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Evolution of collagens

  1. Jean-Yves Exposito†,*,
  2. Caroline Cluzel,
  3. Robert Garrone,
  4. Claire Lethias

Article first published online: 14 OCT 2002

DOI: 10.1002/ar.10162

Issue

The Anatomical Record

The Anatomical Record

Special Issue: Astrobiology

Volume 268, Issue 3, pages 302–316, 1 November 2002

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How to Cite

Exposito, J.-Y., Cluzel, C., Garrone, R. and Lethias, C. (2002), Evolution of collagens. Anat. Rec., 268: 302–316. doi: 10.1002/ar.10162

Author Information

  1. Institut de Biologie et Chimie des Protéines, Université Claude Bernard, Lyon, France

  1. †

    Fax: +33-4-72-72-26-04

*Institut de Biologie et Chimie des Protéines, CNRS UMR 5086, Université Claude Bernard, 7 passage du Vercors, 69367 Lyon Cedex 07, France

Publication History

  1. Issue published online: 14 OCT 2002
  2. Article first published online: 14 OCT 2002
  3. Manuscript Accepted: 28 FEB 2002
  4. Manuscript Received: 14 DEC 2001

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LITERATURE CITED

  • Ackley BD, Crew JR, Elamaa H, Pihlajaniemi T, Kuo CJ, Kramer JM. 2001. The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J Cell Biol 152: 1219–1232.
  • Anderson CM, Wagner TA, Perret M, He ZH, He D, Kohorn BD. 2001. WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47: 197–206.
  • Andersson L, Freeman MW. 1998. Functional changes in scavenger receptor binding conformation are induced by charge mutants spanning the entire collagen domain. J Biol Chem 273: 19592–19601.
  • Andrews RK, Berndt MC. 2000. Snake venom modulators of platelet adhesion receptors and their ligands. Toxicon 38: 775–791.
  • Bailey WJ, Kim J, Wagner GP, Ruddle FH. 1997. Phylogenetic reconstruction of vertebrate Hox cluster duplications. Mol Biol Evol 14: 843–853.
  • Birk DE, Silver FH. 1984. Kinetic analysis of collagen fibrillogenesis: II. Corneal and scleral type I collagen. Coll Relat Res 4: 265–277.
  • Boute N, Exposito JY, Boury-Esnault N, Vacelet J, Noro N, Miyazaki K, Yoshizato K, Garrone R. 1996. Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol Cell 88: 37–44.
  • Bowring SA, Grotzinger JP, Isachsen CE, Knoll AH, Pelechaty SM, Kolosov P. 1993. Calibrating rates of early Cambrian evolution. Science 261: 1293–1298.
  • Burrows NP. 1999. The molecular genetics of the Ehlers-Danlos syndrome. Clin Exp Dermatol 24: 99–106.
    Direct Link:
  • Canfield DE, Teske A. 1996. Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature 382: 127–132.
  • Chen M, Keene DR, Costa FK, Tahk SH, Woodley DT. 2001. The carboxyl terminus of type VII collagen mediates antiparallel dimer formation and constitutes a new antigenic epitope for epidermolysis Bullosa acquisita autoantibodies. J Biol Chem 276: 21649–21655.
  • Choi JK, Ishido S, Jung JU. 2000. The collagen repeat sequence is a determinant of the degree of herpesvirus saimiri STP transforming activity. J Virol 74: 8102–8110.
  • Christiano AM, Hoffman GG, Chung-Honet LC, Lee S, Cheng W, Uitto J, Greenspan DS. 1994. Structural organization of the human type VII collagen gene (COL7A1), composed of more exons than any previously characterized gene. Genomics 21: 169–179.
  • Cluzel C, Lethias C, Garrone R, Exposito JY. 2000. Production in mammalian cells of chimeric human/sea urchin procollagen molecules displaying distinct versions of the minor triple helix. J Biochem (Tokyo) 128: 957–963.
