; Chen, H.; Luo, X.; Ouyang, J.; He, M.; Du, X.; Chen, L. Exosomes: Roles and therapeutic potential in osteoarthritis. Bone Res. 2020, 8, 25. [Google Scholar] [CrossRef]
- Mazzucco, L.; Balbo, V.; Cattana, E.; Guaschino, R.; Borzini, P. Not every PRP-gel is born equal. Evaluation of growth factor availability for tissues through four PRP-gel preparations: Fibrinet®, RegenPRP-Kit®, Plateltex® and one manual procedure. Vox Sang. 2009, 97, 110–118. [Google Scholar] [CrossRef]
- Pavlovic, V.; Ciric, M.; Jovanovic, V.; Stojanovic, P. Platelet Rich Plasma: A short overview of certain bioactive components. Open Med. 2016, 11, 242–247. [Google Scholar] [CrossRef] [PubMed]
- Marmotti, A.; Rossi, R.; Castoldi, F.; Roveda, E.; Michielon, G.; Peretti, G.M. PRP and Articular Cartilage: A Clinical Update. Biomed. Res. Int. 2015, 2015, 542502. [Google Scholar] [CrossRef] [PubMed]
- Chang, K.-V.; Hung, C.-Y.; Aliwarga, F.; Wang, T.-G.; Han, D.-S.; Chen, W.-S. Comparative effectiveness of platelet-rich plasma injections for treating knee joint cartilage degenerative pathology: A systematic review and meta-analysis. Arch. Phys. Med. Rehabil. 2014, 95, 562–575. [Google Scholar] [CrossRef]
- Yausep, O.E.; Madhi, I.; Trigkilidas, D. Platelet rich plasma for treatment of osteochondral lesions of the talus: A systematic review of clinical trials. J. Orthop. 2020, 18, 218–225. [Google Scholar] [CrossRef]
- Scioli, M.G.; Bielli, A.; Gentile, P.; Cervelli, V.; Orlandi, A. Combined treatment with platelet-rich plasma and insulin favours chondrogenic and osteogenic differentiation of human adipose-derived stem cells in three-dimensional collagen scaffolds. J. Tissue Eng. Regen. Med. 2017, 11, 2398–2410. [Google Scholar] [CrossRef]
- Yan, W.; Xu, X.; Xu, Q.; Sun, Z.; Jiang, Q.; Shi, D. Platelet-rich plasma combined with injectable hyaluronic acid hydrogel for porcine cartilage regeneration: A 6-month follow-up. Regen. Biomater. 2020, 7, 77–90. [Google Scholar] [CrossRef] [Green Version]
- Chang, N.J.; Erdenekhuyag, Y.; Chou, P.H.; Chu, C.J.; Lin, C.C.; Shie, M.Y. Therapeutic Effects of the Addition of Platelet-Rich Plasma to Bioimplants and Early Rehabilitation Exercise on Articular Cartilage Repair. Am. J. Sports Med. 2018, 46, 2232–2241. [Google Scholar] [CrossRef]
- Chahla, J.; Cinque, M.E.; Piuzzi, N.S.; Mannava, S.; Geeslin, A.G.; Murray, I.R.; Dornan, G.J.; Muschler, G.F.; LaPrade, R.F. A call for standardization in platelet-rich plasma preparation protocols and composition reporting. J. Bone Jt. Surg. 2017, 99, 1769–1779. [Google Scholar] [CrossRef]
- Bellavia, D.; Veronesi, F.; Carina, V.; Costa, V.; Raimondi, L.; De Luca, A.; Alessandro, R.; Fini, M.; Giavaresi, G. Gene therapy for chondral and osteochondral regeneration: Is the future now? Cell. Mol. Life Sci. 2018, 75, 649–667. [Google Scholar] [CrossRef]
- Yan, X.; Chen, Y.R.; Song, Y.F.; Yang, M.; Ye, J.; Zhou, G.; Yu, J.K. Scaffold-based gene therapeutics for osteochondral tissue engineering. Front. Pharmacol. 2020, 10, 1534. [Google Scholar] [CrossRef]
- Gonzalez-Fernandez, T.; Rathan, S.; Hobbs, C.; Pitacco, P.; Freeman, F.E.; Cunniffe, G.M.; Dunne, N.J.; McCarthy, H.O.; Nicolosi, V.; O’Brien, F.J.; et al. Pore-forming bioinks to enable spatio-temporally defined gene delivery in bioprinted tissues. J. Control. Release 2019, 301, 13–27. [Google Scholar] [CrossRef]
- Lee, Y.H.; Wu, H.C.; Yeh, C.W.; Kuan, C.H.; Liao, H.T.; Hsu, H.C.; Tsai, J.C.; Sun, J.S.; Wang, T.W. Enzyme-crosslinked gene-activated matrix for the induction of mesenchymal stem cells in osteochondral tissue regeneration. Acta Biomater. 2017, 63, 210–226. [Google Scholar] [CrossRef]
- Rowland, C.R.; Glass, K.A.; Ettyreddy, A.R.; Gloss, C.C.; Matthews, J.R.L.; Huynh, N.P.T.; Guilak, F. Regulation of decellularized tissue remodeling via scaffold-mediated lentiviral delivery in anatomically-shaped osteochondral constructs. Biomaterials 2018, 177, 161–175. [Google Scholar] [CrossRef] [PubMed]
- Madry, H.; Gao, L.; Rey-Rico, A.; Venkatesan, J.K.; Müller-Brandt, K.; Cai, X.; Goebel, L.; Schmitt, G.; Speicher-Mentges, S.; Zurakowski, D.; et al. Thermosensitive Hydrogel Based on PEO–PPO–PEO Poloxamers for a Controlled In Situ Release of Recombinant Adeno-Associated Viral Vectors for Effective Gene Therapy of Cartilage Defects. Adv. Mater. 2020, 32, 1906508. [Google Scholar] [CrossRef] [Green Version]
- Carlos Rodriguez-Merchan, E.; Valentino, L.A. The role of gene therapy in cartilage repair. Arch. Bone Jt. Surg. 2019, 7, 79–90. [Google Scholar]
- Li, T.; Liu, B.; Chen, K.; Lou, Y.; Jiang, Y.; Zhang, D. Small molecule compounds promote the proliferation of chondrocytes and chondrogenic differentiation of stem cells in cartilage tissue engineering. Biomed. Pharmacother. 2020, 131, 110652. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Zhu, G.; Li, N.; Song, J.; Wang, L.; Shi, X. Small molecules and their controlled release that induce the osteogenic/chondrogenic commitment of stem cells. Biotechnol. Adv. 2015, 33, 1626–1640. [Google Scholar] [CrossRef]
- Johnson, K.; Zhu, S.; Tremblay, M.S.; Payette, J.N.; Wang, J.; Bouchez, L.C.; Meeusen, S.; Althage, A.; Cho, C.Y.; Wu, X.; et al. A stem cell-based approach to cartilage repair. Science (80-) 2012, 336, 717–721. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spakova, T.; Plsikova, J.; Harvanova, D.; Lacko, M.; Stolfa, S.; Rosocha, J. Influence of Kartogenin on Chondrogenic Differentiation of Human Bone Marrow-Derived MSCs in 2D Culture and in Co-Cultivation with OA Osteochondral Explant. Molecules 2018, 23, 181. [Google Scholar] [CrossRef] [Green Version]
- Kwon, J.Y.; Lee, S.H.; Na, H.-S.; Jung, K.; Choi, J.; Cho, K.H.; Lee, C.-Y.; Kim, S.J.; Park, S.-H.; Shin, D.-Y.; et al. Kartogenin inhibits pain behavior, chondrocyte inflammation, and attenuates osteoarthritis progression in mice through induction of IL-10. Sci. Rep. 2018, 8, 13832. [Google Scholar] [CrossRef]
- Liu, C.; Li, Y.; Yang, Z.; Zhou, Z.; Lou, Z.; Zhang, Q. Kartogenin enhances the therapeutic effect of bone marrow mesenchymal stem cells derived exosomes in cartilage repair. Nanomedicine 2019, 15, 273–288. [Google Scholar] [CrossRef]
- Liu, X.; Wei, Y.; Xuan, C.; Liu, L.; Lai, C.; Chai, M.; Zhang, Z.; Wang, L.; Shi, X. A Biomimetic Biphasic Osteochondral Scaffold with Layer-Specific Release of Stem Cell Differentiation Inducers for the Reconstruction of Osteochondral Defects. Adv. Healthc. Mater. 2020, 9, 2000076. [Google Scholar] [CrossRef]
- Nishitani, K.; Shirai, T.; Kobayashi, M.; Kuroki, H.; Azuma, Y.; Nakagawa, Y.; Nakamura, T. Positive Effect of Alendronate on Subchondral Bone Healing and Subsequent Cartilage Repair in a Rabbit Osteochondral Defect Model. Am. J. Sports Med. 2009, 37, 139S–147S. [Google Scholar] [CrossRef]
