The minor collagens in articular cartilage

Yunyun Luo, Dovile Sinkeviciute, Yi He, Morten Karsdal, Yves Henrotin, Ali Mobasheri, Patrik Önnerfjord, Anne Bay-Jensen

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Protein Cell ›› 2017, Vol. 8 ›› Issue (8) : 560-572. DOI: 10.1007/s13238-017-0377-7
MINI-REVIEW
MINI-REVIEW

The minor collagens in articular cartilage

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Abstract

Articular cartilage is a connective tissue consisting of a specialized extracellular matrix (ECM) that dominates the bulk of its wet and dry weight. Type II collagen and aggrecan are the main ECM proteins in cartilage. However, little attention has been paid to less abundant molecular components, especially minor collagens, including type IV, VI, IX, X, XI, XII, XIII, and XIV, etc. Although accounting for only a small fraction of the mature matrix, these minor collagens not only play essential structural roles in the mechanical properties, organization, and shape of articular cartilage, but also fulfil specific biological functions. Genetic studies of these minor collagens have revealed that they are associated with multiple connective tissue diseases, especially degenerative joint disease. The progressive destruction of cartilage involves the degradation of matrix constituents including these minor collagens. The generation and release of fragmented molecules could generate novel biochemical markers with the capacity to monitor disease progression, facilitate drug development and add to the existing toolbox for in vitro studies, preclinical research and clinical trials.

Keywords

collagen / biomarker / arthritis

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Yunyun Luo, Dovile Sinkeviciute, Yi He, Morten Karsdal, Yves Henrotin, Ali Mobasheri, Patrik Önnerfjord, Anne Bay-Jensen. The minor collagens in articular cartilage. Protein Cell, 2017, 8(8): 560‒572 https://doi.org/10.1007/s13238-017-0377-7

References

[1]
AlexopoulosLG, YounI, BonaldoP, GuilakF (2009) Developmental and osteoarthritic changes in Col6a1-knockout mice: biomechanics of type VI collagen in the cartilage pericellular matrix.Arthritis Rheum60(3):771–779
CrossRef Google scholar
[2]
AlizadehBZ, NjajouOT, BijkerkC, MeulenbeltI, De WildtSC, HofmanA, PolsHAP, SlagboomPE, Van DuijnCM (2005) Evidence for a role of the genomic region of the gene encoding for the α1 chain of type IX collagen (COL9A1) in hip osteoarthritis: a population-based study.Arthritis Rheum52(5):1437–1442
CrossRef Google scholar
[3]
AlvarezJ, BalbinM, SantosF, FernandezM, FerrandoS, LopezJM (2000) Different bone growth rates are associated with changes in the expression pattern of types II and X collagens and collagenase 3 in proximal growth plates of the rat tibia.J Bone Miner Res15(1):82–94
CrossRef Google scholar
[4]
AppletonCTG, PitelkaV, HenryJ, BeierF (2007) Global analyses of gene expression in early experimental osteoarthritis.Arthritis Rheum56(6):1854–1868
CrossRef Google scholar
[5]
AraiK, NagashimaY, TakemotoT, NishiyamaT (2008) Mechanical strain increases expression of type XII collagen in murine osteoblastic MC3T3-E1 cells.Cell Struct Funct33(2):203–210
CrossRef Google scholar
[6]
BauerDC, HunterDJ, AbramsonSB, AtturM, CorrM, FelsonD, HeinegårdD, JordanJM, KeplerTB, LaneNE, SaxneT, TyreeB, KrausVB, For the Osteoarthritis Biomarkers Network(2006) Classification of osteoarthritis biomarkers: a proposed approach.Osteoarthritis Cartil14(8):723–727
CrossRef Google scholar
[7]
Bay-JensenA-C, HenrotinY, KarsdalM, MobasheriA (2016) The need for predictive, prognostic, objective and complementary blood-based biomarkers in osteoarthritis (OA).EBioMedicine7:4–6
CrossRef Google scholar
[8]
BidansetDJ, GuidryC, RosenbergLC, ChoiHU, TimplR, HookM (1992) Binding of the proteoglycan decorin to collagen type VI.J Biol Chem267(8):5250–5256
