Abstract
Collagen is the most diffused and common protein in the animal kingdom, responsible for the extracellular framework of all metazoans and, therefore, for animal evolution. It is characterized by a precise wide angle X-ray diffraction pattern (2.8, 4 and 10 Å meridional spacings, and an approximately 11 Å equatorial reflection), and by glycine accounting for 1/3 of the aminoacid residues. The electron microscopical picture of this protein being quite variable (periodate or unperiodate fibrils, and also different periods in various animal groups) different molecular organizations for different tissues or species can be suggested. Doyle et al. (1975) assume the origin of collagen polymorphism to be in the aminoacid sequence, which is responsible also for variations in structure and cross linking. In recent years a number of chains have been described, from the few types present in the triple helix of Cnidaria, to the nine or more chains recognized in the various regions of the mammalian body (Eyre, 1980). Therefore, even if variations in glycosylation, hydroxylation, cross linking are dependent on tissue type, hormonal status and age, a progressive evolution in the molecule itself is quite evident. It is more difficult to relate this process to a phylogenetic design, mainly because in most of invertebrates data on the presence and structure of collagen are completely lacking.
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References
Anya, A.O., 1966, The structure and chemical composition of the nematode cuticle, observations on some oxyurids and Ascaris, Parasitology, 56:179.
Ashhurst, D.E., 1964, Fibrillogenesis in the wax-moth, Galleria mellonella, Q. J. microsc. Sci., 105:391.
Ashhurst, D.E., 1965, The connective tissue sheath of the locust nervous system: its development in the embryo, Q. J. microsc. Sci., 106:61.
Astbury, W.T., 1938, X-ray adventures amongst the proteins, Trans. Faraday Soc., 34:378.
Baccetti, B., 1961a, Primi reperti sulla struttura submicroscopica dello stroma di sostegno di alcuni organi degli insetti, Atti Accademia delle Scienze Torino, 95:343.
Baccetti, B., 1961b, Indagini comparative sulla ultrastruttura della fibrilla collagene nei diversi ordini degli insetti, Redia, 46:1.
Baccetti, B., 1967, Collagen of the earthworms, J. Cell Biol., 34:885.
Bairati, A., 1972, Collagen: an analysis of phylogenetic aspects, Boll. Zool., 39:205.
Bogitsch, B.J., 1962, The chemical nature of metacercarial cysts. I. Histological and histochemical observations on the cysts of Posthodiplostomum minimum, J. Parasitol., 48:55.
Brown, C.H., 1975, “Structural materials in animals,” Pirman Publ., London.
Brown, R.A., Shuttleworth, A., and Weiss, J.B., 1978, Three new a-chains of collagen from a non-basement membrane source, Biochem. Biophys. Res. Commun., 80:866.
Cain, G.D., 1970, Collagen from the giant acanthocephalan Macrocanthorhynchus hirundinaceus, Arch. Biochem. Biophys., 141:264.
Cerfontaine, P., 1890, Recherches sur le système cutané et sur le système musculaire du Lumbricus terrestris, Archs. Biol., Paris, 10:327.
Champetier, G., and Fauré-Fremiet, E., 1938, Etude roentgénographique des kératines sécrétées, C.R. Hebd. Séanc. Acad. Sci., Paris, 207:1133.
Chapman, G., 1966, The structure and function of the mesoglea, in: “The Cnidaria and their Evolution,” W.J. Rees, ed., Symp. Zool. Soc., London, n. 16, Academic Press, London and New York.
Clarke, A.J., Cox, P., and Shepherd, A.M., 1967, Chemical composition of the egg shells of the potato cyste-nematode, Heterodera rostochiensis Woll., Biochem. J., 104:1056.
Coggeshall, R.E., 1966, A fine structural analysis of the epidermis of the earthworm, Lumbricus terrestris L., J. Cell Biol.,28:95.
Conrad, G.W., Kelly, P.T., von der Mark, K., and Edelhauser, H.F., 1981, A comparative study of elasmobranch corneal and scleral collagens, Expl. Eye Res., 32:659.
