Chitosan and Pectin Hydrogels for Tissue Engineering and In Vitro Modeling
Abstract
:1. Introduction
2. Hydrogels as 3D Platforms for Tissue Engineering and In Vitro Model Applications
3. Polysaccharide-Based Hydrogels: Chitosan and Pectin
3.1. Chitosan
3.2. Pectin
4. Ch and Pec Hybrid Hydrogel Systems
5. Biomedical Applications of Ch–Pec Hydrogels
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Caló, E.; Khutoryanskiy, V.V. Biomedical applications of hydrogels: A review of patents and commercial products. Eur. Polym. J. 2015, 65, 252–267. [Google Scholar] [CrossRef]
- Prokopijevic, M.; Prodanovic, O.; Spasojevic, D.; Kovacevic, G.; Polovic, N.; Radotic, K.; Prodanovic, R. Tyramine-modified pectins via periodate oxidation for soybean hull peroxidase induced hydrogel formation and immobilization. Appl. Microbiol. Biotechnol. 2017, 101, 2281–2290. [Google Scholar] [CrossRef]
- Diba, M.; Polini, A.; Petre, D.G.; Zhang, Y.; Leeuwenburgh, S.C. Fiber-reinforced colloidal gels as injectable and moldable biomaterials for regenerative medicine. Mater. Sci. Eng. C 2018, 92, 143–150. [Google Scholar] [CrossRef]
- Liu, H.; Wang, Y.; Cui, K.; Guo, Y.; Zhang, X.; Qin, J. Advances in Hydrogels in Organoids and Organs-on-a-Chip. Adv. Mater. 2019, 31, 1902042. [Google Scholar] [CrossRef]
- Annabi, N.; Tamayol, A.; Uquillas, J.A.; Akbari, M.; Bertassoni, L.E.; Cha, C.; Camci-Unal, G.; Dokmeci, M.R.; Peppas, N.A.; Khademhosseini, A. 25th anniversary article: Rational design and applications of hydrogels in regenerative medicine. Adv. Mater. 2014, 26, 85–124. [Google Scholar] [CrossRef]
- Liaw, C.Y.; Ji, S.; Guvendiren, M. Human tissue models: Engineering 3D hydrogels for personalized in vitro human tissue models (Adv. Healthcare Mater. 4/2018). Adv. Healthc. Mater. 2018, 7, 1870021. [Google Scholar] [CrossRef]
- Thakuri, P.S.; Liu, C.; Luker, G.D.; Tavana, H. Biomaterials-Based Approaches to Tumor Spheroid and Organoid Modeling. Adv. Healthc. Mater. 2018, 7, 1700980. [Google Scholar] [CrossRef] [PubMed]
- Thiele, J.; Ma, Y.; Bruekers, S.M.; Ma, S.; Huck, W.T. 25th anniversary article: Designer hydrogels for cell cultures: A materials selection guide. Adv. Mater. 2014, 26, 125–148. [Google Scholar] [CrossRef]
- Wolf, M.T.; Dearth, C.L.; Sonnenberg, S.B.; Loboa, E.G.; Badylak, S.F. Naturally derived and synthetic scaffolds for skeletal muscle reconstruction. Adv. Drug Deliv. Rev. 2015, 84, 208–221. [Google Scholar] [CrossRef]
- Gjorevski, N.; Sachs, N.; Manfrin, A.; Giger, S.; Bragina, M.E.; Ordóñez-Morán, P.; Clevers, H.; Lutolf, M.P. Designer matrices for intestinal stem cell and organoid culture. Nature 2016, 539, 560–564. [Google Scholar] [CrossRef] [PubMed]
- Greggio, C.; De Franceschi, F.; Figueiredo-Larsen, M.; Gobaa, S.; Ranga, A.; Semb, H.; Lutolf, M.; Grapin-Botton, A. Artificial three-dimensional niches deconstruct pancreas development in vitro. Development 2013, 140, 4452–4462. [Google Scholar] [CrossRef] [PubMed]
- Kamatar, A.; Gunay, G.; Acar, H. Natural and synthetic biomaterials for engineering multicellular tumor spheroids. Polymers 2020, 12, 2506. [Google Scholar] [CrossRef]
- Rosales, A.M.; Anseth, K.S. The design of reversible hydrogels to capture extracellular matrix dynamics. Nat. Rev. Mater. 2016, 1, 15012. [Google Scholar] [CrossRef] [PubMed]
- Wieringa, P.A.; Goncalves de Pinho, A.R.; Micera, S.; van Wezel, R.J.A.; Moroni, L. Biomimetic Architectures for Peripheral Nerve Repair: A Review of Biofabrication Strategies. Adv. Healthc. Mater. 2018, 7, e1701164. [Google Scholar] [CrossRef]
- Blondel, D.; Lutolf, M.P. Bioinspired Hydrogels for 3D Organoid Culture. Chimia 2019, 73, 81–85. [Google Scholar] [CrossRef]
- Yang, J.; Zhang, Y.S.; Yue, K.; Khademhosseini, A. Cell-laden hydrogels for osteochondral and cartilage tissue engineering. Acta Biomater. 2017, 57, 1–25. [Google Scholar] [CrossRef]