- Xing, R.L.; Zhao, L.R.; Wang, P.M. Bisphosphonates therapy for osteoarthritis: A meta-analysis of randomized controlled trials. Springerplus 2016, 5, 1704. [Google Scholar] [CrossRef] [Green Version]
- Shi, Y.; Hu, X.; Cheng, J.; Zhang, X.; Zhao, F.; Shi, W.; Ren, B.; Yu, H.; Yang, P.; Li, Z.; et al. A small molecule promotes cartilage extracellular matrix generation and inhibits osteoarthritis development. Nat. Commun. 2019, 10, 1914. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cook, B.; Rafiq, R.; Lee, H.; Banks, K.M.; El-Debs, M.; Chiaravalli, J.; Glickman, J.F.; Das, B.C.; Chen, S.; Evans, T. Discovery of a Small Molecule Promoting Mouse and Human Osteoblast Differentiation via Activation of p38 MAPK-β. Cell Chem. Biol. 2019, 26, 926–935.e6. [Google Scholar] [CrossRef] [PubMed]
- Stefani, R.M.; Lee, A.J.; Tan, A.R.; Halder, S.S.; Hu, Y.; Guo, X.E.; Stoker, A.M.; Ateshian, G.A.; Marra, K.G.; Cook, J.L.; et al. Sustained low-dose dexamethasone delivery via a PLGA microsphere-embedded agarose implant for enhanced osteochondral repair. Acta Biomater. 2020, 102, 326–340. [Google Scholar] [CrossRef]
- Costa, P.F.; Puga, A.M.; Díaz-Gomez, L.; Concheiro, A.; Busch, D.H.; Alvarez-Lorenzo, C. Additive manufacturing of scaffolds with dexamethasone controlled release for enhanced bone regeneration. Int. J. Pharm. 2015, 496, 541–550. [Google Scholar] [CrossRef]
- Rodrigues, T.; Gomes, M.E.; Reis, R.L.; Rodrigues, M.T.; Gomes, M.E.; Reis, R.L. Current strategies for osteochondral regeneration: From stem cells to pre-clinical approaches. Curr. Opin. Biotechnol. 2011, 22, 726–733. [Google Scholar] [CrossRef] [Green Version]
- Luby, A.O.; Ranganathan, K.; Lynn, J.V.; Nelson, N.S.; Donneys, A.; Buchman, S.R. Stem cells for bone regeneration: Current state and future directions. J. Craniofac. Surg. 2019, 30, 730–735. [Google Scholar] [CrossRef]
- Nam, Y.; Rim, Y.A.; Lee, J.; Ju, J.H. Current Therapeutic Strategies for Stem Cell-Based Cartilage Regeneration. Stem Cells Int. 2018, 2018, 8490489. [Google Scholar] [CrossRef] [Green Version]
- Canadas, R.F.; Pirraco, R.P.; Oliveira, J.M.; Reis, R.L.; Marques, A.P. Stem cells for osteochondral regeneration. In Advances in Experimental Medicine and Biology; Springer New York LLC: New York, NY, USA, 2018; Volume 1059, pp. 219–240. [Google Scholar]
- Maia, F.R.; Carvalho, M.R.; Oliveira, J.M.; Reis, R.L. Tissue engineering strategies for osteochondral repair. In Advances in Experimental Medicine and Biology; Springer New York LLC: New York, NY, USA, 2018; Volume 1059, pp. 353–371. [Google Scholar]
- Panseri, S.; Russo, A.; Cunha, C.; Bondi, A.; Di Martino, A.; Patella, S.; Kon, E. Osteochondral tissue engineering approaches for articular cartilage and subchondral bone regeneration. Knee Surg. Sports Traumatol. Arthrosc. 2012, 20, 1182–1191. [Google Scholar] [CrossRef] [PubMed]
- Oldershaw, R.A.; Baxter, M.A.; Lowe, E.T.; Bates, N.; Grady, L.M.; Soncin, F.; Brison, D.R.; Hardingham, T.E.; Kimber, S.J. Directed differentiation of human embryonic stem cells toward chondrocytes. Nat. Biotechnol. 2010, 28, 1187–1194. [Google Scholar] [CrossRef] [PubMed]
- Toh, W.S.; Lee, E.H.; Cao, T. Potential of Human Embryonic Stem Cells in Cartilage Tissue Engineering and Regenerative Medicine. Stem Cell Rev. Rep. 2011, 7, 544–559. [Google Scholar] [CrossRef] [PubMed]
- Marolt, D.; Campos, I.M.; Bhumiratana, S.; Koren, A.; Petridis, P.; Zhang, G.; Spitalnik, P.F.; Grayson, W.L.; Vunjak-Novakovic, G. Engineering bone tissue from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2012, 109, 8705–8709. [Google Scholar] [CrossRef] [Green Version]
- Kuznetsov, S.A.; Cherman, N.; Robey, P.G. In vivo bone formation by progeny of human embryonic stem cells. Stem Cells Dev. 2011, 20, 269–287. [Google Scholar] [CrossRef] [Green Version]
- Sundelacruz, S.; Kaplan, D.L. Stem cell- and scaffold-based tissue engineering approaches to osteochondral regenerative medicine. Semin. Cell Dev. Biol. 2009, 20, 646–655. [Google Scholar] [CrossRef] [Green Version]
- Mushahary, D.; Spittler, A.; Kasper, C.; Weber, V.; Charwat, V. Isolation, cultivation, and characterization of human mesenchymal stem cells. Cytom. Part A 2018, 93, 19–31. [Google Scholar] [CrossRef] [Green Version]
- Gadjanski, I.; Vunjak-Novakovic, G. Challenges in engineering osteochondral tissue grafts with hierarchical structures. Expert Opin. Biol. Ther. 2015, 15, 1583–1599. [Google Scholar] [CrossRef] [Green Version]
- Ng, J.; Bernhard, J.; Vunjak-Novakovic, G. Mesenchymal Stem Cells for Osteochondral Tissue Engineering. In Methods in Molecular Biology; Humana Press Inc.: Clifton, NJ, USA, 2016; Volume 1416, pp. 35–54. [Google Scholar]
- Jiang, Y.; Wang, D.; Blocki, A.; Tuan, R.S. Mesenchymal stem cells in musculoskeletal tissue engineering. In Principles of Tissue Engineering; Elsevier: Amsterdam, The Netherlands, 2020; pp. 883–915. [Google Scholar]
- Simmons, C.A.; Matlis, S.; Thornton, A.J.; Chen, S.; Wang, C.Y.; Mooney, D.J. Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J. Biomech. 2003, 36, 1087–1096. [Google Scholar] [CrossRef]
- Luo, Z.J.; Seedhom, B.B. Light and low-frequency pulsatile hydrostatic pressure enhances extracellular matrix formation by bone marrow mesenchymal cells: An in-vitro study with special reference to cartilage repair. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 2007, 221, 499–507. [Google Scholar] [CrossRef] [PubMed]
- Im, G.-I.; Shin, Y.W.; Lee, K.B. Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? Osteoarthr. Cartil. 2005, 13, 845–853. [Google Scholar] [CrossRef] [Green Version]
- Niemeyer, P.; Fechner, K.; Milz, S.; Richter, W.; Suedkamp, N.P.; Mehlhorn, A.T.; Pearce, S.; Kasten, P. Comparison of mesenchymal stem cells from bone marrow and adipose tissue for bone regeneration in a critical size defect of the sheep tibia and the influence of platelet-rich plasma. Biomaterials 2010, 31, 3572–3579. [Google Scholar] [CrossRef]
- Caplan, A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 2007, 213, 341–347. [Google Scholar] [CrossRef] [PubMed]
- Mauney, J.R.; Kaplan, D.L.; Volloch, V. Matrix-mediated retention of osteogenic differentiation potential by human adult bone marrow stromal cells during ex vivo expansion. Biomaterials 2004, 25, 3233–3243. [Google Scholar] [CrossRef]
- Agata, H.; Asahina, I.; Watanabe, N.; Ishii, Y.; Kubo, N.; Ohshima, S.; Yamazaki, M.; Tojo, A.; Kagami, H. Characteristic change and loss of in vivo osteogenic abilities of human bone marrow stromal cells during passage. Tissue Eng. Part A 2010, 16, 663–673. [Google Scholar] [CrossRef] [Green Version]
