Abstract
Collagen is one of the most widespread structural proteins in animals, and more than 23 genetically-distinct types of collagen are found in man (for review see [1]). Collagens comprise three polypeptide chains in which glycine (the smallest amino acid) occurs at every third residue position. The repeating Gly-X-Y motif (in which X and Y can be any amino acid and is often proline and hydroxyproline amino acids) is required for three polypeptide chains to assemble into a triple helix. The most abundant collagens are the fibril-forming types I, II, III, V and XI, which contain three polypeptide chains, each containing ~1000 residues, wound into an uninterrupted triple helix of ~295 nm in length (for review see [2]). These collagens occur in the extracellular matrix as D-periodic fibrils (where D = ~ 67 nm, the axial periodicity), which are indeterminate in length [3], and have a near-uniform diameter in the range 12-500 nm depending on tissue and stage of development (see Fig.1). The fibrils are heterotypic and contain more than one genetic type of collagen. For example, collagen fibrils in cartilage comprise type II collagen and minor quantities of type XI collagen and type IX collagen. The type IX collagen is an example of a fibril-associated collagen with interrupted triple helices (FACIT). Fibrils in other tissues contain type I collagen with minor amounts of type III and V collagen. The fibrils are stabilized by interchain covalent crosslinks, which require oxidative deamination of specific lysyl and hydroxylysyl residues by lysyl oxidase(s) (for review see [4]). The fibrils have binding sites on their surfaces for small leucine rich proteoglycans (SLRPs) [5].
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References
Kielty CM, Grant ME (2002) The collagen family: structure, assembly and organization in the extracellular matrix. In: B Steinmann, PM Royce (eds): Connective tissue and its heritable diseases 2nd ed. PM Wiley Liss, New York
Kadler KE, Holmes DF, Trotter J, Chapman JA (1996) Collagen fibril formation. Biochem J 316: 1–11
Parry DAD, Craig, AS (1984) Growth and development of collagen fibrils in connective tissue. In: A Ruggeri, PM Motta (eds): Ultastructure of the connective tissue matrix. Martinus Nijhoff Publishers, 34–64
Smith-Mungo LI, Kagan HM (1998) Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol 16: 387–398
lozzo RI (1999) The biology of the small leucine rich proteoglycans. J Biol Chem 274:18843–18846
Lees JF, Tasab M, Bulleid NJ (1997) Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J 16: 908–916
Kadler KE, Hojima Y, Prockop D J (1987) Assembly of collagen fibrils de novo by enzymic cleavage of the type I pCcollagen by procollagen C-proteinase. Assay of critical concentration demonstrates that the process is an example of classical entropy-driven self assembly. J Biol Chem 262: 15696–15701
Kessler E, Takahara K, Biniaminov L, Brusel M, Greenspan DS (1996) Bone morphogenetic protein-1: The type I procollagen C-proteinase. Science 271: 360–362
Li S-W, Sieron AL, Fertala A, Hojima Y, Arnold WV, Prockop DJ (1996) The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as hone morphogenetic protein-1. Proc Natl Acad Sci USA 93: 5127–5130
Scott IC, Blitz IL, Pappano WN, Imamura Y, Clark TG, Steiglitz BM, Thomas CL, Maas SA, Takahara K, Cho KW, Greenspan DS (1999) Mammalian BMP-1/tolloid-related metalloproteinases, including novel family member mammalian tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis. Developmental Biol 213: 282–300
Chapman JA (1989) The regulation of size and form in the assembly of collagen fibrils in vivo. Biopolymers 28: 1367–1382 (addition: 28: 2201–2205)
Holmes DF, Watson RB, Steinmann B, Kadler KE (1993) Ehlers Danlos syndrome type VIIB. Morphology of type I collagen fibrils is determined by the conformation of the Npropeptide. J Biol Chem 268: 15758–15765
Zhu Y, Oganesian A, Keene DR, Sandell LJ (1999) Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta 1 and BMP-2. J Cell Biol 144: 1069–1080
Coige A, Li S-W, Sieron A, Nusgens BV, Prockop DJ, Lapiere CM (1997) CDNA cloning and expression of bovine procollagen (N-proteinase: a new member of the superfamily of zinc-metalloproteinases with binding sites for cells and other matrix components. Proc Natl Acad Sci USA 94: 2374–2379
