Tissue Engineering and Regenerative Medicine

Korean Tissue Engineering and Regenerative Medicine Society (한국조직공학·재생의학회)
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Collagen Scaffolds in Cartilage Tissue Engineering and Relevant Approaches for Future Development

  • Irawan, Vincent (Department of Materials Science and Engineering, Tokyo Institute of Technology) ;
  • Sung, Tzu-Cheng (Department of Chemical and Materials Engineering, National Central University) ;
  • Higuchi, Akon (Department of Chemical and Materials Engineering, National Central University) ;
  • Ikoma, Toshiyuki (Department of Materials Science and Engineering, Tokyo Institute of Technology)
  • Received : 2018.04.17
  • Accepted : 2018.06.15
  • Published : 2018.12.01
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Abstract

BACKGROUND: Cartilage tissue engineering (CTE) aims to obtain a structure mimicking native cartilage tissue through the combination of relevant cells, three-dimensional scaffolds, and extraneous signals. Implantation of 'matured' constructs is thus expected to provide solution for treating large injury of articular cartilage. Type I collagen is widely used as scaffolds for CTE products undergoing clinical trial, owing to its ubiquitous biocompatibility and vast clinical approval. However, the long-term performance of pure type I collagen scaffolds would suffer from its limited chondrogenic capacity and inferior mechanical properties. This paper aims to provide insights necessary for advancing type I collagen scaffolds in the CTE applications. METHODS: Initially, the interactions of type I/II collagen with CTE-relevant cells [i.e., articular chondrocytes (ACs) and mesenchymal stem cells (MSCs)] are discussed. Next, the physical features and chemical composition of the scaffolds crucial to support chondrogenic activities of AC and MSC are highlighted. Attempts to optimize the collagen scaffolds by blending with natural/synthetic polymers are described. Hybrid strategy in which collagen and structural polymers are combined in non-blending manner is detailed. RESULTS: Type I collagen is sufficient to support cellular activities of ACs and MSCs; however it shows limited chondrogenic performance than type II collagen. Nonetheless, type I collagen is the clinically feasible option since type II collagen shows arthritogenic potency. Physical features of scaffolds such as internal structure, pore size, stiffness, etc. are shown to be crucial in influencing the differentiation fate and secreting extracellular matrixes from ACs and MSCs. Collagen can be blended with native or synthetic polymer to improve the mechanical and bioactivities of final composites. However, the versatility of blending strategy is limited due to denaturation of type I collagen at harsh processing condition. Hybrid strategy is successful in maximizing bioactivity of collagen scaffolds and mechanical robustness of structural polymer. CONCLUSION: Considering the previous improvements of physical and compositional properties of collagen scaffolds and recent manufacturing developments of structural polymer, it is concluded that hybrid strategy is a promising approach to advance further collagen-based scaffolds in CTE.

Keywords

References

  1. Mankin HJ. The response of articular cartilage to mechanical injury. J Bone Joint Surg Am. 1982;64:460-6. https://doi.org/10.2106/00004623-198264030-00022
  2. Pearle AD, Warren RF, Rodeo SA. Basic science of articular cartilage and osteoarthritis. Clin Sports Med. 2005;24:1-12. https://doi.org/10.1016/j.csm.2004.08.007
  3. Hunziker EB. Articular cartilage repair: basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage. 2002;10:432-63. https://doi.org/10.1053/joca.2002.0801
  4. O'Driscoll SW. The healing and regeneration of articular cartilage. J Bone Joint Surg Am. 1998;80:1795-812. https://doi.org/10.2106/00004623-199812000-00011
  5. Camp CL, Stuart MJ, Krych AJ. Current concepts of articular cartilage restoration techniques in the knee. Sports Health. 2014;6:265-73. https://doi.org/10.1177/1941738113508917
  6. Armiento AR, Stoddart MJ, Alini M, Eglin D. Biomaterials for articular cartilage tissue engineering: learning from biology. Acta Biomater. 2018;65:1-20. https://doi.org/10.1016/j.actbio.2017.11.021
  7. Huang BJ, Hu JC, Athanasiou KA. Cell-based tissue engineering strategies used in the clinical repair of articular cartilage. Biomaterials. 2016;98:1-22. https://doi.org/10.1016/j.biomaterials.2016.04.018
  8. Cole BJ, D'Amato M. Autologous chondrocyte implantation. Oper Tech Orthop. 2001;11:115-31. https://doi.org/10.1016/S1048-6666(01)80021-5
  9. Brittberg M. Autologous chondrocyte implantation-technique and long-term follow-up. Injury. 2008;39 Suppl 1:S40-9.
  10. Benya PD, Shaffer JD. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell. 1982;30:215-24. https://doi.org/10.1016/0092-8674(82)90027-7
  11. Higuchi A, Kumar SS, Benelli G, Alarfaj AA, Munusamy MA, Umezawa A, et al. Stem cell therapies for reversing vision loss. Trends Biotechnol. 2017;35:1102-17. https://doi.org/10.1016/j.tibtech.2017.06.016
  12. Higuchi A, Ling QD, Ko YA, Chang Y, Umezawa A. Biomaterials for the feeder-free culture of human embryonic stem cells and induced pluripotent stem cells. Chem Rev. 2011;111:3021-35. https://doi.org/10.1021/cr1003612
  13. Somoza RA, Welter JF, Correa D, Caplan AI. Chondrogenic differentiation of mesenchymal stem cells: challenges and unfulfilled expectations. Tissue Eng Part B Rev. 2014;20:596-608. https://doi.org/10.1089/ten.teb.2013.0771
  14. Nehrer S, Breinan HA, Ramappa A, Shortkroff S, Young G, Minas T, et al. Canine chondrocytes seeded in type I and type II collagen implants investigated in vitro. J Biomed Mater Res. 1997;38:95-104. https://doi.org/10.1002/(SICI)1097-4636(199722)38:2<95::AID-JBM3>3.0.CO;2-B
  15. Shakibaei M, De Souza P, Merker HJ. Integrin expression and collagen type II implicated in maintenance of chondrocyte shape in monolayer culture: an immunomorphological study. Cell Biol Int. 1997;21:115-25. https://doi.org/10.1006/cbir.1996.0118
  16. van Susante JL, Buma P, van Osch GJ, Versleyen D, van der Kraan PM, van der Berg WB, et al. Culture of chondrocytes in alginate and collagen carrier gels. Acta Orthop Scand. 1995;66:549-56. https://doi.org/10.3109/17453679509002314
  17. Lu Z, Doulabi BZ, Huang C, Bank RA, Helder MN. Collagen type II enhances chondrogenesis in adipose tissue-derived stem cells by affecting cell shape. Tissue Eng Part A. 2010;16:81-90.