- Jin, L.; Zhao, W.; Ren, B.; Li, L.; Hu, X.; Zhang, X.; Cai, Q.; Ao, Y.; Yang, X. Osteochondral tissue regenerated via a strategy by stacking pre-differentiated BMSC sheet on fibrous mesh in a gradient. Biomed. Mater. 2019, 14, 065017. [Google Scholar] [CrossRef]
- Yang, Y.; Yang, G.; Song, Y.; Xu, Y.; Zhao, S.; Zhang, W. 3D Bioprinted Integrated Osteochondral Scaffold-Mediated Repair of Articular Cartilage Defects in the Rabbit Knee. J. Med. Biol. Eng. 2020, 40, 71–81. [Google Scholar] [CrossRef]
- Moses, J.C.; Saha, T.; Mandal, B.B. Chondroprotective and osteogenic effects of silk-based bioinks in developing 3D bioprinted osteochondral interface. Bioprinting 2020, 17, e00067. [Google Scholar] [CrossRef]
- Koh, Y.J.; Koh, B.I.; Kim, H.; Joo, H.J.; Jin, H.K.; Jeon, J.; Choi, C.; Lee, D.H.; Chung, J.H.; Cho, C.H.; et al. Stromal vascular fraction from adipose tissue forms profound vascular network through the dynamic reassembly of blood endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 1141–1150. [Google Scholar] [CrossRef] [Green Version]
- To, K.; Zhang, B.; Romain, K.; Mak, C.; Khan, W. Synovium-Derived Mesenchymal Stem Cell Transplantation in Cartilage Regeneration: A PRISMA Review of in vivo Studies. Front. Bioeng. Biotechnol. 2019, 7, 314. [Google Scholar] [CrossRef] [PubMed]
- Ferretti, C. Periosteum derived stem cells for regenerative medicine proposals: Boosting current knowledge. World J. Stem Cells 2014, 6, 266. [Google Scholar] [CrossRef] [PubMed]
- De Coppi, P.; Bartsch, G.; Siddiqui, M.M.; Xu, T.; Santos, C.C.; Perin, L.; Mostoslavsky, G.; Serre, A.C.; Snyder, E.Y.; Yoo, J.J.; et al. Isolation of amniotic stem cell lines with potential for therapy. Nat. Biotechnol. 2007, 25, 100–106. [Google Scholar] [CrossRef]
- Maurmann, N.; Pereira, D.P.; Burguez, D.; de S Pereira, F.D.A.; Inforçatti Neto, P.; Rezende, R.A.; Gamba, D.; da Silva, J.V.L.; Pranke, P. Mesenchymal stem cells cultivated on scaffolds formed by 3D printed PCL matrices, coated with PLGA electrospun nanofibers for use in tissue engineering. Biomed. Phys. Eng. Express 2017, 3, 045005. [Google Scholar] [CrossRef]
- Kassem, M. Mesenchymal stem cells: Biological characteristics and potential clinical applications. Cloning Stem Cells 2004, 6, 369–374. [Google Scholar] [CrossRef] [PubMed]
- Musiał-Wysocka, A.; Kot, M.; Majka, M. The pros and cons of mesenchymal stem cell-based therapies. Cell Transplant. 2019, 28, 801–812. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamanaka, S. Patient-Specific Pluripotent Stem Cells Become Even More Accessible. Cell Stem Cell 2010, 7, 1–2. [Google Scholar] [CrossRef] [Green Version]
- Takahashi, K.; Yamanaka, S. Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors. Cell 2006, 126, 663–676. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castro-Viñuelas, R.; Sanjurjo-Rodríguez, C.; Piñeiro-Ramil, M.; Hermida-Gómez, T.; Fuentes-Boquete, I.; de Toro-Santos, F.; Blanco-García, F.; Díaz-Prado, S. Induced pluripotent stem cells for cartilage repair: Current status and future perspectives. Eur. Cells Mater. 2018, 36, 96–109. [Google Scholar] [CrossRef]
- Tsumaki, N.; Okada, M.; Yamashita, A. iPS cell technologies and cartilage regeneration. Bone 2015, 70, 48–54. [Google Scholar] [CrossRef]
- De Peppo, G.M.; Marcos-Campos, I.; Kahler, D.J.; Alsalman, D.; Shang, L.; Vunjak-Novakovic, G.; Marolt, D. Engineering bone tissue substitutes from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 2013, 110, 8680–8685. [Google Scholar] [CrossRef] [Green Version]
- Csobonyeiova, M.; Polak, S.; Zamborsky, R.; Danisovic, L. iPS cell technologies and their prospect for bone regeneration and disease modeling: A mini review. J. Adv. Res. 2017, 8, 321–327. [Google Scholar] [CrossRef]
- Danišovič, L.; Csobonyeiova, M.; Nicodemou, A.; Novakova, Z.V.; Miko, M.; Zamborský, R.; Varga, I. Generation and characterization of human iPSCs from human fibroblasts in respect to osteochondral regeneration. FASEB J. 2019, 33, lb168. [Google Scholar] [CrossRef]
- Nam, Y.; Rim, Y.A.; Jung, S.M.; Ju, J.H. Cord blood cell-derived iPSCs as a new candidate for chondrogenic differentiation and cartilage regeneration. Stem Cell Res. Ther. 2017, 8, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bastami, F.; Nazeman, P.; Moslemi, H.; Rezai Rad, M.; Sharifi, K.; Khojasteh, A. Induced pluripotent stem cells as a new getaway for bone tissue engineering: A systematic review. Cell Prolif. 2017, 50, e12321. [Google Scholar] [CrossRef] [PubMed]
- Chijimatsu, R.; Ikeya, M.; Yasui, Y.; Ikeda, Y.; Ebina, K.; Moriguchi, Y.; Shimomura, K.; Hart, D.A.; Yoshikawa, H.; Nakamura, N. Characterization of mesenchymal stem cell-like cells derived from human iPSCs via neural crest development and their application for osteochondral repair. Stem Cells Int. 2017, 2017, 1960965. [Google Scholar] [CrossRef] [Green Version]
- Limraksasin, P.; Kondo, T.; Zhang, M.; Okawa, H.; Osathanon, T.; Pavasant, P.; Egusa, H. In vitro fabrication of hybrid bone/cartilage complex using mouse induced pluripotent stem cells. Int. J. Mol. Sci. 2020, 21, 581. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, D.; Hgg, D.A.; Forsman, A.; Ekholm, J.; Nimkingratana, P.; Brantsing, C.; Kalogeropoulos, T.; Zaunz, S.; Concaro, S.; Brittberg, M.; et al. cartilage tissue engineering by the 3d bioprinting of iPS Cells in a nanocellulose/alginate bioink. Sci. Rep. 2017, 7, 658. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Shi, D.; Liu, Y.; Yao, Y.; Dai, J.; Xu, Z.; Chen, D.; Teng, H.; Jiang, Q. In vivo repair of full-thickness cartilage defect with human iPSC-derived mesenchymal progenitor cells in a rabbit model. Exp. Ther. Med. 2017, 14, 239–245. [Google Scholar] [CrossRef] [Green Version]
- Ko, J.Y.; Kim, K.-I.; Park, S.; Im, G.-I. In vitro chondrogenesis and in vivo repair of osteochondral defect with human induced pluripotent stem cells. Biomaterials 2014, 35, 3571–3581. [Google Scholar] [CrossRef]
- Hiramatsu, K.; Sasagawa, S.; Outani, H.; Nakagawa, K.; Yoshikawa, H.; Tsumaki, N. Generation of hyaline cartilaginous tissue from mouse adult dermal fibroblast culture by defined factors. J. Clin. Investig. 2011, 121, 640–657. [Google Scholar] [CrossRef] [Green Version]
- Outani, H.; Okada, M.; Hiramatsu, K.; Yoshikawa, H.; Tsumaki, N. Induction of chondrogenic cells from dermal fibroblast culture by defined factors does not involve a pluripotent state. Biochem. Biophys. Res. Commun. 2011, 411, 607–612. [Google Scholar] [CrossRef]