[9]
BlaschkeUK, EikenberryEF, HulmesDJS, GallaHJ, BrucknerP (2000) Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils.J Biol Chem275(14):10370–10378
CrossRef Google scholar
[10]
BoissierMC, ChiocchiaG, RonziereMC, HerbageD, FournierC (1990) Arthritogenicity of minor cartilage collagens (types IX and XI) in mice.Arthritis Rheum33:1–8
CrossRef Google scholar
[11]
Boot-HandfordRP, TuckwellDS, PlumbDA, Farrington RockC, PoulsomR (2003) A novel and highly conserved collagen (proα1 (XXVII)) with a unique expression pattern and unusual molecular characteristics establishes a new clade within the vertebrate fibrillar collagen family.J Biol Chem278(33):31067–31077
CrossRef Google scholar
[12]
BrewCJ, CleggPD, Boot-HandfordRP, AndrewJG, HardinghamT (2010) Gene expression in human chondrocytes in late osteoarthritis is changed in both fibrillated and intact cartilage without evidence of generalised chondrocyte hypertrophy.Ann Rheum Dis69(1):234–240
CrossRef Google scholar
[13]
BrownJC, GolbikR, MannK, TimplR (1994) Structure and stability of the triple-helical domains of human collagen XIV.Matrix Biol14 (4):287–295
CrossRef Google scholar
[14]
ChenS, MienaltowskiMJ, BirkDE (2015) Regulation of corneal stroma extracellular matrix assembly.Exp Eye Res133:69–80
CrossRef Google scholar
[15]
ChiquetM, BirkDE, BönnemannCG, KochM (2014) Collagen XII: protecting bone and muscle integrity by organizing collagen fibrils.Int J Biochem Cell Biol53:51–54
CrossRef Google scholar
[16]
CremerMA, YeXJ, TeratoK, OwensSW, SeyerJM, KangAH (1994) Type XI collagen-induced arthritis in the Lewis rat. Characterization of cellular and humoral immune responses to native types XI, V, and II collagen and constituent alpha-chains.J. Immunol.153:824–832
[17]
Czarny-RatajczakM, LohinivaJ,RogalaP, KozlowskiK, PeräläM, CarterL, SpectorTD, KolodziejL, SeppänenU, GlazarR, KrólewskiJ, Latos-BielenskaA, Ala-KokkoL (2001) A mutation in COL9A1 causes multiple epiphyseal dysplasia: further evidence for locus heterogeneity.Am J Hum Genet69:969–980
CrossRef Google scholar
[18]
D’AngeloM, YanZ, NooreyazdanM, PacificiM, SarmentDS, BillingsPC, LeboyPS (2000) MMP-13 is induced during chondrocyte hypertrophy.J Cell Biochem77(4):678–693
CrossRef Google scholar
[19]
DanfelterM, ÖnnerfjordP, HeinegårdD (2007) Fragmentation of proteins in cartilage treated with interleukin-1: Specific cleavage of type IX collagen by matrix metalloproteinase 13 releases the NC4 domain.J Biol Chem282(51):36933–36941
CrossRef Google scholar
[20]
EckhardU, HuesgenPF, SchillingO, BellacCL, ButlerGS, CoxJH, DufourA, GoebelerV, KappelhoffR, dem KellerUA, KleinT, LangePF, MarinoG, MorrisonCJ, PrudovaA, RodriguezD, StarrAE, WangY, OverallCM (2016) Active site specificity profiling of the matrix metalloproteinase family: Proteomic identification of 4300 cleavage sites by nine MMPs explored with structural and synthetic peptide cleavage analyses.Matrix Biol49:37–60
CrossRef Google scholar
[21]
EyreDR(1991) The collagens of articular cartilage.Semin Arthritis Rheum21(3):2–11
CrossRef Google scholar
[22]
EyreD (2002) Collagen of articular cartilage.Arthritis Res.4(1):30–35
CrossRef Google scholar
[23]
EyreDR (2004) Collagens and cartilage matrix homeostasis.Clin Orthop Relat Res427(Suppl):S118–S122
CrossRef Google scholar
[24]
EyreDR, AponS, WuJJ, EricssonLH, WalshKA (1987) Collagen type IX: evidence for covalent linkages to type II collagen in cartilage.FEBS Lett220(2):337–341
CrossRef Google scholar
[25]
EyreDR, PietkaT, WeisMA, WuJJ (2004) Covalent cross-linking of the NC1 domain of collagen type IX to collagen type II in cartilage.J Biol Chem279(4):2564–2568
CrossRef Google scholar
[26]
EyreDR, WeisMA, WuJJ (2006) Articular cartilage collagen: an irreplaceable framework?Eur Cells Mater12:57–63