- Jiang, W.; Li, M.; Chen, Z.; Leong, K.W. Cell-laden microfluidic microgels for tissue regeneration. Lab Chip 2016, 16, 4482–4506. [Google Scholar] [CrossRef]
- Aisenbrey, E.A.; Murphy, W.L. Synthetic alternatives to Matrigel. Nat. Rev. Mater. 2020, 5, 539–551. [Google Scholar] [CrossRef]
- Diekjürgen, D.; Grainger, D.W. Polysaccharide matrices used in 3D in vitro cell culture systems. Biomaterials 2017, 141, 96–115. [Google Scholar] [CrossRef]
- Radhakrishnan, J.; Subramanian, A.; Krishnan, U.M.; Sethuraman, S. Injectable and 3D bioprinted polysaccharide hydrogels: From cartilage to osteochondral tissue engineering. Biomacromolecules 2017, 18, 1–26. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Yu, F.; Zheng, L.; Wang, R.; Yan, W.; Wang, Z.; Xu, J.; Wu, J.; Shi, D.; Zhu, L. Natural hydrogels for cartilage regeneration: Modification, preparation and application. J. Orthop. Transl. 2019, 17, 26–41. [Google Scholar] [CrossRef] [PubMed]
- Li, D.Q.; Li, J.; Dong, H.L.; Li, X.; Zhang, J.Q.; Ramaswamy, S.; Xu, F. Pectin in biomedical and drug delivery applications: A review. Int. J. Biol. Macromol. 2021, 185, 49–65. [Google Scholar] [CrossRef]
- Bostanci, N.S.; Buyuksungur, S.; Hasirci, N.; Tezcaner, A. Potential of pectin for biomedical applications: A comprehensive review. J. Biomater. Sci. Polym. Ed. 2022, 33, 1866–1900. [Google Scholar] [CrossRef] [PubMed]
- Eivazzadeh-Keihan, R.; Noruzi, E.B.; Aliabadi, H.A.M.; Sheikhaleslami, S.; Akbarzadeh, A.R.; Hashemi, S.M.; Gorab, M.G.; Maleki, A.; Cohan, R.A.; Mahdavi, M.; et al. Recent advances on biomedical applications of pectin-containing biomaterials. Int. J. Biol. Macromol. 2022, 217, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Do, N.H.N.; Truong, Q.T.; Le, P.K.; Ha, A.C. Recent developments in chitosan hydrogels carrying natural bioactive compounds. Carbohydr. Polym. 2022, 294, 119726. [Google Scholar] [CrossRef] [PubMed]
- Lin, X.; Wang, J.; Wu, X.; Luo, Y.; Wang, Y.; Zhao, Y. Marine-Derived Hydrogels for Biomedical Applications. Adv. Funct. Mater. 2022, 2211323. [Google Scholar] [CrossRef]
- Pella, M.C.G.; Lima-Tenorio, M.K.; Tenorio-Neto, E.T.; Guilherme, M.R.; Muniz, E.C.; Rubira, A.F. Chitosan-based hydrogels: From preparation to biomedical applications. Carbohydr. Polym. 2018, 196, 233–245. [Google Scholar] [CrossRef]
- Huebsch, N.; Mooney, D.J. Inspiration and application in the evolution of biomaterials. Nature 2009, 462, 426–432. [Google Scholar] [CrossRef]
- Hollister, S.J. Porous scaffold design for tissue engineering. Nat. Mater. 2005, 4, 518–524. [Google Scholar] [CrossRef]
- Zhu, T.; Mao, J.; Cheng, Y.; Liu, H.; Lv, L.; Ge, M.; Li, S.; Huang, J.; Chen, Z.; Li, H. Recent progress of polysaccharide-based hydrogel interfaces for wound healing and tissue engineering. Adv. Mater. Interfaces 2019, 6, 1900761. [Google Scholar] [CrossRef] [Green Version]
- Lee, K.Y.; Mooney, D.J. Hydrogels for tissue engineering. Chem. Rev. 2001, 101, 1869–1880. [Google Scholar] [CrossRef] [PubMed]
- Peppas, N.A. Hydrogels and drug delivery. Curr. Opin. Colloid Interface Sci. 1997, 2, 531–537. [Google Scholar] [CrossRef]
- Place, E.S.; Evans, N.D.; Stevens, M.M. Complexity in biomaterials for tissue engineering. Nat. Mater. 2009, 8, 457–470. [Google Scholar] [CrossRef]
- Chaudhuri, O.; Cooper-White, J.; Janmey, P.A.; Mooney, D.J.; Shenoy, V.B. Effects of extracellular matrix viscoelasticity on cellular behaviour. Nature 2020, 584, 535–546. [Google Scholar] [CrossRef]
- Zhu, Y.; Zhang, Q.; Shi, X.; Han, D. Hierarchical hydrogel composite interfaces with robust mechanical properties for biomedical applications. Adv. Mater. 2019, 31, 1804950. [Google Scholar] [CrossRef]
- Gazia, C.; Tamburrini, R.; Asthana, A.; Chaimov, D.; Muir, S.M.; Marino, D.I.; Delbono, L.; Villani, V.; Perin, L.; Di Nardo, P. Extracellular matrix-based hydrogels obtained from human tissues: A work still in progress. Curr. Opin. Organ Transplant. 2019, 24, 604–612. [Google Scholar] [CrossRef] [PubMed]
