Peptide Self-Assembly into Hydrogels for Biomedical Applications Related to Hydroxyapatite
Abstract
:1. Introduction
2. Peptide Self-Assembly
3. Hydroxyapatite
4. Hydroxyapatite Nanocomposites
5. Hydrogels Based on Peptide Self-Assembly with Interest in Tissue Regeneration
6. Nanoparticles and Nanocapsules Based on Peptide Self-Assembly
7. Hard Tissue Regeneration
7.1. Bone Regeneration
7.2. Tooth Regeneration
7.3. Cartilage Regeneration
8. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Kim, S.; Kim, J.H.; Lee, J.S.; Park, C.B. Beta-sheet-forming, self-assembled peptide nanomaterials towards optical, energy, and healthcare applications. Small 2015, 11, 3623–3640. [Google Scholar] [CrossRef] [PubMed]
- Scanlon, S.; Aggeli, A. Self-assembling peptide nanotubes. Nanotoday 2008, 3, 22–30. [Google Scholar] [CrossRef]
- Hartgerink, J.D.; Beniash, E.; Stupp, S.I. Peptide-amphiphile nanofibers: A versatile scaffold for the preparation of self-assembling materials. Proc. Natl. Acad. Sci. USA 2002, 99, 5133–5138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stupp, S.I. Self-assembly and biomaterials. Nano Lett. 2010, 10, 4783–4786. [Google Scholar] [CrossRef] [PubMed]
- Stupp, S.I. Biomaterials for regenerative medicine. MRS Bull. 2005, 30, 546–553. [Google Scholar] [CrossRef]
- Andreetto, E.; Malideli, E.; Yan, L.M.; Kracklauer, M.; Farbiarz, K.; Tatarek-Nossol, M.; Rammes, G.; Prade, E.; Neumüller, T.; Caporale, A.; et al. A hot-segment-based approach for the design of cross-amyloid interaction surface mimics as inhibitors of amyloid self-assembly. Angew. Chem. Int. Ed. Engl. 2015, 54, 13095–13100. [Google Scholar] [CrossRef] [PubMed]
- Li, C.; Adamcik, J.; Mezzenga, R. Biodegradable nanocomposites of amyloid fibrils and graphene with shape-memory and enzyme-sensing properties. Nat. Nanotechnol. 2012, 7, 421–427. [Google Scholar] [CrossRef] [PubMed]
- Jacob, R.S.; Ghosh, D.; Singh, P.K.; Basu, S.K.; Jha, N.N.; Das, S.; Sukul, P.K.; Patil, S.; Sathaye, S.; Kumar, A.; et al. Self healing hydrogels composed of amyloid nano fibrils for cell culture and stem cell differentiation. Biomaterials 2015, 54, 97–105. [Google Scholar] [CrossRef] [PubMed]
- Amit, M.; Yuran, S.; Gazit, E.; Reches, M.; Ashkenasy, N. Tailor-made functional peptide self-assembling nanostructures. Adv. Mater. 2018, 30, e1707083. [Google Scholar] [CrossRef] [PubMed]
- Wei, G.; Su, Z.; Reynolds, N.P.; Arosio, P.; Hamley, I.W.; Gazit, E.; Mezzenga, R. Self-assembling peptide and protein amyloids: From structure to tailored function in nanotechnology. Chem. Soc. Rev. 2017, 46, 4661–4708. [Google Scholar] [CrossRef] [PubMed]
- Knowles, T.P.; Mezzenga, R. Amyloid fibrils as building blocks for natural and artificial functional materials. Adv. Mater. 2016, 28, 6546–6561. [Google Scholar] [CrossRef] [PubMed]
- Ekiz, M.S.; Cinar, G.; Khalily, M.A.; Guler, M.O. Self-assembled peptide nanostructures for functional materials. Nanotechnology 2016, 27, 402002. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reches, M.; Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 2003, 300, 625–627. [Google Scholar] [CrossRef] [PubMed]
- Adler-Abramovich, L.; Gazit, E. The physical properties of supramolecular peptides assemblies: From building block association to technological applications. Chem. Soc. Rev. 2014, 43, 6881–6893. [Google Scholar] [CrossRef] [PubMed]
- Babar, D.G.; Sarkar, S. Self-assembled nanotubes from single fluorescent amino acid. Appl. Nanosci. 2017, 7, 101–107. [Google Scholar] [CrossRef] [Green Version]
- Gyles, D.A.; Castro, L.D.; Silva, J.O.C.; Ribeiro-Costa, R.M. A review of the designs and prominent biomedical advances of natural and synthetic hydrogel formulations. Eur. Polym. J. 2017, 88, 373–392. [Google Scholar] [CrossRef]
- Das, N. Preparation methods and properties of hydrogel: A review. Int. J. Pharm. Pharm. Sci. 2013, 5, 112–117. [Google Scholar]
- Bae, K.H.; Wang, L.S.; Kurisawa, M. Injectable biodegradable hydrogels: Progress and challenges. J. Mater. Chem. B 2013, 1, 5371–5388. [Google Scholar] [CrossRef]
- del Valle, L.J.; Díaz, A.; Puiggalí, J. Hydrogels for biomedical applications: Cellulose, chitosan, and protein/peptide derivatives. Gels 2017, 3, 27. [Google Scholar] [CrossRef]
- Wahl, D.A.; Czernuszka, J.T. Collagen-hydroxyapatite composites for hard tissue repair. Eur. Cell. Mater. 2006, 11, 43–56. [Google Scholar] [CrossRef] [PubMed]
- Dorozhkin, S.V. Calcium orthophosphate bioceramics. Ceram. Int. 2015, 41, 13913–13966. [Google Scholar] [CrossRef]
- Habraken, W.; Habibovic, P.; Epple, M.; Bohner, M. Calcium phosphates in biomedical applications: Materials for the future? Materialstoday 2016, 19, 69–87. [Google Scholar] [CrossRef]
- Turon, P.; del Valle, L.J.; Alemán, C.; Puiggalí, J. Biodegradable and biocompatible systems based on hydroxyapatite nanoparticles. Appl. Sci. 2017, 7, 60. [Google Scholar] [CrossRef]
- Rubert Pérez, C.M.; Stephanopoulos, N.; Sur, S.; Lee, S.S.; Newcomb, C.; Stupp, S.I. The powerful functions of peptide-based bioactive matrices for regenerative medicine. Ann. Biomed. Eng. 2015, 43, 501–514. [Google Scholar] [CrossRef] [PubMed]
- Cui, H.; Webber, M.J.; Stupp, S.I. Self-assembly of peptide amphiphiles: From molecules to nanostructures o biomaterials. Biopolymers 2010, 94, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Hosseinkhani, H.; Hong, P.D.; Yu, D.S. Self-assembled proteins and peptides for regenerative medicine. Chem. Rev. 2013, 113, 4837–4861. [Google Scholar] [CrossRef] [PubMed]
- He, B.; Zhao, J.; Ou, Y.; Jiang, D. Biofunctionalized peptide nanofiber-based composite scaffolds for bone regeneration. Mater. Sci. Eng. C Mater. Biol. Appl. 2018, 90, 728–738. [Google Scholar] [CrossRef] [PubMed]