  18. Takahashi T, Ogasawara T, Asawa Y, Mori Y, Uchinuma E, Takato T, et al. Three-dimensional microenvironments retain chondrocyte phenotypes during proliferation culture. Tissue Eng. 2007;13:1583-92. https://doi.org/10.1089/ten.2006.0322
  19. Pieper JS, van der Kraan PM, Hafmans T, Kamp J, Buma P, van Susante JL, et al. Crosslinked type II collagen matrices: preparation, characterization, and potential for cartilage engineering. Biomaterials. 2002;23:3183-92. https://doi.org/10.1016/S0142-9612(02)00067-4
  20. Galois L, Hutasse S, Cortial D, Rousseau CF, Grossin L, Ronziere MC, et al. Bovine chondrocyte behaviour in three-dimensional type I collagen gel in terms of gel contraction, proliferation and gene expression. Biomaterials. 2006;27:79-90. https://doi.org/10.1016/j.biomaterials.2005.05.098
  21. Li WJ, Jiang YJ, Tuan RS. Chondrocyte phenotype in engineered fibrous matrix is regulated by fiber size. Tissue Eng. 2006;12:1775-85. https://doi.org/10.1089/ten.2006.12.1775
  22. Noriega SE, Hasanova GI, Schneider MJ, Larsen GF, Subramanian A. Effect of fiber diameter on the spreading, proliferation and differentiation of chondrocytes on electrospun chitosan matrices. Cells Tissues Organs. 2012;195:207-21. https://doi.org/10.1159/000325144
  23. Nehrer S, Breinan HA, Ramappa A, Young G, Shortkroff S, Louie LK, et al. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials. 1997;18:769-76. https://doi.org/10.1016/S0142-9612(97)00001-X
  24. Freyria AM, Ronziere MC, Cortial D, Galois L, Hartmann D, Herbage D, et al. Comparative phenotypic analysis of articular chondrocytes cultured within type I or type II collagen scaffolds. Tissue Eng Part A. 2009;15:1233-45. https://doi.org/10.1089/ten.tea.2008.0114
  25. Camper L, Hellman U, Lundgren-Akerlund E. Isolation, cloning, and sequence analysis of the integrin subunit alpha10, a beta1-associated collagen binding integrin expressed on chondrocytes. J Biol Chem. 1998;273:20383-9. https://doi.org/10.1074/jbc.273.32.20383
  26. Schuh E, Kramer J, Rohwedel J, Notbohm H, Muller R, Gutsmann T, et al. Effect of matrix elasticity on the maintenance of the chondrogenic phenotype. Tissue Eng Part A. 2010;16:1281-90. https://doi.org/10.1089/ten.tea.2009.0614
  27. Li X, Chen S, Li J, Wang X, Zhang J, Kawazoe N, et al. 3D culture of chondrocytes in gelatin hydrogels with different stiffness. Polymers (Basel). 2016;8:269. https://doi.org/10.3390/polym8080269
  28. Bates GP, Schor SL, Grant ME. A comparison of the effects of different substrata on chondrocyte morphology and the synthesis of collagen types IX and X. In Vitro Cell Dev Biol. 1987;23:374-80. https://doi.org/10.1007/BF02620995
  29. Duval E, Leclercq S, Elissalde JM, Demoor M, Galera P, Boumediene K. Hypoxia-inducible factor 1alpha inhibits the fibroblast-like markers type I and type III collagen during hypoxia-induced chondrocyte redifferentiation: hypoxia not only induces type II collagen and aggrecan, but it also inhibits type I and type III collagen in the hypoxia-inducible factor 1alpha-dependent redifferentiation of chondrocytes. Arthritis Rheum. 2009;60:3038-48. https://doi.org/10.1002/art.24851
  30. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T. Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol Bioeng. 2006;93:1152-63. https://doi.org/10.1002/bit.20828
  31. Murphy CM, Matsiko A, Haugh MG, Gleeson JP, O'Brien FJ. Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen-glycosaminoglycan scaffolds. J Mech Behav Biomed Mater. 2012;11:53-62. https://doi.org/10.1016/j.jmbbm.2011.11.009
  32. Higuchi A, Ling QD, Kumar SS, Chang Y, Alarfaj AA, Munusamy MA, et al. Physical cues of cell culture materials lead the direction of differentiation lineages of pluripotent stem cells. J Mater Chem B. 2015;3:8032-58. https://doi.org/10.1039/C5TB01276G
  33. Matsiko A, Gleeson JP, O'Brien FJ. Scaffold mean pore size influences mesenchymal stem cell chondrogenic differentiation and matrix deposition. Tissue Eng Part A. 2015;21:486-97. https://doi.org/10.1089/ten.tea.2013.0545
  34. Tamaddon M, Burrows M, Ferreira SA, Dazzi F, Apperley JF, Bradshaw A, et al. Monomeric, porous type II collagen scaffolds promote chondrogenic differentiation of human bone marrow mesenchymal stem cells in vitro. Sci Rep. 2017;7:43519. https://doi.org/10.1038/srep43519
  35. Matsiko A, Levingstone TJ, O'Brien FJ, Gleeson JP. Addition of hyaluronic acid improves cellular infiltration and promotes early-stage chondrogenesis in a collagen-based scaffold for cartilage tissue engineering. J Mech Behav Biomed Mater. 2012;11:41-52. https://doi.org/10.1016/j.jmbbm.2011.11.012
  36. Choi B, Kim S, Lin B, Wu BM, Lee M. Cartilaginous extracellular matrix-modified chitosan hydrogels for cartilage tissue engineering. ACS Appl Mater Interfaces. 2014;6:20110-21. https://doi.org/10.1021/am505723k
  37. Bian L, Hou C, Tous E, Rai R, Mauck RL, Burdick JA. The influence of hyaluronic acid hydrogel crosslinking density and macromolecular diffusivity on human MSC chondrogenesis and hypertrophy. Biomaterials. 2013;34:413-21. https://doi.org/10.1016/j.biomaterials.2012.09.052
  38. Varghese S, Hwang NS, Canver AC, Theprungsirikul P, Lin DW, Elisseeff J. Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol. 2008;27:12-21.
