Skip to main content
SpringerLink
Log in

Collagens in Hyaline Cartilage

  • Chapter
  • First Online:
Cartilage

Abstract

Collagens are the most abundant proteins in mammals and mostly incorporated into the extracellular matrix (ECM) where they form complex supramolecular structures additionally incorporating different non-collagenous components. The ECM of articular cartilage comprises the majority of the tissue volume and thus determines the properties of this unique tissue. The fibrillar matrix – composed of cartilage collagens and associated macromolecules – is responsible for the integrity and stability of the cartilage ECM and determines the mechanical tissue properties, i.e., the load-bearing capacity. Besides the classical cartilage collagens II, IX, and XI, several other collagens were identified in the cartilage ECM during the past years. Among them are fibrillar collagens (collagens III, V, XXIV, and XXVII), network-forming collagens (collagens IV and X), filamentous collagens (collagen VI), and fibrillar-associated collagens with interrupted triple helices (FACITs XII, XIV, XVI, and XXII). Most of them are not specific for cartilage but are also components of many other connective tissue matrices and tissue junctions of the body, i.e., the skin, tendon, muscle, bone, and cornea, demonstrating a crucial redundancy of individual collagen function among different tissue types. This review summarizes information about the role of the different collagens in cartilage homeostasis and formation of fibrillar suprastructures. In addition, the impact of aberrant or loss of collagen expression in transgenic or collagen-knockout mouse models on cartilage matrix structure and physiology is described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agarwal P, Zwolanek D, Keene DR, Schulz JN, Blumbach K, Heinegard D, Zaucke F, Paulsson M, Krieg T, Koch M, Eckes B (2012) Collagen XII and XIV, new partners of cartilage oligomeric matrix protein in the skin extracellular matrix suprastructure. J Biol Chem 287(27):22549–22559. doi:10.1074/jbc.M111.335935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aigner T, Bertling W, Stoss H, Weseloh G, von der Mark K (1993) Independent expression of fibril-forming collagens I, II, and III in chondrocytes of human osteoarthritic cartilage. J Clin Invest 91(3):829–837. doi:10.1172/JCI116303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aigner T, Gluckert K, von der Mark K (1997) Activation of fibrillar collagen synthesis and phenotypic modulation of chondrocytes in early human osteoarthritic cartilage lesions. Osteoarthritis Cartilage 5(3):183–189

    Article  CAS  PubMed  Google Scholar 

  • Alexopoulos LG, Youn I, Bonaldo P, Guilak F (2009) Developmental and osteoarthritic changes in Col6a1-knockout mice: biomechanics of type VI collagen in the cartilage pericellular matrix. Arthritis Rheum 60(3):771–779. doi:10.1002/art.24293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ansorge HL, Meng X, Zhang G, Veit G, Sun M, Klement JF, Beason DP, Soslowsky LJ, Koch M, Birk DE (2009) TYPE xiv collagen regulates fibrillogenesis: premature collagen fibril growth and tissue dysfunction in null MICE. J Biol Chem 284(13):8427–8438. doi:10.1074/jbc.M805582200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asamura K, Abe S, Imamura Y, Aszodi A, Suzuki N, Hashimoto S, Takumi Y, Hayashi T, Fassler R, Nakamura Y, Usami S (2005) Type IX collagen is crucial for normal hearing. Neuroscience 132(2):493–500

    Article  CAS  PubMed  Google Scholar 

  • Aszodi A, Chan D, Hunziker E, Bateman JF, Fassler R (1998a) Collagen II is essential for the removal of the notochord and the formation of intervertebral discs. J Cell Biol 143(5):1399–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aszodi A, Pfeifer A, Wendel M, Hiripi L, Fassler R (1998b) Mouse models for extracellular matrix diseases. J Mol Med (Berl) 76(3–4):238–252

    CAS  Google Scholar 

  • Benninghoff A (1925) Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Zweiter Teil: Der Aufbau des Gelenkknorpels in Seinen Beziehungen zur Funktion. Z Zellforsch 2:783

    Article  Google Scholar 

  • Berthod F, Germain L, Guignard R, Lethias C, Garrone R, Damour O, der RM V, Auger FA (1997) Differential expression of collagens XII and XIV in human skin and in reconstructed skin. J Invest Dermatol 108(5):737–742

    Article  CAS  PubMed  Google Scholar 

  • Bidanset DJ, Guidry C, Rosenberg LC, Choi HU, Timpl R, Hook M (1992) Binding of the proteoglycan decorin to collagen type VI. J Biol Chem 267(8):5250–5256

    CAS  PubMed  Google Scholar 

  • Blaschke UK, Eikenberry EF, Hulmes DJ, Galla HJ, Bruckner P (2000) Collagen XI nucleates self-assembly and limits lateral growth of cartilage fibrils. J Biol Chem 275(14):10370–10378

    Article  CAS  PubMed  Google Scholar 

  • Blumbach K, Niehoff A, Paulsson M, Zaucke F (2008) Ablation of collagen IX and COMP disrupts epiphyseal cartilage architecture. Matrix Biol 27(4):306–318

    Article  CAS  PubMed  Google Scholar 

  • Bohme K, Li Y, Oh PS, Olsen BR (1995) Primary structure of the long and short splice variants of mouse collagen XII and their tissue-specific expression during embryonic development. Dev Dyn 204(4):432–445. doi:10.1002/aja.1002040409

    Article  CAS  PubMed  Google Scholar 

  • Boot-Handford RP, Tuckwell DS (2003) Fibrillar collagen: the key to vertebrate evolution? A tale of molecular incest. Bioessays 25(2):142–151