- Zou, R.; Wang, Q.; Wu, J.; Wu, J.; Schmuck, C.; Tian, H. Peptide self-assembly triggered by metal ions. Chem. Soc. Rev. 2015, 44, 5200–5219. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Liu, K.; Xing, R.; Yan, X. Peptide self-assembly: Thermodynamics and kinetics. Chem. Soc. Rev. 2016, 45, 5589–5604. [Google Scholar] [CrossRef] [PubMed]
- Feng, Z.; Zhang, T.; Wang, H.; Xu, B. Supramolecular catalysis and dynamic assemblies for medicine. Chem. Soc. Rev. 2017, 46, 6470–6479. [Google Scholar] [CrossRef] [PubMed]
- Mason, J.M.; Arndt, K.M. Coiled coil domains: Stability, specificity, and biological implications. Chembiochem 2004, 5, 170–176. [Google Scholar] [CrossRef] [PubMed]
- Woolfson, D.N. Building fibrous biomaterials from alpha-helical and collagen-like coiled-coil peptides. Biopolymers 2010, 94, 118–127. [Google Scholar] [CrossRef] [PubMed]
- Di Lullo, G.A.; Sweeney, S.M.; Korkko, J.; Ala-Kokko, L.; San Antonio, J.D. Mapping the ligand-binding sites and disease-associated mutations on the most abundant protein in the human, type I collagen. J. Biol. Chem. 2002, 277, 4223–4231. [Google Scholar] [CrossRef] [PubMed]
- He, B.; Yuan, X.; Jiang, D. Molecular self-assembly guides the fabrication of peptide nanofiber scaffolds for nerve repair. RSC Adv. 2014, 4, 23610–23621. [Google Scholar] [CrossRef]
- Stephanopoulos, N.; Ortony, J.H.; Stupp, S.I. Self-assembly for the synthesis of functional biomaterials. Acta Mater. 2013, 61, 912–930. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gazit, E. Self-assembled peptide nanostructures: The design of molecular building blocks and their technological utilization. Chem. Soc. Rev. 2007, 36, 1263–1269. [Google Scholar] [CrossRef] [PubMed]
- Sun, L.; Zheng, C.; Webster, T.J. Self-assembled peptide nanomaterials for biomedical applications: Promises and pitfalls. Int. J. Nanomed. 2017, 12, 73–86. [Google Scholar] [CrossRef] [PubMed]
- Luo, Z.; Wang, S.; Zhang, S. Fabrication of self-assembling d-form peptide nanofiber scaffold d-EAK16 for rapid hemostasis. Biomaterials 2011, 32, 2013–2020. [Google Scholar] [CrossRef] [PubMed]
- Luo, Z.; Zhang, S. Designer nanomaterials using chiral self-assembling peptide systems and their emerging benefit for society. Chem. Soc. Rev. 2012, 41, 4736–4754. [Google Scholar] [CrossRef] [PubMed]
- Raspa, A.; Saracino, G.A.A.; Pugliese, R.; Silva, D.; Cigognini, D.; Vescovi, A.; Gelain, F. Complementary Co-assembling peptides: From in silico studies to in vivo application. Adv. Funct. Mater. 2014, 24, 6317–6328. [Google Scholar] [CrossRef]
- Zhang, S.; Holmes, T.C.; DiPersio, C.M.; Hynes, R.O.; Su, X.; Rich, A. Self-complementary oligopeptide matrices support mammalian cell attachment. Biomaterials 1995, 16, 1385–1393. [Google Scholar] [CrossRef]
- Zhang, S.; Altman, M. Peptide self-assembly in functional polymer science and engineering. React. Funct. Polym. 1999, 41, 91–102. [Google Scholar] [CrossRef]
- Zhang, F.; Shi, G.S.; Ren, L.F.; Hu, F.Q.; Li, S.L.; Xie, Z.J. Designer self-assembling peptide scaffold stimulates pre-osteoblast attachment, spreading and proliferation. J. Mater. Sci. Mater. Med. 2009, 20, 1475–1481. [Google Scholar] [CrossRef] [PubMed]
- Horii, A.; Wang, X.; Gelain, F.; Zhang, S. Biological designer self-assembling peptide nanofiber scaffolds significantly enhance osteoblast proliferation, differentiation and 3-D migration. PLoS ONE 2007, 2, e190. [Google Scholar] [CrossRef] [PubMed]
- Garcia, A.; Iglesias, D.; Parisi, E.; Styan, K.E.; Waddington, L.J.; Deganutti, C.; de Zorzi, R.; Grassi, M.; Melchionna, M.; Vargiu, A.V.; Marchesan, S. Chirality effects on peptide self-assembly unraveled from molecules to materials. Chem 2018, 4, 1862–1876. [Google Scholar] [CrossRef]
- Fuertes, A.; Juanes, M.; Granja, J.R.; Montenegro, J. Supramolecular functional assemblies: Dynamic membrane transporters and peptide nanotubular composites. Chem. Commun. 2017, 53, 7861–7871. [Google Scholar] [CrossRef] [PubMed]
- Melchionna, M.; Styan, K.E.; Marchesan, S. The unexpected advantages of using D-amino acids for peptide self-assembly into nanostructured hydrogels for medicine. Curr. Top. Med. Chem. 2016, 16, 2009–2018. [Google Scholar] [CrossRef] [PubMed]
- Hartgerink, J.D.; Beniash, E.; Stupp, S.I. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science 2001, 294, 1684–1688. [Google Scholar] [CrossRef] [PubMed]
- Castelletto, V.; Moulton, C.M.; Cheng, G.; Hamley, I.W.; Hicks, M.R.; Rodger, A.; López-Pérez, D.E.; Revilla, G.; Alemán, C. Self-assembly of Fmoc-tetrapeptides based on RGDS cell adhesion motif. Soft Matter 2011, 7, 11405–11415. [Google Scholar] [CrossRef]
- López-Pérez, D.E.; Revilla, G.; Hamley, I.W.; Alemán, C. Molecular insights into aggregates, made of amphiphilic Fmoc-tetrapeptides. Soft Matter 2013, 9, 11021–11032. [Google Scholar] [CrossRef]
- Zhang, S.; Greenfield, M.A.; Mata, A.; Palmer, L.C.; Bitton, R.; Mantei, J.R.; Aparicio, C.; de la Cruz, M.O.; Stupp, S.I. A self-assembly pathway to aligned monodomain gels. Nat. Mater. 2010, 9, 594–601. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tao, K.; Levin, A.; Adler-Abramovich, L.; Gazit, E. Fmoc-modified amino acids and short peptides: Simple bio-inspired building blocks for the fabrication of functional materials. Chem. Soc. Rev. 2016, 45, 3935–3953. [Google Scholar] [CrossRef] [PubMed]