Cox, G.N., Kusch, M., and Edgar, R.S., 1981, Cuticle of Caenorhabditis elegans: its isolation and partial characterization, J. Cell Biol., 90:7.
Doyle, B.B., Hukins, D.W.L., Hulmes, D.J.S., Miller, A., and Woodhead-Galloway, J., 1975, Collagen polymorphism: its origins in the amino acid sequence, J. Mol. Biol., 91:79.
Eakin, R.M., and Brandenburger, J.L., 1974, Ultrastructural features of a gordian worm (Nematomorpha), J. Ultrastruct. Res., 46:351.
Evans, H.J., Sullivan, C.E., and Piez, K.A., 1976, The resolution of Ascaris cuticle collagen into three chain types, Biochemistry, 15:1435.
Eyre, D.R., 1980, Collagen: molecular diversity in the body’s protein scaffold, Science, 207:1315.
Fauré-Fremiet, E., and Garrault, H., 1944, Proprietés physiques de l’ascarocollagènes, I. Cuticule des Nématodes et Ascarocollagène, Bull. Biol., 78:206.
Fessier, J.H., Bachinger, H.P., Lunstrum, G., and Fessier, L.I., 1982, in: “New Trends in Basement Membrane Research,” K. Kühn, H. Shone, and R. Timpl, eds., Raven Press, New York.
Fleisch, H., and Bisaz, S., 1964, Role of collagen, pyrophosphate and pyrophosphatase in calcification, in: “Bone and Tooth,” Proceedings First European Symposium of the Bone and Tooth Society, H.J.J. Blackwood, ed., Pergamon Press, Oxford.
Fujimoto, D., and Adams, E., 1964, Intra species composition in collagen from cuticle and body of Ascaris and Lumbricus, Biochim. Biophys. Res. Commun., 17:437.
Fujimoto, D., and Prockop, D.J., 1969, Protocollagen proline hydroxylase from Ascaris lumbricoides, J. Biol. Chem., 244:205.
Garrone, R., 1969, Collagène, spongine et squellette mineral chez l’éponge Haliclona rosea (O.S.), J. Micr., 8:581.
Garrone, R., Huc, A., and Junqua, S., 1975, Fine structure and Physicochemical Studies on the Collagen of the Marine Sponge Chondrosia reniformis Nardo, J. Ultrastruct. Res., 52:261.
Goldstein, A., and Adams, E., 1970, Glycylhydroxyprolyl sequences in earthworm cuticle collagen: glycylhydroxyprolylserine, J. Biol. Chem., 245:5478.
Gosline, J.M., 1971, Connective tissue mechanics of Metridium senile. I. Structural and Compositional Aspects, J. Exp. Biol., 55:763.
Grimstone, A.V., Home, R.W., Pantin, C.F.A., and Robson, E.A., 1958, The fine structure of the mesenteries of the sea anemone, Metridium senile, Q. J. micr. Soc., 99:523.
Gross, J., 1963, Comparative biochemistry of collagen, in: “Comparative Biochemistry,” M. Florkin, and H.S. Mason, eds., Elsevier, Amsterdam.
Gross, J., Sokal, Z., and Rougvie, 1956, Structural and chemical studies on the connective tissue of marine sponges, J. Histochem. Cytochem., 4:227.
Hall, D.A., and Saxl, H., 1961, Studies of human and tunicate cellulose and of their relationship to reticulin, Proc. R. Soc. B, 155:202.
Harper, E., Seifter, S., and Scharrer, B., 1967, Electron microscopic and biochemical characterization of collagen in blattarian insects, J. Cell. Biol., 33:385.
Hedley, R.H., and Wakefield, J. St J., 1967, A collagen-like sheath in the arenaceous foraminifer Haliphysema (Protozoa), J. R. microsc. Soc., 87:475.
Hunt, S., Grant, M.E., and Liebovich, S.J., 1970, Polymeric collagen isolated from squid (Loligo peallii) connective tissue, Experientia, 26:1204.
Hung, C.H., Noelken, M.E., and Hudson, H., 1981, Intestinal basement membrane of Ascaris suum. Physical properties of the collagenous domain, J. Biol.Chem., 256:3822.