  39. Chen WC, Yao CL, Chu IM, Wei YH. Compare the effects of chondrogenesis by culture of human mesenchymal stem cells with various type of the chondroitin sulfate C. J Biosci Bioeng. 2011;111:226-31. https://doi.org/10.1016/j.jbiosc.2010.10.002
  40. Higuchi A, Ling QD, Hsu ST, Umezawa A. Biomimetic cell culture proteins as extracellular matrices for stem cell differentiation. Chem Rev. 2012;112:4507-40. https://doi.org/10.1021/cr3000169
  41. Albrecht C, Tichy B, Nurnberger S, Hosiner S, Zak L, Aldrian S, et al. Gene expression and cell differentiation in matrix-associated chondrocyte transplantation grafts: a comparative study. Osteoarthritis Cartilage. 2011;19:1219-27. https://doi.org/10.1016/j.joca.2011.07.004
  42. Zak L, Albrecht C, Wondrasch B, Widhalm H, Vekszler G, Trattnig S, et al. Results 2 years after matrix-associated autologous chondrocyte transplantation using the Novocart 3D scaffold. Am J Sports Med. 2014;42:1618-27. https://doi.org/10.1177/0363546514532337
  43. Saris D, Price A, Widuchowski W, Bertrand-Marchand M, Caron J, Drogset JO, et al. Matrix-applied characterized autologous cultured chondrocytes versus microfracture two-year follow-up of a prospective randomized trial. Am J Sports Med. 2014;42:1384-94. https://doi.org/10.1177/0363546514528093
  44. Petri M, Broese M, Simon A, Liodakis E, Ettinger M, Guenther D, et al. CaReS(MACT) versus microfracture in treating symptomatic patellofemoral cartilage defects: a retrospective matched-pair analysis. J Orthop Sci. 2013;18:38-44. https://doi.org/10.1007/s00776-012-0305-x
  45. Crawford DC, DeBerardino TM, Williams RJ 3rd. NeoCart, an autologous cartilage tissue implant, compared with microfracture for treatment of distal femoral cartilage lesions: an FDA phase-II prospective, randomized clinical trial after two years.. J Bone Joint Surg Am. 2012;94:979-89. https://doi.org/10.2106/JBJS.K.00533
  46. Ochi M, Uchio Y, Kawasaki K, Wakitani S, Iwasa J. Transplantation of cartilage-like tissue made by tissue engineering in the treatment of cartilage defects of the knee. J Bone Joint Surg Am. 2002;84:571-8. https://doi.org/10.1302/0301-620X.84B4.0840571
  47. Keselowsky BG, Collard DM, Garcia AJ. Surface chemistry modulates focal adhesion composition and signaling through changes in integrin binding. Biomaterials. 2004;25:5947-54. https://doi.org/10.1016/j.biomaterials.2004.01.062
  48. Salasznyk RM, Klees RF, Hughlock MK, Plopper GE. ERK signaling pathways regulate the osteogenic differentiation of human mesenchymal stem cells on collagen I and vitronectin. Cell Commun Adhes. 2004;11:137-53. https://doi.org/10.1080/15419060500242836
  49. Franceschi RT. The developmental control of osteoblast-specific gene expression: role of specific transcription factors and the extracellular matrix environment. Crit Rev Oral Biol Med. 1999;10:40-57. https://doi.org/10.1177/10454411990100010201
  50. Wallace DG, Rosenblatt J. Collagen gel systems for sustained delivery and tissue engineering. Adv Drug Deliv Rev. 2003;55:1631-49. https://doi.org/10.1016/j.addr.2003.08.004
  51. Gelse K, Poschl E, Aigner T. Collagens-structure, function, and biosynthesis. Adv Drug Deliv Rev. 2003;55:1531-46. https://doi.org/10.1016/j.addr.2003.08.002
  52. Tulla M, Pentikainen OT, Viitasalo T, Kapyla J, Impola U, Nykvist P, et al. Selective binding of collagen subtypes by integrin ${\alpha}1I$, ${\alpha}2I$, and a10I domains. J Biol Chem. 2001;276:48206-12. https://doi.org/10.1074/jbc.M104058200
  53. Hamaia SW, Luff D, Hunter EJ, Malcor JD, Bihan D, Gullberg D, et al. Unique charge-dependent constraint on collagen recognition by integrin ${\alpha}10{\beta}1$. Matrix Biol. 2017;59:80-94. https://doi.org/10.1016/j.matbio.2016.08.010
  54. Kino-Oka M, Yashiki S, Ota Y, Mushiaki Y, Sugawara K, Yamamoto T, et al. Subculture of chondrocytes on a collagen type I-coated substrate with suppressed cellular dedifferentiation. Tissue Eng. 2005;11:597-608. https://doi.org/10.1089/ten.2005.11.597
  55. Farjanel J, Schurmann G, Bruckner P. Contacts with fibrils containing collagen I, but not collagens II, IX, and XI, can destabilize the cartilage phenotype of chondrocytes. Osteoarthritis Cartilage. 2001;9:S55-63.
  56. Jin GZ, Kim HW. Effects of type I collagen concentration in hydrogel on the growth and phenotypic expression of rat chondrocytes. Tissue Eng Regen Med. 2017;14:383-91. https://doi.org/10.1007/s13770-017-0060-3
  57. Fertala A, Han WB, Ko FK. Mapping critical sites in collagen II for rational design of gene-engineered proteins for cell-supporting materials. J Biomed Mater Res. 2001;57:48-58. https://doi.org/10.1002/1097-4636(200110)57:1<48::AID-JBM1140>3.0.CO;2-S
  58. Lucic D, Mollenhauer J, Kilpatrick KE, Cole AA. N-telopeptide of type II collagen interacts with annexin V on human chondrocytes. Connect Tissue Res. 2003;44:225-39. https://doi.org/10.1080/03008200390248632
  59. Leitinger B, Steplewski A, Fertala A. The D2 period of collagen II contains a specific binding site for the human discoidin domain receptor, DDR2. J Mol Biol. 2004;344:993-1003. https://doi.org/10.1016/j.jmb.2004.09.089
  60. Bengtsson T, Aszodi A, Nicolae C, Hunziker EB, Lundgren- Akerlund E, Fassler R. Loss of alpha10beta1 integrin expression leads to moderate dysfunction of growth plate chondrocytes. J Cell Sci. 2005;118:929-36. https://doi.org/10.1242/jcs.01678
  61. von der Mark K, Mollenhauer J. Annexin V interactions with collagen. Cell Mol Life Sci. 1997;53:539-45. https://doi.org/10.1007/s000180050069
  62. Klatt AR, Paul-Klausch B, Klinger C, Kuhn C, Renno JH, Banerjee M, et al. A critical role for collagen II in cartilage matrix degradation: collagen II induces pro-inflammatory cytokines and MMPs in primary human chondrocytes. J Orthop Res. 2009;27:65-70. https://doi.org/10.1002/jor.20716
  63. Goldring MB. Chondrogenesis, chondrocyte differentiation, and articular cartilage metabolism in health and osteoarthritis. Ther Adv Musculoskelet Dis. 2012;4:269-85. https://doi.org/10.1177/1759720X12448454
  64. Gigante A, Bevilacqua C, Cappella M, Manzotti S, Greco F. Engineered articular cartilage: influence of the scaffold on cell phenotype and proliferation. J Mater Sci Mater Med. 2003;14:713-6. https://doi.org/10.1023/A:1024915817061
  65. Brodkin KR, Garcia AJ, Levenston ME. Chondrocyte phenotypes on different extracellular matrix monolayers. Biomaterials. 2004;25:5929-38. https://doi.org/10.1016/j.biomaterials.2004.01.044
  66. Ohno T, Tanisaka K, Hiraoka Y, Ushida T, Tamaki T, Tateishi T. Effect of type I and type II collagen sponges as 3D scaffolds for hyaline cartilage-like tissue regeneration on phenotypic control of seeded chondrocytes in vitro. Mater Sci Eng C Mater Biol Appl. 2004;24:407-11. https://doi.org/10.1016/j.msec.2003.11.011
  67. Hubka KM, Dahlin RL, Meretoja VV, Kasper FK, Mikos AG. Enhancing chondrogenic phenotype for cartilage tissue engineering: monoculture and coculture of articular chondrocytes and mesenchymal stem cells. Tissue Eng Part B Rev. 2014;20:641-54.
  68. Woltersdorf C, Bonk M, Leitinger B, Huhtala M, Kapyla J, Heino J, et al. The binding capacity of ${\alpha}1{\beta}1-$, ${\alpha}2{\beta}1-$ and ${\alpha}0{\beta}1-$ integrins depends on non-collagenous surface macromolecules rather than the collagens in cartilage fibrils. Matrix Biol. 2017;63:91-105. https://doi.org/10.1016/j.matbio.2017.02.001
  69. Noth U, Rackwitz L, Heymer A, Weber M, Baumann B, Steinert A, et al. Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels. J Biomed Mater Res A. 2007;83:626-35.