    Article  CAS  PubMed  Google Scholar 

  • Boyd LM, Richardson WJ, Allen KD, Flahiff C, Jing L, Li Y, Chen J, Setton LA (2008) Early-onset degeneration of the intervertebral disc and vertebral end plate in mice deficient in type IX collagen. Arthritis Rheum 58(1):164–171

    Article  CAS  PubMed  Google Scholar 

  • Brachvogel B, Zaucke F, Dave K, Norris EL, Stermann J, Dayakli M, Koch M, Gorman JJ, Bateman JF, Wilson R (2013) Comparative proteomic analysis of normal and collagen IX null mouse cartilage reveals altered extracellular matrix composition and novel components of the collagen IX interactome. J Biol Chem 288(19):13481–13492. doi:10.1074/jbc.M112.444810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budde B, Blumbach K, Ylostalo J, Zaucke F, Ehlen HW, Wagener R, Ala-Kokko L, Paulsson M, Bruckner P, Grässel S (2005) Altered integration of matrilin-3 into cartilage extracellular matrix in the absence of collagen IX. Mol Cell Biol 25(23):10465–10478

    Google Scholar 

  • Castagnola P, Tavella S, Gerecke DR, Dublet B, Gordon MK, Seyer J, Cancedda R, van der Rest M, Olsen BR (1992) Tissue-specific expression of type XIV collagen--a member of the FACIT class of collagens. Eur J Cell Biol 59(2):340–347

    CAS  PubMed  Google Scholar 

  • Chan D, Cole WG, Chow CW, Mundlos S, Bateman JF (1995) A COL2A1 mutation in achondrogenesis type II results in the replacement of type II collagen by type I and III collagens in cartilage. J Biol Chem 270(4):1747–1753

    Article  CAS  PubMed  Google Scholar 

  • Chan D, Taylor TK, Cole WG (1993) Characterization of an arginine 789 to cysteine substitution in alpha 1 (II) collagen chains of a patient with spondyloepiphyseal dysplasia. J Biol Chem 268(20):15238–15245

    CAS  PubMed  Google Scholar 

  • Chang J, Nakajima H, Poole CA (1997) Structural colocalisation of type VI collagen and fibronectin in agarose cultured chondrocytes and isolated chondrons extracted from adult canine tibial cartilage. J Anat 190(Pt 4):523–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang J, Poole CA (1996) Sequestration of type VI collagen in the pericellular microenvironment of adult chrondrocytes cultured in agarose. Osteoarthritis Cartilage 4(4):275–285

    Article  CAS  PubMed  Google Scholar 

  • Chanut-Delalande H, Bonod-Bidaud C, Cogne S, Malbouyres M, Ramirez F, Fichard A, Ruggiero F (2004) Development of a functional skin matrix requires deposition of collagen V heterotrimers. Mol Cell Biol 24(13):6049–6057. doi:10.1128/MCB.24.13.6049-6057.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheah KS, Lau ET, Au PK, Tam PP (1991) Expression of the mouse alpha 1(II) collagen gene is not restricted to cartilage during development. Development 111(4):945–953

    CAS  PubMed  Google Scholar 

  • Chiquet M, Birk DE, Bonnemann CG, Koch M (2014) Collagen XII: protecting bone and muscle integrity by organizing collagen fibrils. Int J Biochem Cell Biol 53:51–54. doi:10.1016/j.biocel.2014.04.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Paepe A, Malfait F (2012) The Ehlers-Danlos syndrome, a disorder with many faces. Clin Genet 82(1):1–11. doi:10.1111/j.1399-0004.2012.01858.x

    Article  PubMed  CAS  Google Scholar 

  • Dharmavaram RM, Huynh AI, Jimenez SA (1998) Characterization of human chondrocyte and fibroblast type XII collagen cDNAs. Matrix Biol 16(6):343–348

    Article  CAS  PubMed  Google Scholar 

  • Dreier R, Opolka A, Grifka J, Bruckner P, Grässel S (2008) Collagen IX-deficiency seriously compromises growth cartilage development in mice. Matrix Biol 27(4):319–329

    Google Scholar 

  • Eikenberry EF, Bruckner P (1999) Supramolecular structure of cartilage matrix. In: Seibel MJ, Robins SP, Bilezikian JP (eds) Bone and cartilage metabolism, 1st edn. Academic, San Diego, pp 289–300

    Google Scholar 

  • Exposito JY, Valcourt U, Cluzel C, Lethias C (2010) The fibrillar collagen family. Int J Mol Sci 11(2):407–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyre D (2002) Collagen of articular cartilage. Arthritis Res 4(1):30–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyre DR, Brickley-Parsons DM, Glimcher MJ (1978) Predominance of type I collagen at the surface of avian articular cartilage. FEBS Lett 85(2):259–263

    Article  CAS  PubMed  Google Scholar 

  • Eyre DR, Pietka T, Weis MA, Wu JJ (2004) Covalent cross-linking of the NC1 domain of collagen type IX to collagen type II in cartilage. J Biol Chem 279(4):2568–2574

    Article  CAS  PubMed  Google Scholar 

  • Eyre DR, Weis MA, Wu JJ (2006) Articular cartilage collagen: an irreplaceable framework? Eur Cell Mater 12:57–63

    CAS  PubMed  Google Scholar 

  • Fässler R, Schnegelsberg PN, Dausman J, Shinya T, Muragaki Y, McCarthy MT, Olsen BR, Jaenisch R (1994) Mice lacking alpha 1 (IX) collagen develop noninflammatory degenerative joint disease. Proc Natl Acad Sci U S A 91(11):5070–5074

