MINI-REVIEW

The minor collagens in articular cartilage

  • Yunyun Luo , 1,2 ,
  • Dovile Sinkeviciute 1,3 ,
  • Yi He 1 ,
  • Morten Karsdal 1 ,
  • Yves Henrotin 4 ,
  • Ali Mobasheri 5,6 ,
  • Patrik Önnerfjord 3 ,
  • Anne Bay-Jensen 1
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  • 1. Biomarkers & Research, Nordic Bioscience A/S, Herlev, Denmark
  • 2. Faculty of Healthy and Medical Sciences, University of Copenhagen, Copenhagen, Denmark
  • 3. Department of Clinical Sciences, Medical Faculty, Lund University, Lund, Sweden
  • 4. Bone and Cartilage Research Unit, Institute of Pathology, Level 5, Arthropole Liège, University of Liège, CHU Sart-Tilman, 4000 Liège, Belgium
  • 5. Faculty of Health and Medical Sciences, University of Surrey, Guildford, Surrey GU2 7XH, UK
  • 6. Arthritis Research UK Centre for Sport, Exercise and Osteoarthritis, Arthritis Research UK Centre for Musculoskeletal Ageing Research, Queen’s Medical Centre, Nottingham, NG7 2UH, UK

Received date: 08 Nov 2016

Accepted date: 25 Jan 2017

Published date: 23 Aug 2017

Copyright

2017 The Author(s) 2017. This article is published with open access at Springerlink.com and journal.hep.com.cn

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.

Key words: collagen; biomarker; arthritis

Cite this article

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

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

DOI

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

DOI

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

DOI

4
AppletonCTG, PitelkaV, HenryJ, BeierF (2007) Global analyses of gene expression in early experimental osteoarthritis.Arthritis Rheum56(6):1854–1868

DOI

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

DOI

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

DOI

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

DOI

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

DOI

10
BoissierMC, ChiocchiaG, RonziereMC, HerbageD, FournierC (1990) Arthritogenicity of minor cartilage collagens (types IX and XI) in mice.Arthritis Rheum33:1–8

DOI

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

DOI

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

DOI

13
BrownJC, GolbikR, MannK, TimplR (1994) Structure and stability of the triple-helical domains of human collagen XIV.Matrix Biol14 (4):287–295

DOI

14
ChenS, MienaltowskiMJ, BirkDE (2015) Regulation of corneal stroma extracellular matrix assembly.Exp Eye Res133:69–80

DOI

15
ChiquetM, BirkDE, BönnemannCG, KochM (2014) Collagen XII: protecting bone and muscle integrity by organizing collagen fibrils.Int J Biochem Cell Biol53:51–54

DOI

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

DOI

18
D’AngeloM, YanZ, NooreyazdanM, PacificiM, SarmentDS, BillingsPC, LeboyPS (2000) MMP-13 is induced during chondrocyte hypertrophy.J Cell Biochem77(4):678–693

DOI

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

DOI

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

DOI

21
EyreDR(1991) The collagens of articular cartilage.Semin Arthritis Rheum21(3):2–11

DOI

22
EyreD (2002) Collagen of articular cartilage.Arthritis Res.4(1):30–35

DOI

23
EyreDR (2004) Collagens and cartilage matrix homeostasis.Clin Orthop Relat Res427(Suppl):S118–S122

DOI

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

DOI

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

DOI

26
EyreDR, WeisMA, WuJJ (2006) Articular cartilage collagen: an irreplaceable framework?Eur Cells Mater12:57–63

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

34
GoldringSR, PurduePE, CrottiTN, ShenZ, FlanneryMR, BinderNB, RossFP, McHughKP (2013) Bone remodelling in inflammatory arthritis.Ann Rheum Dis72(Suppl 2):ii52–ii55

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

41
HeinegårdD, SaxneT (2011) The role of the cartilage matrix in osteoarthritis.Nat Rev Rheumatol7(1):50–56

DOI

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

DOI

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

DOI

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

DOI

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

DOI

46
HolmesDF, KadlerKE (2006) The 10+4 microfibril structure of thin cartilage fibrils.Proc Natl Acad Sci USA103(46):17249–17254

DOI

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

DOI

48
IchimuraS, WuJJ, EyreDR (2000) Two-dimensional peptide mapping of cross-linked type IX collagen in human cartilage.Arch Biochem Biophys378(1):33–39

DOI

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

DOI

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

DOI

51
JenkinsE, MossJB, PaceJM, BridgewaterLC (2005) The new collagen gene COL27A1 contains SOX9-responsive enhancer elements.Matrix Biol24(3):177–184

DOI

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

DOI

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

DOI

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

DOI

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

DOI

56
KarsdalMA, ChristiansenC, LadelC, HenriksenK, KrausVB, Bay-JensenAC (2014) Osteoarthritis—a case for personalized health care?Osteoarthritis Cartil22(1):7–16

DOI

57
KarsdalMA, GenoveseF, MadsenEA, Manon-JensenT, SchuppanD (2015) Collagen and tissue turnover as a function of age: implications for fibrosis.J Hepatol64:103–109

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

67
KwanAPL, CummingsCE, ChapmanJA, GrantME (1991) Macromolecular organization of chicken type X collagen in vitro.J Cell Biol114(3):597–604

DOI

68
LaiCH, ChuML (1996) Tissue distribution and developmental expression of type XVI collagen in the mouse.Tissue Cell28 (2):155–164

DOI

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

DOI

70
LeemingDJ, KarsdalMA, RasmussenLM, ScholzeA, TepelM (2013) Association of systemic collagen type IV formation with survival among patients undergoing hemodialysis.PLoS ONE8 (8):e71050

DOI

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

DOI

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

DOI

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

DOI

74
LuckmanSP, ReesE, KwanAPL (2003) Partial characterization of cell-type X collagen interactions.Biochem J372(Pt 2):485–493

DOI

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

DOI

76
MayoJL, HoldenDN, BarrowJR, BridgewaterLC (2009) The transcription factor Lc-Maf participates in Col27a1 regulation during chondrocyte maturation.Exp Cell Res315(13):2293–2300

DOI

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

DOI

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

DOI

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

DOI

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

DOI

81
MyllyharjuJ, KivirikkoKI (2001) Collagens and collagen-related diseases.Ann Med33(1):7–21

DOI

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

DOI

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

DOI

85
PaceJM, CorradoM, MisseroC, ByersPH (2003) Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1.Matrix Biol22(1):3–14

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

94
SandJMB, KnoxAJ, LangeP, SunS, KristensenJH, LeemingDJ, KarsdalMA, BoltonCE, JohnsonSR (2015) Accelerated extracellular matrix turnover during exacerbations of COPD.Respir Res16(1):69

DOI

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

DOI

96
SchmidTM, LinsenmayerTF (1985) Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues.J Cell Biol100(2):598–605

DOI

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

DOI

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

DOI

100
SmithGN, HastyKA, BrandtKD (1989) Type XI collagen is associated with the chondrocyte surface in suspension culture.Matrix9(3):186–192

DOI

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

DOI

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

DOI

103
SussmanMD, OgleRC, BalianG (1984) Biosynthesis and processing of collagens in different cartilaginous tissues.J Orthop Res2(2):134–142

DOI

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

DOI

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

DOI

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

DOI

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

DOI

111
WalkerGD, FischerM, GannonJ, ThompsonRC, OegemaTR (1995) Expression of type-X collagen in osteoarthritis.J Orthop Res13(1):4–12

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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

DOI

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