- Martin, A.D.; Wojciechowski, J.P.; Warren, H.; in het Panhuis, M.; Thordarson, P. Effect of heterocyclic capping groups on the self-assembly of a dipeptide hydrogel. Soft Matter 2016, 12, 2700–2707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lyanage, W.; Vats, K.; Rajbhandary, A.; Benoit, D.S.W.; Nilsson, B.L. Multicomponent dipeptide hydrogels as extracellular matrix-mimetic scaffolds for cell culture applications. Chem. Commun. 2015, 51, 11260–11263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Elliot, J.C. Structure and Chemistry of the Apatites and Other Calcium Orthophosphates, 1st ed.; Elsevier: Amsterdam, The Netherlands, 1994; pp. 1–62. ISBN 9781483290317. [Google Scholar]
- Kay, M.I.; Young, R.A.; Posner, A.S. Crystal structure of hydroxyapatite. Nature 1964, 204, 1050–1052. [Google Scholar] [CrossRef] [PubMed]
- Dorozhkin, S.V.; Epple, M. Biological and medical significance of calcium phosphates. Angew. Chem. Int. Ed. Engl. 2002, 41, 3130–3146. [Google Scholar] [CrossRef]
- Bigi, A.; Boanini, E.; Rubini, K. Hydroxyapatite gels and nanocrystals prepared through a sol-gel process. J. Solid State Chem. 2004, 177, 3092–3098. [Google Scholar] [CrossRef]
- Fowler, C.E.; Li, M.; Mann, S.; Margolis, H.C. Influence of surfactant assembly on the formation of calcium phosphate materials—A model for dental enamel formation. J. Mater. Chem. 2005, 15, 3317–3325. [Google Scholar] [CrossRef]
- Roy, I.; Mitra, S.; Maitra, A.; Mozumdar, S. Calcium phosphate nanoparticles as novel non-viral vectors for targeted gene delivery. Int. J. Pharm. 2003, 250, 25–33. [Google Scholar] [CrossRef] [PubMed]
- Zhang, F.; Zhou, Z.H.; Yang, S.P.; Mao, L.H.; Chen, H.M.; Yu, X.B. Hydrothermal synthesis of hydroxyapatite nanorods in the presence of anionic starburst dendrimer. Mater. Lett. 2005, 59, 1422–1425. [Google Scholar] [CrossRef]
- Bose, S.; Saha, S.K. Synthesis of hydroxyapatite nanopowders via sucrose-templated sol-gel method. J. Am. Ceram. Soc. 2004, 86, 1055–1057. [Google Scholar] [CrossRef]
- Jevtic, M.; Mitric, M.; Skapin, S.; Jancar, B.; Ignjatovic, N.; Uskokovic, D. Crystal structure of hydroxyapatite nanorods synthesized by sonochemical homogeneous precipitation. Cryst. Growth Des. 2008, 8, 2217–2222. [Google Scholar] [CrossRef]
- Bose, S.; Saha, S.K. Synthesis and characterization of hydroxyapatite nanopowders by emulsion technique. Chem. Mater. 2003, 15, 4464–4469. [Google Scholar] [CrossRef]
- Kobayashi, T.; Ono, S.; Hirakura, S.; Oaki, Y.; Imai, H. Morphological variation of hydroxyapatite grown in aqueous solution based on simulated body fluid. CrystEngComm 2012, 14, 1143–1149. [Google Scholar] [CrossRef]
- Bertran, O.; del Valle, L.J.; Revilla-López, G.; Chaves, G.; Cardús, L.; Casas, M.T.; Casanovas, J.; Turon, P.; Puiggalí, J.; Alemán, C. Mineralization of DNA into nanoparticles of hydroxyapatite. Dalton Trans. 2014, 43, 317–327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuo, G.; Wan, Y.; Meng, X.; Zhao, Q.; Ren, K.; Jia, S.; Wang, J. Synthesis and characterization of a lamellar hydroxyapatite/DNA nanohybrid. Mater. Chem. Phys. 2011, 126, 470–475. [Google Scholar] [CrossRef]
- Zhu, S.H.; Huang, B.Y.; Zhou, K.C.; Huang, S.P.; Liu, F.; Li, Y.M.; Xue, Z.G.; Long, Z.G. Hydroxyapatite nanoparticles as a novel gene carrier. J. Nanopart. Res. 2004, 6, 307–311. [Google Scholar] [CrossRef]
- Rivas, M.; del Valle, L.J.; Rodríguez-Rivero, A.M.; Turon, P.; Puiggalí, J.; Alemán, C. Loading of antibiotic into biocoated hydroxyapatite nanoparticles: Smart antitumor platforms with regulated release. ACS Biomater. Sci. Eng. 2018, 4, 3234–3245. [Google Scholar] [CrossRef]
- Bonzani, I.C.; George, J.H.; Stevens, M.M. Novel materials for bone and cartilage regeneration. Curr. Opin. Chem. Biol. 2006, 10, 568–575. [Google Scholar] [CrossRef] [PubMed]
- Song, J.; Malathong, V.; Bertozzi, C.R. Mineralization of synthetic polymer scaffolds: A bottom-up approach for the development of artificial bone. J. Am. Chem. Soc. 2005, 127, 3366–3372. [Google Scholar] [CrossRef] [PubMed]
- Palmer, L.C.; Newcomb, C.J.; Kaltz, S.R.; Spoerke, E.D.; Stupp, S.I. Biomimetic systems for hydroxyapatite mineralization inspired by bone and enamel. Chem. Rev. 2008, 108, 4754–4783. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Liao, S.S.; Cui, F.Z. Hierarchical self-assembly of nano-fibrils in mineralized collagen. Chem. Mater. 2003, 15, 3221–3226. [Google Scholar] [CrossRef]
- Nel, A.; Xia, T.; Mädler, L.; Li, N. Toxic potential of materials at the nanolevel. Science 2006, 311, 622–627. [Google Scholar] [CrossRef] [PubMed]
- Mathieu, L.M.; Bourban, P.E.; Manson, J.A.E. Processing of homogeneous ceramic/polymer blends for bioresorbable composites. Compos. Sci. Technol. 2006, 66, 1606–1614. [Google Scholar] [CrossRef]
- Maiti, P.; Prakash, Y.; Jaya, P. Biodegradable nanocomposites of poly(hydroxybutyrate-co-hydroxyvalerate): The effect of nanoparticles. J. Nanosci. Nanotechnol. 2008, 8, 1858–1866. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Weng, W. Surface modification of hydroxyapatite by stearic acid: Characterization and in vitro behaviors. J. Mater. Sci.: Mater. Med. 2008, 19, 19–25. [Google Scholar] [CrossRef] [PubMed]
- Hong, Z.; Zhang, P.; He, C.; Qui, X.; Liu, A.; Chen, L.; Chen, X.; Jing, X. Nano-composite of poly(L-lactide) and surface grafted hydroxyapatite: Mechanical properties and biocompatibility. Biomaterials 2005, 26, 6296–6304. [Google Scholar] [CrossRef] [PubMed]
- Kato, K.; Eika, Y.; Ikada, Y. In situ hydroxyapatite crystallization for the formation of hydroxyapatite/polymer composites. J. Mater. Sci. 1997, 32, 5533–5554. [Google Scholar] [CrossRef]