CrossRef Google scholar
[27]
FässlerR, SchnegelsbergPN, DausmanJ, ShinyaT, MuragakiY, McCarthyMT, OlsenBR, JaenischR (1994) Mice lacking alpha1 (IX) collagen develop noninflammatory degenerative joint disease.Proc Natl Acad Sci USA91(1):5070–5074
CrossRef Google scholar
[28]
FoldagerCB, TohWS, GomollAH, OlsenBR, SpectorM (2014) Distribution of basement membrane molecules, laminin and collagen type IV, in normal and degenerated cartilage tissues.Cartilage5(2):123–132
CrossRef Google scholar
[29]
FrischholzS, BeierF, GirkontaiteI, WagnerK, PöschlE, TurnayJ, MayerU, Von Der MarkK (1998) Characterization of human type X procollagen and its NC-1 domain expressed as recombinant proteins in HEK293 cells.J Biol Chem273(8):4547–4555
CrossRef Google scholar
[30]
FukuiN, MiyamotoY, NakajimaM, IkedaY, HikitaA, FurukawaH, MitomiH, TanakaN, KatsuragawaY, YamamotoS, SawabeM, JujiT, MoriT, SuzukiR, IkegawaS (2008a) Zonal gene expression of chondrocytes in osteoarthritic cartilage.Arthritis Rheum58(12):3843–3853
CrossRef Google scholar
[31]
FukuiN, IkedaY, OhnukiT, TanakaN, HikitaA, MitomiH, MoriT, JujiT, KatsuragawaY, YamamotoS, SawabeM, YamaneS, SuzukiR, SandellLJ, OchiT (2008b) Regional differences in chondrocyte metabolism in osteoarthritis: a detailed analysis by laser capture microdissection.Arthritis Rheum58 (1):154–163
CrossRef Google scholar
[32]
GannonJM, WalkerG, FischerM, CarpenterR, ThompsonRC, OegemaTR (1991) Localization of type X collagen in canine growth plate and adult canine articular cartilage.J Orthop Res9 (4):485–494
CrossRef Google scholar
[33]
Giry-LozinguezC, Aubert-FoucherE, PeninF, DeléageG, DubletB, Van Der RestM (1998) Identification and characterization of a heparin binding site within the NC1 domain of chicken collagen XIV.Matrix Biol17(2):145–149
CrossRef Google scholar
[34]
GoldringSR, PurduePE, CrottiTN, ShenZ, FlanneryMR, BinderNB, RossFP, McHughKP (2013) Bone remodelling in inflammatory arthritis.Ann Rheum Dis72(Suppl 2):ii52–ii55
CrossRef Google scholar
[35]
GrässelS, TimplR, TanEM, ChuML (1996) Biosynthesis and processing of type XVI collagen in human fibroblasts and smooth muscle cells.Eur J Biochem242:576–584
CrossRef Google scholar
[36]
GregoryKE, KeeneDR, TufaSF, LunstrumGP, MorrisNP (2001) Developmental distribution of collagen type XII in cartilage: association with articular cartilage and the growth plate.J Bone Miner Res16(11):2005–2016
CrossRef Google scholar
[37]
GudmannNS, MunkHL, ChristensenAF, EjstrupL, SørensenGL, LoftAG, KarsdalMA, Bay-JensenA-C, HeY, SiebuhrAS, JunkerP (2016) Chondrocyte activity is increased in psoriatic arthritis and axial spondyloarthritis.Arthritis Res Ther18(1):141
CrossRef Google scholar
[38]
HaggR, HedbomE, MöllersU, AszódiA, FässlerR, MoU, AszoA, FaR (1997) Absence of the α1(IX) chain leads to a functional knock-out of the entire collagen IX protein in mice.J Biol Chem1 (33):20650–20654
CrossRef Google scholar
[39]
HamanoY, ZeisbergM, SugimotoH, LivelyJC, MaeshimaY, YangC, HynesRO, WerbZ, SudhakarA, KalluriR (2003) Physiological levels of tumstatin, a fragment of collagen IV α3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via αVβ3 integrin.Cancer Cell3(6):589–601
CrossRef Google scholar
[40]
HeY, SiebuhrAS, Brandt-hansenNU, WangJ, SuD, ZhengQ, SimonsenO, PetersenKK, Arendt-nielsenL, EskehaveT, HoeckHC, KarsdalMA, Bay-jensenAC (2014) Type X collagen levels are elevated in serum from human osteoarthritis patients and associated with biomarkers of cartilage degradation and inflammation.BMC Musculoskelet Disord15:309
CrossRef Google scholar
[41]
HeinegårdD, SaxneT (2011) The role of the cartilage matrix in osteoarthritis.Nat Rev Rheumatol7(1):50–56
CrossRef Google scholar
[42]
HemmavanhC, KochM, BirkDE, EspanaEM (2013) Abnormal corneal endothelial maturation in collagen XII and XIV Null mice.I nvestig Ophthalmol Vis Sci54(5):3297–3308