- Slaughter, B.V.; Khurshid, S.S.; Fisher, O.Z.; Khademhosseini, A.; Peppas, N.A. Hydrogels in regenerative medicine. Adv. Mater. 2009, 21, 3307–3329. [Google Scholar] [CrossRef]
- Wei, W.; Li, H.; Yin, C.; Tang, F. Research progress in the application of in situ hydrogel system in tumor treatment. Drug Deliv. 2020, 27, 460–468. [Google Scholar] [CrossRef]
- Vasile, C.; Pamfil, D.; Stoleru, E.; Baican, M. New developments in medical applications of hybrid hydrogels containing natural polymers. Molecules 2020, 25, 1539. [Google Scholar] [CrossRef]
- Calder, D.; Fathi, A.; Oveissi, F.; Maleknia, S.; Abrams, T.; Wang, Y.; Maitz, J.; Tsai, K.H.; Maitz, P.; Chrzanowski, W.; et al. Thermoresponsive and Injectable Hydrogel for Tissue Agnostic Regeneration. Adv. Healthc. Mater. 2022, 11, e2201714. [Google Scholar] [CrossRef]
- Lu, P.; Takai, K.; Weaver, V.M.; Werb, Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb. Perspect. Biol. 2011, 3, a005058. [Google Scholar] [CrossRef]
- Fontoura, J.C.; Viezzer, C.; Dos Santos, F.G.; Ligabue, R.A.; Weinlich, R.; Puga, R.D.; Antonow, D.; Severino, P.; Bonorino, C. Comparison of 2D and 3D cell culture models for cell growth, gene expression and drug resistance. Mater. Sci. Eng. C 2020, 107, 110264. [Google Scholar] [CrossRef]
- Morello, G.; Quarta, A.; Gaballo, A.; Moroni, L.; Gigli, G.; Polini, A.; Gervaso, F. A thermo-sensitive chitosan/pectin hydrogel for long-term tumor spheroid culture. Carbohydr. Polym. 2021, 274, 118633. [Google Scholar] [CrossRef] [PubMed]
- Monteiro, M.V.; Gaspar, V.M.; Mendes, L.; Duarte, I.F.; Mano, J.F. Stratified 3D Microtumors as Organotypic Testing Platforms for Screening Pancreatic Cancer Therapies. Small Methods 2021, 5, e2001207. [Google Scholar] [CrossRef] [PubMed]
- Fiore, N.J.; Tamer-Mahoney, J.D.; Beheshti, A.; Nieland, T.J.F.; Kaplan, D.L. 3D biocomposite culture enhances differentiation of dopamine-like neurons from SH-SY5Y cells: A model for studying Parkinson’s disease phenotypes. Biomaterials 2022, 290, 121858. [Google Scholar] [CrossRef] [PubMed]
- Stanzione, A.; Polini, A.; La Pesa, V.; Quattrini, A.; Romano, A.; Gigli, G.; Moroni, L.; Gervaso, F. Thermosensitive chitosan-based hydrogels supporting motor neuron-like NSC-34 cell differentiation. Biomater. Sci. 2021, 9, 7492–7503. [Google Scholar] [CrossRef]
- Liu, C.; Mejia, D.L.; Chiang, B.; Luker, K.E.; Luker, G.D. Hybrid collagen alginate hydrogel as a platform for 3D tumor spheroid invasion. Acta Biomater. 2018, 75, 213–225. [Google Scholar] [CrossRef]
- Zhang, Y.; Peng, L.; Hu, K.; Gu, N. Stress Relaxation-Induced Colon Tumor Multicellular Spheroid Culture Based on Biomimetic Hydrogel for Nanoenzyme Ferroptosis Sensitization Evaluation. Adv. Healthc. Mater. 2023, 12, e2202009. [Google Scholar] [CrossRef]
- Dimitriou, P.; Li, J.; Tornillo, G.; McCloy, T.; Barrow, D. Droplet Microfluidics for Tumor Drug-Related Studies and Programmable Artificial Cells. Glob. Chall. 2021, 5, 2000123. [Google Scholar] [CrossRef]
- Khan, A.H.; Zhou, S.P.; Moe, M.; Ortega Quesada, B.A.; Bajgiran, K.R.; Lassiter, H.R.; Dorman, J.A.; Martin, E.C.; Pojman, J.A.; Melvin, A.T. Generation of 3D Spheroids Using a Thiol-Acrylate Hydrogel Scaffold to Study Endocrine Response in ER(+) Breast Cancer. ACS Biomater. Sci. Eng. 2022, 8, 3977–3985. [Google Scholar] [CrossRef]
- Guimarães, C.F.; Gasperini, L.; Marques, A.P.; Reis, R.L. The stiffness of living tissues and its implications for tissue engineering. Nat. Rev. Mater. 2020, 5, 351–370. [Google Scholar] [CrossRef]
- Blache, U.; Ford, E.M.; Ha, B.; Rijns, L.; Chaudhuri, O.; Dankers, P.Y.W.; Kloxin, A.M.; Snedeker, J.G.; Gentleman, E. Engineered hydrogels for mechanobiology. Nat. Rev. Methods Prim. 2022, 2, 98. [Google Scholar] [CrossRef]
- Cuenot, S.; Gelebart, P.; Sinquin, C.; Colliec-Jouault, S.; Zykwinska, A. Mechanical relaxations of hydrogels governed by their physical or chemical crosslinks. J. Mech. Behav. Biomed. Mater. 2022, 133, 105343. [Google Scholar] [CrossRef]