  70. Rutgers M, Saris DB, Vonk LA, van Rijen MH, Akrum V, Langeveld D, et al. Effect of collagen type I or type II on chondrogenesis by cultured human articular chondrocytes. Tissue Eng Part A. 2013;19:59-65. https://doi.org/10.1089/ten.tea.2011.0416
  71. Schedel J, Distler O, Woenckhaus M, Gay RE, Simmen B, Michel BA, et al. Discrepancy between mRNA and protein expression of tumour suppressor maspin in synovial tissue may contribute to synovial hyperplasia in rheumatoid arthritis. Ann Rheum Dis. 2004;63:1205-11. https://doi.org/10.1136/ard.2003.006312
  72. Lu ZF, Doulabi BZ, Wuisman PI, Bank RA, Helder MN. Influence of collagen type II and nucleus pulposus cells on aggregation and differentiation of adipose tissue-derived stem cells. J Cell Mol Med. 2008;12:2812-22. https://doi.org/10.1111/j.1582-4934.2008.00278.x
  73. Vincent I, Tomomei S, Toshiyuki I. Magnetite/hydroxyapatite composite particles-assisted pore alignment of tilapia fish scale collagen-based scaffold. Key Eng Mater. 2016;696:121-8. https://doi.org/10.4028/www.scientific.net/KEM.696.121
  74. Zhang J, Yang Z, Li C, Dou Y, Li Y, Thote T, et al. Cells behave distinctly within sponges and hydrogels due to differences of internal structure. Tissue Eng Part A. 2013;19:2166-75. https://doi.org/10.1089/ten.tea.2012.0393
  75. Nuernberger S, Cyran N, Albrecht C, Redl H, Vecsei V, Marlovits S. The influence of scaffold architecture on chondrocyte distribution and behavior in matrix-associated chondrocyte transplantation grafts. Biomaterials. 2011;32:1032-40. https://doi.org/10.1016/j.biomaterials.2010.08.100
  76. Wise JK, Yarin AL, Megaridis CM, Cho M. Chondrogenic differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superficial zone of articular cartilage. Tissue Eng Part A. 2009;15:913-21. https://doi.org/10.1089/ten.tea.2008.0109
  77. Matthews JA, Wnek GE, Simpson DG, Bowlin GL. Electrospinning of collagen nanofibers. Biomacromolecules. 2002;3:232-8. https://doi.org/10.1021/bm015533u
  78. Matthews JA, Boland ED, Wnek GE, Simpson DG, Bowlin GL. Electrospinning of collagen type II: a feasibility study. J Bioact Compat Polym. 2003;18:125-34. https://doi.org/10.1177/0883911503018002003
  79. Yunoki S, Ikoma T, Monkawa A, Ohta K, Kikuchi M, Sotome S, et al. Control of pore structure and mechanical property in hydroxyapatite/collagen composite using unidirectional ice growth. Mater Lett. 2006;60:999-1002. https://doi.org/10.1016/j.matlet.2005.10.064
  80. Ikoma T, Kobayashi H, Tanaka J, Walsh D, Mann S. Physical properties of type I collagen extracted from fish scales of Pagrus major and Oreochromis niloticas. Int J Biol Macromol. 2003;32:199-204. https://doi.org/10.1016/S0141-8130(03)00054-0
  81. Kawamata H, Kuwaki S, Mishina T, Ikoma T, Tanaka J, Nozaki R. Hierarchical viscosity of aqueous solution of tilapia scale collagen investigated via dielectric spectroscopy between 500 MHz and 2.5 THz. Sci Rep. 2017;7:45398. https://doi.org/10.1038/srep45398
  82. Yang YL, Motte S, Kaufman LJ. Pore size variable type I collagen gels and their interaction with glioma cells. Biomaterials. 2010;31:5678-88. https://doi.org/10.1016/j.biomaterials.2010.03.039
  83. Lee CR, Grodzinsky AJ, Spector M. The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials. 2001;22:3145-54. https://doi.org/10.1016/S0142-9612(01)00067-9
  84. Vickers SM, Squitieri LS, Spector M. Effects of cross-linking type II collagen-GAG scaffolds on chondrogenesis in vitro: dynamic pore reduction promotes cartilage formation. Tissue Eng. 2006;12:1345-55. https://doi.org/10.1089/ten.2006.12.1345
  85. Zhang J, Wu Y, Thote T, Lee EH, Ge Z, Yang Z. The influence of scaffold microstructure on chondrogenic differentiation of mesenchymal stem cells. Biomed Mater. 2014;9:035011. https://doi.org/10.1088/1748-6041/9/3/035011
  86. Miot S, Woodfield T, Daniels AU, Suetterlin R, Peterschmitt I, Heberer M, et al. Effects of scaffold composition and architecture on human nasal chondrocyte redifferentiation and cartilaginous matrix deposition. Biomaterials. 2005;26:2479-89. https://doi.org/10.1016/j.biomaterials.2004.06.048
  87. Chao PG, Yodmuang S, Wang X, Sun L, Kaplan DL, Vunjak- Novakovic G. Silk hydrogel for cartilage tissue engineering. J Biomed Mater Res B Appl Biomater. 2010;95:84-90.
  88. Lee P, Tran K, Chang W, Shelke NB, Kumbar SG, Yu X. Influence of chondroitin sulfate and hyaluronic acid presence in nanofibers and its alignment on the bone marrow stromal cells: cartilage regeneration. J Biomed Nanotechnol. 2014;10:1469-79. https://doi.org/10.1166/jbn.2014.1831
  89. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science. 2005;310:1139-43. https://doi.org/10.1126/science.1116995
  90. Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials. 2000;21:2529-43. https://doi.org/10.1016/S0142-9612(00)00121-6
  91. Lv H, Wang H, Zhang Z, Yang W, Liu W, Li Y, et al. Biomaterial stiffness determines stem cell fate. Life Sci. 2017;178:42-8. https://doi.org/10.1016/j.lfs.2017.04.014
  92. Koay EJ, Shieh AC, Athanasiou KA. Creep indentation of single cells. J Biomech Eng. 2003;125:334-41. https://doi.org/10.1115/1.1572517
  93. Freeman PM, Natarajan RN, Kimura JH, Andriacchi TP. Chondrocyte cells respond mechanically to compressive loads. J Orthop Res. 1994;12:311-20. https://doi.org/10.1002/jor.1100120303
  94. Sanz-Ramos P, Mora G, Vicente-Pascual M, Ochoa I, Alcaine C, Moreno R, et al. Response of sheep chondrocytes to changes in substrate stiffness from 2 to 20 Pa: effect of cell passaging. Connect Tissue Res. 2013;54:159-66. https://doi.org/10.3109/03008207.2012.762360
  95. Schuh E, Hofmann S, Stok K, Notbohm H, Mu ller R, Rotter N. Chondrocyte redifferentiation in 3D: the effect of adhesion site density and substrate elasticity. J Biomed Mater Res A. 2012;100:38-47.