    Google Scholar 

  • Fitzgerald J, Rich C, Zhou FH, Hansen U (2008) Three novel collagen VI chains, alpha4(VI), alpha5(VI), and alpha6(VI). J Biol Chem 283(29):20170–20180. doi:10.1074/jbc.M710139200

    Article  CAS  PubMed  Google Scholar 

  • Foldager CB, Toh WS, Gomoll AH, Olsen BR, Spector M (2014) Distribution of basement membrane molecules, laminin and collagen type IV, in normal and degenerated cartilage tissues. Cartilage 5(2):123–132. doi:10.1177/1947603513518217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Font B, Eichenberger D, Rosenberg LM, van der Rest M (1996) Characterization of the interactions of type XII collagen with two small proteoglycans from fetal bovine tendon, decorin and fibromodulin. Matrix Biol 15(5):341–348

    Article  CAS  PubMed  Google Scholar 

  • Furthmayr H, Wiedemann H, Timpl R, Odermatt E, Engel J (1983) Electron-microscopical approach to a structural model of intima collagen. Biochem J 211(2):303–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furuto DK, Miller EJ (1983) Different levels of glycosylation contribute to the heterogeneity of alpha 1(II) collagen chains derived from a transplantable rat chondrosarcoma. Arch Biochem Biophys 226(2):604–611

    Article  CAS  PubMed  Google Scholar 

  • Gannon JM, Walker G, Fischer M, Carpenter R, Thompson RC Jr, Oegema TR Jr (1991) Localization of type X collagen in canine growth plate and adult canine articular cartilage. J Orthop Res 9(4):485–494. doi:10.1002/jor.1100090404

    Article  CAS  PubMed  Google Scholar 

  • Gara SK, Grumati P, Urciuolo A, Bonaldo P, Kobbe B, Koch M, Paulsson M, Wagener R (2008) Three novel collagen VI chains with high homology to the alpha3 chain. J Biol Chem 283(16):10658–10670

    Article  CAS  PubMed  Google Scholar 

  • Garofalo S, Metsaranta M, Ellard J, Smith C, Horton W, Vuorio E, de Crombrugghe B (1993) Assembly of cartilage collagen fibrils is disrupted by overexpression of normal type II collagen in transgenic mice. Proc Natl Acad Sci U S A 90(9):3825–3829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grassel S, Bauer RJ (2013) Collagen XVI in health and disease. Matrix Biol 32(2):64–73. doi:10.1016/j.matbio.2012.11.001

    Article  PubMed  CAS  Google Scholar 

  • Gregory KE, Keene DR, Tufa SF, Lunstrum GP, Morris NP (2001) Developmental distribution of collagen type XII in cartilage: association with articular cartilage and the growth plate. J Bone Miner Res 16(11):2005–2016. doi:10.1359/jbmr.2001.16.11.2005

    Article  CAS  PubMed  Google Scholar 

  • Guilak F, Alexopoulos LG, Upton ML, Youn I, Choi JB, Cao L, Setton LA, Haider MA (2006) The pericellular matrix as a transducer of biomechanical and biochemical signals in articular cartilage. Ann N Y Acad Sci 1068:498–512. doi:10.1196/annals.1346.011

    Article  CAS  PubMed  Google Scholar 

  • Guo BR, Zhang X, Chen G, Zhang JG, Sun LD, Du WD, Zhang Q, Cui Y, Zhu J, Tang XF, Xiao R, Liu Y, Li M, Tang HY, Yang X, Cheng H, Li M, Gao M, Li P, Wang JB, Xu FP, Zuo XB, Zheng XD, Zhang XG, Yang L, Liu JJ, Wang J, Yang S, Zhang XJ (2012) Exome sequencing identifies a COL14A1 mutation in a large Chinese pedigree with punctate palmoplantar keratoderma. J Med Genet 49(9):563–568. doi:10.1136/jmedgenet-2012-100868

    Article  CAS  PubMed  Google Scholar 

  • Hagg R, Bruckner P, Hedbom E (1998) Cartilage fibrils of mammals are biochemically heterogeneous: differential distribution of decorin and collagen IX. J Cell Biol 142(1):285–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagg R, Hedbom E, Mollers U, Aszodi A, Fässler R, Bruckner P (1997) Absence of the alpha1(IX) chain leads to a functional knock-out of the entire collagen IX protein in mice. J Biol Chem 272(33):20650–20654

    Google Scholar 

  • Hansen U, Bruckner P (2003) Macromolecular specificity of collagen fibrillogenesis: fibrils of collagens I and XI contain a heterotypic alloyed core and a collagen I sheath. J Biol Chem 278(39):37352–37359

    Article  CAS  PubMed  Google Scholar 

  • Hartmann DJ, Magloire H, Ricard-Blum S, Joffre A, Couble ML, Ville G, Herbage D (1983) Light and electron immunoperoxidase localization of minor disulfide-bonded collagens in fetal calf epiphyseal cartilage. Coll Relat Res 3(4):349–357

    Article  CAS  PubMed  Google Scholar 

  • Hedbom E, Heinegard D (1993) Binding of fibromodulin and decorin to separate sites on fibrillar collagens. J Biol Chem 268(36):27307–27312

    CAS  PubMed  Google Scholar 

  • Heino J (2007) The collagen family members as cell adhesion proteins. Bioessays 29(10):1001–1010. doi:10.1002/bies.20636