CrossRef Google scholar
[43]
HenrotinY, SanchezC, Bay-JensenAC, MobasheriA (2016) Osteoarthritis biomarkers derived from cartilage extracellular matrix: current status and future perspectives.Ann Phys Rehabil Med59(3):145–148
CrossRef Google scholar
[44]
HidaM, HamanakaR, OkamotoO, YamashitaK, SasakiT, YoshiokaH, MatsuoN (2014) Nuclear factor y (NF-Y) regulates the proximal promoter activity of the mouse collagen α1(XI) gene (Col11a1) in chondrocytes.In Vitro Cell Dev Biol Anim50(4):358–366
CrossRef Google scholar
[45]
HjortenR, HansenU, UnderwoodRA, TelferHE, FernandesRJ, KrakowD, SebaldE, Wachsmann-HogiuS, BrucknerP, JacquetR, LandisWJ, ByersPH, PaceJM (2007) Type XXVII collagen at the transition of cartilage to bone during skeletogenesis.Bone41 (4):535–542
CrossRef Google scholar
[46]
HolmesDF, KadlerKE (2006) The 10+4 microfibril structure of thin cartilage fibrils.Proc Natl Acad Sci USA103(46):17249–17254
CrossRef Google scholar
[47]
HuebnerJL, JohnsonKA, KrausVB, TerkeltaubRA (2009) Transglutaminase 2 is a marker of chondrocyte hypertrophy and osteoarthritis severity in the Hartley guinea pig model of knee OA.Osteoarthritis Cartil17(8):1056–1064
CrossRef Google scholar
[48]
IchimuraS, WuJJ, EyreDR (2000) Two-dimensional peptide mapping of cross-linked type IX collagen in human cartilage.Arch Biochem Biophys378(1):33–39
CrossRef Google scholar
[49]
JakkulaE, MelkoniemiM, KivirantaI, LohinivaJ, RäinäSS, PeräläM, WarmanML, AhonenK, KrögerH, GöringHHH, Ala-KokkoL (2005) The role of sequence variations within the genes encoding collagen II, IX and XI in non-syndromic, early-onset osteoarthritis.Osteoarthritis Cartil13(6):497–507
CrossRef Google scholar
[50]
JengL, HsuH-P, SpectorM (2013) Tissue-engineered cartilaginous constructs for the treatment of caprine cartilage defects, including distribution of laminin and type IV collagen.Tissue Eng Part A19 (19–20):2267–2274
CrossRef Google scholar
[51]
JenkinsE, MossJB, PaceJM, BridgewaterLC (2005) The new collagen gene COL27A1 contains SOX9-responsive enhancer elements.Matrix Biol24(3):177–184
CrossRef Google scholar
[52]
KarsdalMA, HenriksenK, LeemingDJ, MitchellP, DuffinK, BarascukN, KlicksteinL, AggarwalP, NemirovskiyO, ByrjalsenI, QvistP, Bay-JensenAC, DamEB, MadsenSH, ChristiansenC (2009) Biochemical markers and the FDA Critical Path: how biomarkers may contribute to the understanding of pathophysiology and provide unique and necessary tools for drug development.Biomarkers14(3):181–202
CrossRef Google scholar
[53]
KarsdalMA, HenriksenK, LeemingDJ, WoodworthT, VassiliadisE, Bay-JensenA-C (2010) Novel combinations of Post-Translational Modification (PTM) neo-epitopes provide tissue-specific biochemical markers—are they the cause or the consequence of the disease?Clin Biochem43(10–11):793–804
CrossRef Google scholar
[54]
KarsdalMA, NielsenMJ, SandJM, HenriksenK, GenoveseF, Bay-JensenA-C, SmithV, AdamkewiczJI, ChristiansenC, LeemingDJ (2013a) Extracellular matrix remodeling: the common denominator in connective tissue diseases. Possibilities for evaluation and current understanding of the matrix as more than a passive architecture, but a key player in tissue failure.Assay Drug Dev Technol11(2):70–92
CrossRef Google scholar
[55]
KarsdalMA, Bay-JensenAC, LeemingDJ, HenriksenK, ChristiansenC (2013b) Quantification of ‘end products’ of tissue destruction in inflammation may reflect convergence of cytokine and signaling pathways—implications for modern clinical chemistry.Biomarkers18(5):375–378
CrossRef Google scholar
[56]
KarsdalMA, ChristiansenC, LadelC, HenriksenK, KrausVB, Bay-JensenAC (2014) Osteoarthritis—a case for personalized health care?Osteoarthritis Cartil22(1):7–16
CrossRef Google scholar
[57]
