The minor collagens in articular cartilage

doi:10.1007/s13238-017-0377-7

Protein Cell

2017, Vol. 8

Issue (8) : 560-572 https://doi.org/10.1007/s13238-017-0377-7

MINI-REVIEW

The minor collagens in articular cartilage

Yunyun Luo^1,²(

), Dovile Sinkeviciute^1,³, Yi He¹, Morten Karsdal¹, Yves Henrotin⁴, Ali Mobasheri^5,⁶, Patrik Önnerfjord³, Anne Bay-Jensen¹

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

Download: PDF(648 KB)
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

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

Corresponding Author(s): Yunyun Luo

Issue Date: 23 August 2017

Cite this article:

Yunyun Luo,Dovile Sinkeviciute,Yi He, et al. The minor collagens in articular cartilage[J]. Protein Cell, 2017, 8(8): 560-572.

URL:

https://academic.hep.com.cn/pac/EN/10.1007/s13238-017-0377-7
https://academic.hep.com.cn/pac/EN/Y2017/V8/I8/560

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 https://doi.org/10.1002/art.24293
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 https://doi.org/10.1002/art.21020
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 https://doi.org/10.1359/jbmr.2000.15.1.82
4	AppletonCTG, PitelkaV, HenryJ, BeierF (2007) Global analyses of gene expression in early experimental osteoarthritis.Arthritis Rheum56(6):1854–1868 https://doi.org/10.1002/art.22711
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 https://doi.org/10.1247/csf.08025
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 https://doi.org/10.1016/j.joca.2006.04.001
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 https://doi.org/10.1016/j.ebiom.2016.05.004
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 https://doi.org/10.1074/jbc.275.14.10370
10	BoissierMC, ChiocchiaG, RonziereMC, HerbageD, FournierC (1990) Arthritogenicity of minor cartilage collagens (types IX and XI) in mice.Arthritis Rheum33:1–8 https://doi.org/10.1002/art.1780330101
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 https://doi.org/10.1074/jbc.M212889200
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 https://doi.org/10.1136/ard.2008.097139
13	BrownJC, GolbikR, MannK, TimplR (1994) Structure and stability of the triple-helical domains of human collagen XIV.Matrix Biol14 (4):287–295 https://doi.org/10.1016/0945-053X(94)90194-5
14	ChenS, MienaltowskiMJ, BirkDE (2015) Regulation of corneal stroma extracellular matrix assembly.Exp Eye Res133:69–80 https://doi.org/10.1016/j.exer.2014.08.001
15	ChiquetM, BirkDE, BönnemannCG, KochM (2014) Collagen XII: protecting bone and muscle integrity by organizing collagen fibrils.Int J Biochem Cell Biol53:51–54 https://doi.org/10.1016/j.biocel.2014.04.020
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 https://doi.org/10.1086/324023
18	D’AngeloM, YanZ, NooreyazdanM, PacificiM, SarmentDS, BillingsPC, LeboyPS (2000) MMP-13 is induced during chondrocyte hypertrophy.J Cell Biochem77(4):678–693 https://doi.org/10.1002/(SICI)1097-4644(20000615)77:4<678::AID-JCB15>3.0.CO;2-P
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 https://doi.org/10.1074/jbc.M702491200
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 https://doi.org/10.1016/j.matbio.2015.09.003
21	EyreDR(1991) The collagens of articular cartilage.Semin Arthritis Rheum21(3):2–11 https://doi.org/10.1016/0049-0172(91)90035-X
22	EyreD (2002) Collagen of articular cartilage.Arthritis Res.4(1):30–35 https://doi.org/10.1186/ar380
23	EyreDR (2004) Collagens and cartilage matrix homeostasis.Clin Orthop Relat Res427(Suppl):S118–S122 https://doi.org/10.1097/01.blo.0000144855.48640.b9
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 https://doi.org/10.1016/0014-5793(87)80842-6
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 https://doi.org/10.1074/jbc.M311653200
26	EyreDR, WeisMA, WuJJ (2006) Articular cartilage collagen: an irreplaceable framework?Eur Cells Mater12:57–63 https://doi.org/10.22203/eCM.v012a07
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 https://doi.org/10.1073/pnas.91.11.5070
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 https://doi.org/10.1177/1947603513518217
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 https://doi.org/10.1074/jbc.273.8.4547
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 https://doi.org/10.1002/art.24036
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 https://doi.org/10.1002/art.23175
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 https://doi.org/10.1002/jor.1100090404
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 https://doi.org/10.1016/S0945-053X(98)90027-0