Colige A, Beschin A, Samyn B, Goebels Y, Beeumen JV, Nusgens BV, Lapiere CM (1995) Characterization and partial amino acid sequencing of a 107-kDa procollagen I N-proteinase purified by affinity chromatography on immobilized type XIV collagen. J Biol Chem 270: 16724–16730
Fernandes RJ, Hirohata S, Engle JM, Colige A, Cohn DH, Eyre DR, Apte SS (2000) Pro-collagen II amino propeptide processing by ADAMTS-3. Insights on dermatosparaxis. J Biol Chem 276: 31502–31509
Hojima Y, van der Rest M, Prockop DJ (1985) Type I procollagen carboxyl terminal proteinase from chick embryo tendons — purification and characterisation. J Biol Chem 260: 5996–6003
Kadler KE, Hojima Y, Prockop DJ (1990) Collagen fibrilsin vitrogrow from pointed tips in the C- to N-terminal direction. Biochem J 268: 339–343
Holmes DF, Chapman JA, Prockop DJ, Kadler KE (1992) Growing tips of type I collagen fibrils formed in vitro are near-paraboloidal in shape, implying a reciprocal relationship between accretion and diameter. Proc Natl Acad Sci USA 89: 9855–9859
Holmes DF, Watson RB, Chapman JA, Kadler KE (1996) Enzymic control of collagen fibril shape. J Mol Biol 261: 93–97
Holmes DF, Graham HK, Kadler KE (1998) Collagen fibrils forming in developing tendon show an early and abrupt limitation in diameter at the growing tips unobserved in cell-free systems. J Mol Biol 283: 1049–1058
Holmes DF, Lowe MP, Chapman JA (1994) Vertebrate (chick) collagen fibrils formed in vivo can exhibit a reversal in molecular polarity. J Mol Biol 235: 80–83
Graham HK, Holmes DF, Watson RB, Kadler KE (2000) Identification of collagen fibril fusion during vertebrate tendon morphogenesis. The process relies on molecular recognition sequences in unipolar fibrils and is regulated by collagen-proteoglycan interaction. J Mol Biol 295: 891–902
Birk DE, Nurminskaya MV, Zycband EI (1995) Collagen fibrillogenesis in-situ — fibril segments undergo postdepositional modifications resulting in linear and lateral growth during matrix development. Developmental Dynamics 202:229–243
Birk DE, Hahn RA, Linsenmayer CY, Zycband EI (1996) Characterization of collagen fibril segments from chicken embryo cornea, dermis and tendon. Matrix Biology 15: 111–118
Birk DE, Zycband EI, Woodruff S, Winkelmann DA, Trelstad RL (1997) Collagen fibrillogenesis in situ: Fibril segments become long fibrils as the developing tendon matures. Developmental Dynamics 208: 291–298
Wess TJ, Hammersley AP, Wess L, Miller A (1998) A consensus model for molecular packing of type I collagen. J Struct Biol 122: 92–100
Eikenberry EF, Childs B, Sheren SB, Parry DA, Craig AS, Brodsky B (1984) Crystalline fibril structure of type II collagen in lamprey notochord sheath. J Mol Biol 176: 261–277
Hulmes DJS, Miller A (1979) Quasi-hexagonal molecular packing in collagen fibrils. Nature 282: 878–880
Fraser RDB, MacRae TP, Miller A (1987) Molecular packing in type I collagen fibrils. J Mol Biol 193: 115–125
Miller A, Tocchetti D (1981) Calculated x-ray diffraction pattern from a quasi-hexago-nal model for the molecular arrangement in collagen. Int J Biol Macromol 3: 9–18
Smith JW (1968) Molecular packing in native collagen. Nature 219: 157–158
Piez KA, Trus BL (1978) Sequence regularities and packing of collagen molecules. J Mol Biol 122: 419–432
Piez KA, Trus BL (1981) A new model for packing of type I collagen molecules in the native fibril. Biosci Rep 1: 801–810
Wess TJ, Hammersley AP, Wess L, Miller A (1998) Molecular packing of type I collagen in tendon. J Mol Biol 275: 255–267
Holmes DF, Gilpin CJ, Baldock C, Ziese U, Koster AJ, Kadler KE (2001) Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organisation. Proc Natl Aced Sci USA 98: 7307–7312
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Kadler, K.E., Holmes, D.F. (2002). Electron microscope studies of collagen fibril formation in cornea, skin and tendon: Implications for collagen fibril assembly and structure in other tissues. In: Hascall, V.C., Kuettner, K.E. (eds) The Many Faces of Osteoarthritis. Birkhäuser, Basel. https://doi.org/10.1007/978-3-0348-8133-3_12
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DOI: https://doi.org/10.1007/978-3-0348-8133-3_12
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