- Chen, F.-M.; Liu, X. Advancing biomaterials of human origin for tissue engineering. Prog. Polym. Sci. 2016, 53, 86–168. [Google Scholar] [CrossRef] [PubMed]
- Assaad, E.; Maire, M.; Lerouge, S. Injectable thermosensitive chitosan hydrogels with controlled gelation kinetics and enhanced mechanical resistance. Carbohydr. Polym. 2015, 130, 87–96. [Google Scholar] [CrossRef]
- Birch, N.P.; Barney, L.E.; Pandres, E.; Peyton, S.R.; Schiffman, J.D. Thermal-responsive behavior of a cell compatible chitosan/pectin hydrogel. Biomacromolecules 2015, 16, 1837–1843. [Google Scholar] [CrossRef]
- Hiorth, M.; Kjøniksen, A.-L.; Knudsen, K.D.; Sande, S.A.; Nyström, B. Structural and dynamical properties of aqueous mixtures of pectin and chitosan. Eur. Polym. J. 2005, 41, 1718–1728. [Google Scholar] [CrossRef]
- Kumar, M.N.R. A review of chitin and chitosan applications. React. Funct. Polym. 2000, 46, 1–27. [Google Scholar] [CrossRef]
- Neufeld, L.; Bianco-Peled, H. Pectin–chitosan physical hydrogels as potential drug delivery vehicles. Int. J. Biol. Macromol. 2017, 101, 852–861. [Google Scholar] [CrossRef]
- Nordby, M.H.; Kjøniksen, A.-L.; Nyström, B.; Roots, J. Thermoreversible gelation of aqueous mixtures of pectin and chitosan. Rheology. Biomacromolecules 2003, 4, 337–343. [Google Scholar] [CrossRef]
- Ventura, I.; Bianco-Peled, H. Small-angle X-ray scattering study on pectin–chitosan mixed solutions and thermoreversible gels. Carbohydr. Polym. 2015, 123, 122–129. [Google Scholar] [CrossRef] [PubMed]
- Martau, G.A.; Mihai, M.; Vodnar, D.C. The Use of Chitosan, Alginate, and Pectin in the Biomedical and Food Sector-Biocompatibility, Bioadhesiveness, and Biodegradability. Polymers 2019, 11, 1837. [Google Scholar] [CrossRef] [PubMed]
- Ahsan, S.M.; Thomas, M.; Reddy, K.K.; Sooraparaju, S.G.; Asthana, A.; Bhatnagar, I. Chitosan as biomaterial in drug delivery and tissue engineering. Int. J. Biol. Macromol. 2018, 110, 97–109. [Google Scholar] [CrossRef]
- Kozen, B.G.; Kircher, S.J.; Henao, J.; Godinez, F.S.; Johnson, A.S. An alternative hemostatic dressing: Comparison of CELOX, HemCon, and QuikClot. Acad. Emerg. Med. 2008, 15, 74–81. [Google Scholar] [CrossRef]
- Ueno, H.; Mori, T.; Fujinaga, T. Topical formulations and wound healing applications of chitosan. Adv. Drug Deliv. Rev. 2001, 52, 105–115. [Google Scholar] [CrossRef] [PubMed]
- Scalera, F.; Monteduro, A.G.; Maruccio, G.; Blasi, L.; Gervaso, F.; Mazzotta, E.; Malitesta, C.; Piccirillo, C. Sustainable chitosan-based electrical responsive scaffolds for tissue engineering applications. Sustain. Mater. Technol. 2021, 28, e00260. [Google Scholar] [CrossRef]
- Scalera, F.; Pereira, S.I.A.; Bucciarelli, A.; Tobaldi, D.M.; Quarta, A.; Gervaso, F.; Castro, P.M.L.; Polini, A.; Piccirillo, C. Chitosan-hydroxyapatite composites made from sustainable sources: A morphology and antibacterial study. Mater. Today Sustain. 2023, 100334. [Google Scholar] [CrossRef]
- Nitti, P.; Gallo, N.; Palazzo, B.; Sannino, A.; Polini, A.; Verri, T.; Barca, A.; Gervaso, F. Effect of l-Arginine treatment on the in vitro stability of electrospun aligned chitosan nanofiber mats. Polym. Test. 2020, 91, 106758. [Google Scholar] [CrossRef]
- Scialla, S.; Barca, A.; Palazzo, B.; D’Amora, U.; Russo, T.; Gloria, A.; De Santis, R.; Verri, T.; Sannino, A.; Ambrosio, L.; et al. Bioactive chitosan-based scaffolds with improved properties induced by dextran-grafted nano-maghemite and l-arginine amino acid. J. Biomed. Mater. Res. A 2019, 107, 1244–1252. [Google Scholar] [CrossRef]
- Izzo, D.; Palazzo, B.; Scalera, F.; Gullotta, F.; lapesa, V.; Scialla, S.; Sannino, A.; Gervaso, F. Chitosan scaffolds for cartilage regeneration: Influence of different ionic crosslinkers on biomaterial properties. Int. J. Polym. Mater. Polym. Biomater. 2018, 68, 936–945. [Google Scholar] [CrossRef]