  • Cluzel C, Lethias C, Humbert F, Garrone R, Exposito JY. 2001. Characterization of fibrosurfin, an interfibrillar component of sea urchin catch connective tissues. J Biol Chem 276: 18108–18114.
  • Colombatti A, Doliana R, Bot S, Canton A, Mongiat M, Mungiguerra G, Paron-Cilli S, Spessotto P. 2000. The EMILIN protein family. Matrix Biol 19: 289–301.
  • Coyne KJ, Qin XX, Waite JH. 1997. Extensible collagen in mussel byssus: a natural block copolymer. Science 277: 1830–1832.
  • Davey ME, O'Toole GA. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64: 847–867.
  • Davis JG, Oberholtzer JC, Burns FR, Greene MI. 1995. Molecular cloning and characterization of an inner ear-specific structural protein. Science 267: 1031–1034.
  • DeRobertis EM, Sasai Y. 1996. A common plan for dorsoventral patterning in Bilateria. Nature 380: 37–40.
  • Deutzmann R, Fowler S, Zhang X, Boone K, Dexter S, Boot-Handford RP, Rachel R, Sarras JrMP. 2000. Molecular, biochemical and functional analysis of a novel and developmentally important fibrillar collagen (Hcol-I) in hydra. Development 127: 4669–4680.
  • Doi T, Higashino K, Kurihara Y, Wada Y, Miyazaki T, Nakamura H, Uesugi S, Imanishi T, Kawabe Y, Itakura H, Yasaki H, Matsumoto A, Kodama T. 1993. Charged collagen structure mediates the recognition of negatively charged macromolecules by macrophage scavenger receptors. J Biol Chem 268: 2126–2133.
  • Doliana R, Canton A, Bucciotti F, Mongiat M, Bonaldo P, Colombatti A. 2000. Structure, chromosomal localization, and promoter analysis of the human Elastin Microfibril Interfase Located proteIN (EMILIN) gene. J Biol Chem 275: 785–792.
  • Doolittle RF. 1995. The multiplicity of domains in proteins. Annu Rev Biochem 64: 287–314.
  • Dublet B, Vernet T, van der Rest M. 1999. Schmid's metaphyseal chondrodysplasia mutations interfere with folding of the C-terminal domain of human collagen X expressed in Escherichia coli. J Biol Chem 274: 18909–18915.
  • Elshourbagy NA, Li X, Terrett J, Vanhorn S, Gross MS, Adamou JE, Anderson KM, Webb CL, Lysko PG. 2000. Molecular characterization of a human scavenger receptor, human MARCO. Eur J Biochem 267: 919–926.
    Direct Link:
  • Engel J. 1997. Versatile collagens in invertebrates. Science 277: 1785–1786.
  • Engel J, Kammerer RA. 2000. What are oligomerization domains good for? Matrix Biol 19: 283–288.
  • Erickson PR, Herzberg MC. 1987. A collagen-like immunodeterminant on the surface of Streptococcus sanguis induces platelet aggregation. J Immunol 138: 3360–3366.
  • Exposito JY, Garrone R. 1990. Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families. Proc Natl Acad Sci USA 87: 6669–6673.
  • Exposito JY, Ouazana R, Garrone R. 1990. Cloning and sequencing of a Porifera partial cDNA coding for a short-chain collagen. Eur J Biochem 190: 401–406.
    Direct Link:
  • Exposito JY, Le Guellec D, Lu Q, Garrone R. 1991. Short chain collagens in sponges are encoded by a family of closely related genes. J Biol Chem 266: 21923–21928.
  • Exposito JY, D'Alessio M, Solursh M, Ramirez F. 1992a. Sea urchin homolog of vertebrate pro-α2(I) collagen gene. J Biol Chem 267: 15559–15562.
  • Exposito JY, D'Alessio M, Ramirez F. 1992b. Novel amino-propeptide configuration in a fibrillar procollagen undergoing alternative splicing. J Biol Chem 267: 17404–17408.