Isemberg, H.D., Lavine, L.S., Mandell, C., and Weissfellner, H., 1965, Laboratory studies with coccolithophorid calcification, Stud. Trop. Oceanogr., 155.
Isemberg, H.D., Douglas, S.D., Lavine, L.S., Spicer, S.S., and Weissfellner, H., 1966, A protozoan model of hard tissue formation, Ann. N.Y. Acad. Sci., 136:155.
Isemura, M., Ikenaka, T., and Matsushina, Y., 1973, Comparative study of carbohydrate-protein complexes. I. The structures of glycopeptides derived from cuttlefish skin collagen, J. Biochem., (Tokyo), 74:11.
Isemura, M., and Ikenaka, T., 1977, Collagen glycopeptides from the sea cucumber Stichopus japoneus, Experientia, 33:871.
Jope, M., 1967, The protein of brachiopod shell. I. Aminoacid composition and implied protein taxonomy, Comp. Biochem. Physiol. 20:593.
Jope, M., 1969, Protein of brachiopod shells.V. Shell protein from fossil inarticulates: Amino acid composition and disc electrophoresis of fossil articulate shell protein, Comp. Biochem. Physiol., 30:225.
Jope, M., 1971, Constituents of brachiopod shells, in: “Comprehensive Biochemistry”, M. Florkin, and E.H. Stotz, eds., Elsevier, Amsterdam.
Josse, J., and Harrington, W.F., 1964, Role of pyrrolidine residues in the structures and stabilization of collagen, J. Molec. Biol., 9:269.
Katzman, R.L., and Kang, A.H., 1972, The presence of fucose, mannose and glucosamine-containing heteropolysaccharide in collagen from the sea anemone Metridium dianthus, J. Biol. Chem., 247:5486.
Katzman, R.L., and Jeanloz, R.W., 1970, The carbohydrate chemistry of invertebrate connective tissue, in: “Chemistry and Molecular Biology of the Intercellular Matrix”, E.A. Balazs, ed., Vol. 1, Academic Press, New York.
Kefalides, N.A., 1973, Structure and biosynthesis of basement membranes, Int. Rev. Conn. Tissue Res., 6:63.
Kenchington, W., 1969, Silk secretion in Sawflies, J. Morphol., 127:355.
Kimura, S., 1972, Marine invertebrate collagens. V. Neutral sugar compositions and glycosylated hydroxylysine contents of several collagens, Nippon Suisan Gakkaishi, 38:1153.
Kimura, S., 1971a, Marine invertebrate collagens. III. Characterization of cuticle collagen in annelids, Nippon Suisan Gakkaishi, 37:419.
Kimura, S., 1971b, Marine invertebrate collagens. IV. Structural differences in collagen from cuticles and intestines of Neanthes diversicolor, Nippon Suisan Gakkaishi, 37:432.
Kimura, S., Kobayashi, N., and Kubota, M., 1972, Marine invertebrate collagens. VI. Properties of collagen from a ascidian, Halocynthia roretzi, Nippon Suisan Gakkaishi, 38:1163.
Kimura, S., Takema, Y., and Kubota, M., 1981, Octopus skin collagen. Isolation and characterization of collagen comprising two distinct chains, J. Biol. Chem., 265:13230.
Kimura, S., Nagaoka, Y., and Kubota, M., 1969, Marine invertebrate collagens. I. Collagens from crustaceans and molluscans, Nippon Suisan Gakkaishi, 35:743.
Kimura, S., and Kubota, M., 1968, Properties of collagen from the abalone, Nippon Suisan Gakkaishi, 34:925.
Kimura, S., and Matsuura, F., 1974, The chain compositions of several invertebrate collagens, J. Biochem., 75:1231.
Kimura, S., and Tanzer, M.L., 1977, Nereis cuticle collagen: isolation and characterization of two distinct subunits, Biochemistry, 16:2554.
Kuttan, R., and Radhakrishnan, A.N., 1973, Biochemistry of the hydroxyprolines, Adv. Enzymol, 37:273.
Leach, A.A., 1957, The amino acid composition of amphibian, reptilian, and avian gelatins, Biochem. J., 67:83.