- Chenite, A.; Buschmann, M.; Wang, D.; Chaput, C.; Kandani, N. Rheological characterisation of thermogelling chitosan/glycerol-phosphate solutions. Carbohydr. Polym. 2001, 46, 39–47. [Google Scholar] [CrossRef]
- Lavertu, M.; Filion, D.; Buschmann, M.D. Heat-induced transfer of protons from chitosan to glycerol phosphate produces chitosan precipitation and gelation. Biomacromolecules 2008, 9, 640–650. [Google Scholar] [CrossRef]
- Zhou, H.Y.; Jiang, L.J.; Cao, P.P.; Li, J.B.; Chen, X.G. Glycerophosphate-based chitosan thermosensitive hydrogels and their biomedical applications. Carbohydr. Polym. 2015, 117, 524–536. [Google Scholar] [CrossRef] [PubMed]
- Saeednia, L.; Yao, L.; Cluff, K.; Asmatulu, R. Sustained releasing of methotrexate from injectable and thermosensitive chitosan–carbon nanotube hybrid hydrogels effectively controls tumor cell growth. ACS Omega 2019, 4, 4040–4048. [Google Scholar] [CrossRef] [PubMed]
- Huang, G.; Li, F.; Zhao, X.; Ma, Y.; Li, Y.; Lin, M.; Jin, G.; Lu, T.J.; Genin, G.M.; Xu, F. Functional and biomimetic materials for engineering of the three-dimensional cell microenvironment. Chem. Rev. 2017, 117, 12764–12850. [Google Scholar] [CrossRef] [PubMed]
- Stanzione, A.; Polini, A.; La Pesa, V.; Romano, A.; Quattrini, A.; Gigli, G.; Moroni, L.; Gervaso, F. Development of injectable thermosensitive chitosan-based hydrogels for cell encapsulation. Appl. Sci. 2020, 10, 6550. [Google Scholar] [CrossRef]
- Fukuda, J.; Khademhosseini, A.; Yeo, Y.; Yang, X.; Yeh, J.; Eng, G.; Blumling, J.; Wang, C.-F.; Kohane, D.S.; Langer, R. Micromolding of photocrosslinkable chitosan hydrogel for spheroid microarray and co-cultures. Biomaterials 2006, 27, 5259–5267. [Google Scholar] [CrossRef]
- Liu, B.-H.; Yeh, H.-Y.; Lin, Y.-C.; Wang, M.-H.; Chen, D.C.; Lee, B.-H.; Hsu, S.-H. Spheroid formation and enhanced cardiomyogenic potential of adipose-derived stem cells grown on chitosan. BioResearch Open Access 2013, 2, 28–39. [Google Scholar] [CrossRef]
- Yang, M.; He, S.; Su, Z.; Yang, Z.; Liang, X.; Wu, Y. Thermosensitive injectable chitosan/collagen/β-glycerophosphate composite hydrogels for enhancing wound healing by encapsulating mesenchymal stem cell spheroids. ACS Omega 2020, 5, 21015–21023. [Google Scholar] [CrossRef]
- Liu, Y.; Guan, Y.; Zhang, Y. Chitosan as inter-cellular linker to accelerate multicellular spheroid generation in hydrogel scaffold. Polymer 2015, 77, 366–376. [Google Scholar] [CrossRef]
- Chang, F.C.; Levengood, S.L.; Cho, N.; Chen, L.; Wang, E.; Yu, J.S.; Zhang, M. Crosslinked Chitosan-PEG Hydrogel for Culture of Human Glioblastoma Cell Spheroids and Drug Screening. Adv. Ther. 2018, 1, 1800058. [Google Scholar] [CrossRef] [PubMed]
- Rinaudo, M. Chitin and chitosan: Properties and applications. Prog. Polym. Sci. 2006, 31, 603–632. [Google Scholar] [CrossRef]
- Hansson, A.; Hashom, N.; Falson, F.; Rousselle, P.; Jordan, O.; Borchard, G. In vitro evaluation of an RGD-functionalized chitosan derivative for enhanced cell adhesion. Carbohydr. Polym. 2012, 90, 1494–1500. [Google Scholar] [CrossRef]
- Kafi, M.A.; Aktar, K.; Todo, M.; Dahiya, R. Engineered chitosan for improved 3D tissue growth through Paxillin-FAK-ERK activation. Regen. Biomater. 2020, 7, 141–151. [Google Scholar] [CrossRef]
- Sacco, P.; Furlani, F.; De Marzo, G.; Marsich, E.; Paoletti, S.; Donati, I. Concepts for Developing Physical Gels of Chitosan and of Chitosan Derivatives. Gels 2018, 4, 67. [Google Scholar] [CrossRef]
- Tarricone, E.; Elia, R.; Mattiuzzo, E.; Faggian, A.; Pozzuoli, A.; Ruggieri, P.; Brun, P. The Viability and Anti-Inflammatory Effects of Hyaluronic Acid-Chitlac-Tracimolone Acetonide- beta-Cyclodextrin Complex on Human Chondrocytes. Cartilage 2021, 13, 920S–924S. [Google Scholar] [CrossRef]
- Pizzolitto, C.; Esposito, F.; Sacco, P.; Marsich, E.; Gargiulo, V.; Bedini, E.; Donati, I. Sulfated lactose-modified chitosan. A novel synthetic glycosaminoglycan-like polysaccharide inducing chondrocyte aggregation. Carbohydr. Polym. 2022, 288, 119379. [Google Scholar] [CrossRef] [PubMed]