KarsdalMA, GenoveseF, MadsenEA, Manon-JensenT, SchuppanD (2015) Collagen and tissue turnover as a function of age: implications for fibrosis.J Hepatol64:103–109
CrossRef Google scholar
[58]
KassnerA, HansenU, MiosgeN, ReinhardtDP, AignerT, Bruckner-TudermanL, BrucknerP, GrässelS (2003) Discrete integration of collagen XVI into tissue-specific collagen fibrils or beaded microfibrils.Matrix Biol22(2):131–143
CrossRef Google scholar
[59]
KassnerA, TiedemannK, NotbohmH, LudwigT, MörgelinM, ReinhardtDP, ChuML, BrucknerP, GrässelS (2004) Molecular structure and interaction of recombinant human type XVI collagen.J Mol Biol339(4):835–853
CrossRef Google scholar
[60]
KeeneDR, LunstrumGP, MorrisNP, StoddardDW, BurgesonRE (1991) Two type XII-like collagens localize to the surface of banded collagen fibrils.J Cell Biol113(4):971–978
CrossRef Google scholar
[61]
KochM, SchulzeJ, HansenU, AshwodtT, KeeneDR, BrunkenWJ, BurgesonRE, BrucknerP, Bruckner- L (2004) A novel marker of tissue junctions, collagen XXII.J Biol Chem279(21):22514–22521
CrossRef Google scholar
[62]
KojimaT, MwaleF, YasudaT, GirardC, PooleAR, LavertyS (2001) Early degradation of type IX and type II collagen with the onset of experimental inflammatory arthritis.Arthritis Rheum44(1):120–127
CrossRef Google scholar
[63]
KrausVB, BlancoFJ, EnglundM, KarsdalMA, LohmanderLS (2015a) Call for standardized definitions of osteoarthritis and risk stratification for clinical trials and clinical use.Osteoarthritis Cartil23(8):1233–1241
CrossRef Google scholar
[64]
KrausVB, BlancoFJ, EnglundM, HenrotinY, LohmanderLS, LosinaE, ÖnnerfjordP, PersianiS (2015b) OARSI clinical trials recommendations: soluble biomarker assessments in clinical trials in osteoarthritis.Osteoarthritis Cartilage23(5):686–697
CrossRef Google scholar
[65]
KuivaniemiH, TrompG, ProckopDJ(1997) Mutations in fibrillar collagens (types I, II, III, and XI), fibril-associated collagen (type IX), and network-forming collagen (type X) cause a spectrum of disease of bone, cartilage, and blood vessels.Hum Mutat9 (4):300–315
CrossRef Google scholar
[66]
KvistAJ, NyströmA, HultenbyK, SasakiT,TaltsJF, AspbergA (2008) The major basement membrane components localize to the chondrocyte pericellular matrix—a cartilage basement membrane equivalent?Matrix Biol27(1):22–33
CrossRef Google scholar
[67]
KwanAPL, CummingsCE, ChapmanJA, GrantME (1991) Macromolecular organization of chicken type X collagen in vitro.J Cell Biol114(3):597–604
CrossRef Google scholar
[68]
LaiCH, ChuML (1996) Tissue distribution and developmental expression of type XVI collagen in the mouse.Tissue Cell28 (2):155–164
CrossRef Google scholar
[69]
LeeSJ, KimMJ, KeeSJ, SongSK, KweonSS, ShinMH, ParkDJ, ParkYW, LeeSS, KimTJ (2013) Association study of the candidate gene for knee osteoarthritis in Koreans.Rheumatol Int33(3):783–786
CrossRef Google scholar
[70]
LeemingDJ, KarsdalMA, RasmussenLM, ScholzeA, TepelM (2013) Association of systemic collagen type IV formation with survival among patients undergoing hemodialysis.PLoS ONE8 (8):e71050
CrossRef Google scholar
[71]
LohinivaJ, PaassiltaP, SeppänenU, VierimaaO, KivirikkoS, Ala-KokkoL (2000) Splicing mutations in the COL3 domain of collagen IX cause multiple epiphyseal dysplasia.Am J Med Genet90:216–222
CrossRef Google scholar
[72]
LoughlinJ, MustafaZ, DowlingB, SouthamL, MarcellineL, RäinäSS, Ala-KokkoL, ChapmanK (2002) Finer linkage mapping of a primary hip osteoarthritis susceptibility locus on chromosome 6.Eur J Hum Genet10(9):562–568
CrossRef Google scholar
[73]
LuS, CarlsenS, HanssonAS, HolmdahlR (2002) Immunization of rats with homologous type XI collagen leads to chronic and relapsing arthritis with different genetics and joint pathology than arthritis induced with homologous type II collagen.J Autoimmun18:199–211
CrossRef Google scholar
[74]
LuckmanSP, ReesE, KwanAPL (2003) Partial characterization of cell-type X collagen interactions.Biochem J372(Pt 2):485–493
