Cartilage tissue engineering (CTE) provides a promising solution for osteoarthritis, with scaffold materials playing a crucial role in supporting cell activity. There have been many studies of various scaffold materials, yet few studies have directly compared the effects of marine collagen fibrils on chondrocyte chondrogenesis. This study determined the effects of types I and II collagen fibrils derived from sturgeon on ATDC5 cell chondrogenesis. The CCK-8 results showed that type I fibrils promoted ATDC5 cell proliferation more effectively than type II fibrils. Alcian Blue staining results revealed that cells cultured on type II fibrils secreted more proteoglycans than those on type I fibrils. The mRNA expression analysis indicated that type I fibrils initiated cell differentiation at an early stage, but simultaneously induced premature hypertrophy, suggesting that type I fibrils were difficult to maintain the chondrogenic phenotype in long-term culture. In contrast, type II fibrils generally enhanced the expression of chondrogenic genes, but also upregulated matrix metalloproteinase collagen-degrading enzymes, thereby accelerating the matrix degradation process. These findings suggested the potential of sturgeon collagen as a CTE scaffold material, and identified the different effects of types I and II collagen fibrils on ATDC5 cell chondrogenesis, to provide a theoretical foundation for selecting suitable scaffold biomaterials, based on different needs, while also providing new insights for the application of marine collagen.
Camarero-EspinosaSRothen-RutishauserBFosterEJ, et al.Articular cartilage: from formation to tissue engineering. Biomater Sci2016; 4: 734–767. https://doi.org/10.1039/c6bm00068a
Sophia FoxAJBediARodeoSA. The basic science of articular cartilage: structure, composition, and function. Sport Health2009; 1: 461–468. https://doi.org/10.1177/1941738109350438
6.
KohRHJinYKimJ, et al.Inflammation-modulating hydrogels for osteoarthritis cartilage tissue engineering. Cells2020; 9: 419. https://doi.org/10.3390/cells9020419
7.
HarrellCRMarkovicBSFellabaumC, et al.Mesenchymal stem cell-based therapy of osteoarthritis: current knowledge and future perspectives. Biomed Pharmacother2019; 109: 2318–2326. https://doi.org/10.1016/j.biopha.2018.11.099
8.
WasyłeczkoMSikorskaWChwojnowskiA. Review of synthetic and hybrid scaffolds in cartilage tissue engineering. Membranes2020; 10: 1–28. https://doi.org/10.3390/membranes10110348
DongCLvY. Application of collagen scaffold in tissue engineering: recent advances and new perspectives. Polymers2016; 8: 42. https://doi.org/10.3390/polym8020042
11.
ZhaoXHuDAWuD, et al.Applications of biocompatible scaffold materials in stem cell-based cartilage tissue engineering. Front Bioeng Biotechnol2021; 9: 603444. https://doi.org/10.3389/fbioe.2021.603444
12.
TallawiMRoselliniEBarbaniN, et al.Strategies for the chemical and biological functionalization of scaffolds for cardiac tissue engineering: a review. J R Soc Interface2015; 12: 20150254. https://doi.org/10.1098/rsif.2015.0254
13.
WangYDuMWuT, et al.The application of ECM-Derived biomaterials in cartilage tissue engineering. Mechanobiology in Medicine2023; 1: 100007. https://doi.org/10.1016/j.mbm.2023.100007
JiangY-HLouY-YLiT-H, et al.Cross-linking methods of type I collagen-based scaffolds for cartilage tissue engineering. Am J Transl Res2022; 14: 1146–1159. https://www.ajtr.org
16.
OhnoTTanisakaKHiraokaY, et al.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 C2004; 24: 407–411. https://doi.org/10.1016/j.msec.2003.11.011
17.
TakahashiTOgasawaraTAsawaY, et al.Three-dimensional microenvironments retain chondrocyte phenotypes during proliferation culture. Tissue Eng2007; 13: 1583–1592. https://doi.org/10.1089/ten.2006.0322
18.
ZhengLFanHSSunJ, et al.Chondrogenic differentiation of mesenchymal stem cells induced by collagen-based hydrogel: an in vivo study. J Biomed Mater Res2010; 93: 783–792. https://doi.org/10.1002/jbm.a.32588
19.