- Medelin, M.; Porrelli, D.; Aurand, E.R.; Scaini, D.; Travan, A.; Borgogna, M.A.; Cok, M.; Donati, I.; Marsich, E.; Scopa, C.; et al. Exploiting natural polysaccharides to enhance in vitro bio-constructs of primary neurons and progenitor cells. Acta Biomater. 2018, 73, 285–301. [Google Scholar] [CrossRef]
- Lapomarda, A.; De Acutis, A.; Chiesa, I.; Fortunato, G.M.; Montemurro, F.; De Maria, C.; Mattioli Belmonte, M.; Gottardi, R.; Vozzi, G. Pectin-GPTMS-based biomaterial: Toward a sustainable bioprinting of 3D scaffolds for tissue engineering application. Biomacromolecules 2019, 21, 319–327. [Google Scholar] [CrossRef]
- Munarin, F.; Tanzi, M.C.; Petrini, P. Advances in biomedical applications of pectin gels. Int. J. Biol. Macromol. 2012, 51, 681–689. [Google Scholar] [CrossRef]
- May, C.D. Industrial pectins: Sources, production and applications. Carbohydr. Polym. 1990, 12, 79–99. [Google Scholar] [CrossRef]
- McCann, M.; Roberts, K. Plant cell wall architecture: The role of pectins. In Progress in Biotechnology; Elsevier: Amsterdam, The Netherlands, 1996; Volume 14, pp. 91–107. [Google Scholar]
- Mishra, R.; Banthia, A.; Majeed, A. Pectin based formulations for biomedical applications: A review. Asian J. Pharm. Clin. Res. 2012, 5, 1–7. [Google Scholar]
- Thibault, J.-F.; Ralet, M.-C. Physico-chemical properties of pectins in the cell walls and after extraction. In Advances in Pectin and Pectinase Research; Springer: Berlin/Heidelberg, Germany, 2003; pp. 91–105. [Google Scholar]
- Li, D.Q.; Wang, S.Y.; Meng, Y.J.; Guo, Z.W.; Cheng, M.M.; Li, J. Fabrication of self-healing pectin/chitosan hybrid hydrogel via Diels-Alder reactions for drug delivery with high swelling property, pH-responsiveness, and cytocompatibility. Carbohydr. Polym. 2021, 268, 118244. [Google Scholar] [CrossRef] [PubMed]
- Tan, H.; Chen, W.; Liu, Q.; Yang, G.; Li, K. Pectin Oligosaccharides Ameliorate Colon Cancer by Regulating Oxidative Stress- and Inflammation-Activated Signaling Pathways. Front. Immunol. 2018, 9, 1504. [Google Scholar] [CrossRef] [PubMed]
- Grant, G.T. Biological interactions between polysaccharides and divalent cations: The egg-box model. FEBS Lett. 1973, 32, 195–198. [Google Scholar] [CrossRef]
- Moreira, H.R.; Munarin, F.; Gentilini, R.; Visai, L.; Granja, P.L.; Tanzi, M.C.; Petrini, P. Injectable pectin hydrogels produced by internal gelation: pH dependence of gelling and rheological properties. Carbohydr. Polym. 2014, 103, 339–347. [Google Scholar] [CrossRef]
- Liu, L.; Fishman, M.L.; Hicks, K.B. Pectin in controlled drug delivery–a review. Cellulose 2007, 14, 15–24. [Google Scholar] [CrossRef]
- Cao, L.; Lu, W.; Mata, A.; Nishinari, K.; Fang, Y. Egg-box model-based gelation of alginate and pectin: A review. Carbohydr. Polym. 2020, 242, 116389. [Google Scholar] [CrossRef]
- Qi, X.; Al-Ghazzewi, F.H.; Tester, R.F. Dietary fiber, gastric emptying, and carbohydrate digestion: A mini-review. Starch-Stärke 2018, 70, 1700346. [Google Scholar] [CrossRef]
- Meng, Y.-J.; Wang, S.-Y.; Guo, Z.-W.; Cheng, M.-M.; Li, J.; Li, D.-Q. Design and preparation of quaternized pectin-Montmorillonite hybrid film for sustained drug release. Int. J. Biol. Macromol. 2020, 154, 413–420. [Google Scholar] [CrossRef]
- Shitrit, Y.; Davidovich-Pinhas, M.; Bianco-Peled, H. Shear thinning pectin hydrogels physically cross-linked with chitosan nanogels. Carbohydr. Polym. 2019, 225, 115249. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Zheng, D.; Ma, Y.; Dai, J.; Li, C.; Xiao, S.; Liu, K.; Liu, J.; Wang, L.; Lei, J. Self-assembled nanoparticles platform based on pectin-dihydroartemisinin conjugates for codelivery of anticancer drugs. ACS Biomater. Sci. Eng. 2017, 4, 1641–1650. [Google Scholar] [CrossRef]