- Outani, H.; Okada, M.; Yamashita, A.; Nakagawa, K.; Yoshikawa, H.; Tsumaki, N. Direct induction of chondrogenic cells from human dermal fibroblast culture by defined factors. PLoS ONE 2013, 8, e77365. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Wu, M.H.; Cheung, M.P.L.; Sham, M.H.; Akiyama, H.; Chan, D.; Cheah, K.S.E.; Cheung, M. Reprogramming of dermal fibroblasts into osteo-chondrogenic cells with elevated osteogenic potency by defined transcription factors. Stem Cell Rep. 2017, 8, 1587–1599. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Okita, K.; Matsumura, Y.; Sato, Y.; Okada, A.; Morizane, A.; Okamoto, S.; Hong, H.; Nakagawa, M.; Tanabe, K.; Tezuka, K.I.; et al. A more efficient method to generate integration-free human iPS cells. Nat. Methods 2011, 8, 409–412. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Turner, M.; Leslie, S.; Martin, N.G.; Peschanski, M.; Rao, M.; Taylor, C.J.; Trounson, A.; Turner, D.; Yamanaka, S.; Wilmut, I. Toward the development of a global induced pluripotent stem cell library. Cell Stem Cell 2013, 13, 382–384. [Google Scholar] [CrossRef] [Green Version]
- Jung, Y.; Bauer, G.; Nolta, J.A. Concise Review: Induced Pluripotent stem cell-derived mesenchymal stem cells: Progress toward safe clinical products. Stem Cells 2012, 30, 42–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, L.; GJVM, V.O.; Malda, J.; Stoddart, M.J.; Lai, Y.; Richards, R.G.; Ki-wai Ho, K.; Qin, L. Innovative tissue-engineered strategies for osteochondral defect repair and regeneration: Current progress and challenges. Adv. Healthc. Mater. 2020, 9, 2001008. [Google Scholar] [CrossRef]
- Canadas, R.F.; Marques, A.P.; Reis, R.L.; Oliveira, J.M. Bioreactors and microfluidics for osteochondral interface maturation. In Advances in Experimental Medicine and Biology; Springer New York LLC: New York, NY, USA, 2018; Volume 1059, pp. 395–420. [Google Scholar]
- Wendt, D.; Jakob, M.; Martin, I. Bioreactor-based engineering of osteochondral grafts: From model systems to tissue manufacturing. J. Biosci. Bioeng. 2005, 100, 489–494. [Google Scholar] [CrossRef]
- Nesic, D.; Whiteside, R.; Brittberg, M.; Wendt, D.; Martin, I.; Mainil-varlet, P. Cartilage tissue engineering for degenerative joint disease. Adv. Drug Deliv. Rev. 2006, 58, 300–322. [Google Scholar] [CrossRef]
- Radisic, M.; Park, H.; Gerecht, S.; Cannizzaro, C.; Langer, R.; Vunjak-Novakovic, G. Biomimetic approach to cardiac tissue engineering. Philos. Trans. R. Soc. B Biol. Sci. 2007, 362, 1357–1368. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vunjak-Novakovic, G.; Meinel, L.; Altman, G.; Kaplan, D. Bioreactor cultivation of osteochondral grafts. Orthod. Craniofac. Res. 2005, 8, 209–218. [Google Scholar] [CrossRef]
- Taya, M.; Kino-oka, M. Bioreactors for Animal Cell Cultures. In Comprehensive Biotechnology, 2nd ed.; Elsevier Inc.: Dordrecht, The Netherlands, 2011; Volume 2, pp. 373–382. ISBN 9780080885049. [Google Scholar]
- Hammond, T.G.; Hammond, J.M. Optimized suspension culture: The rotating-wall vessel. Am. J. Physiol. Physiol. 2001, 281, F12–F25. [Google Scholar] [CrossRef] [PubMed]
- Vunjak-Novakovic, G.; Searby, N.; De Luis, J.; Freed, L.E. Microgravity Studies of Cells and Tissues. Ann. N. Y. Acad. Sci. 2002, 974, 504–517. [Google Scholar] [CrossRef]
- Sladkova, M.; de Peppo, G. Bioreactor Systems for Human Bone Tissue Engineering. Processes 2014, 2, 494–525. [Google Scholar] [CrossRef] [Green Version]
- Song, K.; Li, W.; Wang, H.; Zhang, Y.; Li, L.; Wang, Y.; Wang, H.; Wang, L.; Liu, T. Development and Fabrication of a Two-Layer Tissue Engineered Osteochondral Composite Using Hybrid Hydrogel-Cancellous Bone Scaffolds in a Spinner Flask. Biomed. Mater. 2016, 11, 065002. [Google Scholar] [CrossRef]
- Gaspar, D.A.; Gomide, V.; Monteiro, F.J. The role of perfusion bioreactors in bone tissue engineering. Biomatter 2012, 2, 167–175. [Google Scholar] [CrossRef] [Green Version]
- Gonçalves, A.; Costa, P.; Rodrigues, M.T.; Dias, I.R.; Reis, R.L.; Gomes, M.E. Effect of flow perfusion conditions in the chondrogenic differentiation of bone marrow stromal cells cultured onto starch based biodegradable scaffolds. Acta Biomater. 2011, 7, 1644–1652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liao, J.; Guo, X.; Grande-Allen, K.J.; Kasper, F.K.; Mikos, A.G. Bioactive polymer/extracellular matrix scaffolds fabricated with a flow perfusion bioreactor for cartilage tissue engineering. Biomaterials 2010, 31, 8911–8920. [Google Scholar] [CrossRef] [Green Version]
- Daly, A.C.; Sathy, B.N.; Kelly, D.J. Engineering large cartilage tissues using dynamic bioreactor culture at defined oxygen conditions. J. Tissue Eng. 2018, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Harvestine, J.N.; Gonzalez-Fernandez, T.; Sebastian, A.; Hum, N.R.; Genetos, D.C.; Loots, G.G.; Leach, J.K. Osteogenic preconditioning in perfusion bioreactors improves vascularization and bone formation by human bone marrow aspirates. Sci. Adv. 2020, 6, eaay2387. [Google Scholar] [CrossRef] [Green Version]
- Lee, P.S.; Eckert, H.; Hess, R.; Gelinsky, M.; Rancourt, D.; Krawetz, R.; Cuniberti, G.; Scharnweber, D. Developing a customized perfusion bioreactor prototype with controlled positional variability in oxygen partial pressure for bone and cartilage tissue engineering. Tissue Eng. Part C Methods 2017, 23, 286–297. [Google Scholar] [CrossRef]
- Baumgartner, W.; Otto, L.; Hess, S.C.; Stark, W.J.; Märsmann, S.; Bürgisser, G.M.; Calcagni, M.; Cinelli, P.; Buschmann, J. Cartilage/bone interface fabricated under perfusion: Spatially organized commitment of adipose-derived stem cells without medium supplementation. J. Biomed. Mater. Res. Part B Appl. Biomater. 2019, 107, 1833–1843. [Google Scholar] [CrossRef]
- Lin, Z.; Li, Z.; Li, E.N.; Li, X.; Del Duke, C.J.; Shen, H.; Hao, T.; O’Donnell, B.; Bunnell, B.A.; Goodman, S.B.; et al. Osteochondral tissue chip derived from iPSCs: Modeling OA pathologies and testing drugs. Front. Bioeng. Biotechnol. 2019, 7, 411. [Google Scholar] [CrossRef]
- Martin, I.; Wendt, D.; Heberer, M. The role of bioreactors in tissue engineering. Trends Biotechnol. 2004, 22, 80–86. [Google Scholar] [CrossRef]
- Lovecchio, J.; Gargiulo, P.; Vargas Luna, J.L.; Giordano, E.; Sigurjónsson, Ó.E. A standalone bioreactor system to deliver compressive load under perfusion flow to hBMSC-seeded 3D chitosan-graphene templates. Sci. Rep. 2019, 9, 16854. [Google Scholar] [CrossRef] [PubMed]
- Chunqiu, Z.; Xin, D.; Han, W.; Weimin, Z.; Dong, Z. Perfusion-compression bioreactor as the optimum choice for growing large-sized engineered bone constructs in vitro. Biosci. Hypotheses 2008, 1, 319–323. [Google Scholar] [CrossRef]