34	GoldringSR, PurduePE, CrottiTN, ShenZ, FlanneryMR, BinderNB, RossFP, McHughKP (2013) Bone remodelling in inflammatory arthritis.Ann Rheum Dis72(Suppl 2):ii52–ii55 https://doi.org/10.1136/annrheumdis-2012-202199
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 https://doi.org/10.1111/j.1432-1033.1996.0576r.x
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 https://doi.org/10.1359/jbmr.2001.16.11.2005
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 https://doi.org/10.1186/s13075-016-1040-z
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 https://doi.org/10.1074/jbc.272.33.20650
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 https://doi.org/10.1016/S1535-6108(03)00133-8
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 https://doi.org/10.1186/1471-2474-15-309
41	HeinegårdD, SaxneT (2011) The role of the cartilage matrix in osteoarthritis.Nat Rev Rheumatol7(1):50–56 https://doi.org/10.1038/nrrheum.2010.198
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 https://doi.org/10.1167/iovs.12-11456
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 https://doi.org/10.1016/j.rehab.2016.03.004
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 https://doi.org/10.1007/s11626-013-9692-3
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 https://doi.org/10.1016/j.bone.2007.06.024
46	HolmesDF, KadlerKE (2006) The 10+4 microfibril structure of thin cartilage fibrils.Proc Natl Acad Sci USA103(46):17249–17254 https://doi.org/10.1073/pnas.0608417103
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 https://doi.org/10.1016/j.joca.2009.02.015
48	IchimuraS, WuJJ, EyreDR (2000) Two-dimensional peptide mapping of cross-linked type IX collagen in human cartilage.Arch Biochem Biophys378(1):33–39 https://doi.org/10.1006/abbi.2000.1805
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 https://doi.org/10.1016/j.joca.2005.02.005
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 https://doi.org/10.1089/ten.tea.2013.0013
51	JenkinsE, MossJB, PaceJM, BridgewaterLC (2005) The new collagen gene COL27A1 contains SOX9-responsive enhancer elements.Matrix Biol24(3):177–184 https://doi.org/10.1016/j.matbio.2005.02.004
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 https://doi.org/10.1080/13547500902777608
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 https://doi.org/10.1016/j.clinbiochem.2010.03.015
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 https://doi.org/10.1089/adt.2012.474
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 https://doi.org/10.3109/1354750X.2013.789084
56	KarsdalMA, ChristiansenC, LadelC, HenriksenK, KrausVB, Bay-JensenAC (2014) Osteoarthritis—a case for personalized health care?Osteoarthritis Cartil22(1):7–16 https://doi.org/10.1016/j.joca.2013.10.018
57	KarsdalMA, GenoveseF, MadsenEA, Manon-JensenT, SchuppanD (2015) Collagen and tissue turnover as a function of age: implications for fibrosis.J Hepatol64:103–109 https://doi.org/10.1016/j.jhep.2015.08.014
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 https://doi.org/10.1016/S0945-053X(03)00008-8
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 https://doi.org/10.1016/j.jmb.2004.03.042
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 https://doi.org/10.1083/jcb.113.4.971
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 https://doi.org/10.1074/jbc.M400536200
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 https://doi.org/10.1002/1529-0131(200101)44:1<120::AID-ANR16>3.0.CO;2-X
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 https://doi.org/10.1016/j.joca.2015.03.036
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 https://doi.org/10.1016/j.joca.2015.03.002
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 https://doi.org/10.1002/(SICI)1098-1004(1997)9:4<300::AID-HUMU2>3.0.CO;2-9
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 https://doi.org/10.1016/j.matbio.2007.07.007
67	KwanAPL, CummingsCE, ChapmanJA, GrantME (1991) Macromolecular organization of chicken type X collagen in vitro.J Cell Biol114(3):597–604 https://doi.org/10.1083/jcb.114.3.597
68	LaiCH, ChuML (1996) Tissue distribution and developmental expression of type XVI collagen in the mouse.Tissue Cell28 (2):155–164 https://doi.org/10.1016/S0040-8166(96)80004-8
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 https://doi.org/10.1007/s00296-011-2191-5
70	LeemingDJ, KarsdalMA, RasmussenLM, ScholzeA, TepelM (2013) Association of systemic collagen type IV formation with survival among patients undergoing hemodialysis.PLoS ONE8 (8):e71050 https://doi.org/10.1371/journal.pone.0071050
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 https://doi.org/10.1002/(SICI)1096-8628(20000131)90:3<216::AID-AJMG6>3.0.CO;2-1