  • Exposito JY, van der Rest M, Garrone R. 1993. The complete intron/exon structure of Ephydatia mülleri fibrillar collagen gene suggests a mechanism for the evolution of an ancestral gene module. J Mol Evol 37: 254–259.
  • Exposito JY, Boute N, Deleage G, Garrone R. 1995. Characterization of two genes coding for a similar four-cysteine motif of the amino-terminal propeptide of a sea urchin fibrillar collagen. Eur J Biochem 234: 59–65.
    Direct Link:
  • Exposito JY, Cluzel C, Lethias C, Garrone R. 2000. Tracing the evolution of vertebrate fibrillar collagens from an ancestral α chain. Matrix Biol 19: 275–279.
  • Ezer S, Bayes M, Elomaa O, Schlessinger D, Kere J. 1999. Ectodysplasin is a collagenous trimeric type II membrane protein with a tumor necrosis factor-like domain and co-localizes with cytoskeletal structures at lateral and apical surfaces of cells. Hum Mol Genet 8: 2079–2086.
  • Fields GB. 1991. A model for interstitial collagen catabolism by mammalian collagenases. J Theor Biol 153: 585–602.
  • Fitzgerald J, Bateman JF. 2001. A new FACIT of the collagen family: COL21A1. FEBS Lett 505: 275–280.
  • Fitzgerald J, Morgelin M, Selan C, Wiberg C, Keene DR, Lamande SR, Bateman JF. 2001. The N-terminal N5 subdomain of the α3(VI) chain is important for collagen VI microfibril formation. J Biol Chem 276: 187–193.
  • Fowler SJ, Jose S, Zhang X, Deutzmann R, Sarras JrMP, Boot-Handford RP. 2000. Characterization of hydra type IV collagen. Type IV collagen is essential for head regeneration and its expression is up-regulated upon exposure to glucose. J Biol Chem 275: 39589–39599.
  • Gaill F, Wiedemann H, Mann K, Kuhn K, Timpl R, Engel J. 1991. Molecular characterization of cuticle and interstitial collagens from worms collected at deep sea hydrothermal vents. J Mol Biol 221: 209–223.
  • Garrone R. 1978. Phylogenesis of connective tissue. In: RobertL, editor. Morphological aspects and biosynthesis of sponge intercellular matrix. Basel: S. Karger. 250 p.
  • Garrone R. 1999. Evolution of metazoan collagens. Prog Mol Subcell Biol 21: 119–139.
  • Gatalica B, Pulkkinen L, Li K, Kuokkanen K, Tyynänen M, McGrath JA, Uitto J. 1997. Cloning of the human type XVII collagen gene (COL17A1), and detection of novel mutations in generalized atrophic benign epidermolysis bullosa. Am J Hum Genet 60: 352–365.
  • Giguère Y, Rousseau F. 2000. The genetics of osteoporosis: ‘complexities and difficulties’. Clin Genet 57: 161–169.
    Direct Link:
  • Gilbert W. 1978. Why genes in pieces? Nature 271: 501.
  • Guo XD, Kramer JM. 1989. The two Caenorhabditis elegans basement membrane (type IV) collagen genes are located on separate chromosomes. J Biol Chem 264: 17574–17582.
  • Hakansson K, Reid KB. 2000. Collectin structure: a review. Protein Sci 9: 1607–1617.
    Direct Link:
  • Hudson BG, Reeders ST, Tryggvason K. 1993. Type IV collagen: structure, gene organization, and role in human diseases. Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J Biol Chem 268: 26033–26036.
  • Hynes RO, Zhao Q. 2000. The evolution of cell adhesion. J Cell Biol 150: F89–F95.
  • Hynes WL, Hancock L, Ferretti JJ. 1995. Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity. Infect Immunol 63: 3015–3020.
  • Johnstone IL. 2000. Cuticle collagen genes. Expression in Caenorhabditis elegans. Trends Genet 16: 21–27.
  • Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T. 2001. Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem 276: 19959–19965.