- Vityazev, F.V.; Khramova, D.S.; Saveliev, N.Y.; Ipatova, E.A.; Burkov, A.A.; Beloserov, V.S.; Belyi, V.A.; Kononov, L.O.; Martinson, E.A.; Litvinets, S.G. Pectin–glycerol gel beads: Preparation, characterization and swelling behaviour. Carbohydr. Polym. 2020, 238, 116166. [Google Scholar] [CrossRef] [PubMed]
- Niu, R.; Qin, Z.; Ji, F.; Xu, M.; Tian, X.; Li, J.; Yao, F. Hybrid pectin–Fe3+/polyacrylamide double network hydrogels with excellent strength, high stiffness, superior toughness and notch-insensitivity. Soft Matter. 2017, 13, 9237–9245. [Google Scholar] [CrossRef] [PubMed]
- Neves, S.C.; Gomes, D.B.; Sousa, A.; Bidarra, S.J.; Petrini, P.; Moroni, L.; Barrias, C.C.; Granja, P.L. Biofunctionalized pectin hydrogels as 3D cellular microenvironments. J. Mater. Chem. B 2015, 3, 2096–2108. [Google Scholar] [CrossRef]
- Assifaoui, A.; Bouyer, F.; Chambin, O.; Cayot, P. Silica-coated calcium pectinate beads for colonic drug delivery. Acta Biomater. 2013, 9, 6218–6225. [Google Scholar] [CrossRef]
- Merli, M.; Sardelli, L.; Baranzini, N.; Grimaldi, A.; Jacchetti, E.; Raimondi, M.T.; Briatico-Vangosa, F.; Petrini, P.; Tunesi, M. Pectin-based bioinks for 3D models of neural tissue produced by a pH-controlled kinetics. Front. Bioeng. Biotechnol 2022, 2022, 1032542. [Google Scholar] [CrossRef]
- Pacelli, S.; Paolicelli, P.; Pepi, F.; Garzoli, S.; Polini, A.; Tita, B.; Vitalone, A.; Casadei, M.A. Gellan gum and polyethylene glycol dimethacrylate double network hydrogels with improved mechanical properties. J. Polym. Res. 2014, 21, 409. [Google Scholar] [CrossRef]
- Li, X.; Su, X. Multifunctional smart hydrogels: Potential in tissue engineering and cancer therapy. J. Mater. Chem. B 2018, 6, 4714–4730. [Google Scholar] [CrossRef]
- Zhao, Z.; Vizetto-Duarte, C.; Moay, Z.K.; Setyawati, M.I.; Rakshit, M.; Kathawala, M.H.; Ng, K.W. Composite hydrogels in three-dimensional in vitro models. Front. Bioeng. Biotechnol. 2020, 8, 611. [Google Scholar] [CrossRef]
- Dhand, A.P.; Galarraga, J.H.; Burdick, J.A. Enhancing biopolymer hydrogel functionality through interpenetrating networks. Trends Biotechnol. 2021, 39, 519–538. [Google Scholar] [CrossRef]
- Sun, X.-F.; Zeng, Q.; Wang, H.; Hao, Y. Preparation and swelling behavior of pH/temperature responsive semi-IPN hydrogel based on carboxymethyl xylan and poly (N-isopropyl acrylamide). Cellulose 2019, 26, 1909–1922. [Google Scholar] [CrossRef]
- Tunesi, M.; Raimondi, I.; Russo, T.; Colombo, L.; Micotti, E.; Brandi, E.; Cappelletti, P.; Cigada, A.; Negro, A.; Ambrosio, L. Hydrogel-based delivery of Tat-fused protein Hsp70 protects dopaminergic cells in vitro and in a mouse model of Parkinson’s disease. NPG Asia Mater. 2019, 11, 28. [Google Scholar] [CrossRef]
- Michailidou, G.; Terzopoulou, Z.; Kehagia, A.; Michopoulou, A.; Bikiaris, D.N. Preliminary evaluation of 3D printed chitosan/pectin constructs for biomedical applications. Mar. Drugs 2021, 19, 36. [Google Scholar] [CrossRef] [PubMed]
- da Costa, M.P.M.; de Mello Ferreira, I.L.; de Macedo Cruz, M.T. New polyelectrolyte complex from pectin/chitosan and montmorillonite clay. Carbohydr. Polym. 2016, 146, 123–130. [Google Scholar] [CrossRef]
- Li, D.-Q.; Wang, S.-Y.; Meng, Y.-J.; Li, J.-F.; Li, J. An injectable, self-healing hydrogel system from oxidized pectin/chitosan/γ-Fe2O3. Int. J. Biol. Macromol. 2020, 164, 4566–4574. [Google Scholar] [CrossRef]
- Cheikh, D.; García-Villén, F.; Majdoub, H.; Zayani, M.B.; Viseras, C. Complex of chitosan pectin and clay as diclofenac carrier. Appl. Clay Sci. 2019, 172, 155–164. [Google Scholar] [CrossRef]
- Giacomazza, D.; Sabatino, M.; Catena, A.; Leone, M.; San Biagio, P.; Dispenza, C. Maltose-conjugated chitosans induce macroscopic gelation of pectin solutions at neutral pH. Carbohydr. Polym. 2014, 114, 141–148. [Google Scholar] [CrossRef] [PubMed]
- Luppi, B.; Bigucci, F.; Abruzzo, A.; Corace, G.; Cerchiara, T.; Zecchi, V. Freeze-dried chitosan/pectin nasal inserts for antipsychotic drug delivery. Eur. J. Pharm. Biopharm. 2010, 75, 381–387. [Google Scholar] [CrossRef]