- Van Wie, B. A flow perfusion bioreactor with controlled mechanical stimulation: Application in cartilage tissue engineering and beyond. J. Stem Cell Ther. Transplant. 2018, 2, 15–34. [Google Scholar] [CrossRef] [Green Version]
- Marijanovic, I.; Antunovic, M.; Matic, I.; Panek, M.; Ivkovic, A. Bioreactor-Based Bone Tissue Engineering. In Advanced Techniques in Bone Regeneration; InTechOpen: London, UK, 2016. [Google Scholar]
- Vainieri, M.L.; Wahl, D.; Alini, M.; van Osch, G.J.V.M.; Grad, S. Mechanically stimulated osteochondral organ culture for evaluation of biomaterials in cartilage repair studies. Acta Biomater. 2018, 81, 256–266. [Google Scholar] [CrossRef] [PubMed]
- Braccini, A.; Wendt, D.; Jaquiery, C.; Jakob, M.; Heberer, M.; Kenins, L.; Wodnar-Filipowicz, A.; Quarto, R.; Martin, I. Three-dimensional perfusion culture of human bone marrow cells and generation of osteoinductive grafts. Stem Cells 2005, 23, 1066–1072. [Google Scholar] [CrossRef]
- Davisson, T.; Sah, R.L.; Ratcliffe, A. Perfusion increases cell content and matrix synthesis in chondrocyte three-dimensional cultures. Tissue Eng. 2002, 8, 807–816. [Google Scholar] [CrossRef]
- Wendt, D.; Marsano, A.; Jakob, M.; Heberer, M.; Martin, I. Oscillating perfusion of cell suspensions through three-dimensional scaffolds enhances cell seeding efficiency and uniformity. Biotechnol. Bioeng. 2003, 84, 205–214. [Google Scholar] [CrossRef]
- Williams, G.R.; Raimi-Abraham, B.T.; Luo, C.J. Nanofibres in Drug Delivery; UCL Press: London, UK, 2018; ISBN 1787350185. [Google Scholar]
- Gupta, P.; Wilkes, G.L. Some investigations on the fiber formation by utilizing a side-by-side bicomponent electrospinning approach. Polymer (Guildf) 2003, 44, 6353–6359. [Google Scholar] [CrossRef]
- Peng, L.; Jiang, S.; Seuß, M.; Fery, A.; Lang, G.; Scheibel, T.; Agarwal, S. Two-in-One Composite Fibers with Side-by-Side Arrangement of Silk Fibroin and Poly(l-lactide) by Electrospinning. Macromol. Mater. Eng. 2016, 301, 48–55. [Google Scholar] [CrossRef]
- Lin, H.Y.; Tsai, W.C.; Chang, S.H. Collagen-PVA aligned nanofiber on collagen sponge as bi-layered scaffold for surface cartilage repair. J. Biomater. Sci. Polym. Ed. 2017, 28, 664–678. [Google Scholar] [CrossRef] [PubMed]
- Zhu, W.; Masood, F.; O’Brien, J.; Zhang, L.G. Highly aligned nanocomposite scaffolds by electrospinning and electrospraying for neural tissue regeneration. Nanomed. Nanotechnol. Biol. Med. 2015, 11, 693–704. [Google Scholar] [CrossRef] [PubMed]
- Szewczyk, P.K.; Stachewicz, U. The impact of relative humidity on electrospun polymer fibers: From structural changes to fiber morphology. Adv. Colloid Interface Sci. 2020, 286, 102315. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.; Chyu, J.; Zumwalt, M. Recent Progress of Fabrication of Cell Scaffold by Electrospinning Technique for Articular Cartilage Tissue Engineering. Int. J. Biomater. 2018, 2018, 1953636. [Google Scholar] [CrossRef] [Green Version]
- Asadian, M.; Chan, K.V.; Norouzi, M.; Grande, S.; Cools, P.; Morent, R.; De Geyter, N. Fabrication and plasma modification of nanofibrous tissue engineering scaffolds. Nanomaterials 2020, 10, 119. [Google Scholar] [CrossRef] [Green Version]
- Ren, X.; Li, J.; Li, J.; Jiang, Y.; Li, L.; Yao, Q.; Ke, Q.; Xu, H. Aligned porous fibrous membrane with a biomimetic surface to accelerate cartilage regeneration. Chem. Eng. J. 2019, 370, 1027–1038. [Google Scholar] [CrossRef]
- Ferraris, S.; Spriano, S.; Scalia, A.C.; Cochis, A.; Rimondini, L.; Cruz-Maya, I.; Guarino, V.; Varesano, A.; Vineis, C. Topographical and biomechanical guidance of electrospun fibers for biomedical applications. Polymers 2020, 12, 2896. [Google Scholar] [CrossRef] [PubMed]
- Raic, A.; Friedrich, F.; Kratzer, D.; Bieback, K.; Lahann, J.; Lee-Thedieck, C. Potential of electrospun cationic BSA fibers to guide osteogenic MSC differentiation via surface charge and fibrous topography. Sci. Rep. 2019, 9, 20003. [Google Scholar] [CrossRef]
- Tan, F.; Liu, J.; Song, K.; Liu, M.; Wang, J. Effect of surface charge on osteoblastic proliferation and differentiation on a poly(ethylene glycol)-diacrylate hydrogel. J. Mater. Sci. 2018, 53, 908–920. [Google Scholar] [CrossRef]
- Persano, L.; Camposeo, A.; Tekmen, C.; Pisignano, D. Industrial Upscaling of Electrospinning and Applications of Polymer Nanofibers: A Review. Macromol. Mater. Eng. 2013, 298, 504–520. [Google Scholar] [CrossRef]
- Ura, D.P.; Rosell-Llompart, J.; Zaszczyńska, A.; Vasilyev, G.; Gradys, A.; Szewczyk, P.K.; Knapczyk-Korczak, J.; Avrahami, R.; Šišková, A.O.; Arinstein, A.; et al. The role of electrical polarity in electrospinning and on the mechanical and structural properties of as-spun fibers. Materials 2020, 13, 4169. [Google Scholar] [CrossRef]
- Moreira, A.; Lawson, D.; Onyekuru, L.; Dziemidowicz, K.; Angkawinitwong, U.; Costa, P.F.; Radacsi, N.; Williams, G.R. Protein encapsulation by electrospinning and electrospraying. J. Control. Release 2021, 329, 1172–1197. [Google Scholar] [CrossRef]
- Liu, J.; Fang, Q.; Yu, X.; Wan, Y.; Xiao, B. Chitosan-based nanofibrous membrane unit with gradient compositional and structural features for mimicking calcified layer in osteochondral matrix. Int. J. Mol. Sci. 2018, 19, 2330. [Google Scholar] [CrossRef] [Green Version]
- Brunelle, A.R.; Horner, C.B.; Low, K.; Ico, G.; Nam, J. Electrospun thermosensitive hydrogel scaffold for enhanced chondrogenesis of human mesenchymal stem cells. Acta Biomater. 2018, 66, 166–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gunes, O.C.; Albayrak, A.Z.; Tasdemir, S.; Sendemir, A. Wet-electrospun PHBV nanofiber reinforced carboxymethyl chitosan-silk hydrogel composite scaffolds for articular cartilage repair. J. Biomater. Appl. 2020, 35, 515–531. [Google Scholar] [CrossRef]
- Silva, J.C.; Udangawa, R.N.; Chen, J.; Mancinelli, C.D.; Garrudo, F.F.F.; Mikael, P.E.; Cabral, J.M.S.; Ferreira, F.C.; Linhardt, R.J. Kartogenin-loaded coaxial PGS/PCL aligned nanofibers for cartilage tissue engineering. Mater. Sci. Eng. C 2020, 107, 110291. [Google Scholar] [CrossRef]
- Davoodi, P.; Srinivasan, M.P.; Wang, C.H. Effective co-delivery of nutlin-3a and p53 genes: Via core-shell microparticles for disruption of MDM2-p53 interaction and reactivation of p53 in hepatocellular carcinoma. J. Mater. Chem. B 2017, 5, 5816–5834. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Y.; Wu, Y.; Zhou, Y.; Wu, J.; Wang, X.; Qu, Y.; Wang, Y.; Zhang, Y.; Yu, Q. Photothermally Activated Electrospun Nanofiber Mats for High-Efficiency Surface-Mediated Gene Transfection. ACS Appl. Mater. Interfaces 2020, 12, 7905–7914. [Google Scholar] [CrossRef]