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 https://doi.org/10.1038/sj.ejhg.5200848
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 https://doi.org/10.1006/jaut.2001.0581
74	LuckmanSP, ReesE, KwanAPL (2003) Partial characterization of cell-type X collagen interactions.Biochem J372(Pt 2):485–493 https://doi.org/10.1042/bj20021572
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 https://doi.org/10.1002/art.24443
76	MayoJL, HoldenDN, BarrowJR, BridgewaterLC (2009) The transcription factor Lc-Maf participates in Col27a1 regulation during chondrocyte maturation.Exp Cell Res315(13):2293–2300 https://doi.org/10.1016/j.yexcr.2009.04.020
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 https://doi.org/10.1016/S0006-291X(88)80040-8
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 https://doi.org/10.1086/522377
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 https://doi.org/10.1136/ard.42.6.680
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 https://doi.org/10.1093/rheumatology/39.3.299
81	MyllyharjuJ, KivirikkoKI (2001) Collagens and collagen-related diseases.Ann Med33(1):7–21 https://doi.org/10.3109/07853890109002055
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 https://doi.org/10.1073/pnas.90.7.2870
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 https://doi.org/10.1016/j.matbio.2006.09.010
85	PaceJM, CorradoM, MisseroC, ByersPH (2003) Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1.Matrix Biol22(1):3–14 https://doi.org/10.1016/S0945-053X(03)00007-6
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 https://doi.org/10.1006/excr.1993.1134
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 https://doi.org/10.1371/journal.pone.0029422
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 https://doi.org/10.3727/096368910X550215
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 https://doi.org/10.1016/S1063-4584(97)80014-3
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 https://doi.org/10.1002/art.38300
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 https://doi.org/10.1074/jbc.M502210200
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 https://doi.org/10.1371/journal.pone.0084934
94	SandJMB, KnoxAJ, LangeP, SunS, KristensenJH, LeemingDJ, KarsdalMA, BoltonCE, JohnsonSR (2015) Accelerated extracellular matrix turnover during exacerbations of COPD.Respir Res16(1):69 https://doi.org/10.1186/s12931-015-0225-3
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 https://doi.org/10.1016/j.clinbiochem.2016.09.003
96	SchmidTM, LinsenmayerTF (1985) Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues.J Cell Biol100(2):598–605 https://doi.org/10.1083/jcb.100.2.598
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 https://doi.org/10.1111/j.1601-6343.2004.00308.x
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 https://doi.org/10.1089/ten.tea.2014.0375
100	SmithGN, HastyKA, BrandtKD (1989) Type XI collagen is associated with the chondrocyte surface in suspension culture.Matrix9(3):186–192 https://doi.org/10.1016/S0934-8832(89)80049-6
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 https://doi.org/10.1186/ar2822
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 https://doi.org/10.1371/journal.pone.0144525
103	SussmanMD, OgleRC, BalianG (1984) Biosynthesis and processing of collagens in different cartilaginous tissues.J Orthop Res2(2):134–142 https://doi.org/10.1002/jor.1100020204
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 https://doi.org/10.1016/j.joca.2011.12.003
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 https://doi.org/10.1016/j.joca.2010.01.012
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 https://doi.org/10.1371/journal.pone.0024753
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 https://doi.org/10.1016/j.matbio.2009.05.003
111	WalkerGD, FischerM, GannonJ, ThompsonRC, OegemaTR (1995) Expression of type-X collagen in osteoarthritis.J Orthop Res13(1):4–12 https://doi.org/10.1002/jor.1100130104
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 https://doi.org/10.1074/jbc.M100625200
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 https://doi.org/10.1002/art.11233
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 https://doi.org/10.1074/jbc.M411036200
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 https://doi.org/10.1089/tea.2007.0272
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 https://doi.org/10.1083/jcb.115.1.209
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 https://doi.org/10.1002/art.39034
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 https://doi.org/10.1042/BJ20130642