- Laurencin, C.T.; Kumbar, S.G.; Nukavarapu, S.P. Nanotechnology and orthopedics: A personal perspective. WIREs. Nanomed. Nanobiotechnol. 2009, 1, 6–10. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.W.; Song, J.H.; Kim, H.E. Nanofiber generation of gelatin–hydroxyapatite biomimetics for guided tissue regeneration. Adv. Funct. Mater. 2005, 15, 1988–1994. [Google Scholar] [CrossRef]
- Jaiswal, A.K.; Chhabra, H.; Soni, V.P.; Bellare, J.R. Enhanced mechanical strength and biocompatibility of electrospun polycaprolactone-gelatin scaffold with surface deposited nano-hydroxyapatite. Mater. Sci. Eng. C 2013, 33, 2376–2385. [Google Scholar] [CrossRef] [PubMed]
- Honghe, Z. Interaction mechanism in sol-gel transition of alginate solutions by addition of divalent cations. Carbohydr. Res. 1997, 302, 97–101. [Google Scholar] [CrossRef]
- Thien, D.V.H.; Hsiao, S.W.; Ho, M.H.; Li, C.H.; Shih, J.L. Electrospun chitosan/hydroxyapatite nanofibers for bone tissue engineering. J. Mater. Sci. 2013, 48, 1640–1645. [Google Scholar] [CrossRef]
- Tóth, M.; Gergely, G.; Lukács, I.E.; Wéber, F.; Tóth, A.L.; Illés, L.; Balázsi, C. Production of polymer nanofibers containing hydroxyapatite by electrospinning. Mater. Sci. Forum 2010, 659, 257–262. [Google Scholar] [CrossRef]
- Wang, L.; Feng, H.L.; Mei, F.; Hu, X.Y.; Deng, X.L.; Yang, X.P.; Tang, J.M.; Wang, X.Z. Observation of human periodontal ligament cells cultured on electrospun PLLA/HA biomaterial. Acta Anatom. Sin. 2008, 4, 573–577. [Google Scholar]
- Lao, L.; Wang, Y.; Zhu, Y.; Zhang, Y.; Gao, C. Poly(lactide-co-glycolide)/hydroxyapatite nanofibrous scaffolds fabricated by electrospinning for bone tissue engineering. J. Mater. Sci. Mater. Med. 2011, 22, 1873–1884. [Google Scholar] [CrossRef] [PubMed]
- Doustgani, A.; Vasheghani-Farahani, E.; Soleimani, M.; Hashemi-Najafabadi, S. Process optimization of electrospun polycaprolactone and nanohydroxyapatite composite nanofibers using response surface methodology. J. Nanosci. Nanotechnol. 2013, 13, 4708–4714. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.C.; Choi, H.W.; Lee, H.J.; Kim, K.J.; Chany, J.H.; Kim, S.Y.; Choi, J.; Oh, K.S.; Jeong, Y.K. In-situ synthesis of reactive hydroxyapatite nano-crystals for a novel approach of surface grafting polymerization. J. Mater. Chem. 2007, 17, 174–180. [Google Scholar] [CrossRef]
- Li, H.Y.; Chen, Y.F.; Xie, Y.S. Nanocomposites of cross-linking polyanhydrides and hydroxyapatite needles: Mechanical and degradable properties. Mater. Lett. 2004, 58, 2819–2823. [Google Scholar] [CrossRef]
- Song, J.H.; Kim, H.E.; Kim, H.W. Electrospun fibrous web of collagen-apatite precipitated nanocomposite for bone regeneration. J. Mater. Sci. Mater. Med. 2008, 19, 2925–2932. [Google Scholar] [CrossRef] [PubMed]
- Kikuchi, M.; Itoh, S.; Ichinose, S.; Shinomiya, K.; Tanaka, J. Self-organization mechanism in a bone-like hydroxyapatite/collagen nanocomposite synthesized in vitro and its biological reaction in vivo. Biomaterials 2001, 22, 1705–1711. [Google Scholar] [CrossRef]
- Kikuchi, M.; Ikoma, T.; Itoh, S.; Matsumoto, H.N.; Koyama, Y.; Takakuda, K.; Shinomiya, K.; Tanaka, J. Biomimetic synthesis of bone-like nanocomposites using the self-organization mechanism of hydroxyapatite and collagen. Compos. Sci. Technol. 2004, 64, 819–825. [Google Scholar] [CrossRef]
- Prajapati, S.; Tao, J.; Ruan, Q.; De Yoreo, J.J.; Moradian-Oldak, J. Matrix metalloproteinase-20 mediates dental enamel biomineralization by preventing protein occlusion inside apatite crystals. Biomaterials 2016, 75, 260–270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, K.; Zhang, Z.; Li, D.; Zhang, W.; Yu, X.; Liu, W.; Gong, C.; Wei, G.; Su, Z. Biomimetic ultralight, highly porous, shape-adjustable, and biocompatible 3D graphene minerals via incorporation of self-assembled peptide nanosheets. Adv. Funct. Mater. 2018, 28, 1801056. [Google Scholar] [CrossRef]
- Takeuchi, A.; Ohtsuki, C.; Miyazaki, T.; Tanaka, H.; Yamazaki, M.; Tanihara, M. Deposition of bone-like apatite on silk fiber in a solution that mimics extracellular fluid. J. Biomed. Mater. Res. A 2003, 65, 283–289. [Google Scholar] [CrossRef] [PubMed]
- Wei, G.; Reichert, J.; Bossert, J.; Jandt, K.D. Novel biopolymeric template for the nucleation and growth of hydroxyapatite crystals based on self-assembled fibrinogen fibrils. Biomacromolecules 2008, 9, 3258–3267. [Google Scholar] [CrossRef] [PubMed]
- Nonoyama, T.; Ogasawara, H.; Tanaka, M.; Higuchi, M.; Kinoshita, T. Calcium phosphate biomineralization in peptide hydrogels for injectable bone-filling materials. Soft Matter 2012, 8, 11531–11536. [Google Scholar] [CrossRef]
- Ceylan, H.; Kocabey, H.; Gulsuner, U.; Balcik, O.S.; Guler, M.O.; Tekinay, A.B. Bone-like mineral nucleating peptide nanofibers induce differentiation of human mesenchymal stem cells into mature osteoblasts. Biomacromolecules 2014, 15, 2407–2418. [Google Scholar] [CrossRef] [PubMed]
- Eren, E.D.; Tansik, G.; Tekinay, A.B.; Guler, M.O. Mineralized peptide nanofiber gels for enhanced osteogenic differentiation. Chemnanomat 2018, 4, 837–845. [Google Scholar] [CrossRef]
- Sargeant, T.D.; Aparicio, C.; Goldberger, J.E.; Cui, H.; Stupp, S.I. Mineralization of peptide amphiphile nanofibers and its effect on the differentiation of human mesenchymal stem cells. Acta Biomater. 2012, 8, 2456–2465. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anderson, J.M.; Patterson, J.L.; Vines, J.B.; Javed, A.; Gilbert, S.R.; Jun, H.W. Biphasic peptide amphiphile nanomatrix embedded with hydroxyapatite nanoparticles for stimulated osteoinductive response. ACS Nano 2011, 5, 9463–9479. [Google Scholar] [CrossRef] [PubMed]