    Article  CAS  PubMed  Google Scholar 

  • Hjorten R, Hansen U, Underwood RA, Telfer HE, Fernandes RJ, Krakow D, Sebald E, Wachsmann-Hogiu S, Bruckner P, Jacquet R, Landis WJ, Byers PH, Pace JM (2007) Type XXVII collagen at the transition of cartilage to bone during skeletogenesis. Bone 41(4):535–542. doi:10.1016/j.bone.2007.06.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoyland JA, Thomas JT, Donn R, Marriott A, Ayad S, Boot-Handford RP, Grant ME, Freemont AJ (1991) Distribution of type X collagen mRNA in normal and osteoarthritic human cartilage. Bone Miner 15(2):151–163

    Article  CAS  PubMed  Google Scholar 

  • Hu K, Xu L, Cao L, Flahiff CM, Brussiau J, Ho K, Setton LA, Youn I, Guilak F, Olsen BR, Li Y (2006) Pathogenesis of osteoarthritis-like changes in the joints of mice deficient in type IX collagen. Arthritis Rheum 54(9):2891–2900

    Article  CAS  PubMed  Google Scholar 

  • Hufnagel SB, Weaver KN, Hufnagel RB, Bader PI, Schorry EK, Hopkin RJ (2014) A novel dominant COL11A1 mutation resulting in a severe skeletal dysplasia. Am J Med Genet A 164A(10):2607–2612. doi:10.1002/ajmg.a.36688

    Article  PubMed  CAS  Google Scholar 

  • Hunziker EB, Michel M, Studer D (1997) Ultrastructure of adult human articular cartilage matrix after cryotechnical processing. Microsc Res Tech 37(4):271–284. doi:10.1002/(SICI)1097-0029(19970515)37:4<271::AID-JEMT3>3.0.CO;2-O

    Article  CAS  PubMed  Google Scholar 

  • Izu Y, Sun M, Zwolanek D, Veit G, Williams V, Cha B, Jepsen KJ, Koch M, Birk DE (2011) Type XII collagen regulates osteoblast polarity and communication during bone formation. J Cell Biol 193(6):1115–1130. doi:10.1083/jcb.201010010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins E, Moss JB, Pace JM, Bridgewater LC (2005) The new collagen gene COL27A1 contains SOX9-responsive enhancer elements. Matrix Biol 24(3):177–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamper M, Hamann N, Prein C, Clausen-Schaumann H, Farkas Z, Aszodi A, Niehoff A, Paulsson M, Zaucke F (2015) Early changes in morphology, bone mineral density and matrix composition of vertebrae lead to disc degeneration in aged collagen IX -/- mice. Matrix Biol. doi:10.1016/j.matbio.2015.09.005

    PubMed  Google Scholar 

  • Kannu P, Bateman J, Savarirayan R (2012) Clinical phenotypes associated with type II collagen mutations. J Paediatr Child Health 48(2):E38–E43. doi:10.1111/j.1440-1754.2010.01979.x

    Article  PubMed  Google Scholar 

  • Kassner A, Hansen U, Miosge N, Reinhardt DP, Aigner T, Bruckner-Tuderman L, Bruckner P, Grässel S (2003) Discrete integration of collagen XVI into tissue-specific collagen fibrils or beaded microfibrils. Matrix Biol 22(2):131–143

    Google Scholar 

  • Keene DR, Engvall E, Glanville RW (1988) Ultrastructure of type VI collagen in human skin and cartilage suggests an anchoring function for this filamentous network. J Cell Biol 107(5):1995–2006

    Article  CAS  PubMed  Google Scholar 

  • Keene DR, Oxford JT, Morris NP (1995) Ultrastructural localization of collagen types II, IX, and XI in the growth plate of human rib and fetal bovine epiphyseal cartilage: type XI collagen is restricted to thin fibrils. J Histochem Cytochem 43(10):967–979

    Article  CAS  PubMed  Google Scholar 

  • Kielty CM, Whittaker SP, Grant ME, Shuttleworth CA (1992) Type VI collagen microfibrils: evidence for a structural association with hyaluronan. J Cell Biol 118(4):979–990

    Article  CAS  PubMed  Google Scholar 

  • Kimura T, Nakata K, Tsumaki N, Miyamoto S, Matsui Y, Ebara S, Ochi T (1996) Progressive degeneration of articular cartilage and intervertebral discs. An experimental study in transgenic mice bearing a type IX collagen mutation. Int Orthop 20(3):177–181

    Article  PubMed  Google Scholar 

  • Kirsch T, von der Mark K (1991) Isolation of human type X collagen and immunolocalization in fetal human cartilage. Eur J Biochem 196(3):575–580

    Article  CAS  PubMed  Google Scholar 

  • Knupp C, Pinali C, Munro PM, Gruber HE, Sherratt MJ, Baldock C, Squire JM (2006) Structural correlation between collagen VI microfibrils and collagen VI banded aggregates. J Struct Biol 154(3):312–326. doi:10.1016/j.jsb.2006.03.023

    Article  CAS  PubMed  Google Scholar 

  • Koch M, Laub F, Zhou P, Hahn RA, Tanaka S, Burgeson RE, Gerecke DR, Ramirez F, Gordon MK (2003) Collagen XXIV, a vertebrate fibrillar collagen with structural features of invertebrate collagens: selective expression in developing cornea and bone. J Biol Chem 278(44):43236–43244. doi:10.1074/jbc.M302112200