[1]	Jiaxing Cui, Hongfei Cui, Mingran Yang, Shiyu Du, Junfeng Li, Yingxue Li, Liyang Liu, Xuegong Zhang, Shao Li. Tongue coating microbiome as a potential biomarker for gastritis including precancerous cascade[J]. Protein Cell, 2019, 10(7): 496-509.
[2]	Xiaoying Chen,Kunshan Zhang,Liqiang Zhou,Xinpei Gao,Junbang Wang,Yinan Yao,Fei He,Yuping Luo,Yongchun Yu,Siguang Li,Liming Cheng,Yi E. Sun. Coupled electrophysiological recording and single cell transcriptome analyses revealed molecular mechanisms underlying neuronal maturation[J]. Protein Cell, 2016, 07(03): 175-186.
[3]	Haiyan Chu,Ting Wu,Wenyu Wu,Wenzhen Tu,Shuai Jiang,Sidi Chen,Yanyun Ma,Qingmei Liu,Xiaodong Zhou,Li Jin,Jiucun Wang. Involvement of collagen-binding heat shock protein 47 in scleroderma-associated fibrosis[J]. Protein Cell, 2015, 6(8): 589-598.
[4]	Ming Fang, Reed Jacob, Owen McDougal, Julia Thom Oxford. Minor fibrillar collagens, variable regions alternative splicing, intrinsic disorder, and tyrosine sulfation[J]. Prot Cell, 2012, 3(6): 419-433.
[5]	Hui Dai, Xiao-Ming Gao. Elevated levels of serum antibodies against alpha-1, 6-glucan in patients with systemic lupus erythematosus or rheumatoid arthritis[J]. Prot Cell, 2011, 2(9): 739-744.
[6]	Takuma Hayashi, Akiko Horiuchi, Tanri Shiozawa, Kenji Sano, Nobuyoshi Hiraoka, Yae Kanai, Susumu Tonegawa, Ikuo Konishi, . Mice-lacking LMP2, immuno-proteasome subunit, as an animal model of spontaneous uterine leiomyosarcoma[J]. Protein Cell, 2010, 1(8): 711-717.
[7]	Hans-Christian Siebert, Monika Burg-Roderfeld, Thomas Eckert, Sabine St?tzel, Ulrike Kirch, Tammo Diercks, Martin J. Humphries, Martin Frank, Rainer Wechselberger, Emad Tajkhorshid, Steffen Oesser. Interaction of the α2A domain of integrin with small collagen fragments[J]. Prot Cell, 2010, 1(4): 393-405.
[8]	Edward A. Lin, Chuan-Ju Liu, . The role of ADAMTSs in arthritis[J]. Protein Cell, 2010, 1(1): 33-47.

Viewed

Full text

Abstract

Cited

Shared

Discussed