  • Khaleduzzaman M, Sumiyoshi H, Ueki Y, Inoguchi K, Ninomiya Y, Yoshioka H. 1997. Structure of the human type XIX collagen (COL19A1) gene, which suggests it has arisen from an ancestor gene of the FACIT family. Genomics 45: 304–312.
  • Kishore U, Eggleton P, Reid KB. 1997. Modular organization of carbohydrate recognition domains in animal lectins. Matrix Biol 15: 583–592.
  • Kishore U, Reid KB. 1999. Modular organization of proteins containing C1q-like globular domain. Immunopharmacology 42: 15–21.
  • Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ. 2000. The collagen-binding A-domains of integrins α(1)β(1) and α(2)β(1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275: 35–40.
  • Knoll AH, Carroll SB. 1999. Early animal evolution: emerging views from comparative biology and geology. Science 284: 2129–2137.
  • Koch M, Foley JE, Hahn R, Zhou P, Burgeson RE, Gerecke DR, Gordon MK. 2001. α1(XX) collagen, a new member of the collagen subfamily, fibril-associated collagens with interrupted triple helices. J Biol Chem 276: 23120–23126.
  • Kohorn BD. 2001. WAKs: cell wall associated kinases. Curr Opin Cell Biol 13: 529–533.
  • Kolkman JA, Stemmer WP. 2001. Directed evolution of proteins by exon shuffling. Nat Biotechnol 19: 423–428.
  • Kondo N, Kondo J. 1992. Identification of novel blood proteins specific for mammalian hibernation. J Biol Chem 267: 473–478.
  • Krasko A, Lorenz B, Batel R, Schröder HC, Müller IM, Müller WE. 2000. Expression of silicatein and collagen genes in the marine sponge Suberites domuncula is controlled by silicate and myotrophin. Eur J Biochem 267: 4878–4887.
    Direct Link:
  • Krejci E, Thomine S, Boschetti N, Legay C, Sketelj J, Massoulie J. 1997. The mammalian gene of acetylcholinesterase-associated collagen. J Biol Chem 272: 22840–22847.
  • Kuivaniemi H, Tromp G, Prockop DJ. 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 diseases of bone, cartilage, and blood vessels. Hum Mutat 9: 300–315.
    Direct Link:
  • Kvist AP, Latvanlehto A, Sund M, Horelli-Kuitunen N, Rehn M, Palotie A, Beier D, Pihlajaniemi T. 1999. Complete exon-intron organization and chromosomal location of the gene for mouse type XIII collagen (col13a1) and comparison with its human homologue. Matrix Biol 18: 261–274.
  • Kvist AP, Latvanlehto A, Sund M, Eklund L, Vaisanen T, Hagg P, Sormunen R, Komulainen J, Fassler R, Pihlajaniemi T. 2001. Lack of cytosolic and transmembrane domains of type XIII collagen results in progressive myopathy. Am J Pathol 159: 1581–1592.
  • Lawson PR, Perkins VC, Holmskov U, Reid KBM. 1999. Genomic organization of the mouse gene for lung surfactant protein D. Am J Respir Cell Mol Biol 20: 953–963.
  • Ledger PW, Franc S. 1978. Calcification of the collagenous axial skeleton of Veretillum cynomorium pall. (Cnidaria: Pennatulacea). Cell Tissue Res 192: 249–266.
  • Lethias C, Exposito JY, Garrone R. 1997. Collagen fibrillogenesis during sea urchin development: retention of SURF motifs from the N-propeptide of the 2α chain in mature fibrils. Eur J Biochem 245: 434–440.
    Direct Link:
  • Linsenmayer TF, Gibney E, Igoe F, Gordon MK, Fitch JM, Fessler LI, Birk DE. 1993. Type V collagen: molecular structure and fibrillar organization of the chicken α1(V) NH2-terminal domain, a putative regulator of corneal fibrillogenesis. J Cell Biol 121: 1181–1189.