- Ghosh, M.; Halperin-Sternfelds, M.; Grigoriants, I.; Lee, J.; Nam, K.T.; Adler-Abramovich, L. Arginine-presenting peptide hydrogels decorated with hydroxyapatite as biomimetic scaffold for bone reneration. Biomacromolecules 2017, 18, 3541–3550. [Google Scholar] [CrossRef] [PubMed]
- Temenoff, J.S.; Park, H.; Jabbari, E.; Sheffield, T.L.; LeBaron, R.G.; Ambrose, C.G.; Mikos, A.G. In vitro osteogenic differentiation of marrow stromal cells encapsulated in biodegradable hydrogels. J. Biomed. Mater. Res. Part A 2004, 70, 235–244. [Google Scholar] [CrossRef] [PubMed]
- Benoit, D.S.; Durney, A.R.; Anseth, K.S. The effect of heparin-functionalized PEG hydrogels on three-dimensional human mesenchymal stem cell osteogenic differentiation. Biomaterials 2007, 28, 66–77. [Google Scholar] [CrossRef] [PubMed]
- Yokoi, H.; Kinoshita, T.; Zhang, S. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc. Natl. Acad. Sci. USA 2005, 102, 8414–8419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Holmes, T.; de Lacalle, S.; Su, X.; Rich, A.; Zhang, S. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc. Natl. Acad. Sci. USA 2000, 97, 6728–6733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bakota, E.L.; Wang, Y.; Danesh, F.R.; Hartgerink, J.D. Injectable multidomain peptide nanofiber hydrogel as a delivery agent for stem cell secretome. Biomacromolecules 2011, 12, 1651–1657. [Google Scholar] [CrossRef] [PubMed]
- Kretsinger, J.K.; Haines, L.A.; Ozbas, B.; Pochan, D.J.; Schneider, J.P. Cytocompatibility of self-assembled beta-hairpin peptide hydrogel surfaces. Biomaterials 2005, 26, 5177–5186. [Google Scholar] [CrossRef] [PubMed]
- Nagai, Y.; Yokoi, H.; Kaihara, K.; Naruse, K. The mechanical stimulation of cells in 3D culture within a self-assembling peptide hydrogel. Biomaterials 2012, 33, 1044–1051. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jung, J.P.; Gasiorowski, J.Z.; Collier, J.H. Fibrillar peptide gels in biotechnology and biomedicine. Biopolymers 2009, 94, 49–59. [Google Scholar] [CrossRef] [PubMed]
- Mi, K.; Wang, G.; Liu, Z.; Feng, Z.; Huang, B.; Zhao, X. Influence of a self-assembling peptide, RADA16, compared with collagen I and matrigel on the malignant phenotype of human breast-cancer cells in 3D cultures and in vivo. Macromol. Biosci. 2009, 9, 437–443. [Google Scholar] [CrossRef] [PubMed]
- Semino, C.E. Self-assembling peptides: From bio-inspired materials to bone regeneration. J. Dent. Res. 2008, 87, 606–616. [Google Scholar] [CrossRef] [PubMed]
- Beniash, E.; Hartgerink, J.D.; Storrie, H.; Stendahl, J.C.; Stupp, S.I. Self-assembling peptide amphiphile nanofiber matrices for cell entrapment. Acta Biomater. 2005, 1, 387–397. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.M.; Kushwaha, M.; Tambralli, A.; Bellis, S.L.; Camata, R.P.; Jun, H.W. Osteogenic differentiation of human mesenchymal stem cells directed by extracellular matrix-mimicking ligands in a biomimetic self-assembled peptide amphiphile nanomatrix. Biomacromolecules 2009, 10, 2935–2944. [Google Scholar] [CrossRef] [PubMed]
- Andukuri, A.; Minor, W.P.; Kushwaha, M.; Anderson, J.M.; Jun, H.W. Effect of endothelium mimicking self-assembled nanomatrices on cell adhesion and spreading of human endothelial cells and smooth muscle cells. Nanomedicine 2010, 6, 289–297. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, J.K.; Anderson, J.; Jun, H.W.; Repka, M.A.; Jo, S. Self-assembling peptide amphiphile-based nanofiber gel for bioresponsive cisplatin delivery. Mol. Pharm. 2009, 6, 978–985. [Google Scholar] [CrossRef] [PubMed]
- Anderson, J.M.; Andukuri, A.; Lim, D.J.; Jun, H.W. Modulating the gelation properties of self-assembling peptide amphiphiles. ACS Nano 2009, 3, 3447–3454. [Google Scholar] [CrossRef] [PubMed]
- Amosi, N.; Zarzhitsky, S.; Gilsohn, E.; Salnikov, O.; Monsonego-Ornan, E.; Shahar, R.; Rapaport, H. Acidic peptide hydrogel scaffolds enhance calcium phosphate mineral turnover into bone tissue. Acta Biomater. 2012, 8, 2466–2475. [Google Scholar] [CrossRef] [PubMed]
- Green, H.; Ochbaum, G.; Gitelman-Povimonsky, A.; Bitton, R.; Rapaport, H. RGD-presenting peptides in amphiphilic and anionic-sheet hydrogels for improved interactions with cells. RSC Adv. 2018, 8, 10072–10080. [Google Scholar] [CrossRef]
- Gungormus, M.; Branco, M.; Fong, H.; Schneider, J.P.; Tamerler, C.; Sarikaya, M. Self assembled bi-functional peptide hydrogels with biomineralization-directing peptides. Biomaterials 2010, 31, 7266–7274. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.Y.; Choi, J.H.; Xu, Z.H. Microbial cell-surface display. Trends Biotechnol. 2003, 21, 45–52. [Google Scholar] [CrossRef]
- Sarikaya, M.; Tamerler, C.; Jen, A.K.; Schulten, K.; Baneyx, F. Molecular biomimetics: Nanotechnology through biology. Nat. Mater. 2003, 2, 577–585. [Google Scholar] [CrossRef] [PubMed]
- Sarikaya, M. Biomimetics: Materials fabrication through biology. Proc. Natl. Acad. Sci. USA 1999, 96, 14183–14185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sarikaya, M.; Tamerler, C.; Schwartz, D.T.; Baneyx, F.O. Materials assembly and formation using engineered polypeptides. Annu. Rev. Mater. Res. 2004, 34, 373–408. [Google Scholar] [CrossRef]
- Tamerler, C.; Khatayevich, D.; Gungormus, M.; Kacar, T.; Oren, E.E.; Hnilova, M.; Sarikaya, M. Molecular biomimetics: GEPI-based biological routes to technology. Biopolymers 2010, 94, 78–94. [Google Scholar] [CrossRef] [PubMed]
- Parisi-Amon, A.; Lo, D.D.; Montoro, D.T.; Dewi, R.E.; Longaker, M.T.; Heilshorn, S.C. Protein-nanoparticle hydrogels that self-assemble in response to peptide-based molecular recognition. ACS Biomater. Sci. Eng. 2017, 3, 750–756. [Google Scholar] [CrossRef]