    Article  CAS  PubMed  Google Scholar 

  • Koch M, Schulze J, Hansen U, Ashwodt T, Keene DR, Brunken WJ, Burgeson RE, Bruckner P, Bruckner-Tuderman L (2004) A novel marker of tissue junctions, collagen XXII. J Biol Chem 279(21):22514–22521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kvist AJ, Nystrom A, Hultenby K, Sasaki T, Talts JF, Aspberg A (2008) The major basement membrane components localize to the chondrocyte pericellular matrix--a cartilage basement membrane equivalent? Matrix Biol 27(1):22–33. doi:10.1016/j.matbio.2007.07.007

    Article  CAS  PubMed  Google Scholar 

  • Lam NP, Li Y, Waldman AB, Brussiau J, Lee PL, Olsen BR, Xu L (2007) Age-dependent increase of discoidin domain receptor 2 and matrix metalloproteinase 13 expression in temporomandibular joint cartilage of type IX and type XI collagen-deficient mice. Arch Oral Biol 52(6):579–584

    Article  CAS  PubMed  Google Scholar 

  • Lammi PE, Lammi MJ, Hyttinen MM, Panula H, Kiviranta I, Helminen HJ (2002) Site-specific immunostaining for type X collagen in noncalcified articular cartilage of canine stifle knee joint. Bone 31(6):690–696

    Article  CAS  PubMed  Google Scholar 

  • Lampe AK, Bushby KM (2005) Collagen VI related muscle disorders. J Med Genet 42(9):673–685. doi:10.1136/jmg.2002.002311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehto M, Sims TJ, Bailey AJ (1985) Skeletal muscle injury--molecular changes in the collagen during healing. Res Exp Med (Berl) 185(2):95–106

    Article  CAS  Google Scholar 

  • Lethias C, Descollonges Y, Garrone R, van der Rest M (1993) Expression of type XIV collagen during the differentiation of fetal bovine skin: immunolabeling with monoclonal antibody is prominent in morphogenetic areas. J Invest Dermatol 101(1):92–99

    Article  CAS  PubMed  Google Scholar 

  • Li SW, Prockop DJ, Helminen H, Fassler R, Lapvetelainen T, Kiraly K, Peltarri A, Arokoski J, Lui H, Arita M et al (1995a) Transgenic mice with targeted inactivation of the Col2 alpha 1 gene for collagen II develop a skeleton with membranous and periosteal bone but no endochondral bone. Genes Dev 9(22):2821–2830

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Lacerda DA, Warman ML, Beier DR, Yoshioka H, Ninomiya Y, Oxford JT, Morris NP, Andrikopoulos K, Ramirez F, Wardell BB, Lifferth GD, Teuscher C, Woodward SR, Taylor BA, Seegmiller RE, Olsen BR (1995b) A fibrillar collagen gene, Col11a1, is essential for skeletal morphogenesis. Cell 80:423–430

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Xu L, Olsen BR (2007) Lessons from genetic forms of osteoarthritis for the pathogenesis of the disease. Osteoarthritis Cartilage 15(10):1101–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorenz J, Seebach E, Hackmayer G, Greth C, Bauer RJ, Kleinschmidt K, Bettenworth D, Bohm M, Grifka J, Grassel S (2014) Melanocortin 1 receptor-signaling deficiency results in an articular cartilage phenotype and accelerates pathogenesis of surgically induced murine osteoarthritis. PLoS One 9(9):e105858. doi:10.1371/journal.pone.0105858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marcelino J, McDevitt CA (1995) Attachment of articular cartilage chondrocytes to the tissue form of type VI collagen. Biochim Biophys Acta 1249(2):180–188

    Article  PubMed  Google Scholar 

  • Martel-Pelletier J, Boileau C, Pelletier JP, Roughley PJ (2008) Cartilage in normal and osteoarthritis conditions. Best Pract Res Clin Rheumatol 22(2):351–384

    Article  CAS  PubMed  Google Scholar 

  • Matsuo N, Tanaka S, Yoshioka H, Koch M, Gordon MK, Ramirez F (2008) Collagen XXIV (Col24a1) gene expression is a specific marker of osteoblast differentiation and bone formation. Connect Tissue Res 49(2):68–75. doi:10.1080/03008200801913502

    Article  CAS  PubMed  Google Scholar 

  • McAlinden A (2014) Alternative splicing of type II procollagen: IIB or not IIB? Connect Tissue Res 55(3):165–176. doi:10.3109/03008207.2014.908860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendler M, Eich-Bender SG, Vaughan L, Winterhalter KH, Bruckner P (1989) Cartilage contains mixed fibrils of collagen types II, IX, and XI. J Cell Biol 108(1):191–197

    Article  CAS  PubMed  Google Scholar 

  • Miller EJ, Matukas VJ (1969) Chick cartilage collagen: a new type of alpha 1 chain not present in bone or skin of the species. Proc Natl Acad Sci U S A 64(4):1264–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller-Glauser W, Humbel B, Glatt M, Strauli P, Winterhalter KH, Bruckner P (1986) On the role of type IX collagen in the extracellular matrix of cartilage: type IX collagen is localized to intersections of collagen fibrils. J Cell Biol 102(5):1931–1939

    Google Scholar 

  • Mundlos S, Chan D, McGill J, Bateman JF (1996) An alpha 1(II) Gly913 to Cys substitution prevents the matrix incorporation of type II collagen which is replaced with type I and III collagens in cartilage from a patient with hypochondrogenesis. Am J Med Genet 63(1):129–136. doi:10.1002/(SICI)1096-8628(19960503)63:1<129::AID-AJMG23>3.0.CO;2-P

    Article  CAS  PubMed  Google Scholar 

  • Myllyharju J, Kivirikko KI (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet 20(1):33–43