CrossRef Google scholar
[75]
MatsumotoT, CooperGM, GharaibehB, MeszarosLB, LiG, UsasA, FuFH, HuardJ (2009) Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of musclederived stem cells expressing bone morphogenetic protein 4 and soluble Flt-1.Arthritis Rheum60(5):1390–1405
CrossRef Google scholar
[76]
MayoJL, HoldenDN, BarrowJR, BridgewaterLC (2009) The transcription factor Lc-Maf participates in Col27a1 regulation during chondrocyte maturation.Exp Cell Res315(13):2293–2300
CrossRef Google scholar
[77]
McDevittCA, PahlJA, AyadS, MillerRR, UratsujiM, AndrishJT (1988) Experimental osteoarthritic articular cartilage is enriched in guanidine soluble type VI collagen.Biochem Biophys Res Commun157:250–255
CrossRef Google scholar
[78]
MioF, ChibaK, HiroseY, KawaguchiY, MikamiY, OyaT, MoriM, KamataM, MatsumotoM, OzakiK, TanakaT, TakahashiA, KuboT, KimuraT, ToyamaY, IkegawaS (2007) A functional polymorphism in COL11A1, which encodes the alpha 1 chain of type XI collagen, is associated with susceptibility to lumbar disc herniation.Am J Hum Genet81(6):1271–1277
CrossRef Google scholar
[79]
MorganK, EvansHB, FirthSA, SmithMN, AyadS, WeissJB, LennoxPJ (1983) Holt, 1 Alpha 2 alpha 3 alpha collagen is arthritogenic.Ann Rheum Dis42(6):680–683
CrossRef Google scholar
[80]
MustafaZ, ChapmanK, IrvenC, CarrAJ, ClipshamK, ChitnavisJ, SinsheimerJS, BloomfieldVA, McCartneyM, CoxO, SykesB, LoughlinJ (2000) Linkage analysis of candidate genes as susceptibility loci for osteoarthritis-suggestive linkage of COL9A1 to female hip osteoarthritis.Rheumatology (Oxford)39(3):299–306
CrossRef Google scholar
[81]
MyllyharjuJ, KivirikkoKI (2001) Collagens and collagen-related diseases.Ann Med33(1):7–21
CrossRef Google scholar
[82]
NakataK, OnoK, MiyazakiJ, OlsenBR, MuragakiY, AdachiE, YamamuraK, KimuraT (1993) Osteoarthritis associated with mild chondrodysplasia in transgenic mice expressing alpha-1(IX) collagen chains with a central deletion.Proc Natl Acad Sci USA90(7):2870–2874
CrossRef Google scholar
[83]
NishiyamaT, McDonoughAM, BrunsRR, BurgesonRE (1994) Type XII and XIV collagens mediate interactions between banded collagen fibers in vitro and may modulate extracellular matrix deformability.J Biol Chem269(45):28193–28199
[84]
OpolkaA, RatzingerS, SchubertT, SpiegelHU, GrifkaJ, BrucknerP, ProbstA, GrässelS (2007) Collagen IX is indispensable for timely maturation of cartilage during fracture repair in mice.Matrix Biol26(2):85–95
CrossRef Google scholar
[85]
PaceJM, CorradoM, MisseroC, ByersPH (2003) Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1.Matrix Biol22(1):3–14
CrossRef Google scholar
[86]
PfaffM, AumailleyM, SpecksU, KnolleJ, ZerwesHG, TimplR (1993) Integrin and Arg-Gly-Asp dependence of cell adhesion to the native and unfolded triple helix of collagen type VI.Exp Cell Res206(1):167–176
CrossRef Google scholar
[87]
PlumbDA, FerraraL, TorbicaT, KnowlesL, MironovA, KadlerKE, BriggsMD, Boot-HandfordRP (2011) Collagen XXVII organises the pericellular matrix in the growth plate.PLoS ONE6(12): e29422
CrossRef Google scholar
[88]
PolacekM, BruunJ-A, ElvenesJ, FigenschauY, MartinezI (2011) The secretory profiles of cultured human articular chondrocytes and mesenchymal stem cells: implications for autologous cell transplantation strategies.Cell Transplant20(9):1381–1393
CrossRef Google scholar
[89]
PooleCA, GilbertRT, HerbageD, HartmannDJ (1997) Immunolocalization of type IX collagen in normal and spontaneously osteoarthritic canine tibial cartilage and isolated chondrons.Osteoarthritis Cartil5:191–204
CrossRef Google scholar
[90]
ReiserK, McCormickRJ, RuckerRB (1992) Enzymatic and nonenzymatic cross-linking of collagen and elastin.FASEB J6 (7):2439–2449
[91]