FarjanelJSchürmannGBrucknerP. Contacts with fibrils containing collagen I, but not collagens II, IX, and XI, can destabilize the cartilage phenotype of chondrocytes. Osteoarthr Cartil2001; 9: S55–S63. https://doi.org/10.1053/joca.2001.0445
20.
TamaddonMBurrowsMFerreiraSA, et al.Monomeric, porous type II collagen scaffolds promote chondrogenic differentiation of human bone marrow mesenchymal stem cells in vitro. Sci Rep2017; 7: 43519. https://doi.org/10.1038/srep43519
21.
PiperigkouZBainantzouDMakriN, et al.Enhancement of mesenchymal stem cells’ chondrogenic potential by type II collagen-based bioscaffolds. Mol Biol Rep2023; 50: 5125–5135. https://doi.org/10.1007/s11033-023-08461-x
KlattARPaul-KlauschBKlingerC, 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 Res2009; 27: 65–70. https://doi.org/10.1002/jor.20716
24.
LiHChenRJiaZ, et al.Original article porous fish collagen for cartilage tissue engineering. Am J Transl Res2020; 12: 6107–6121. https://www.ajtr.org
ZhangXOokawaMTanY, et al.Biochemical characterisation and assessment of fibril-forming ability of collagens extracted from bester sturgeon Huso huso × Acipenser ruthenus. Food Chem2014; 160: 305–312. https://doi.org/10.1016/j.foodchem.2014.03.075
28.
MoroiSMiuraTTamuraT, et al.Self-assembled collagen fibrils from the swim bladder of bester sturgeon enable alignment of MC3T3-E1 cells and enhance osteogenic differentiation. Mater Sci Eng C2019; 104: 109925. https://doi.org/10.1016/j.msec.2019.109925
29.
ShiLUraKTakagiY. Effects of self-assembled type II collagen fibrils on the morphology and growth of pre-chondrogenic ATDC5 cells. Osteoarthr Cartil Open2024; 6: 100450. https://doi.org/10.1016/j.ocarto.2024.100450
30.
CarvalhoAMMarquesAPSilvaTH, et al.Evaluation of the potential of collagen from codfish skin as a biomaterial for biomedical applications. Mar Drugs2018; 16: 495. https://doi.org/10.3390/md16120495
ZhangXAdachiSUraK, et al.Properties of collagen extracted from Amur sturgeon Acipenser schrenckii and assessment of collagen fibrils in vitro. Int J Biol Macromol2019; 137: 809–820. https://doi.org/10.1016/j.ijbiomac.2019.07.021
33.
MengDTanakaHKobayashiT, et al.The effect of alkaline pretreatment on the biochemical characteristics and fibril-forming abilities of types I and II collagen extracted from bester sturgeon by-products. Int J Biol Macromol2019; 131: 572–580. https://doi.org/10.1016/j.ijbiomac.2019.03.091
34.
ZhangXChenXYangT, et al.The effects of different crossing-linking conditions of genipin on type I collagen scaffolds: an in vitro evaluation. Cell Tissue Bank2014; 15: 531–541. https://doi.org/10.1007/s10561-014-9423-3
35.
ChangoorANeleaMMéthotS, et al.Structural characteristics of the collagen network in human normal, degraded and repair articular cartilages observed in polarized light and scanning electron microscopies. Osteoarthr Cartil2011; 19: 1458–1468. https://doi.org/10.1016/j.joca.2011.09.007
36.
BettingerCJLangerRBorensteinJT. Engineering substrate topography at the Micro- and nanoscale to control cell function. Angewandte Chemie - International Edition2009; 48: 5406–5415. https://doi.org/10.1002/anie.200805179
37.
Dede ErenALucassenAWATuvshindorjU, et al.Cells dynamically adapt to surface geometry by remodeling their focal adhesions and actin cytoskeleton. Front Cell Dev Biol2022; 10: 863721. https://doi.org/10.3389/fcell.2022.863721
38.
BaharlooBTextorMBrunetteDM. Substratum roughness alters the growth, area, and focal adhesions of epithelial cells, and their proximity to titanium surfaces. J Biomed Mater Res2005; 74: 12–22. https://doi.org/10.1002/jbm.a.30321
39.