  • Long M. 2001. Evolution of novel genes. Curr Opin Genet Dev 11: 673–680.
  • Ma Y, Shida H, Kawasaki T. 1997. Functional expression of human mannan-binding proteins (MBPs) in human hepatoma cell lines infected by recombinant vaccinia virus: post-translational modification, molecular assembly, and differentiation of serum and liver MBP. J Biochem 122: 810–818.
  • Mann K, Mechling DE, Bachinger HP, Eckerskorn C, Gaill F, Timpl R. 1996. Glycosylated threonine but not 4-hydroxyproline dominates the triple helix stabilizing positions in the sequence of a hydrothermal vent worm cuticle collagen. J Mol Biol 261: 255–266.
  • Matsushita M, Endo Y, Fujita T. 2000. Cutting edge: complement-activating complex of ficolin and mannose-binding lectin-associated serine protease. J Immunol 164: 2281–2284.
  • Miura S, Kimura S. 1985. Jellyfish mesogloea collagen. Characterization of molecules as α1α2α3 heterotrimers. J Biol Chem 260: 15352–15356.
  • Morton LF, Peachey AR, Zijenah LS, Goodall AH, Humphries MJ, Barnes MJ. 1994. Conformation-dependent platelet adhesion to collagen involving integrin α2β1-mediated and other mechanisms: multiple α2β1-recognition sites in collagen type I. Biochem J 299: 791–797.
  • Müller WE. 1997. Origin of metazoan adhesion molecules and adhesion receptors as deduced from cDNA analyses in the marine sponge Geodia cydonium: a review. Cell Tissue Res 289: 383–395.
  • Müller WE, Koziol C, Müller IM, Wiens M. 1999. Towards an understanding of the molecular basis of immune responses in sponges: the marine demosponge Geodia cydonium as a model. Microsc Res Tech 44: 219–236.
    Direct Link:
  • Myllyharju J, Kivirikko KI. 2001. Collagens and collagen-related diseases. Ann Med 33: 7–21.
  • Nieswandt B, Brakebusch C, Bergmeier W, Schulte V, Bouvard D, Mokhtari-Nejad R, Lindhout T, Heemskerk JW, Zirngibl H, Fassler R. 2001. Glycoprotein VI but not α2β1 integrin is essential for platelet interaction with collagen. EMBO J 20: 2120–2130.
  • Ohtani K, Suzuki Y, Eda S, Kawai T, Kase T, Keshi H, Sakai Y, Fukuoh A, Sakamoto T, Itabe H, Suzutani T, Ogasawara M, Yoshida I, Wakamiya N. 2001. The membrane type collectin CL-P1 is a scavenger receptor on vascular endothelial cells. J Biol Chem 276: 44222–44228.
  • Oohashi T, Ueki Y, Sugimoto M, Ninomiya Y. 1995. Isolation and structure of the COL4A6 gene encoding human α6(IV) collagen chain and comparison with other type IV collagen genes. J Biol Chem 270: 26863–26867.
  • Pancer Z, Kruse M, Müller I, Müller WE. 1997. On the origin of Metazoan adhesion receptors: cloning of integrin α subunit from the sponge Geodia cydonium. Mol Biol Evol 14: 391–398.
  • Patthy L. 1996. Exon shuffling and other ways of module exchange. Matrix Biol 15: 301–310.
  • Patthy L. 1999. Genome evolution and the evolution of exon-shuffling—a review. Gene 238: 103–114.
  • Patti JM, Bremell T, Krajewska-Pietrasik D, Abdelnour A, Tarkowski A, Ryden C, Hook M. 1994. The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect Immun 62: 152–161.
  • Philippe H, Germot A, Moreira D. 2000. The new phylogeny of eukaryotes. Curr Opin Genet Dev 10: 596–601.
  • Pihlajaniemi T, Tryggvason K, Myers JC, Kurkinen M, Lebo R, Cheung MC, Prockop DJ, Boyd CD. 1985. cDNA clones coding for the pro-α1(IV) chain of human type IV procollagen reveal an unusual homology of amino acid sequences in two halves of the carboxyl-terminal domain. J Biol Chem 260: 7681–7687.