  96. Skotak M, Noriega S, Larsen G, Subramanian A. Electrospun cross-linked gelatin fibers with controlled diameter: the effect of matrix stiffness on proliferative and biosynthetic activity of chondrocytes cultured in vitro. J Biomed Mater Res A. 2010;95:828-36.
  97. Li WJ, Cooper JA, Mauck RL, Tuan RS. Fabrication and characterization of six electrospun poly(a-hydroxy ester)-based fibrous scaffolds for tissue engineering applications. Acta Biomater. 2006;2:377-85. https://doi.org/10.1016/j.actbio.2006.02.005
  98. Park JS, Chu JS, Tsou AD, Diop R, Tang Z, Wang A, et al. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-${\beta}$. Biomaterials. 2011;32:3921-30. https://doi.org/10.1016/j.biomaterials.2011.02.019
  99. Woods A, Wang G, Beier F. RhoA/ROCK signaling regulates Sox9 expression and actin organization during chondrogenesis. J Biol Chem. 2005;280:11626-34. https://doi.org/10.1074/jbc.M409158200
  100. Li YY, Choy TH, Ho FC, Chan PB. Scaffold composition affects cytoskeleton organization, cell-matrix interaction and the cellular fate of human mesenchymal stem cells upon chondrogenic differentiation. Biomaterials. 2015;52:208-20. https://doi.org/10.1016/j.biomaterials.2015.02.037
  101. Liu SQ, Tian Q, Hedrick JL, Po Hui JH, Ee PL, Yang YY. Biomimetic hydrogels for chondrogenic differentiation of human mesenchymal stem cells to neocartilage. Biomaterials. 2010;31:7298-307. https://doi.org/10.1016/j.biomaterials.2010.06.001
  102. Nam J, Johnson J, Lannutti JJ, Agarwal S. Modulation of embryonic mesenchymal progenitor cell differentiation via control over pure mechanical modulus in electrospun nanofibers. Acta Biomater. 2011;7:1516-24. https://doi.org/10.1016/j.actbio.2010.11.022
  103. Toh WS, Lim TC, Kurisawa M, Spector M. Modulation of mesenchymal stem cell chondrogenesis in a tunable hyaluronic acid hydrogel microenvironment. Biomaterials. 2012;33:3835-45. https://doi.org/10.1016/j.biomaterials.2012.01.065
  104. Lv H, Li L, Sun M, Zhang Y, Chen L, Rong Y, et al. Mechanism of regulation of stem cell differentiation by matrix stiffness. Stem Cell Res Ther. 2015;6:103. https://doi.org/10.1186/s13287-015-0083-4
  105. Zhang Q, Lu H, Kawazoe N, Chen G. Pore size effect of collagen scaffolds on cartilage regeneration. Acta Biomater. 2014;10:2005-13. https://doi.org/10.1016/j.actbio.2013.12.042
  106. Griffon DJ, Sedighi MR, Schaeffer DV, Eurell JA, Johnson AL. Chitosan scaffolds: interconnective pore size and cartilage engineering. Acta Biomater. 2006;2:313-20. https://doi.org/10.1016/j.actbio.2005.12.007
  107. Nava MM, Draghi L, Giordano C, Pietrabissa R. The effect of scaffold pore size in cartilage tissue engineering. J Appl Biomater Funct Mater. 2016;14:e223-9.
  108. Lin S, Sangaj N, Razafiarison T, Zhang C, Varghese S. Influence of physical properties of biomaterials on cellular behavior. Pharm Res. 2011;28:1422-30. https://doi.org/10.1007/s11095-011-0378-9
  109. Bryant SJ, Anseth KS. Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels. J Biomed Mater Res. 2002;59:63-72. https://doi.org/10.1002/jbm.1217
  110. Zhao Y, Tan K, Zhou Y, Ye Z, Tan WS. A combinatorial variation in surface chemistry and pore size of three-dimensional porous poly(e-caprolactone) scaffolds modulates the behaviors of mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl. 2016;59:193-202. https://doi.org/10.1016/j.msec.2015.10.017
  111. Oh SH, Kim TH, Im GI, Lee JH. Investigation of pore size effect on chondrogenic differentiation of adipose stem cells using a pore size gradient scaffold. Biomacromolecules. 2010;11:1948-55. https://doi.org/10.1021/bm100199m
  112. Im GI, Ko JY, Lee JH. Chondrogenesis of adipose stem cells in a porous polymer scaffold: influence of the pore size. Cell Transplant. 2012;21:2397-405. https://doi.org/10.3727/096368912X638865
  113. Malladi P, Xu Y, Chiou M, Giaccia AJ, Longaker MT. Effect of reduced oxygen tension on chondrogenesis and osteogenesis in adipose-derived mesenchymal cells. Am J Physiol Cell Physiol. 2006;290:C1139-46. https://doi.org/10.1152/ajpcell.00415.2005
  114. Buxton AN, Zhu J, Marchant R, West JL, Yoo JU, Johnstone B. Design and characterization of poly(ethylene glycol) photopolymerizable semi-interpenetrating networks for chondrogenesis of human mesenchymal stem cells. Tissue Eng. 2007;13:2549-60. https://doi.org/10.1089/ten.2007.0075
  115. Shanmugasundaram S, Chaudhry H, Arinzeh TL. Microscale versus nanoscale scaffold architecture for mesenchymal stem cell chondrogenesis. Tissue Eng Part A. 2011;17:831-40. https://doi.org/10.1089/ten.tea.2010.0409
  116. Bean AC, Tuan RS. Fiber diameter and seeding density influence chondrogenic differentiation of mesenchymal stem cells seeded on electrospun poly(e-caprolactone) scaffolds. Biomed Mater. 2015;10:015018. https://doi.org/10.1088/1748-6041/10/1/015018
  117. Chen G, Ushida T, Tateishi T. Scaffold design for tissue engineering. Macromol Biosci. 2002;2:67-77. https://doi.org/10.1002/1616-5195(20020201)2:2<67::AID-MABI67>3.0.CO;2-F
  118. Chen CW, Tsai YH, Deng WP, Shih SN, Fang CL, Burch JG, et al. Type I and II collagen regulation of chondrogenic differentiation by mesenchymal progenitor cells. J Orthop Res. 2005;23:446-53. https://doi.org/10.1016/j.orthres.2004.09.002
  119. Bax DV, Davidenko N, Gullberg D, Hamaia SW, Farndale RW, Best SM, et al. Fundamental insight into the effect of carbodiimide crosslinking on cellular recognition of collagen-based scaffolds. Acta Biomater. 2017;49:218-34. https://doi.org/10.1016/j.actbio.2016.11.059
  120. Raghunath J, Rollo J, Sales KM, Butler PE, Seifalian AM. Biomaterials and scaffold design: key to tissue-engineering cartilage. Biotechnol Appl Biochem. 2007;46:73-84. https://doi.org/10.1042/BA20060134
  121. Hardy JG, Scheibel TR. Composite materials based on silk proteins. Prog Polym Sci. 2010;35:1093-115. https://doi.org/10.1016/j.progpolymsci.2010.04.005
  122. Altman GH, Diaz F, Jakuba C, Calabro T, Horan RL, Chen J, et al. Silk-based biomaterials. Biomaterials. 2003;24:401-16. https://doi.org/10.1016/S0142-9612(02)00353-8
  123. Yeo IS, Oh JE, Jeong L, Lee TS, Lee SJ, Park WH, et al. Collagen-based biomimetic nanofibrous scaffolds: preparation and characterization of collagen/silk fibroin bicomponent nanofibrous structures. Biomacromolecules. 2008;9:1106-16. https://doi.org/10.1021/bm700875a
  124. Meinel L, Hofmann S, Karageorgiou V, Zichner L, Langer R, Kaplan D, et al. Engineering cartilage-like tissue using human mesenchymal stem cells and silk protein scaffolds. Biotechnol Bioeng. 2004;88:379-91. https://doi.org/10.1002/bit.20252
  125. Wang J, Yang Q, Cheng N, Tao X, Zhang Z, Sun X, et al. Collagen/silk fibroin composite scaffold incorporated with PLGA microsphere for cartilage repair. Mater Sci Eng C Mater Biol Appl. 2016;61:705-11. https://doi.org/10.1016/j.msec.2015.12.097
  126. Wang J, Zhou W, Hu W, Zhou L, Wang S, Zhang S. Collagen/silk fibroin bi-template induced biomimetic bone-like substitutes. J Biomed Mater Res A. 2011;99:327-34.