ZhangXAzumaNHagiharaS, et al.Characterization of type I and II procollagen α1chain in Amur sturgeon (Acipenser schrenckii) and comparison of their gene expression. Gene2016; 579: 8–16. https://doi.org/10.1016/j.gene.2015.12.038
ZeltzCGullbergD. Correction to the integrin-collagen connection - a glue for tissue repair?J Cell Sci2016; 129: 653–664. https://doi.org/10.1242/jcs.188672
42.
WoodsAWangGBeierF. Regulation of chondrocyte differentiation by the act in cytoskeleton and adhesive interactions. J Cell Physiol2007; 213: 1–8. https://doi.org/10.1002/jcp.21110
43.
KilmerCEBattistoniCMCoxA, et al.Collagen type i and II blend hydrogel with autologous mesenchymal stem cells as a scaffold for articular cartilage defect repair. ACS Biomater Sci Eng2020; 6: 3464–3476. https://doi.org/10.1021/acsbiomaterials.9b01939
44.
ChenWWeiYChuI, et al.Effect of chondroitin sulphate C on the in vitro and in vivo chondrogenesis of mesenchymal stem cells in crosslinked type II collagen scaffolds. J Tissue Eng Regen Med2013; 7(8): 665–672. https://doi.org/10.1002/term.1463
45.
MengDLiWLengX, et al.Extraction of chondroitin sulfate and type II collagen from sturgeon (acipenser gueldenstaedti) notochord and characterization of their hybrid fibrils. Process Biochemistry2023; 124: 180–188. https://doi.org/10.1016/j.procbio.2022.11.026
46.
YuKOrnitzDM. The FGF ligand-receptor signaling system in chondrogenesis, osteogenesis and vascularization of the endochondral skeleton. Int Congr Ser2007; 1302: 67–78. https://doi.org/10.1016/j.ics.2006.09.021
47.
KnuthCAAndres SastreEFahyNB, et al.Collagen type x is essential for successful mesenchymal stem cell-mediated cartilage formation and subsequent endochondral ossification. Eur Cell Mater2019; 38: 106–122. https://doi.org/10.22203/eCM.v038a09
48.
SandyaSAchanMASudhakaranPR, et al.Multiple matrix metalloproteinases in type II collagen induced arthritis. Indian J Clin Biochem2009; 24: 42–48. https://doi.org/10.1007/s12291-009-0007-0
49.
StoopRVan Der KraanPMBumaP, et al.Denaturation of type II collagen in articular cartilage in experimental murine arthritis. Evidence for collagen degradation in both reversible and irreversible cartilage damage. J Pathol1999; 188: 329–337. https://doi.org/10.1002/(SICI)1096-9896(199907)188:3<329::AID-PATH371>3.0.CO;2-B
50.
Lundgren-ÅkerlundEAszòdiA. Integrin α10β1:A collagen receptor critical in skeletal development, I domain integrins. Adv Exp Med Biol2014; 819: 61–71. https://doi.org/10.1007/978-94-017-9153-3_4
OrgelJPROMadhurapantulaRS. A structural prospective for collagen receptors such as DDR and their binding of the collagen fibril. Biochim Biophys Acta Mol Cell Res2019; 1866: 118478. https://doi.org/10.1016/j.bbamcr.2019.04.008
DieterleMPHusariARolauffsB, et al.Integrins, cadherins and channels in cartilage mechanotransduction: perspectives for future regeneration strategies. Expet Rev Mol Med2021; 23: 1–16. https://doi.org/10.1017/erm.2021.16
55.
VargheseSHwangNSCanverAC, et al.Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol2008; 27: 12–21. https://doi.org/10.1016/j.matbio.2007.07.002
56.
StuartKPaderiJSnyderPW, et al.Collagen-binding peptidoglycans inhibit MMP mediated collagen degradation and reduce dermal scarring. PLoS One2011; 6: e22139. https://doi.org/10.1371/journal.pone.0022139
57.
WangLChenXWangS, et al.Ferrous/ferric ions crosslinked type II collagen multifunctional hydrogel for advanced osteoarthritis treatment. Adv Healthcare Mater2024; 13: 2302833. https://doi.org/10.1002/adhm.202302833