- Zhang, L.; Chan, J.M.; Gu, F.X.; Rhee, J.W.; Wang, A.Z.; Radovic-Moreno, A.F.; Alexis, F.; Langer, R.; Farokhzad, O.C. Self-assembled lipid–polymer hybrid nanoparticles: A robust drug delivery platform. ACS Nano 2008, 2, 1696–1702. [Google Scholar] [CrossRef] [PubMed]
- Appel, E.A.; Tibbitt, M.W.; Greer, J.M.; Fenton, O.S.; Kreuels, K.; Anderson, D.G.; Langer, R. Exploiting electrostatic interactions in polymer-nanoparticle hydrogels. ACS Macro Lett. 2015, 4, 848–852. [Google Scholar] [CrossRef]
- McCarthy, H.O.; McCaffrey, J.; McCrudden, C.M.; Zholobenko, A.; Ali, A.A.; McBride, J.W.; Massey, A.S.; Pentlavalli, S.; Chen, K.H.; Cole, G.; et al. Development and characterization of self-assembling nanoparticles using a bio-inspired amphipathic peptide for gene delivery. J. Control. Release 2014, 189, 141–149. [Google Scholar] [CrossRef] [PubMed]
- Massey, A.S.; Pentlavalli, S.; Cunningham, R.; McCrudden, C.M.; McErlean, E.M.; Redpathhlam, P.; Ali, A.A.; Annett, S.; McBride, J.W.; McCaffrey, J.; et al. Potentiating the anticancer properties of bisphosphonates by nanocomplexation with the cationic amphipathic peptide, RALA. Mol. Pharm. 2016, 13, 1217–1228. [Google Scholar] [CrossRef] [PubMed]
- Ibrahim, T.; Mercatali, L.; Sacanna, E.; Tesei, A.; Carloni, S.; Ulivi, P.; Liverani, C.; Fabbri, F.; Zanoni, M.; Zoli, W.; Amadori, D. Inhibition of breast cancer cell proliferation in repeated and non-repeated treatment with zoledronic acid. Cancer Cell Int. 2012, 12, 48–60. [Google Scholar] [CrossRef] [PubMed]
- Mani, J.; Vallo, S.; Barth, K.; Makarevic, J.; Juengel, E.; Bartsch, G.; Wiesner, C.; Haferkamp, A.; Blaheta, R.A. Zoledronic acid influences growth, migration and invasive activity of prostate cancer cells in vitro. Prostate Cancer Prostatic Dis. 2012, 15, 250–255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murphy, C.M.; O’Brien, F.J.; Little, D.G.; Schindeler, A. Cell-scaffold interactions in the bone tissue engineering triad. Eur. Cell Mater 2013, 26, 120–132. [Google Scholar] [CrossRef] [PubMed]
- Tsukamoto, J.; Naruse, K.; Nagai, Y.; Kan, S.; Nakamura, N.; Hata, M.; Omi, M.; Hayashi, T.; Kawai, T.; Matsubara, T. Efficacy of a self-assembling peptide hydrogel, SPG-178-gel, for bone regeneration and three-dimensional osteogenic induction of dental pulp stem cells. Tissue Eng. Part A 2017, 23, 1394–1402. [Google Scholar] [CrossRef] [PubMed]
- Pittenger, M.F.; Mackay, A.M.; Beck, S.C.; Jaiswal, R.K.; Douglas, R.; Mosca, J.D.; Moorman, M.A.; Simonetti, D.W.; Craig, S.; Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284, 143–147. [Google Scholar] [CrossRef] [PubMed]
- Wu, G.; Pan, M.; Wang, X.; Wen, J.; Cao, S.; Li, Z.; Li, Y.; Qian, C.; Liu, Z.; Wu, W.; et al. Osteogenesis of peripheral blood mesenchymal stem cells in self assembling peptide nanofiber for healing critical size calvarial bony defect. Sci. Rep. 2015, 5, 16681. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stenderup, K.; Justesen, J.; Clausen, C.; Kassem, M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003, 33, 919–926. [Google Scholar] [CrossRef] [PubMed]
- Gronthos, S.; Brahim, J.; Li, W.; Fisher, L.W.; Cherman, N.; Boyde, A.; DenBesten, P.; Robey, P.G.; Shi, S. Stem cell properties of human dental pulp stem cells. J. Dent. Res. 2002, 81, 531–535. [Google Scholar] [CrossRef] [PubMed]
- Mankani, M.H.; Afghani, S.; Franco, J.; Launey, M.; Marshall, S.; Marshall, G.W.; Nissenson, R.; Lee, J.; Tomsia, A.P.; Saiz, E. Lamellar spacing in cuboid hydroxyapatite scaffolds regulates bone formation by human bone marrow stromal cells. Tissue Eng. Part A 2011, 17, 1615–1623. [Google Scholar] [CrossRef] [PubMed]
- Bokhari, M.A.; Akay, G.; Zhang, S.; Birch, M.A. The enhancement of osteoblast growth and differentiation in vitro on a peptide hydrogel—polyHIPE polymer hybrid material. Biomaterials 2005, 26, 5198–5208. [Google Scholar] [CrossRef] [PubMed]
- Botchwey, E.A.; Dupree, M.A.; Pollack, S.R.; Levine, E.M.; Laurencin, C.T. Tissue engineered bone: Measurement of nutrient transport in three dimensional matrices. J. Biomed. Mater. Res. A 2003, 67, 357–367. [Google Scholar] [CrossRef] [PubMed]
- Shea, L.D.; Smiley, E.; Bonadio, J.; Mooney, D.J. DNA delivery from polymer matrices for tissue engineering. Nat. Biotechnol. 1999, 17, 551–554. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Wu, G.; Cao, Y.; Liu, C.; Jin, Y.; Wang, Y.; Yang, L.; Guo, J.; Zhu, L. Self-assembling peptide and nHA/CTS composite scaffolds promote bone regeneration through increasing seed cell adhesion. Mater. Sci. Eng. C 2018, 93, 445–454. [Google Scholar] [CrossRef] [PubMed]
- Hamada, K.; Hirose, M.; Yamashita, T.; Ohgushi, H. Spatial distribution of mineralized bone matrix produced by marrow mesenchymal stem cells in self-assembling peptide hydrogel scaffold. J. Biomed. Mater. Res. A 2008, 84, 128–136. [Google Scholar] [CrossRef] [PubMed]
- Genové, E.; Shen, C.; Zhang, S.; Semino, C.E. The effect of functionalized self-assembling peptide scaffolds on human aortic endothelial cell function. Biomaterials 2005, 26, 3341–3351. [Google Scholar] [CrossRef] [PubMed]
- Semino, C.E.; Merok, J.R.; Crane, G.G.; Panagiotakos, G.; Zhang, S. Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 2003, 71, 262–270. [Google Scholar] [CrossRef] [PubMed]
- Shivachar, A. Chapter 8: Isolation and culturing of glial, neuronal and neural stem cell types encapsulated in biodegradable peptide hydrogel. In Topics in Tissue Engineering; Ashammakhi, N., Reis, R., Chiellini, F., Eds.; Biomaterials and Tissue Engineering Group: Oulu, Finland, 2008; Volume 4, pp. 1–22. Available online: https://www.oulu.fi/spareparts/ebook_topics_in_t_e_vol4/index.html (accessed on 10 December 2018).