Lewis, M.S., and Piez, K.A., 1964, The characterization of collagen from the skin of the dogfish shark, Squalus acanthias, J.Biol. Chem., 239:3336.
Ledger, P.W., and Franc, S., 1978, Calcification of the collagenous axial skeleton of Veretillum cynomorium Pall.(Cnidaria: Pennatulacea), Cell Tissue Res., 192:249.
Lucas, F., and Rudall, K.M., 1968, Extracellular fibrous proteins: the silk, in: “Comprehensive Biochemistry, Vol. 26B, Extracellular and Supporting Structures”, M. Florkin, and E.H. Stotz, eds., Elsevier, New York.
Marks, M.H., Bear, R.S., and Blake, C.H., 1949, X-ray diffraction evidence of collagen type protein fibres in the Echinodermat`, Coelenterata, and Porifera, J. Exp. Zool., 111:55.
Maser, M.D., and Rice, R.V., 1963, Soluble earthworm cuticle collagen: A possible dimer of tropocollagen, J. Cell Biol., 18:569.
Mathews, M.B., 1975, Connective tissue, Macromolecular structure and Evolution, Springer Verlag, Berlin, Heidelberg, New York.
Mayne, R., and Zettergren, J.G., 1980, Type IV collagen from chicken muscular tissues. Isolation and characterization of the pepsin resistant fragments, Biochemistry, 19:4065.
McBride, O.W., and Harrington, W.F., 1967, Helix-coil transition in collagen. Evidence for a single-stranded triple helix, Biochemistry, 6:1499.
Miller, E.J., and Mathews, M.B., 1974, Characterization of notochord collagen as a cartilage-type collagen, Biochem. Biophys. Res. Commun., 60:424.
Monson, J.M., Natzle, L., Friedman, J., and McCarthy, B.L., 1982, Expression and novel structure of a collagen gene in Drosophila, Proc. Natl. Acad. Sci., 79:1761.
Murray, L.W., Tanzer, M.L., and Cooke, P., 1981, Nereis cuticle collagen: relationship of fiber ultrastructure to biochemical and biophysical properties, J. Ultrastruct. Res., 76:27.
Nordwig, A., and Hayduk, U., 1967, A contribution to the evolution of collagen, J. Molec. Biol., 26:351.
Nordwig, A., and Hayduk, U., 1969, Invertebrate collagens: isolation, characterization and phylogenetic aspects, J. Molec. Biol. 44:161.
Nordwig, A., Nowack, H., and Hieber-Rogall, E., 1973, Sea anemone collagen: further evidence for the existence of only one a chain type, J.Molec. Evol., 2:175.
Olsson, R., 1961, The skin of Amphioxus, Z. Zellforsch., 54:90.
Peczon, B.D., Venable, J.H., Beams, C.G.Jr., and Hudson, B.G., 1975, Intestinal basement membrane of Ascaris suum. Preparation, morphology and composition, Biochemistry, 14:4069.
Person, P., and Philpott, D.E., 1969, The nature and significance of invertebrate cartilage, Biol. Rev., 44:1.
Philpott, D.E., and Person, P., 1970, The biology of cartilage. II. Invertebrate cartilages: squid head cartilage, J. Morphol., 131:417.
Picken, L.E.R., Pryor, M.G.M., and Swann, M.M., 1947, Orientation of fibrils in natural membranes, Nature, London, 159:434.
Piez, K.A., 1965, Characterization of a collagen from codfish skin containing three chromatographically different chains, Biochemistry, 4:2590.
Piez, K.A., and Gross, J., 1959, The amino acid composition and morphology of some invertebrate and vertebrate collagens, Biochim. Biophys. Acta., 34:24.
Pikkarainen, J., 1968, The molecular structure of vertebrate skin collagens, Acta Physiol. Scand. Suppl. 309.
Pikkarainen, J., Rantanen, J., Vastamaki, M., Lampiaho, K., Kari, A., and Kulonen, E., 1968, On collagens of invertebrates with special reference to Mytilus edulis, Eur. J. Biochem., 4:555.