  127. Chen L, Hu J, Ran J, Shen X, Tong H. Preparation and evaluation of collagen-silk fibroin/hydroxyapatite nanocomposites for bone tissue engineering. Int J Biol Macromol. 2014;65:1-7. https://doi.org/10.1016/j.ijbiomac.2014.01.003
  128. Lv Q, Feng Q, Hu K, Cui F. Three-dimensional fibroin/collagen scaffolds derived from aqueous solution and the use for HepG2 culture. Polymer (Guildf). 2005;46:12662-9. https://doi.org/10.1016/j.polymer.2005.10.137
  129. Chomchalao P, Pongcharoen S, Sutheerawattananonda M, Tiyaboonchai W. Fibroin and fibroin blended three-dimensional scaffolds for rat chondrocyte culture. Biomed Eng Online. 2013;12:28. https://doi.org/10.1186/1475-925X-12-28
  130. Sun K, Li H, Li R, Nian Z, Li D, Xu C. Silk fibroin/collagen and silk fibroin/chitosan blended three-dimensional scaffolds for tissue engineering. Eur J Orthop Surg Traumatol. 2015;25:243-9.
  131. Di Martino A, Sittinger M, Risbud MV. Chitosan: a versatile biopolymer for orthopaedic tissue-engineering. Biomaterials. 2005;26:5983-90. https://doi.org/10.1016/j.biomaterials.2005.03.016
  132. Suh JK, Matthew HW. Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: a review. Biomaterials. 2000;21:2589-98. https://doi.org/10.1016/S0142-9612(00)00126-5
  133. Chicatun F, Pedraza CE, Muja N, Ghezzi CE, McKee MD, Nazhat SN. Effect of chitosan incorporation and scaffold geometry on chondrocyte function in dense collagen type I hydrogels. Tissue Eng Part A. 2013;19:2553-64. https://doi.org/10.1089/ten.tea.2013.0114
  134. Yan J, Li X, Liu L, Wang F, Zhu TW, Zhang Q. Potential use of collagen-chitosan-hyaluronan tri-copolymer scaffold for cartilage tissue engineering. Artif Cells Blood Substit Immobil Biotechnol. 2006;34:27-39. https://doi.org/10.1080/10731190500430024
  135. Tan W, Krishnaraj R, Desai TA. Evaluation of nanostructured composite collagen-chitosan matrices for tissue engineering. Tissue Eng. 2001;7:203-10. https://doi.org/10.1089/107632701300062831
  136. Chen Z, Mo X, He C, Wang H. Intermolecular interactions in electrospun collagen-chitosan complex nanofibers. Carbohydr Polym. 2008;72:410-8. https://doi.org/10.1016/j.carbpol.2007.09.018
  137. Yan LP, Wang YJ, Ren L, Wu G, Caridade SG, Fan JB, et al. Genipin-cross-linked collagen/chitosan biomimetic scaffolds for articular cartilage tissue engineering applications. J Biomed Mater Res A. 2010;95:465-75.
  138. Haaparanta AM, Jarvinen E, Cengiz IF, Ella V, Kokkonen HT, Kiviranta I, et al. Preparation and characterization of collagen/PLA, chitosan/PLA, and collagen/chitosan/PLA hybrid scaffolds for cartilage tissue engineering. J Mater Sci Mater Med. 2014;25:1129-36. https://doi.org/10.1007/s10856-013-5129-5
  139. Raftery RM, Woods B, Marques ALP, Moreira-Silva J, Silva TH, Cryan SA, et al. Multifunctional biomaterials from the sea: assessing the effects of chitosan incorporation into collagen scaffolds on mechanical and biological functionality. Acta Biomater. 2016;43:160-9. https://doi.org/10.1016/j.actbio.2016.07.009
  140. Dai W, Kawazoe N, Lin X, Dong J, Chen G. The influence of structural design of PLGA/collagen hybrid scaffolds in cartilage tissue engineering. Biomaterials. 2010;31:2141-52. https://doi.org/10.1016/j.biomaterials.2009.11.070