- Cheng, G.; Yin, C.; Tu, H.; Jiang, S.; Wang, Q.; Zhou, X.; Xing, X.; Xie, C.; Shi, X.; Du, Y.; et al. Controlled Co-delivery of Growth Factors through Layer-by-Layer Assembly of Core–Shell Nanofibers for Improving Bone Regeneration. ACS Nano 2019, 13, 6372–6382. [Google Scholar] [CrossRef]
- Liu, C.; Wang, C.; Zhao, Q.; Li, X.; Xu, F.; Yao, X.; Wang, M. Incorporation and release of dual growth factors for nerve tissue engineering using nanofibrous bicomponent scaffolds. Biomed. Mater. 2018, 13, 44107. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, Y.; Gilbert-Honick, J.; Somers, S.M.; Mao, H.Q.; Grayson, W.L. Modified cell-electrospinning for 3D myogenesis of C2C12s in aligned fibrin microfiber bundles. Biochem. Biophys. Res. Commun. 2019, 516, 558–564. [Google Scholar] [CrossRef]
- Yu, F.; Li, M.; Yuan, Z.; Rao, F.; Fang, X.; Jiang, B.; Wen, Y.; Zhang, P. Mechanism research on a bioactive resveratrol–PLA–gelatin porous nano-scaffold in promoting the repair of cartilage defect. Int. J. Nanomed. 2018, 13, 7845–7858. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khader, A.; Arinzeh, T.L. Biodegradable zinc oxide composite scaffolds promote osteochondral differentiation of mesenchymal stem cells. Biotechnol. Bioeng. 2020, 117, 194–209. [Google Scholar] [CrossRef]
- Horner, C.B.; Maldonado, M.; Tai, Y.; Rony, R.M.I.K.; Nam, J. Spatially Regulated Multiphenotypic Differentiation of Stem Cells in 3D via Engineered Mechanical Gradient. ACS Appl. Mater. Interfaces 2019, 11, 45479–45488. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Huang, J.; Shao, H.; Hu, X.; Cao, C.; Fan, S.; Song, L.; Zhang, Y. Silk scaffolds with gradient pore structure and improved cell infiltration performance. Mater. Sci. Eng. C 2019, 94, 179–189. [Google Scholar] [CrossRef]
- Stachewicz, U.; Szewczyk, P.K.; Kruk, A.; Barber, A.H.; Czyrska-Filemonowicz, A. Pore shape and size dependence on cell growth into electrospun fiber scaffolds for tissue engineering: 2D and 3D analyses using SEM and FIB-SEM tomography. Mater. Sci. Eng. C 2019, 95, 397–408. [Google Scholar] [CrossRef]
- Dalton, P.D.; Vaquette, C.; Farrugia, B.L.; Dargaville, T.R.; Brown, T.D.; Hutmacher, D.W. Electrospinning and additive manufacturing: Converging technologies. Biomater. Sci. 2013, 1, 171–185. [Google Scholar] [CrossRef]
- Mailley, D.; Hébraud, A.; Schlatter, G. A review on the impact of humidity during electrospinning: From the nanofiber structure engineering to the applications. Macromol. Mater. Eng. 2021, 2100115. [Google Scholar] [CrossRef]
- Nam, J.; Huang, Y.; Agarwal, S.; Lannutti, J. Improved cellular infiltration in electrospun fiber via engineered porosity. Tissue Eng. 2007, 13, 2249–2257. [Google Scholar] [CrossRef] [Green Version]
- Joshi, M.K.; Pant, H.R.; Tiwari, A.P.; Kim, H.J.; Park, C.H.; Kim, C.S. Multi-layered macroporous three-dimensional nanofibrous scaffold via a novel gas foaming technique. Chem. Eng. J. 2015, 275, 79–88. [Google Scholar] [CrossRef]
- Jiang, J.; Carlson, M.A.; Teusink, M.J.; Wang, H.; MacEwan, M.R.; Xie, J. Expanding two-dimensional electrospun nanofiber membranes in the third dimension by a modified gas-foaming technique. ACS Biomater. Sci. Eng. 2015, 1, 991–1001. [Google Scholar] [CrossRef]
- Leong, M.F.; Chan, W.Y.; Chian, K.S. Cryogenic electrospinning: Proposed mechanism, process parameters and its use in engineering of bilayered tissue structures. Nanomedicine 2013, 8, 555–566. [Google Scholar] [CrossRef]
- Vaquette, C.; Cooper-White, J.J. Increasing electrospun scaffold pore size with tailored collectors for improved cell penetration. Acta Biomater. 2011, 7, 2544–2557. [Google Scholar] [CrossRef]
- Zhu, X.; Cui, W.; Li, X.; Jin, Y. Electrospun fibrous mats with high porosity as potential scaffolds for skin tissue engineering. Biomacromolecules 2008, 9, 1795–1801. [Google Scholar] [CrossRef]
- Hodge, J.; Quint, C. The improvement of cell infiltration in an electrospun scaffold with multiple synthetic biodegradable polymers using sacrificial PEO microparticles. J. Biomed. Mater. Res. Part A 2019, 107, 1954–1964. [Google Scholar] [CrossRef]
- Voorneveld, J.; Oosthuysen, A.; Franz, T.; Zilla, P.; Bezuidenhout, D. Dual electrospinning with sacrificial fibers for engineered porosity and enhancement of tissue ingrowth. J. Biomed. Mater. Res. Part B Appl. Biomater. 2017, 105, 1559–1572. [Google Scholar] [CrossRef]
- Si, Y.; Yu, J.; Tang, X.; Ge, J.; Ding, B. Ultralight nanofibre-assembled cellular aerogels with superelasticity and multifunctionality. Nat. Commun. 2014, 5, 5802. [Google Scholar] [CrossRef] [Green Version]
- Chen, W.; Chen, S.; Morsi, Y.; El-Hamshary, H.; El-Newhy, M.; Fan, C.; Mo, X. Superabsorbent 3D scaffold based on electrospun nanofibers for cartilage tissue engineering. ACS Appl. Mater. Interfaces 2016, 8, 24415–24425. [Google Scholar] [CrossRef]
- Xu, Y.; Wu, J.; Wang, H.; Li, H.; Di, N.; Song, L.; Li, S.; Li, D.; Xiang, Y.; Liu, W.; et al. Fabrication of electrospun poly(l-Lactide-co-ε-Caprolactone)/collagen nanoyarn network as a novel, three-dimensional, macroporous, aligned scaffold for tendon tissue engineering. Tissue Eng. Part C Methods 2013, 19, 925–936. [Google Scholar] [CrossRef] [Green Version]
- Eom, S.; Park, S.M.; Hong, H.; Kwon, J.; Oh, S.R.; Kim, J.; Kim, D.S. Hydrogel-assisted electrospinning for fabrication of a 3d complex tailored nanofiber macrostructure. ACS Appl. Mater. Interfaces 2020, 12, 51212–51224. [Google Scholar] [CrossRef] [PubMed]
- Radacsi, N.; Nuansing, W. Fabrication of 3D and 4D polymer micro- and nanostructures based on electrospinning. In 3D and 4D Printing of Polymer Nanocomposite Materials: Processes, Applications, and Challenges; Elsevier: Amsterdam, The Netherlands, 2019; pp. 191–229. ISBN 9780128168059. [Google Scholar]
- Sun, B.; Long, Y.-Z.; Yu, F.; Li, M.-M.; Zhang, H.-D.; Li, W.-J.; Xu, T.-X. Self-assembly of a three-dimensional fibrous polymer sponge by electrospinning. Nanoscale 2012, 4, 2134–2137. [Google Scholar] [CrossRef]
- Ahirwal, D.; Hébraud, A.; Kádár, R.; Wilhelm, M.; Schlatter, G. From self-assembly of electrospun nanofibers to 3D cm thick hierarchical foams. Soft Matter 2013, 9, 3164–3172. [Google Scholar] [CrossRef]
- Vong, M.; Speirs, E.; Klomkliang, C.; Akinwumi, I.; Nuansing, W.; Radacsi, N. Controlled three-dimensional polystyrene micro- and nano-structures fabricated by three-dimensional electrospinning. RSC Adv. 2018, 8, 15501–15512. [Google Scholar] [CrossRef] [Green Version]
- Nedjari, S.; Schlatter, G.; Hébraud, A. Thick electrospun honeycomb scaffolds with controlled pore size. Mater. Lett. 2015, 142, 180–183. [Google Scholar] [CrossRef]