    Article  CAS  PubMed  Google Scholar 

  • Nakata K, Ono K, Miyazaki J, Olsen BR, Muragaki Y, Adachi E, Yamamura K, Kimura T (1993) Osteoarthritis associated with mild chondrodysplasia in transgenic mice expressing alpha 1(IX) collagen chains with a central deletion. Proc Natl Acad Sci U S A 90(7):2870–2874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman B, Wallis GA (2003) Skeletal dysplasias caused by a disruption of skeletal patterning and endochondral ossification. Clin Genet 63(4):241–251

    Article  CAS  PubMed  Google Scholar 

  • Niyibizi C, Eyre DR (1989) Identification of the cartilage alpha 1(XI) chain in type V collagen from bovine bone. FEBS Lett 242(2):314–318

    Article  CAS  PubMed  Google Scholar 

  • Niyibizi C, Eyre DR (1994) Structural characteristics of cross-linking sites in type V collagen of bone. Chain specificities and heterotypic links to type I collagen. Eur J Biochem 224(3):943–950

    Article  CAS  PubMed  Google Scholar 

  • Niyibizi C, Visconti CS, Kavalkovich K, Woo SL (1995) Collagens in an adult bovine medial collateral ligament: immunofluorescence localization by confocal microscopy reveals that type XIV collagen predominates at the ligament-bone junction. Matrix Biol 14(9):743–751

    Article  CAS  PubMed  Google Scholar 

  • Opolka A, Ratzinger S, Schubert T, Spiegel HU, Grifka J, Bruckner P, Probst A, Grässel S (2007) Collagen IX is indispensable for timely maturation of cartilage during fracture repair in mice. Matrix Biol 26(2):85–95

    Google Scholar 

  • Pace JM, Corrado M, Missero C, Byers PH (2003) Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1. Matrix Biol 22(1):3–14

    Article  CAS  PubMed  Google Scholar 

  • Patra D, Sandell LJ (2012) Antiangiogenic and anticancer molecules in cartilage. Expert Rev Mol Med 14:e10. doi:10.1017/erm.2012.3

    Article  CAS  PubMed  Google Scholar 

  • Plumb DA, Dhir V, Mironov A, Ferrara L, Poulsom R, Kadler KE, Thornton DJ, Briggs MD, Boot-Handford RP (2007) Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens. J Biol Chem 282(17):12791–12795. doi:10.1074/jbc.C700021200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poole CA, Ayad S, Gilbert RT (1992) Chondrons from articular cartilage. V. Immunohistochemical evaluation of type VI collagen organisation in isolated chondrons by light, confocal and electron microscopy. J Cell Sci 103(Pt 4):1101–1110

    CAS  PubMed  Google Scholar 

  • Poole CA, Gilbert RT, Herbage D, Hartmann DJ (1997) Immunolocalization of type IX collagen in normal and spontaneously osteoarthritic canine tibial cartilage and isolated chondrons. Osteoarthritis Cartilage 5(3):191–204

    Article  CAS  PubMed  Google Scholar 

  • Posthumus M, September AV, O’Cuinneagain D, van der Merwe W, Schwellnus MP, Collins M (2010) The association between the COL12A1 gene and anterior cruciate ligament ruptures. Br J Sports Med 44(16):1160–1165. doi:10.1136/bjsm.2009.060756

    Article  PubMed  Google Scholar 

  • Raine EV, Dodd AW, Reynard LN, Loughlin J (2013) Allelic expression analysis of the osteoarthritis susceptibility gene COL11A1 in human joint tissues. BMC Musculoskelet Disord 14:85. doi:10.1186/1471-2474-14-85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reichenberger E, Aigner T, von der Mark K, Stoss H, Bertling W (1991) In situ hybridization studies on the expression of type X collagen in fetal human cartilage. Dev Biol 148(2):562–572

    Article  CAS  PubMed  Google Scholar 

  • Ricard-Blum S (2011) The collagen family. Cold Spring Harb Perspect Biol 3(1):a004978

    Article  PubMed  PubMed Central  Google Scholar 

  • Ricard-Blum S, Ballut L (2011) Matricryptins derived from collagens and proteoglycans. Front Biosci 16:674–697

    Article  CAS  Google Scholar 

  • Ricard-Blum S, Ruggiero F (2005) The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol Biol(Paris) 53(7):430–442

    CAS  Google Scholar 

  • Richards AJ, Yates JR, Williams R, Payne SJ, Pope FM, Scott JD, Snead MP (1996) A family with Stickler syndrome type 2 has a mutation in the COL11A1 gene resulting in the substitution of glycine 97 by valine in alpha 1 (XI) collagen. Hum Mol Genet 5(9):1339–1343

    Article  CAS  PubMed  Google Scholar 

  • Ryan MC, Sandell LJ (1990) Differential expression of a cysteine-rich domain in the amino-terminal propeptide of type II (cartilage) procollagen by alternative splicing of mRNA. J Biol Chem 265(18):10334–10339

    CAS  PubMed  Google Scholar 

  • Sandell LJ (2014) Novel functions for type II procollagen. Connect Tissue Res 55(1):20–25. doi:10.3109/03008207.2013.867340

    Article  CAS  PubMed  Google Scholar 

  • Savontaus M, Metsaranta M, Vuorio E (1997) Mutation in type II collagen gene disturbs spinal development and gene expression patterns in transgenic Del1 mice. Lab Invest 77(6):591–600

    CAS  PubMed  Google Scholar 

  • Schmid TM, Bonen DK, Luchene L, Linsenmayer TF (1991) Late events in chondrocyte differentiation: hypertrophy, type X collagen synthesis and matrix calcification. Vivo 5(5):533–540