- Guo, J.; Su, H.; Zeng, Y.; Liang, Y.X.; Wong, W.M.; Ellis-Behnke, R.G.; So, K.F.; Wu, W. Reknitting the injured spinal cord by self-assembling peptide nanofiber scaffold. Nanomedicine 2007, 3, 311–321. [Google Scholar] [CrossRef] [PubMed]
- Ando, K.; Imagama, S.; Kobayashi, K.; Ito, K.; Tsushima, M.; Morozumi, M.; Tanaka, S.; Machino, M.; Ota, K.; Nishida, K.; et al. Effects of a self-assembling peptide as a scaffold on bone formation in a defect. PLoS ONE 2018, 13, e0190833. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.C.; Yang, J.; Kopecek, J. Hybrid hydrogels self-assembled from graft copolymers containing complementary β-sheets as hydroxyapatite nucleation scaffolds. Biomaterials 2011, 32, 5341–5353. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mata, A.; Geng, Y.; Henrikson, K.J.; Aparicio, C.; Stock, S.R.; Satcher, R.L.; Stupp, S.I. Bone regeneration mediated by biomimetic mineralization of a nanofiber matrix. Biomaterials 2010, 31, 6004–6012. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jadlowiec, J.; Koch, H.; Zhang, X.; Campbell, P.G.; Seyedain, M.; Sfeir, C. Phosphophoryn regulates the gene expression and differentiation of NIH3T3, MC3T3-E1, and human mesenchymal stem cells via the integrin/MAPK signaling pathway. J. Biol. Chem. 2004, 279, 53323–53330. [Google Scholar] [CrossRef] [PubMed]
- Yusufoglu, Y.; Hu, Y.; Kanapathipillai, M.; Kramer, M.; Kalay, Y.E.; Thiyagarajan, P.; Akinc, M.; Schmidt-Rohr, K.; Mallapragada, S. Bioinspired synthesis of self-assembled calcium phosphate nanocomposites using block copolymer-peptide conjugates. J. Mater. Res. 2008, 23, 3196–3212. [Google Scholar] [CrossRef]
- Ng, M.H.; Duski, S.; Tan, K.K.; Yusof, M.R.; Low, K.C.; Rose, I.M.; Mohamed, Z.; Saim, A.B.; Idrus, R.B.H. Repair of segmental load-bearing bone defect by autologous mesenchymal stem cells and plasma-derived fibrin impregnated ceramic block results in early recovery of limb function. Biomed. Res. Int. 2014, 345910, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Nkenke, E.; Neukam, F.W. Autogenous bone harvesting and grafting in advanced jaw resorption: Morbidity, resorption and implant survival. Eur. J. Oral Implantol. 2014, 7, S203–S217. [Google Scholar] [PubMed]
- Gu, H.; Xiong, Z.; Yin, X.; Li, B.; Mei, N.; Li, G.; Wang, C. Bone regeneration in a rabbit ulna defect model: Use of allogeneic adipose-derived stem cells with low immunogenicity. Cell Tissue Res. 2014, 358, 453–464. [Google Scholar] [CrossRef] [PubMed]
- Laurencin, C.; Khan, Y.; El-Amin, S.F. Bone graft substitutes. Expert Rev. Med. Devices 2006, 3, 49–57. [Google Scholar] [CrossRef] [PubMed]
- Huang, Q.; Zou, Y.; Arno, M.C.; Chen, S.; Wang, T.; Gao, J.; Dove, A.P.; Du, J. Hydrogel scaffolds for differentiation of adipose-derived stem cells. Chem. Soc. Rev. 2017, 46, 6255–6275. [Google Scholar] [CrossRef] [PubMed]
- Dong, L.; Wang, S.J.; Zhao, X.R.; Zhu, Y.F.; Yu, J.K. 3D-printed poly(ε-caprolactone) scaffold integrated with cell-laden chitosan hydrogels for bone tissue engineering. Sci. Rep. 2017, 7, 13412. [Google Scholar] [CrossRef] [PubMed]
- Dehsorkhi, A.; Castelletto, V.; Hamley, I.W. Self-assembling amphiphilic peptides. J. Pept. Sci. 2014, 20, 453–467. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, H.; Cheng, Y.; Chen, J.; Chang, F.; Wang, J.; Ding, J.; Chen, X. Component effect of stem cell-loaded thermosensitive polypeptide hydrogels on cartilage repair. Acta Biomater. 2018, 73, 103–111. [Google Scholar] [CrossRef] [PubMed]
- Mohammadi, M.; Alibolandi, M.; Abnous, K.; Salmasi, Z.; Jaafari, M.R.; Ramezani, M. Fabrication of hybrid scaffold based on hydroxyapatite-biodegradable nanofibers incorporated with liposomal formulation of BMP-2 peptide for bone tissue engineering. Nanomedicine 2018, 14, 1987–1997. [Google Scholar] [CrossRef] [PubMed]
- Babitha, S.; Annamalai, M.; Dykas, M.M.; Saha, S.; Poddar, K.; Venugopal, J.R.; Ramakrishna, S.; Venkatesa, T.; Korrapati, P.S. Fabrication of a biomimetic Zein PDA nanofibrous scaffold impregnated with BMP-2 peptide conjugated TiO2 nanoparticle for bone tissue engineering. J. Tissue Eng. Regen. Med. 2018, 12, 991–1001. [Google Scholar] [CrossRef] [PubMed]
- Quan, C.; Zhang, Z.; Liang, P.; Zheng, J.; Wang, J.; Hou, Y.; Tang, Q. Bioactive gel self-assembled from phosphorylate biomimetic peptide: A potential scaffold for enhanced osteogenesis. Int. J. Biol. Macromol. 2019, 121, 1054–1060. [Google Scholar] [CrossRef] [PubMed]
- Hannig, M.; Hannig, C. Nanomaterials in preventive dentistry. Nat. Nanotechnol. 2010, 5, 565–569. [Google Scholar] [CrossRef] [PubMed]
- Elkassas, D.; Arafa, A. The innovative applications of therapeutic nanostructures in dentistry. Nanomedicine 2017, 13, 1543–1562. [Google Scholar] [CrossRef] [PubMed]
- Huang, Z.; Newcomb, C.J.; Bringas, P., Jr.; Stupp, S.I.; Snead, M.L. Biological synthesis of tooth enamel by an artificial matrix. Biomaterials 2010, 31, 9202–9211. [Google Scholar] [CrossRef] [PubMed]
- Paine, M.L.; White, S.N.; Luo, W.; Fong, H.; Sarikaya, M.; Snead, M.L. Regulated gene expression dictates enamel structure and tooth function. Matrix Biol. 2001, 20, 273–292. [Google Scholar] [CrossRef]
- Fincham, A.G.; Moradian-Oldak, J.; Diekwisch, T.G.; Lyaruu, D.M.; Wright, J.T.; Bringas, P., Jr.; Slavkin, H.C. Evidence for amelogenin “nanospheres” as functional components of secretory-stage enamel matrix. J. Struct. Biol. 1995, 115, 50–59. [Google Scholar] [CrossRef] [PubMed]
- Fukumoto, S.; Kiba, T.; Hall, B.; Iehara, N.; Nakamura, T.; Longenecker, G.; Krebsbach, P.H.; Nanci, A.; Kulkarni, A.B.; Yamada, Y. Ameloblastin is a cell adhesion molecule required for maintaining the differentiation state of ameloblasts. J. Cell Biol. 2004, 167, 973–983. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Simmer, J.P.; Hu, J.C. Expression, structure, and function of enamel proteinases. Connect Tissue Res. 2002, 43, 441–449. [Google Scholar] [CrossRef] [PubMed]
- Brunton, P.A.; Davis, R.P.; Burke, J.L.; Smith, A.; Aggeli, A.; Brookes, S.J.; Kirkham, J. Treatment of early caries lesions using biomimetic self-assembling peptides—A clinical safety trial. Br. Dent. J. 2013, 215, E1–E6. [Google Scholar] [CrossRef] [PubMed]
- Kirkham, J.; Firth, A.; Vemals, D.; Boden, N.; Robinson, C.; Shore, R.C.; Brookes, S.J.; Aggeli, A. Self-assembling peptide scaffolds promote enamel remineralization. J. Dent. Res. 2007, 86, 426–430. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, F.; Kurokawa, H.; Shibasaki, S.; Kawamoto, R.; Murayama, R.; Miyazaki, M. Ultrasonic assessment of the effects of self-assembling peptide scaffolds on preventing enamel demineralization. Acta Odontol. Scand. 2016, 74, 142–147. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Ning, T.; Cao, Y.; Zhang, W.; Mei, M.; Chu, C. A novel self-assembled oligopeptide amphiphile for biomimitic mineralization of enamel. BMC Biotechnol. 2014, 14, 32–43. [Google Scholar] [CrossRef] [PubMed]