Rodriguez-FontenlaC, CalazaM, EvangelouE, ValdesAM, ArdenN, BlancoFJ, CarrA, ChapmanK, DeloukasP, DohertyM, EskoT, Garcés AletáCM, Gomez-Reino CarnotaJJ, HelgadottirH, HofmanA, JonsdottirI, KerkhofHJM, KloppenburgM, McCaskieA, NtzaniEE, OllierWER, OreiroN, PanoutsopoulouK, RalstonSH, RamosYF, RianchoJA, RivadeneiraF, SlagboomPE, StyrkarsdottirU, ThorsteinsdottirU, ThorleifssonG, TsezouA, UitterlindenAG, WallisGA, WilkinsonJM, ZhaiG, ZhuY, FelsonDT, IoannidisJPA, LoughlinJ, MetspaluA, MeulenbeltI, StefanssonK, Van MeursJB, ZegginiE, SpectorTD, GonzalezA (2014) Assessment of osteoarthritis candidate genes in a metaanalysis of nine genome-wide association studies.Arthritis Rheumatol.66(4):940–949
CrossRef Google scholar
[92]
RuehlM, ErbenU, SchuppanD, WagnerC, ZellerA, FreiseC, Al-HasaniH, LoesekannM, NotterM, WittigBM, ZeitzM, DieterichW, SomasundaramR (2005) The elongated first fibronectin type III domain of collagen XIV is an inducer of quiescence and differentiation in fibroblasts and preadipocytes.J Biol Chem280 (46):38537–38543
CrossRef Google scholar
[93]
SandJM, LarsenL, HogaboamC, MartinezF, HanM, LarsenMR, NawrockiA, ZhengQ, KarsdalMA, LeemingDJ (2013) MMP mediated degradation of type IV collagen alpha 1 and alpha 3 chains reflects basement membrane remodeling in experimental and clinical fibrosis—validation of two novel biomarker assays.PLoS ONE8(12):1–12
CrossRef Google scholar
[94]
SandJMB, KnoxAJ, LangeP, SunS, KristensenJH, LeemingDJ, KarsdalMA, BoltonCE, JohnsonSR (2015) Accelerated extracellular matrix turnover during exacerbations of COPD.Respir Res16(1):69
CrossRef Google scholar
[95]
SandJM, MartinezG, MidjordAK, KarsdalMA, LeemingDJ, LangeP (2016) Characterization of serological neo-epitope biomarkers reflecting collagen remodeling in clinically stable chronic obstructive pulmonary disease.Clin Biochem49(15):1144–1151
CrossRef Google scholar
[96]
SchmidTM, LinsenmayerTF (1985) Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues.J Cell Biol100(2):598–605
CrossRef Google scholar
[97]
SchmidTM, MayneR, JeffreyJJ, LinsenmayerTF (1986) Type X collagen contains two cleavage sites for a vertebrate collagenase.J Biol Chem261(9):4184–4189
[98]
ShenG (2005) The role of type X collagen in facilitating and regulating endochondral ossification of articular cartilage.Orthod Craniofac Res8(1):11–17
CrossRef Google scholar
[99]
SmeriglioP, DhulipalaL, LaiJH, GoodmanSB, DragooJL, SmithRL, MaloneyWJ, YangF, BhutaniN (2015) Collagen VI enhances cartilage tissue generation by stimulating chondrocyte proliferation.Tissue Eng Part A21(3–4):840–849
CrossRef Google scholar
[100]
SmithGN, HastyKA, BrandtKD (1989) Type XI collagen is associated with the chondrocyte surface in suspension culture.Matrix9(3):186–192
CrossRef Google scholar
[101]
SteinertAF, ProffenB, KunzM, HendrichC, GhivizzaniSC, NöthU, RethwilmA, EulertJ, EvansCH (2009) Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer.Arthritis Res Ther11(5): R148
CrossRef Google scholar
[102]
SunS, HenriksenK, KarsdalMA, ByrjalsenI, RittwegerJ, ArmbrechtG, BelavyDL, FelsenbergD, NedergaardAF (2015) Collagen type III and VI turnover in response to long-term immobilization.PLoS ONE10(12):e0144525
CrossRef Google scholar
[103]
SussmanMD, OgleRC, BalianG (1984) Biosynthesis and processing of collagens in different cartilaginous tissues.J Orthop Res2(2):134–142
CrossRef Google scholar
[104]
TaylorDW, AhmedN, ParrenoJ, LunstrumGP, GrossAE, DiamandisEP, KandelRA (2014) Collagen type XII and versican are present in the early stages of cartilage tissue formation by both redifferentating passaged and primary chondrocytes.Tissue Eng Part A21(3–4):683–693
[105]
van der KraanPM, van den BergWB (2012) Chondrocyte hypertrophy and osteoarthritis: role in initiation and progression of cartilage degeneration?Osteoarthritis Cartilage20(3):223–232
CrossRef Google scholar
[106]