  141. Aspberg A. Cartilage proteoglycans. In: Grassel S, Aszodi A, editors. Cartilage. Springer; 2016. p. 1-22.
  142. Knudson W, Loeser RF. CD44 and integrin matrix receptors participate in cartilage homeostasis. Cell Mol Life Sci. 2002;59:36-44. https://doi.org/10.1007/s00018-002-8403-0
  143. Mahmood TA, Miot S, Frank O, Martin I, Riesle J, Langer R, et al. Modulation of chondrocyte phenotype for tissue engineering by designing the biologic-polymer carrier interface. Biomacromolecules. 2006;7:3012-8. https://doi.org/10.1021/bm060489+
  144. Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M. Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels. J Cell Physiol. 1999;179:142-8. https://doi.org/10.1002/(SICI)1097-4652(199905)179:2<142::AID-JCP4>3.0.CO;2-Q
  145. Zhang L, Li K, Xiao W, Zheng L, Xiao Y, Fan H, et al. Preparation of collagen-chondroitin sulfate-hyaluronic acid hybrid hydrogel scaffolds and cell compatibility in vitro. Carbohydr Polym. 2011;84:118-25. https://doi.org/10.1016/j.carbpol.2010.11.009
  146. van Susante JLC, Pieper J, Buma P, van Kuppevelt TH, van Beuningen H, van Der Kraan PM, et al. Linkage of chondroitinsulfate to type I collagen scaffolds stimulates the bioactivity of seeded chondrocytes in vitro. Biomaterials. 2001;22:2359-69. https://doi.org/10.1016/S0142-9612(00)00423-3
  147. Ko CS, Huang JP, Huang CW, Chu IM. Type II collagen-chondroitin sulfate-hyaluronan scaffold cross-linked by genipin for cartilage tissue engineering. J Biosci Bioeng. 2009;107:177-82. https://doi.org/10.1016/j.jbiosc.2008.09.020
  148. Zhu H, Mitsuhashi N, Klein A, Barsky LW, Weinberg K, Barr ML, et al. The role of the hyaluronan receptor CD44 in mesenchymal stem cell migration in the extracellular matrix. Stem Cells. 2006;24:928-35. https://doi.org/10.1634/stemcells.2005-0186
  149. Allemann F, Mizuno S, Eid K, Yates KE, Zaleske D, Glowacki J. Effects of hyaluronan on engineered articular cartilage extracellular matrix gene expression in 3-dimensional collagen scaffolds. J Biomed Mater Res. 2001;55:13-9. https://doi.org/10.1002/1097-4636(200104)55:1<13::AID-JBM20>3.0.CO;2-G
  150. Taguchi T, Ikoma T, Tanaka J. An improved method to prepare hyaluronic acid and type II collagen composite matrices. J Biomed Mater Res. 2002;61:330-6. https://doi.org/10.1002/jbm.10147
  151. Liao E, Yaszemski M, Krebsbach P, Hollister S. Tissue-engineered cartilage constructs using composite hyaluronic acid/collagen I hydrogels and designed poly(propylene fumarate) scaffolds. Tissue Eng. 2007;13:537-50. https://doi.org/10.1089/ten.2006.0117
  152. Nishimoto S, Takagi M, Wakitani S, Nihira T, Yoshida T. Effect of chondroitin sulfate and hyaluronic acid on gene expression in a three-dimensional culture of chondrocytes. J Biosci Bioeng. 2005;100:123-6. https://doi.org/10.1263/jbb.100.123
  153. Vazquez-Portalatin N, Kilmer CE, Panitch A, Liu JC. Characterization of collagen type I and II blended hydrogels for articular cartilage tissue engineering. Biomacromolecules. 2016;17:3145-52. https://doi.org/10.1021/acs.biomac.6b00684
  154. Guo Y, Yuan T, Xiao Z, Tang P, Xiao Y, Fan Y, et al. Hydrogels of collagen/chondroitin sulfate/hyaluronan interpenetrating polymer network for cartilage tissue engineering. J Mater Sci Mater Med. 2012;23:2267-79. https://doi.org/10.1007/s10856-012-4684-5
  155. Li X, Teng Y, Liu J, Lin H, Fan Y, Zhang X. Chondrogenic differentiation of BMSCs encapsulated in chondroinductive polysaccharide/collagen hybrid hydrogels. J Mater Chem B. 2017;5:5109-19. https://doi.org/10.1039/C7TB01020F
  156. Sionkowska A. Current research on the blends of natural and synthetic polymers as new biomaterials: review. Prog Polym Sci. 2011;36:1254-76. https://doi.org/10.1016/j.progpolymsci.2011.05.003
  157. Mehrasa M, Anarkoli AO, Rafienia M, Ghasemi N, Davary N, Bonakdar S, et al. Incorporation of zeolite and silica nanoparticles into electrospun PVA/collagen nanofibrous scaffolds: the influence on the physical, chemical properties and cell behavior. Int J Polym Mater. 2016;65:457-65. https://doi.org/10.1080/00914037.2015.1129958
  158. Lin HY, Tsai WC, Chang SH. Collagen-PVA aligned nanofiber on collagen sponge as bi-layered scaffold for surface cartilage repair. J Biomater Sci Polym Ed. 2017;28:664-78. https://doi.org/10.1080/09205063.2017.1295507
  159. Mansur HS, Sadahira CM, Souza AN, Mansur AAP. FTIR spectroscopy characterization of poly (vinyl alcohol) hydrogel with different hydrolysis degree and chemically crosslinked with glutaraldehyde. Mater Sci Eng C Mater Biol Appl. 2008;28:539-48. https://doi.org/10.1016/j.msec.2007.10.088
  160. Wan WK, Campbell G, Zhang ZF, Hui AJ, Boughner DR. Optimizing the tensile properties of polyvinyl alcohol hydrogel for the construction of a bioprosthetic heart valve stent. J Biomed Mater Res. 2002;63:854-61. https://doi.org/10.1002/jbm.10333
  161. Yousefi AM, Hoque ME, Prasad RGSV, Uth N. Current strategies in multiphasic scaffold design for osteochondral tissue engineering: a review. J Biomed Mater Res A. 2015;103:2460-81. https://doi.org/10.1002/jbm.a.35356
  162. Ohyabu Y, Adegawa T, Yoshioka T, Ikoma T, Shinozaki K, Uemura T, et al. A collagen sponge incorporating a hydroxyapatite/chondroitinsulfate composite as a scaffold for cartilage tissue engineering. J Biomater Sci Polym Ed. 2009;20:1861-74. https://doi.org/10.1163/156856208X386462
  163. Ohyabu Y, Adegawa T, Yoshioka T, Ikoma T, Uemura T, Tanaka J. Cartilage regeneration using a porous scaffold, a collagen sponge incorporating a hydroxyapatite/chondroitinsulfate composite. Mater Sci Eng B Solid State Mater Adv Technol. 2010;173:204-7. https://doi.org/10.1016/j.mseb.2009.12.008
  164. Chen S, Zhang Q, Kawazoe N, Chen G. Effect of high molecular weight hyaluronic acid on chondrocytes cultured in collagen/hyaluronic acid porous scaffolds. RSC Adv. 2015;5:94405-10. https://doi.org/10.1039/C5RA18755A
  165. Kreger ST, Voytik-Harbin SL. Hyaluronan concentration within a 3D collagen matrix modulates matrix viscoelasticity, but not fibroblast response. Matrix Biol. 2009;28:336-46. https://doi.org/10.1016/j.matbio.2009.05.001
  166. Jia L, Duan Z, Fan D, Mi Y, Hui J, Chang L. Human-like collagen/nano-hydroxyapatite scaffolds for the culture of chondrocytes. Mater Sci Eng C Mater Biol Appl. 2013;33:727-34. https://doi.org/10.1016/j.msec.2012.10.025
  167. Szczesny SE, Aeppli C, David A, Mauck RL. Fatigue loading of tendon results in collagen kinking and denaturation but does not change local tissue mechanics. J Biomech. 2018;71:251-6. https://doi.org/10.1016/j.jbiomech.2018.02.014
  168. Nakada A, Shigeno K, Sato T, Hatayama T, Wakatsuki M, Nakamura T. Optimal dehydrothermal processing conditions to improve biocompatibility and durability of a weakly denatured collagen scaffold. J Biomed Mater Res B Appl Biomater. 2017;105:2301-7. https://doi.org/10.1002/jbm.b.33766
  169. Zeugolis DI, Khew ST, Yew ES, Ekaputra AK, Tong YW, Yung LY, et al. Electro-spinning of pure collagen nano-fibres-just an expensive way to make gelatin? Biomaterials. 2008;29:2293-305. https://doi.org/10.1016/j.biomaterials.2008.02.009
  170. Grover CN, Cameron RE, Best SM. Investigating the morphological, mechanical and degradation properties of scaffolds comprising collagen, gelatin and elastin for use in soft tissue engineering. J Mech Behav Biomed Mater. 2012;10:62-74. https://doi.org/10.1016/j.jmbbm.2012.02.028
  171. Tuckwell DS, Ayad S, Grant ME, Takigawa M, Humphries MJ. Conformation dependence of integrin-type II collagen binding. Inability of collagen peptides to support alpha 2 beta 1 binding, and mediation of adhesion to denatured collagen by a novel alpha 5 beta 1-fibronectin bridge. J Cell Sci. 1994;107:993-1005.