    CAS  Google Scholar 

  • Schmid TM, Linsenmayer TF (1985) Immunohistochemical localization of short chain cartilage collagen (type X) in avian tissues. J Cell Biol 100(2):598–605

    Article  CAS  PubMed  Google Scholar 

  • Schmid TM, Popp RG, Linsenmayer TF (1990) Hypertrophic cartilage matrix. Type X collagen, supramolecular assembly, and calcification. Ann N Y Acad Sci 580:64–73

    Article  CAS  PubMed  Google Scholar 

  • Seegmiller R, Fraser FC, Sheldon H (1971) A new chondrodystrophic mutant in mice. Electron microscopy of normal and abnormal chondrogenesis. J Cell Biol 48(3):580–593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw LM, Olsen BR (1991) FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci 16(5):191–194

    Article  CAS  PubMed  Google Scholar 

  • Sherratt MJ, Wess TJ, Baldock C, Ashworth J, Purslow PP, Shuttleworth CA, Kielty CM (2001) Fibrillin-rich microfibrils of the extracellular matrix: ultrastructure and assembly. Micron 32(2):185–200

    Article  CAS  PubMed  Google Scholar 

  • Sherwin AF, Carter DH, Poole CA, Hoyland JA, Ayad S (1999) The distribution of type VI collagen in the developing tissues of the bovine femoral head. Histochem J 31(9):623–632

    Article  CAS  PubMed  Google Scholar 

  • Smeriglio P, Dhulipala L, Lai JH, Goodman SB, Dragoo JL, Smith RL, Maloney WJ, Yang F, Bhutani N (2015) Collagen VI enhances cartilage tissue generation by stimulating chondrocyte proliferation. Tissue Eng Part A 21(3–4):840–849. doi:10.1089/ten.TEA.2014.0375

    Article  CAS  PubMed  Google Scholar 

  • Stoop R, Buma P, van der Kraan PM, Hollander AP, Billinghurst RC, Meijers TH, Poole AR, van den Berg WB (2001) Type II collagen degradation in articular cartilage fibrillation after anterior cruciate ligament transection in rats. Osteoarthritis Cartilage 9(4):308–315. doi:10.1053/joca.2000.0390

    Article  CAS  PubMed  Google Scholar 

  • Suzuki N, Asamura K, Kikuchi Y, Takumi Y, Abe S, Imamura Y, Hayashi T, Aszodi A, Fassler R, Usami S (2005) Type IX collagen knock-out mouse shows progressive hearing loss. Neurosci Res 51(3):293–298

    Article  CAS  PubMed  Google Scholar 

  • Sweeney E, Roberts D, Jacenko O (2011) Altered matrix at the chondro-osseous junction leads to defects in lymphopoiesis. Ann N Y Acad Sci 1237:79–87. doi:10.1111/j.1749-6632.2011.06227.x

    Article  CAS  PubMed  Google Scholar 

  • Taylor DW, Ahmed N, Parreno J, Lunstrum GP, Gross AE, Diamandis EP, Kandel RA (2015) 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 A 21(3–4):683–693. doi:10.1089/ten.TEA.2014.0103

    Article  CAS  PubMed  Google Scholar 

  • van der Kraan PM, Stoop R, Meijers TH, Poole AR, van den Berg WB (2001) Expression of type X collagen in young and old C57Bl/6 and Balb/c mice. Relation with articular cartilage degeneration. Osteoarthritis Cartilage 9(2):92–100. doi:10.1053/joca.2000.0364

    Article  PubMed  Google Scholar 

  • Vaughan L, Mendler M, Huber S, Bruckner P, Winterhalter KH, Irwin MI, Mayne R (1988) D-periodic distribution of collagen type IX along cartilage fibrils. J Cell Biol 106(3):991–997

    Article  CAS  PubMed  Google Scholar 

  • Vikkula M, Mariman EC, Lui VC, Zhidkova NI, Tiller GE, Goldring MB, van Beersum SE, de Waal Malefijt MC, van den Hoogen FH, Ropers HH et al (1995) Autosomal dominant and recessive osteochondrodysplasias associated with the COL11A2 locus. Cell 80(3):431–437

    Article  CAS  PubMed  Google Scholar 

  • Vikkula M, Metsaranta M, Ala-Kokko L (1994) Type II collagen mutations in rare and common cartilage diseases. Ann Med 26(2):107–114

    Google Scholar 

  • Von der Mark K, Gauss V, von der MH, Muller P (1977) Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature 267(5611):531–532

    Google Scholar 

  • Von der Mark K, Kirsch T, Nerlich A, Kuss A, Weseloh G, Gluckert K, Stoss H (1992) Type X collagen synthesis in human osteoarthritic cartilage. Indication of chondrocyte hypertrophy. Arthritis Rheum 35(7):806–811

    Google Scholar 

  • Wachsmuth L, Soder S, Fan Z, Finger F, Aigner T (2006) Immunolocalization of matrix proteins in different human cartilage subtypes. Histol Histopathol 21(5):477–485

    CAS  PubMed  Google Scholar 

  • Walchli C, Koch M, Chiquet M, Odermatt BF, Trueb B (1994) Tissue-specific expression of the fibril-associated collagens XII and XIV. J Cell Sci 107(Pt 2):669–681

    CAS  PubMed  Google Scholar 

  • Walker GD, Fischer M, Gannon J, Thompson RC Jr, Oegema TR Jr (1995) Expression of type-X collagen in osteoarthritis. J Orthop Res 13(1):4–12. doi:10.1002/jor.1100130104