  • Primorac D, Rowe DW, Mottes M, Barisic I, Anticevic D, Mirandola S, Gomez Lira M, Kalajzic I, Kusec V, Glorieux FH. 2001. Osteogenesis imperfecta at the beginning of bone and joint decade. Croat Med J 42: 393–415.
  • Rasmussen M, Eden A, Bjorck L. 2000. SclA, a novel collagen-like surface protein of Streptococcus pyogenes. Infect Immun 68: 6370–6377.
  • Saito M, Takenouchi Y, Kunisaki N, Kimura S. 2001. Complete primary structure of rainbow trout type I collagen consisting of α1(I)α2(I)α3(I) heterotrimers. Eur J Biochem 268: 2817–2827.
    Direct Link:
  • Saitta B, Wang YM, Renkart L, Zhang RZ, Pan TC, Timpl R, Chu ML. 1991. The exon organization of the triple-helical coding regions of the human α1(VI) and α2(VI) collagen genes is highly similar. Genomics 11: 145–153.
  • Sankoff D. 2001. Gene and genome duplication. Curr Opin Genet Dev 11: 681–684.
  • Sarras JrMP, Deutzmann R. 2001. Hydra and Niccolo Paganini (1782–1840)—two peas in a pod? The molecular basis of extracellular matrix structure in the invertebrate, Hydra. BioEssays 23: 716–724.
    Direct Link:
  • Savage B, Almus-Jacobs F, Ruggeri ZM. 1998. Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 94: 657–666.
  • Schröder HC, Krasko A, Batel R, Skorokhod A, Pahler S, Kruse M, Müller IM, Müller WE. 2000. Stimulation of protein (collagen) synthesis in sponge cells by a cardiac myotrophin-related molecule from Suberites domuncula. FASEB J 14: 2022–2031.
  • Sekine H, Kenjo A, Azumi K, Ohi G, Takahashi M, Kasukawa R, Ichikawa N, Nakata M, Mizuochi T, Matsushita M, Endo Y, Fujita T. 2001. An ancient lectin-dependent complement system in an ascidian: novel lectin isolated from the plasma of the solitary ascidian, Halocynthia roretzi. J Immunol 167: 4504–4510.
  • Sertie AL, Sossi V, Camargo AA, Zatz M, Brahe C, Passos-Bueno MR. 2000. Collagen XVIII, containing an endogenous inhibitor of angiogenesis and tumor growth, plays a critical role in the maintenance of retinal structure and in neural tube closure (Knobloch syndrome). Hum Mol Genet 9: 2051–2058.
  • Shah NK, Sharma M, Kirkpatrick A, Ramshaw JA, Brodsky B. 1997. Gly-Gly-containing triplets of low stability adjacent to a type III collagen epitope. Biochemistry 36: 5878–5883.
  • Shapiro L, Scherer PE. 1998. The crystal structure of a complement-1q family protein suggests an evolutionary link to tumor necrosis factor. Curr Biol 8: 335–338.
  • Shirai H, Murakami T, Yamada Y, Doi T, Hamakubo T, Kodama T. 1999. Structure and function of type I and II macrophage scavenger receptors. Mech Age Dev 111: 107–121.
  • Sicot FX, Exposito JY, Masselot M, Garrone R, Deutsch J, Gaill F. 1997. Cloning of an annelid fibrillar collagen gene and phylogenetic analysis of vertebrate and invertebrate collagens. Eur J Biochem 246: 50–58.
    Direct Link:
  • Sicot FX, Mesnage M, Masselot M, Exposito JY, Garrone R, Deutsch J, Gaill F. 2000. Molecular adaptation to an extreme environment: origin of the thermal stability of the pompeii worm collagen. J Mol Biol 302: 811–820.
  • Smith NG, Knight R, Hurst LD. 1999. Vertebrate genome evolution: a slow shuffle or a big bang? Bioessays 21: 697–703.
    Direct Link:
  • Snellman A, Tu H, Vaisanen T, Kvist AP, Huhtala P, Pihlajaniemi T. 2000. A short sequence in the N-terminal region is required for the trimerization of type XIII collagen and is conserved in other collagenous transmembrane proteins. EMBO J 19: 5051–5059.