- Aggeli, A.; Bell, M.; Boden, N.; Keen, J.N.; Knowles, P.F.; McLeish, T.C.B.; Pitkeathly, M.; Radford, S.E. Responsive gels formed by the spontaneous self-assembly of peptides into polymeric β-sheet tapes. Nature 1997, 386, 259–262. [Google Scholar] [CrossRef] [PubMed]
- Alkilzy, M.; Santamaria, R.M.; Schmoeckel, J.; Splieth, C.H. Treatment of carious lesions using self-assembling peptides. Adv. Dent. Res. 2018, 29, 42–47. [Google Scholar] [CrossRef] [PubMed]
- Romanelli, S.M.; Fath, K.R.; Phekoo, A.P.; Knoll, G.A.; Barnejee, I.A. Layer-by-layer assembly of peptide based bioorganic–inorganic hybrid scaffolds and their interactions with osteoblastic MC3T3-E1 cells. Mater. Sci. Eng. C 2015, 51, 316–328. [Google Scholar] [CrossRef] [PubMed]
- Simecek, J.W.; Diefenderfer, K.E.; Cohen, M.E. An evaluation of replacement rates for posterior resin-based composite and amalgam restorations in U.S. Navy and Marine Corps recruits. J. Am. Dent. Assoc. 2009, 140, 200–209. [Google Scholar] [CrossRef] [PubMed]
- Ye, Q.; Spencer, P.; Yuca, E.; Tamerler, C. Engineered peptide repairs adhesive-dentin interface. Macromol. Mater. Eng. 2017, 302, 1600487. [Google Scholar] [CrossRef] [PubMed]
- Wang, R.; Wang, Q.; Wang, X.; Tian, L.; Liu, H.; Zhao, M.; Peng, C.; Cai, Q.; Shi, Y. Enhancement of nano-hydroxyapatite bonding to dentin through a collagen/calcium dual-affinitive peptide for dentinal tubule occlusion. J. Biomater. Appl. 2014, 29, 268–277. [Google Scholar] [CrossRef] [PubMed]
- Lopez, A.D.; Mathers, C.D.; Ezzati, M.; Jamison, D.T.; Murray, C.J. Global and regional burden of disease and risk factors, 2001: Systematic analysis of population health data. Lancet 2006, 367, 1747–1757. [Google Scholar] [CrossRef]
- Katta, J.; Stapleton, T.; Ingham, E.; Jin, Z.; Fisher, J. The effect of glycosaminoglycan depletion on the friction and deformation of articular cartilage. Proc. Inst. Mech. Eng. H 2008, 222, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Khan, I.M.; Gilbert, S.J.; Singhrao, S.K.; Duance, V.C.; Archer, C.W. Cartilage integration: Evaluation of the reasons for failure of integration during cartilage repair. A review. Eur. Cell. Mater. 2008, 16, 26–39. [Google Scholar] [CrossRef] [PubMed]
- Davies, L.C.; Blain, E.J.; Caterson, B.; Duance, V.C. Chondroitin sulphate impedes the migration of a subpopulation of articular cartilage chondrocytes. Osteoarthritis Cartilage 2008, 16, 855–864. [Google Scholar] [CrossRef] [PubMed]
- Huey, D.J.; Hu, J.C.; Athanasiou, K.A. Unlike bone, cartilage regeneration remains elusive. Science 2012, 338, 917–921. [Google Scholar] [CrossRef] [PubMed]
- Nehrer, S.; Spector, M.; Minas, T. Histologic analysis of tissue after failed cartilage repair procedures. Clin. Orthop. Relat. Res. 1999, 365, 149–162. [Google Scholar] [CrossRef] [PubMed]
- Brown, W.E.; Huey, D.J.; Hu, J.C.; Athanasiou, K.A. Functional self-assembled neocartilage as part of a biphasic osteochondral construct. PLoS ONE 2018, 13, e0195261. [Google Scholar] [CrossRef] [PubMed]
- Roelofs, A.J.; Rocke, J.P.; De Bari, C. Cell-based approaches to joint surface repair: A research perspective. Osteoarthritis Cartilage 2013, 21, 892–900. [Google Scholar] [CrossRef] [PubMed]
- Johnstone, B.; Hering, T.M.; Caplan, A.I.; Goldberg, V.M.; Yoo, J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 1998, 238, 265–272. [Google Scholar] [CrossRef] [PubMed]
- Zhou, G.; Liu, W.; Cui, L.; Wang, X.; Liu, T.; Cao, Y. Repair of porcine articular osteochondral defects in non-weightbearing areas with autologous bone marrow stromal cells. Tissue Eng. 2006, 12, 3209–3221. [Google Scholar] [CrossRef] [PubMed]
- Kisiday, J.D.; Kopesky, P.W.; Evans, C.H.; Grodzinsky, A.J.; McIlwraith, C.W.; Frisbie, D.D. Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J. Orthop. Res. 2008, 26, 322–331. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kisiday, J.D.; Colbath, A.C.; Tangtrongsup, S. Effect of culture duration on chondrogenic preconditioning of equine bone marrow mesenchymal stem cells in self-assembling peptide hydrogel. J. Orthoped. Res. 2018. [CrossRef] [PubMed]
- Schuman, L.; Buma, P.; Versleyen, D.; de Man, B.; van der Kraan, P.M.; van den Berg, W.B.; Homminga, G.N. Chondrocyte behaviour within different types of collagen gel in vitro. Biomaterials 1995, 16, 809–814. [Google Scholar] [CrossRef]
- Häuselmann, H.J.; Fernandes, R.J.; Mok, S.S.; Schmid, T.M.; Block, J.A.; Aydelotte, M.B.; Kuettner, K.E.; Thonar, E.J. Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads. J. Cell Sci. 1994, 107, 17–27. [Google Scholar] [PubMed]
- Freed, L.E.; Marquis, J.C.; Nohria, A.; Emmanual, J.; Mikos, A.G.; Langer, R. Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J. Biomed. Mater. Res. 1993, 27, 11–23. [Google Scholar] [CrossRef] [PubMed]
- Bryant, S.J.; Anseth, K.S. The effects of scaffold thickness on tissue engineered cartilage in photocrosslinked poly(ethylene oxide) hydrogels. Biomaterials 2001, 22, 619–626. [Google Scholar] [CrossRef]
- Kisiday, J.; Jin, M.; Kurz, B.; Hung, H.; Semino, C.; Zhang, S.; Grodzinsky, A.J. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: Implications for cartilage tissue repair. Proc. Natl. Acad. Sci. USA 2002, 99, 9996–10001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barco, A.; Ingham, E.; Fisher, J.; Fermor, H.; Davies, R.P.W. On the design and efficacy assessment of self-assembling peptide-based hydrogel-glycosaminoglycan mixtures for potential repair of early stage cartilage degeneration. J. Pep. Sci. 2018, 24, e3114. [Google Scholar] [CrossRef] [PubMed]
© 2019 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 (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rivas, M.; del Valle, L.J.; Alemán, C.; Puiggalí, J. Peptide Self-Assembly into Hydrogels for Biomedical Applications Related to Hydroxyapatite. Gels 2019, 5, 14. https://doi.org/10.3390/gels5010014
Rivas M, del Valle LJ, Alemán C, Puiggalí J. Peptide Self-Assembly into Hydrogels for Biomedical Applications Related to Hydroxyapatite. Gels. 2019; 5(1):14. https://doi.org/10.3390/gels5010014
Chicago/Turabian StyleRivas, Manuel, Luís J. del Valle, Carlos Alemán, and Jordi Puiggalí. 2019. "Peptide Self-Assembly into Hydrogels for Biomedical Applications Related to Hydroxyapatite" Gels 5, no. 1: 14. https://doi.org/10.3390/gels5010014
APA StyleRivas, M., del Valle, L. J., Alemán, C., & Puiggalí, J. (2019). Peptide Self-Assembly into Hydrogels for Biomedical Applications Related to Hydroxyapatite. Gels, 5(1), 14. https://doi.org/10.3390/gels5010014