    Article  CAS  PubMed  Google Scholar 

  • Wang CJ, Iida K, Egusa H, Hokugo A, Jewett A, Nishimura I (2008) Trabecular bone deterioration in col9a1+/- mice associated with enlarged osteoclasts adhered to collagen IX-deficient bone. J Bone Miner Res 23(6):837–849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Bryan J, Franz C, Havlioglu N, Sandell LJ (2010) Type IIB procollagen NH(2)-propeptide induces death of tumor cells via interaction with integrins alpha(V)beta(3) and alpha(V)beta(5). J Biol Chem 285(27):20806–20817. doi:10.1074/jbc.M110.118521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warman ML, Cormier-Daire V, Hall C, Krakow D, Lachman R, LeMerrer M, Mortier G, Mundlos S, Nishimura G, Rimoin DL, Robertson S, Savarirayan R, Sillence D, Spranger J, Unger S, Zabel B, Superti-Furga A (2011) Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet A 155A(5):943–968. doi:10.1002/ajmg.a.33909

    Article  PubMed  CAS  Google Scholar 

  • Watt SL, Lunstrum GP, McDonough AM, Keene DR, Burgeson RE, Morris NP (1992) Characterization of collagen types XII and XIV from fetal bovine cartilage. J Biol Chem 267(28):20093–20099

    CAS  PubMed  Google Scholar 

  • Wiberg C, Heinegard D, Wenglen C, Timpl R, Morgelin M (2002) Biglycan organizes collagen VI into hexagonal-like networks resembling tissue structures. J Biol Chem 277(51):49120–49126. doi:10.1074/jbc.M206891200

    Article  CAS  PubMed  Google Scholar 

  • Wiberg C, Klatt AR, Wagener R, Paulsson M, Bateman JF, Heinegard D, Morgelin M (2003) Complexes of matrilin-1 and biglycan or decorin connect collagen VI microfibrils to both collagen II and aggrecan. J Biol Chem 278(39):37698–37704

    Article  CAS  PubMed  Google Scholar 

  • Wood A, Ashhurst DE, Corbett A, Thorogood P (1991) The transient expression of type II collagen at tissue interfaces during mammalian craniofacial development. Development 111(4):955–968

    CAS  PubMed  Google Scholar 

  • Wotton SF, Duance VC (1994) Type III collagen in normal human articular cartilage. Histochem J 26(5):412–416

    Article  CAS  PubMed  Google Scholar 

  • Wu JJ, Eyre DR (1995) Structural analysis of cross-linking domains in cartilage type XI collagen. Insights on polymeric assembly. J Biol Chem 270(32):18865–18870

    Article  CAS  PubMed  Google Scholar 

  • Wu JJ, Eyre DR, Slayter HS (1987) Type VI collagen of the intervertebral disc. Biochemical and electron-microscopic characterization of the native protein. Biochem J 248(2):373–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JJ, Weis MA, Kim LS, Carter BG, Eyre DR (2009) Differences in chain usage and cross-linking specificities of cartilage type V/XI collagen isoforms with age and tissue. J Biol Chem 284(9):5539–5545. doi:10.1074/jbc.M806369200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JJ, Weis MA, Kim LS, Eyre DR (2010) Type III collagen, a fibril network modifier in articular cartilage. J Biol Chem 285(24):18537–18544. doi:10.1074/jbc.M110.112904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu JJ, Woods PE, Eyre DR (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 Chem 267(32):23007–23014

    CAS  PubMed  Google Scholar 

  • Xin W, Heilig J, Paulsson M, Zaucke F (2015) Collagen II regulates chondroycte integrin expression profile and differentiation. Connect Tissue Res 56(4):307–314. doi:10.3109/03008207.2015.1026965

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Flahiff CM, Waldman BA, Wu D, Olsen BR, Setton LA, Li Y (2003) Osteoarthritis-like changes and decreased mechanical function of articular cartilage in the joints of mice with the chondrodysplasia gene (cho). Arthritis Rheum 48(9):2509–2518. doi:10.1002/art.11233

    Article  CAS  PubMed  Google Scholar 

  • Young BB, Gordon MK, Birk DE (2000a) Expression of type XIV collagen in developing chicken tendons: association with assembly and growth of collagen fibrils. Dev Dyn 217(4):430–439. doi:10.1002/(SICI)1097-0177(200004)217:4<430::AID-DVDY10>3.0.CO;2–5

    Article  CAS  PubMed  Google Scholar 

  • Young RD, Lawrence PA, Duance VC, Aigner T, Monaghan P (2000b) Immunolocalization of collagen types II and III in single fibrils of human articular cartilage. J Histochem Cytochem 48(3):423–432

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Orthopaedic Surgery, Experimental Orthopaedics, University of Regensburg, ZMB/BioPark 1, Am BioPark 9, Regensburg, 93053, Germany

    Susanne Grässel Ph.D.

Authors
  1. Susanne Grässel Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susanne Grässel Ph.D. .

Editor information

Editors and Affiliations

  1. Orthopäd.KlinikUniversitätsklinikum.Rege, Orthopäd.KlinikfürdieUniversität.Regen., Regensburg, Germany

    Susanne Grässel

  2. Dept.ofGen.,Trauma&ReconstructionSurgery, Ludwig-Maximilians-University, Munich, Germany

    Attila Aszódi

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Grässel, S. (2016). Collagens in Hyaline Cartilage. In: Grässel, S., Aszódi, A. (eds) Cartilage. Springer, Cham. https://doi.org/10.1007/978-3-319-29568-8_2

Download citation

Publish with us

Policies and ethics

Search

Navigation