  • Su MW, Suzuki HR, Bieker JJ, Solursh M, Ramirez F. 1991. Expression of two nonallelic type II procollagen genes during Xenopus laevis embryogenesis is characterized by stage-specific production of alternatively spliced transcripts. J Cell Biol 115: 565–575.
  • Sutherland IW. 2001. The biofilm matrix—an immobilized but dynamic microbial environment. Trends Microbiol 9: 222–227.
  • Takahara K, Hoffman GG, Greenspan DS. 1995. Complete structural organization of the human α1(V) collagen gene (COL5A1): divergence from the conserved organization of other characterized fibrillar collagen genes. Genomics 29: 588–597.
  • Tillet E, Franc JM, Franc S, Garrone R. 1996. The evolution of fibrillar collagens: a sea-pen collagen shares common features with vertebrate type V collagen. Comp Biochem Physiol B 113: 239–246.
  • Towe KM. 1970. Oxygen-collagen priority and the early metazoan fossil record. Proc Natl Acad Sci USA 65: 781–788.
  • Trotter JA, Koob TJ. 1994. Biochemical characterization of fibrillar collagen from the mutable spine ligament of the sea urchin Eucidaris tribuloides. Comp Biochem Physiol 107B: 125–134.
  • Välkkilä M, Melkoniemi M, Kvist L, Kuivaniemi H, Tromp G, Ala-Kokko L. 2001. Genomic organization of the human COL3A1 andCOL5A2 genes: COL5A2 has evolved differently than the other minor fibrillar collagen genes. Matrix Biol 20: 357–366.
  • van der Rest M, Garrone R. 1991. Collagen family of proteins. FASEB J 5: 2814–2823.
  • Vogel KG, Trotter JA. 1987. The effect of proteoglycans on the morphology of collagen fibrils formed in vitro. Coll Relat Res 7: 105–114.
  • Vuoristo MM, Pihlajamaa T, Vandenberg P, Prockop DJ, Ala-Kokko L. 1995. The human COL11A2 gene structure indicates that the gene has not evolved with the genes for the major fibrillar collagens. J Biol Chem 270: 22873–22881.
  • Wray GA, Levinton JS, Shapiro LH. 1996. Molecular evidence for deep precambrian divergences among metazoan phyla. Science 274: 568573.
  • Yamada Y, Avvedimento VE, Mudryj M, Ohkubo H, Vogeli G, Irani M, Pastan I, de Crombrugghe B. 1980. The collagen gene: evidence for its evolutionary assembly by amplification of a DNA segment containing an exon of 54 bp. Cell 22: 887–892.
  • Yasothornsrikul S, Davis WJ, Cramer G, Kimbrell DA, Dearolf CR. 1997. Viking: identification and characterization of a second type IV collagen in Drosophila. Gene 198: 17–25.
  • Yokota T, Oritani K, Takahashi I, Ishikawa J, Matsuyama A, Ouchi N, Kihara S, Funahashi T, Tenner AJ, Tomiyama Y, Matsuzawa Y. 2000. Adiponectin, a new member of the family of soluble defense collagens, negatively regulates the growth of myelomonocytic progenitors and the functions of macrophages. Blood 96: 1723–1732.
  • Yoneda C, Hirayama Y, Nakaya M, Matsubara Y, Irie S, Hatae K, Watabe S. 1999. The occurrence of two types of collagen proα-chain in the abalone Haliotis discus muscle. Eur J Biochem 261: 714–721.
    Direct Link:
  • Zatterstrom UK, Felbor U, Fukai N, Olsen BR. 2000. Collagen XVIII/endostatin structure and functional role in angiogenesis. Cell Struct Funct 25: 97–101.
  • Zhang Y, Suankratay C, Zhang XH, Lint TF, Gewurz H. 1999. Lysis via the lectin pathway of complement activation: minireview and lectin pathway enhancement of endotoxin-initiated hemolysis. Immunopharmacology 42: 81–90.
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