Pipa, R.L., and Woolever, P.S., 1965, Insect neurometamorphosis. II. The fine structure of perineural connective tissue, adipohemocytes and the shortening central nerve cord of a moth, Galleria mellonella, Z. Zellforsch. mikrosk. Anat., 68:80.
Plummer, J.M., 1966, Collagen formation in Achatinidae associated with a specific cell type, Proc. Malacol. Soc. Lond., 37:189.
Pucci Minafra, I., Galante, R., and Minafra, S., 1978, Identification of collagen in the Aristotle lanternae of Paracentrotus lividus, J. Submicr. Cytol., 10:53.
Randall, J.T., Fraser, R.D.B., Jackson, S.F., Martin, A.V.W., and North, A.C.T., 1952, Aspects of collagen structure, Nature, Lond., 169:1029.
Rhodes, R.K., and Miller, E.J., 1978, Physicochemical characterization and molecular organization of the collagen A and B chains, Biochemistry, 17:3442.
Rhodes, R.K., Gibson, K.D., and Miller, E.J., 1981, Isolation and characterization of the cyanogen bromide peptides derived from the human α2(V) collagen chain, Biochemistry, 20:3117.
Richard, A.G., and Schneider, D., 1958, Ueber die complexen Bau der Membranen des Bindegewebes von Insekten, Z.Naturf., 13b:680.
Rigby, B.J., 1968, Thermal transitions in some invertebrate collagens and their relation to amino acid content and environmental temperature, in: “Symposium on Fibrous Proteins, Australia 1967”, W.G. Grewther, ed., Butterworth, Sidney.
Rigby, B.J., and Mason, P., 1967, Thermal transitions in gastropod collagen and their correlation with environmental temperature, Aust. J. Biol. Sci., 20:265.
Rudall, K.M., 1955, The distribution of collagen and chitin, in: “Fibrous Proteins and their Biological Significance”, M. Brown, and J.F. Danielli, eds., Symp. Soc. Exper. Biol. 9, Academic Press, New York.
Rudall, K.M., 1968, Comparative biology and biochemistry of collagen, in: “Treatise on Collagen”, B.S. Gould, ed., Vol. II Part A, Academic Press, London and New York.
Rudall, K.M., 1965, Protein in polysaccharide interactions in chiti-nous structures, in: “Structure and function of connective and skeletal tissue”, S. Fitton Jackson, R.D. Harkness, S.M. Partridge, and G.R. Tristan, eds., Butterworths, London.
Thompson, H.C., Jr, and Thompson, M.H., 1968, Isolation and amino acid composition of the collagen of the white shrimp (Penaeus setiferus).I., Comp.Biochem. Physiol., 27:127.
Thompson, H.C., Jr., and Thompson, M.H., 1970, Isolation and amino acid composition of the collagen of the white shrimp (Penaeus setiferous). II., Comp. Biochem. Physiol., 35:471.
Toole, B.P., Kang, A.H., Trelstad, R.L., and Gross, J., 1972, Collagen heterogeneity within different growth regions of long bone of rachitic and non rachitic chicks, Biochem. J., 127:715.
Travis, D.F., François, C.J., Bonar, L.C., and Glimcher, M.J., 1967, Comparative studies of the organic matrices of invertebrate mineralized tissues, J. Ultrastruct. Res., 18:519.
Trelstad, R.L., Kang, A.H., and Gross, J., 1971, Characterization of a new type collagen in the embryonic chick skin, Fedn. Proc., 30:1196 bis.
Vitellaro-Zuccarello, L., 1979, Fine structure of isolated fibrils from the cuticle of Lumbricus sp., Cell Tissue Res., 201:459.
Watson, M.R., and Silvester, N.R., 1959, Studies of invertebrate collagen preparation, Biochem. J., 71:578.
Watson, M.R., 1958, The chemical composition of earthworm cuticle, Biochem. J., 68:416.
Williams, A.P., 1960, The chemical composition of snail gelatin, Biochem. J., 74:304.
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Baccetti, B. (1985). Collagen and Animal Phylogeny. In: Bairati, A., Garrone, R. (eds) Biology of Invertebrate and Lower Vertebrate Collagens. NATO ASI Series, vol 93. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-7636-1_2
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