Van der RestRM (1987) Structure and function of collagen types.Academic Press, New York
[107]
van SpilWE, DeGrootJ, LemsWF, OostveenJCM, LafeberFPJG (2010) Serum and urinary biochemical markers for knee and hiposteoarthritis: a systematic review applying the consensus BIPED criteria.Osteoarthritis Cartil18(5):605–612
CrossRef Google scholar
[108]
VeidalSS, KarsdalMA, VassiliadisE, NawrockiA, LarsenMR, NguyenQHT, HägglundP, LuoY, ZhengQ, VainerB, LeemingDJ (2011) MMP mediated degradation of type VI collagen is highly associated with liver Fibrosis- Identification and validation of a novel biochemical marker assay.PLoS ONE6(9):1–9
CrossRef Google scholar
[109]
WachsmuthL, SöderS, FanZ, FingerF, AignerT (2006) Immunolocalization of matrix proteins in different human cartilage subtypes.Histol Histopathol21(4–6):477–485
[110]
WagenerR, GaraSK, KobbeB, PaulssonM, ZauckeF (2009) The knee osteoarthritis susceptibility locus DVWA on chromosome 3p24.3 is the 5′ part of the split COL6A4 gene.Matrix Biol28 (6):307–310
CrossRef Google scholar
[111]
WalkerGD, FischerM, GannonJ, ThompsonRC, OegemaTR (1995) Expression of type-X collagen in osteoarthritis.J Orthop Res13(1):4–12
CrossRef Google scholar
[112]
WangG, ZhangY, ZhaoX, MengC, MaL, KongY (2015) MicroRNA-411 inhibited matrix metalloproteinase 13 expression in human chondrocytes.Am J Transl Res7(10):2000–2006
[113]
WattSL, LunstrumsGP, McdonoughAM, KeeneDR, BurgesonsRE, MorrissllNP (1992) Characterization of collagen types XII and XIV from fetal bovine cartilage.Biochemistry267(28):20093–20099
[114]
WibergC, HedbomE, KhairullinaA, LamandéSR, OldbergÅ, TimplR, MörgelinM, HeinegårdD (2001) Biglycan and decorin bind close to the N-terminal region of the collagen VI triple helix.J Biol Chem276(22):18947–18952
CrossRef Google scholar
[115]
WuJJ, LarkMW, ChunLE, EyreDR (1991) Sites of stromelysin cleavage in collagen types II, IX, X, and XI of cartilage.J Biol Chem266(9):5625–5628
[116]
WuJJ, WoodsPE, EyreDR (1992) Identification of cross-linking sites in bovine cartilage type-IX collagen reveals an antiparallel type-II-type-IX molecular relationship and type-IX to type-IX bonding.J Biol Chem267(32):23007–23014
[117]
XuL, FlahiffCM, WaldmanBA, WuD, OlsenBR, SettonLA, LiY (2003) Osteoarthritis-like changes and decreased mechanical function of articular cartilage in the joints of mice with the chondrodysplasia gene (cho).Arthritis Rheum48(9):2509–2518
CrossRef Google scholar
[118]
XuL, PengH, WuD, HuK, GoldringMB, OlsenBE, LiY(2005) Activation of the discoidin domain receptor 2 induces expression of matrix metalloproteinase 13 associated with osteoarthritis in mice.J Biol Chem280(1):548–555
CrossRef Google scholar
[119]
XuJ, WangW, LudemanM, ChengK, HayamiT, LotzJC, KapilaS (2008) Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels.Tissue Eng Part A14(5):667–680
CrossRef Google scholar
[120]
YamagataM, YamadaKM, YamadaSS, ShinomuraT, TanakaH, NishidaY, ObaraM, KimataK (1991) The complete primary structure of type XII collagen shows a chimeric molecule with reiterated fibronectin type III motifs, von Willebrand factor A motifs, a domain homologous to a noncollagenous region of type IX collagen, and short collagenous domains with an Arg-Gly-Asp site.J Cell Biol115(1):209–221
CrossRef Google scholar
[121]
ZelenskiNA, LeddyHA, Sanchez-AdamsJ, ZhangJ, BonaldoP, LiedtkeW, GuilakF (2015) Type VI collagen regulates pericellular matrix properties, chondrocyte swelling, and mechanotransduction in mouse articular cartilage.Arthritis Rheumatol67(5):1286–1294
CrossRef Google scholar
[122]
ZwolanekD, VeitG, EbleJA, GullbergD, RuggieroF, HeinoJ, MeierM, StetefeldJ, KochM (2014) Collagen XXII binds to collagenbinding integrins via the novel motifs GLQGER and GFKGER.Biochem J459(1):217–227
CrossRef Google scholar

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