- Keirouz, A.; Chung, M.; Kwon, J.; Fortunato, G.; Radacsi, N. 2D and 3D electrospinning technologies for the fabrication of nanofibrous scaffolds for skin tissue engineering: A review. WIREs Nanomed. Nanobiotechnol. 2020, 12, e1626. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Shafiq, M.; Liu, M.; Morsi, Y.; Mo, X. Advanced fabrication for electrospun three-dimensional nanofiber aerogels and scaffolds. Bioact. Mater. 2020, 5, 963–979. [Google Scholar] [CrossRef]
- Bongiovanni Abel, S.; Montini Ballarin, F.; Abraham, G.A. Combination of electrospinning with other techniques for the fabrication of 3D polymeric and composite nanofibrous scaffolds with improved cellular interactions. Nanotechnology 2020, 31, 172002. [Google Scholar] [CrossRef]
- Brown, T.D.; Dalton, P.D.; Hutmacher, D.W. Melt electrospinning today: An opportune time for an emerging polymer process. Prog. Polym. Sci. 2016, 56, 116–166. [Google Scholar] [CrossRef]
- Brown, T.D.; Dalton, P.D.; Hutmacher, D.W. Direct writing by way of melt electrospinning. Adv. Mater. 2011, 23, 5651–5657. [Google Scholar] [CrossRef] [PubMed]
- Hochleitner, G.; Jüngst, T.; Brown, T.D.; Hahn, K.; Moseke, C.; Jakob, F.; Dalton, P.D.; Groll, J. Additive manufacturing of scaffolds with sub-micron filaments via melt electrospinning writing. Biofabrication 2015, 7, 035002. [Google Scholar] [CrossRef] [PubMed]
- Tamay, D.G.; Dursun Usal, T.; Alagoz, A.S.; Yucel, D.; Hasirci, N.; Hasirci, V. 3D and 4D Printing of Polymers for Tissue Engineering Applications. Front. Bioeng. Biotechnol. 2019, 7, 164. [Google Scholar] [CrossRef] [PubMed]
- Guzzi, E.A.; Tibbitt, M.W. Additive Manufacturing of Precision Biomaterials. Adv. Mater. 2020, 32, 1901994. [Google Scholar] [CrossRef]
- Hu, X.; Man, Y.; Li, W.; Li, L.; Xu, J.; Parungao, R.; Wang, Y.; Zheng, S.; Nie, Y.; Liu, T.; et al. 3D bio-printing of CS/Gel/HA/Gr hybrid osteochondral scaffolds. Polymers 2019, 11, 1601. [Google Scholar] [CrossRef] [Green Version]
- Kosik-Kozioł, A.; Costantini, M.; Mróz, A.; Idaszek, J.; Heljak, M.; Jaroszewicz, J.; Kijeńska, E.; Szöke, K.; Frerker, N.; Barbetta, A.; et al. 3D bioprinted hydrogel model incorporating β-tricalcium phosphate for calcified cartilage tissue engineering. Biofabrication 2019, 11, 035016. [Google Scholar] [CrossRef]
- Zhu, S.; Chen, P.; Chen, Y.; Li, M.; Chen, C.; Lu, H. 3D-printed extracellular matrix/polyethylene glycol diacrylate hydrogel incorporating the anti-inflammatory phytomolecule honokiol for regeneration of osteochondral defects. Am. J. Sports Med. 2020, 48, 2808–2818. [Google Scholar] [CrossRef]
- Chen, L.; Deng, C.; Li, J.; Yao, Q.; Chang, J.; Wang, L.; Wu, C. 3D printing of a lithium-calcium-silicate crystal bioscaffold with dual bioactivities for osteochondral interface reconstruction. Biomaterials 2019, 196, 138–150. [Google Scholar] [CrossRef]
- Dang, W.; Wang, X.; Li, J.; Deng, C.; Liu, Y.; Yao, Q.; Wang, L.; Chang, J.; Wu, C. 3D printing of Mo-containing scaffolds with activated anabolic responses and bi-lineage bioactivities. Theranostics 2018, 8, 4372–4392. [Google Scholar] [CrossRef]
- Gao, F.; Xu, Z.; Liang, Q.; Liu, B.; Li, H.; Wu, Y.; Zhang, Y.; Lin, Z.; Wu, M.; Ruan, C.; et al. Direct 3D Printing of High Strength Biohybrid Gradient Hydrogel Scaffolds for Efficient Repair of Osteochondral Defect. Adv. Funct. Mater. 2018, 28, 1706644. [Google Scholar] [CrossRef]
- Chen, P.; Zheng, L.; Wang, Y.; Tao, M.; Xie, Z.; Xia, C.; Gu, C.; Chen, J.; Qiu, P.; Mei, S.; et al. Desktop-stereolithography 3D printing of a radially oriented extracellular matrix/mesenchymal stem cell exosome bioink for osteochondral defect regeneration. Theranostics 2019, 9, 2439–2459. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Esworthy, T.; Lee, S.J.; Miao, S.; Cui, H.; Plesiniak, M.; Fenniri, H.; Webster, T.; Rao, R.D.; Zhang, L.G. 3D Printed scaffolds with hierarchical biomimetic structure for osteochondral regeneration. Nanomed. Nanotechnol. Biol. Med. 2019, 19, 58–70. [Google Scholar] [CrossRef] [PubMed]
- Wang, K.-C.; Egelhoff, T.T.; Caplan, A.I.; Welter, J.F.; Baskaran, H. ROCK Inhibition Promotes the Development of Chondrogenic Tissue by Improved Mass Transport. Tissue Eng. Part A 2018, 24, 1218–1227. [Google Scholar] [CrossRef]
- Woods, A.; Wang, G.; Beier, F. RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J. Biol. Chem. 2005, 280, 11626–11634. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Yu, F.; Shi, J.; Shen, S.; Teng, H.; Yang, J.; Wang, X.; Jiang, Q. In situ repair of bone and cartilage defects using 3D scanning and 3D printing. Sci. Rep. 2017, 7, 9416. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, K.; Zhao, T.; Yang, L.; Wang, P.; Jin, J.; Teng, H.; Xia, D.; Zhu, L.; Li, L.; Jiang, Q.; et al. Application of robotic-assisted in situ 3D printing in cartilage regeneration with HAMA hydrogel: An in vivo study. J. Adv. Res. 2020, 23, 123–132. [Google Scholar] [CrossRef]
- Akilbekova, D.; Mektepbayeva, D. Patient specific in situ 3D printing. In 3D Printing in Medicine; Elsevier Inc.: Amsterdam, The Netherlands, 2017; pp. 91–113. ISBN 9780081007266. [Google Scholar]
- Galarraga, J.H.; Kwon, M.Y.; Burdick, J.A. 3D bioprinting via an in situ crosslinking technique towards engineering cartilage tissue. Sci. Rep. 2019, 9, 19987. [Google Scholar] [CrossRef]
- Mao, M.; He, J.; Li, X.; Zhang, B.; Lei, Q.; Liu, Y.; Li, D. The Emerging Frontiers and Applications of High-Resolution 3D Printing. Micromachines 2017, 8, 113. [Google Scholar] [CrossRef]
- Lim, K.S.; Levato, R.; Costa, P.F.; Castilho, M.D.; Alcala-Orozco, C.R.; Van Dorenmalen, K.M.A.; Melchels, F.P.W.; Gawlitta, D.; Hooper, G.J.; Malda, J.; et al. Bio-resin for high resolution lithography-based biofabrication of complex cell-laden constructs. Biofabrication 2018, 10, 034101. [Google Scholar] [CrossRef]
- You, S.; Wang, P.; Schimelman, J.; Hwang, H.H.; Chen, S. High-fidelity 3D printing using flashing photopolymerization. Addit. Manuf. 2019, 30, 100834. [Google Scholar] [CrossRef]
- Zhang, B.; Li, S.; Hingorani, H.; Serjouei, A.; Larush, L.; Pawar, A.A.; Goh, W.H.; Sakhaei, A.H.; Hashimoto, M.; Kowsari, K.; et al. Highly stretchable hydrogels for UV curing based high-resolution multimaterial 3D printing. J. Mater. Chem. B 2018, 6, 3246–3253. [Google Scholar] [CrossRef]
- Paz, V.F.; Emons, M.; Obata, K.; Ovsianikov, A.; Peterhänsel, S.; Frenner, K.; Reinhardt, C.; Chichkov, B.; Morgner, U.; Osten, W. Development of functional sub-100 nm structures with 3D two-photon polymerization technique and optical methods for characterization. J. Laser Appl. 2012, 24, 042004. [Google Scholar] [CrossRef] [Green Version]
- Tan, D.; Li, Y.; Qi, F.; Yang, H.; Gong, Q.; Dong, X.; Duan, X. Reduction in feature size of two-photon polymerization using SCR500. Appl. Phys. Lett. 2007, 90, 071106. [Google Scholar] [CrossRef]