- Tentor, F.R.; de Oliveira, J.H.; Scariot, D.B.; Lazarin-Bidóia, D.; Bonafé, E.G.; Nakamura, C.V.; Venter, S.A.S.; Monteiro, J.P.; Muniz, E.C.; Martins, A.F. Scaffolds based on chitosan/pectin thermosensitive hydrogels containing gold nanoparticles. Int. J. Biol. Macromol. 2017, 102, 1186–1194. [Google Scholar] [CrossRef]
- Torpol, K.; Sriwattana, S.; Sangsuwan, J.; Wiriyacharee, P.; Prinyawiwatkul, W. Optimising chitosan–pectin hydrogel beads containing combined garlic and holy basil essential oils and their application as antimicrobial inhibitor. Int. J. Food Sci. Technol. 2019, 54, 2064–2074. [Google Scholar] [CrossRef]
- Long, J.; Etxeberria, A.E.; Nand, A.V.; Bunt, C.R.; Ray, S.; Seyfoddin, A. A 3D printed chitosan-pectin hydrogel wound dressing for lidocaine hydrochloride delivery. Mater. Sci. Eng. C 2019, 104, 109873. [Google Scholar] [CrossRef] [PubMed]
- Martins, J.G.; Camargo, S.E.; Bishop, T.T.; Popat, K.C.; Kipper, M.J.; Martins, A.F. Pectin-chitosan membrane scaffold imparts controlled stem cell adhesion and proliferation. Carbohydr. Polym. 2018, 197, 47–56. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Cong, Y.; Osi, A.R.; Zhou, Y.; Huang, F.; Zaccaria, R.P.; Chen, J.; Wang, R.; Fu, J. Direct 3D printed biomimetic scaffolds based on hydrogel microparticles for cell spheroid growth. Adv. Funct. Mater. 2020, 30, 1910573. [Google Scholar] [CrossRef]
- Coimbra, P.; Ferreira, P.; De Sousa, H.; Batista, P.; Rodrigues, M.; Correia, I.; Gil, M. Preparation and chemical and biological characterization of a pectin/chitosan polyelectrolyte complex scaffold for possible bone tissue engineering applications. Int. J. Biol. Macromol. 2011, 48, 112–118. [Google Scholar] [CrossRef]
- Konovalova, M.V.; Markov, P.A.; Durnev, E.A.; Kurek, D.V.; Popov, S.V.; Varlamov, V.P. Preparation and biocompatibility evaluation of pectin and chitosan cryogels for biomedical application. J. Biomed. Mater. Res. A 2017, 105, 547–556. [Google Scholar] [CrossRef]
- Ghorbani, M.; Roshangar, L.; Rad, J.S. Development of reinforced chitosan/pectin scaffold by using the cellulose nanocrystals as nanofillers: An injectable hydrogel for tissue engineering. Eur. Polym. J. 2020, 130, 109697. [Google Scholar] [CrossRef]
- Morello, G.; Polini, A.; Scalera, F.; Rizzo, R.; Gigli, G.; Gervaso, F. Preparation and Characterization of Salt-Mediated Injectable Thermosensitive Chitosan/Pectin Hydrogels for Cell Embedding and Culturing. Polymers 2021, 13, 2674. [Google Scholar] [CrossRef]
- Leung, C.M.; De Haan, P.; Ronaldson-Bouchard, K.; Kim, G.-A.; Ko, J.; Rho, H.S.; Chen, Z.; Habibovic, P.; Jeon, N.L.; Takayama, S. A guide to the organ-on-a-chip. Nat. Rev. Methods Primers 2022, 2, 33. [Google Scholar] [CrossRef]
- Polini, A.; del Mercato, L.L.; Barra, A.; Zhang, Y.S.; Calabi, F.; Gigli, G. Towards the development of human immune-system-on-a-chip platforms. Drug Discov. Today 2019, 24, 517–525. [Google Scholar] [CrossRef]
- Polini, A.; Moroni, L. The convergence of high-tech emerging technologies into the next stage of organ-on-a-chips. Biomater. Biosyst. 2021, 1, 100012. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 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
Morello, G.; De Iaco, G.; Gigli, G.; Polini, A.; Gervaso, F. Chitosan and Pectin Hydrogels for Tissue Engineering and In Vitro Modeling. Gels 2023, 9, 132. https://doi.org/10.3390/gels9020132
Morello G, De Iaco G, Gigli G, Polini A, Gervaso F. Chitosan and Pectin Hydrogels for Tissue Engineering and In Vitro Modeling. Gels. 2023; 9(2):132. https://doi.org/10.3390/gels9020132
Chicago/Turabian StyleMorello, Giulia, Gianvito De Iaco, Giuseppe Gigli, Alessandro Polini, and Francesca Gervaso. 2023. "Chitosan and Pectin Hydrogels for Tissue Engineering and In Vitro Modeling" Gels 9, no. 2: 132. https://doi.org/10.3390/gels9020132