  172. Lv Q, Hu K, Feng Q, Cui F. Fibroin/collagen hybrid hydrogels with crosslinking method: preparation, properties, and cytocompatibility. J Biomed Mater Res A. 2008;84:198-207.
  173. Sensini A, Gualandi C, Cristofolini L, Tozzi G, Dicarlo M, Teti G, et al. Biofabrication of bundles of poly (lactic acid)-collagen blends mimicking the fascicles of the human Achille tendon. Biofabrication. 2017;9:015025. https://doi.org/10.1088/1758-5090/aa6204
  174. Maisani M, Ziane S, Ehret C, Levesque L, Siadous R, Le Meins JF, et al. A new composite hydrogel combining the biological properties of collagen with the mechanical properties of a supramolecular scaffold for bone tissue engineering. J Tissue Eng Regen Med. 2018;12:e1489-500. https://doi.org/10.1002/term.2569
  175. Klumpp D, Rudisile M, Kuhnle RI, Hess A, Bitto FF, Arkudas A, et al. Three-dimensional vascularization of electrospun PCL/collagen-blend nanofibrous scaffolds in vivo. J Biomed Mater Res A. 2012;100:2302-11.
  176. Prabhakaran MP, Venugopal J, Ramakrishna S. Electrospun nanostructured scaffolds for bone tissue engineering. Acta Biomater. 2009;5:2884-93. https://doi.org/10.1016/j.actbio.2009.05.007
  177. Chen G, Sato T, Ushida T, Hirochika R, Shirasaki Y, Ochiai N, et al. The use of a novel PLGA fiber/collagen composite web as a scaffold for engineering of articular cartilage tissue with adjustable thickness. J Biomed Mater Res A. 2003;67:1170-80.
  178. Yen HJ, Tseng CS, Hsu SH, Tsai CL. Evaluation of chondrocyte growth in the highly porous scaffolds made by fused deposition manufacturing (FDM) filled with type II collagen. Biomed Microdevices. 2009;11:615-24. https://doi.org/10.1007/s10544-008-9271-7
  179. Reboredo JW, Weigel T, Steinert A, Rackwitz L, Rudert M, Walles H. Investigation of migration and differentiation of human mesenchymal stem cells on five-layered collagenous electrospun scaffold mimicking native cartilage structure. Adv Healthc Mater. 2016;5:2191-8. https://doi.org/10.1002/adhm.201600134
  180. Chen G, Sato T, Ushida T, Hirochika R, Tateishi T. Redifferentiation of dedifferentiated bovine chondrocytes when cultured in vitro in a PLGA-collagen hybrid mesh. FEBS Lett. 2003;542:95-9. https://doi.org/10.1016/S0014-5793(03)00354-5
  181. Chen CH, Shyu VB, Chen JP, Lee MY. Selective laser sintered poly-e-caprolactone scaffold hybridized with collagen hydrogel for cartilage tissue engineering. Biofabrication. 2014;6:015004. https://doi.org/10.1088/1758-5082/6/1/015004
  182. Tanaka Y, Yamaoka H, Nishizawa S, Nagata S, Ogasawara T, Asawa Y, et al. The optimization of porous polymeric scaffolds for chondrocyte/atelocollagen based tissue-engineered cartilage. Biomaterials. 2010;31:4506-16. https://doi.org/10.1016/j.biomaterials.2010.02.028
  183. Deponti D, Di Giancamillo A, Gervaso F, Domenicucci M, Domeneghini C, Sannino A, et al. Collagen scaffold for cartilage tissue engineering: the benefit of fibrin glue and the proper culture time in an infant cartilage model. Tissue Eng Part A. 2014;20:1113-26. https://doi.org/10.1089/ten.tea.2013.0171
  184. Xu T, Binder KW, Albanna MZ, Dice D, Zhao W, Yoo JJ, et al. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication. 2013;5:015001.

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  21. A Comparative Review of Natural and Synthetic Biopolymer Composite Scaffolds vol.13, pp.7, 2018, https://doi.org/10.3390/polym13071105
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  23. Decellularized sturgeon cartilage extracellular matrix scaffold inhibits chondrocyte hypertrophy in vitro and in vivo vol.15, pp.8, 2018, https://doi.org/10.1002/term.3222
  24. Biomaterial-Assisted Regenerative Medicine vol.22, pp.16, 2021, https://doi.org/10.3390/ijms22168657
  25. A Comparison of the Capacity of Mesenchymal Stromal Cells for Cartilage Regeneration Depending on Collagen-Based Injectable Biomimetic Scaffold Type vol.11, pp.8, 2018, https://doi.org/10.3390/life11080756
  26. Current Insights into Collagen Type I vol.13, pp.16, 2021, https://doi.org/10.3390/polym13162642
  27. Layer-specific stem cell differentiation in tri-layered tissue engineering biomaterials: Towards development of a single-stage cell-based approach for osteochondral defect repair vol.12, pp.None, 2018, https://doi.org/10.1016/j.mtbio.2021.100173
  28. Mechanotransducive Biomimetic Systems for Chondrogenic Differentiation In Vitro vol.22, pp.18, 2018, https://doi.org/10.3390/ijms22189690
  29. Optimization of extracellular matrix production from human induced pluripotent stem cell‐derived fibroblasts for scaffold fabrication for application in wound healing vol.109, pp.10, 2018, https://doi.org/10.1002/jbm.a.37173
  30. Immunoengineering the next generation of arthritis therapies vol.133, pp.None, 2021, https://doi.org/10.1016/j.actbio.2021.03.062
  31. Decellularized and biological scaffolds in dental and craniofacial tissue engineering: a comprehensive overview vol.15, pp.None, 2021, https://doi.org/10.1016/j.jmrt.2021.08.083
  32. 3D bioprinted silk fibroin hydrogels for tissue engineering vol.16, pp.12, 2018, https://doi.org/10.1038/s41596-021-00622-1
  33. In vivo biocompatibility evaluation of in situ-forming polyethylene glycol-collagen hydrogels in corneal defects vol.11, pp.1, 2018, https://doi.org/10.1038/s41598-021-03270-3
  34. Controlled Differentiation of Mesenchymal Stem Cells into Hyaline Cartilage in miR-140-Activated Collagen Hydrogel vol.13, pp.2, 2021, https://doi.org/10.1177/19476035211047627
  35. Combinations of Hydrogels and Mesenchymal Stromal Cells (MSCs) for Cartilage Tissue Engineering-A Review of the Literature vol.7, pp.4, 2021, https://doi.org/10.3390/gels7040217
  36. Childhood Cartilage ECM Enhances the Chondrogenesis of Endogenous Cells and Subchondral Bone Repair of the Unidirectional Collagen-dECM Scaffolds in Combination with Microfracture vol.13, pp.48, 2018, https://doi.org/10.1021/acsami.1c19447
  37. Biomaterial-mediated presentation of wnt5a mimetic ligands enhances chondrogenesis and metabolism of stem cells by activating non-canonical Wnt signaling vol.281, pp.None, 2022, https://doi.org/10.1016/j.biomaterials.2021.121316