- Zheng, L.; Kurselis, K.; El-Tamer, A.; Hinze, U.; Reinhardt, C.; Overmeyer, L.; Chichkov, B. Nanofabrication of High-Resolution Periodic Structures with a Gap Size Below 100 nm by Two-Photon Polymerization. Nanoscale Res. Lett. 2019, 14, 134. [Google Scholar] [CrossRef] [Green Version]
- Aguilar-de-Leyva, Á.; Linares, V.; Casas, M.; Caraballo, I. 3D Printed Drug Delivery Systems Based on Natural Products. Pharmaceutics 2020, 12, 620. [Google Scholar] [CrossRef] [PubMed]
- Lim, S.H.; Kathuria, H.; Tan, J.J.Y.; Kang, L. 3D printed drug delivery and testing systems—A passing fad or the future? Adv. Drug Deliv. Rev. 2018, 132, 139–168. [Google Scholar] [CrossRef]
- Chen, W.; Xu, Y.; Liu, Y.; Wang, Z.; Li, Y.; Jiang, G.; Mo, X.; Zhou, G. Three-dimensional printed electrospun fiber-based scaffold for cartilage regeneration. Mater. Des. 2019, 179, 107886. [Google Scholar] [CrossRef]
- Chen, W.; Xu, Y.; Li, Y.; Jia, L.; Mo, X.; Jiang, G.; Zhou, G. 3D printing electrospinning fiber-reinforced decellularized extracellular matrix for cartilage regeneration. Chem. Eng. J. 2020, 382, 122986. [Google Scholar] [CrossRef]
- He, X.X.; Zheng, J.; Yu, G.F.; You, M.H.; Yu, M.; Ning, X.; Long, Y.Z. Near-Field Electrospinning: Progress and Applications. J. Phys. Chem. C 2017, 121, 8663–8678. [Google Scholar] [CrossRef]
- Chen, H.; Malheiro, A.D.B.F.B.; Van Blitterswijk, C.; Mota, C.; Wieringa, P.A.; Moroni, L. Direct Writing Electrospinning of Scaffolds with Multidimensional Fiber Architecture for Hierarchical Tissue Engineering. ACS Appl. Mater. Interfaces 2017, 9, 38187–38200. [Google Scholar] [CrossRef] [PubMed]
- Han, Y.; Lian, M.; Sun, B.; Jia, B.; Wu, Q.; Qiao, Z.; Dai, K. Preparation of high precision multilayer scaffolds based on Melt Electro-Writing to repair cartilage injury. Theranostics 2020, 10, 10214–10230. [Google Scholar] [CrossRef] [PubMed]
- Miao, S.; Zhu, W.; Castro, N.J.; Nowicki, M.; Zhou, X.; Cui, H.; Fisher, J.P.; Zhang, L.G. 4D printing smart biomedical scaffolds with novel soybean oil epoxidized acrylate. Sci. Rep. 2016, 6, 27226. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.H.; Seo, Y.B.; Yeon, Y.K.; Lee, Y.J.; Park, H.S.; Sultan, M.T.; Lee, J.M.; Lee, J.S.; Lee, O.J.; Hong, H.; et al. 4D-bioprinted silk hydrogels for tissue engineering. Biomaterials 2020, 260, 120281. [Google Scholar] [CrossRef] [PubMed]
- Zhu, P.; Yang, W.; Wang, R.; Gao, S.; Li, B.; Li, Q. 4D Printing of Complex Structures with a Fast Response Time to Magnetic Stimulus. ACS Appl. Mater. Interfaces 2018, 10, 36435–36442. [Google Scholar] [CrossRef]
- Wang, C.; Yue, H.; Liu, J.; Zhao, Q.; He, Z.; Li, K.; Lu, B.; Huang, W.; Wei, Y.; Tang, Y.; et al. Advanced reconfigurable scaffolds fabricated by 4D printing for treating critical-size bone defects of irregular shapes. Biofabrication 2020, 12, 045025. [Google Scholar] [CrossRef] [PubMed]
- Armiento, A.R.; Stoddart, M.J.; Alini, M.; Eglin, D. Biomaterials for articular cartilage tissue engineering: Learning from biology. Acta Biomater. 2018, 65, 1–20. [Google Scholar] [CrossRef]
- Samvelyan, H.J.; Hughes, D.; Stevens, C.; Staines, K.A. Models of Osteoarthritis: Relevance and New Insights. Calcif. Tissue Int. 2020, 1, 3. [Google Scholar] [CrossRef] [Green Version]
- Meng, X.; Ziadlou, R.; Grad, S.; Alini, M.; Wen, C.; Lai, Y.; Qin, L.; Zhao, Y.; Wang, X. Animal Models of Osteochondral Defect for Testing Biomaterials. Biochem. Res. Int. 2020, 2020, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Kwon, H.; Brown, W.E.; Lee, C.A.; Wang, D.; Paschos, N.; Hu, J.C.; Athanasiou, K.A. Surgical and tissue engineering strategies for articular cartilage and meniscus repair. Nat. Rev. Rheumatol. 2019, 15, 550–570. [Google Scholar] [CrossRef]
- Bicho, D.; Pina, S.; Reis, R.L.; Oliveira, J.M. Commercial Products for Osteochondral Tissue Repair and Regeneration. In Advances in Experimental Medicine and Biology; Springer New York LLC: New York, NY, USA, 2018; Volume 1058, pp. 415–428. [Google Scholar]
Cell Type | Advantages | Disadvantages | ||
---|---|---|---|---|
Pluripotent | Embryonic Stem Cells (ESCs) | High differentiation and self-renewal capacity; Off-the-shelf source | Ethical concerns; Tumorigenic potential and genomic instability; Heterogeneous differentiation | |
Induced Pluripotent Stem Cells (iPSCs) | High differentiation and self-renewal capacity; Patient-specific therapy; Minimally invasive harvest technique for autologous iPSCs; Off-the-shelf source | Tumorigenic potential and genomic instability; Difficulty in achieving uniform differentiation; High cost | ||
Multipotent | Mesenchymal Stem Cells (MSCs) | Bone Marrow-Derived Stem Cells (BMSCs) | High chondrogenic and osteogenic potential | Invasive harvest technique; Low collection yields force them to be heavily expanded before sufficient numbers are attained (longer waiting times and higher risk of de-differentiation); Differentiation potential declines with increasing age Possibility of forming heterogeneous cell populations |
Adipose-Derived Stem Cells (ASCs) | Minimally invasive isolation procedure with high yields | Lower chondrogenic and osteogenic potential than BMSCs | ||
Emerging MSC types: synovial tissue MSCs (SMSCs), periosteum-derived MSCs (PMSCs), umbilical cord MSCs (UCMSCs), amniotic membrane and fluid MSCs (AFSCs) | ||||
Unipotent | Primary cells (chondrocytes and osteoblasts) | Native phenotype; No need for osteogenic/chondrogenic differentiation protocols; Easy accessibilityImmunocompatibility (autologous sources) | Limited lifespan; Low proliferation potential; Risk of de-differentiation or loss of function during expansion; Limited cell numbers obtained during isolation; Risk of donor-site morbidity and infection upon autologous cell isolation |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gonçalves, A.M.; Moreira, A.; Weber, A.; Williams, G.R.; Costa, P.F. Osteochondral Tissue Engineering: The Potential of Electrospinning and Additive Manufacturing. Pharmaceutics 2021, 13, 983. https://doi.org/10.3390/pharmaceutics13070983
Gonçalves AM, Moreira A, Weber A, Williams GR, Costa PF. Osteochondral Tissue Engineering: The Potential of Electrospinning and Additive Manufacturing. Pharmaceutics. 2021; 13(7):983. https://doi.org/10.3390/pharmaceutics13070983
Chicago/Turabian StyleGonçalves, Andreia M., Anabela Moreira, Achim Weber, Gareth R. Williams, and Pedro F. Costa. 2021. "Osteochondral Tissue Engineering: The Potential of Electrospinning and Additive Manufacturing" Pharmaceutics 13, no. 7: 983. https://doi.org/10.3390/pharmaceutics13070983