Skip to main content
SpringerLink
Log in

Collagen Biosynthesis

  • Chapter
Cell Biology of Extracellular Matrix

Abstract

The biosynthesis of the collagen components of connective tissues involves the regulated expression of members of the large collagen gene superfamily as well as complex interactions between primary collagen translation products and several cotranslational and posttranslational modifying enzymes (for review, see Vuorio and de Crombrugghe, 1990; Mayne and Burgeson, 1987; Ninomiya et al., 1990; Fleischmajer et al., 1990). Although the total number of genes that code for collagenous polypeptides has not yet been established, more that 25 genes have been cloned and characterized and the number is rapidly increasing. In addition, several proteins (Clq, acetylcholinesterase, conglutinin, macrophage scavenger receptor, surfactant proteins, mannose-binding lectins) that are not usually included among the collagens contain triple-helical sequence domains and are therefore also collagenous in nature.

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 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Barker, D. F., Hostikka, S. L., Zhou, J., Chow, L. T., Oliphant, A. R., Gerken, S. C., Gregory, M. C., Skolnick, M. R, Atkin, C. L., and Tryggvason, K., 1990, Identification of mutations in the COL4A5 collagen gene in Alport syndrome, Science 248:1224–1227.

    Article  PubMed  CAS  Google Scholar 

  • Bassuk, J. A., and Berg, R. A., 1989, Protein disulphide isomerase, a multifunctional endoplasmic reticulum protein, Matrix 9:244–258.

    Article  PubMed  CAS  Google Scholar 

  • Bateman, J. F., Lamande, S. R., Dahl, H.-H. M., Chan, D., and Mascara, T., 1989, A frameshift mutation results in a truncated nonfunctional carboxyl-terminal proal(I) propeptide of type I collagen in osteogenesis imperfecta, J. Biol. Chem. 264:10960–10964.

    PubMed  CAS  Google Scholar 

  • Becker, V., Timpl, R., Helle, O., and Prockop, D. J., 1976, NH2-terminal extensions on skin collagen from sheep with a genetic defect in conversion of procollagen into collagen Biochemistry 15:2853–2862.

    CAS  Google Scholar 

  • Bennet, V. D., and Adams, S L., 1990, Identification of a cartilage-specific promoter within intron 2 of the chick a2(I) collagen gene, J. Biol. Chem. 265:2223–2230.

    Google Scholar 

  • Berg, R. A., and Prockop, D. J., 1973, Affinity column purification of protocollagen proline hydroxylase from chick embryos and further characterization of the enzyme, J. Biol. Chem. 248:1175–1182.

    PubMed  CAS  Google Scholar 

  • Berg, R. A., Kao, W. Y., and Kedersha, L. L., 1980, The assembly of tetrameric prolyl hydroxylase in tendon fibroblasts from newly synthesized a-subunits and from preformed cross-reacting protein, Biochem. J. 189:491–499.

    PubMed  CAS  Google Scholar 

  • Bernard, M., Yoshioka, H., Rodriguez, E., van der Rest, M., Kimura, T., Ninomiya, Y., and Olsen, B. R., 1988, Cloning and sequencing of proal(XI) collagen cDNA demonstrates that type XI belongs to the fibrillar class of collagens and reveals that the expression of the gene is not restricted to cartilaginous tissue, J. Biol. Chem. 263:17159–17166.

    PubMed  CAS  Google Scholar 

  • Boado, R. J., Campbell, D. A., and Chopra, I. J., 1988, Nucleotide sequence of rat liver iodothyronine 5’-monodeiodinase (5’MD): Its identity with the protein disulfide isomerase, Biochem. Biophys. Res. Commun. 155:1287–1304.

    Article  Google Scholar 

  • Boedtker, H., Finer, M., and Aho, S., 1985, The structure of the chicken a2 collagen gene, Ann. N.Y. Acad. Sci. 470:85–116.

    Article  Google Scholar 

  • Bonaldo, P., Russo, V., Bucciotti, F., Doliana, R., and Colombatti, A., 1990, Structural and functional features of the a3 chain indicate a bridging role for chicken collagen VI in connective tissues, Biochemistry 29:1245–1254.

    Article  PubMed  CAS  Google Scholar 

  • Bornstein, P., and McKay, J., 1988, The first intron of the al(I) collagen gene contains several transcriptional regulatory elements, J. Biol. Chem. 263:1603–1606.

    PubMed  CAS  Google Scholar 

  • Bornstein, P., and Sage, H., 1980, Structurally distinct collagen types, Annu. Rev. Biochem. 49:957–1003.

    Article  PubMed  CAS  Google Scholar 

  • Bornstein, P., and Sage, H., 1989, Regulation of collagen gene expressionProg. Nucleic Acid Res. Mol. Biol. 37:67–106.

    Article  PubMed  CAS  Google Scholar 

  • Bornstein, P., McKay, J., Morishima, J. K., Devarayalu, S., and Gelinas, R. E., 1987, Regulatory elements of the first intron contribute to transcriptional control of the human a1(I) collagen gene, Proc. Natl. Acad. Sci. USA 84:8869–8873.

    Article  PubMed  CAS  Google Scholar 

  • Bornstein, P., McKay, J., Liska, D. J., Apone, S., and Devarayalu, S., 1988, Interactions between the promoter and first intron are involved in transcriptional control of a1(I) collagen gene expression, Mol. Cell. Biol. 8:4851–4857.

    PubMed  CAS  Google Scholar 

  • Breindl, M., Harbers, K., and Jaenisch, R., 1984, Retrovirus-induced lethal mutation in collagen I gene of mice is associated with an altered chromatin structure, Cell 38:9–16.

    Article  PubMed  CAS  Google Scholar 

  • Bruns, R. R., Hulmes, D. J. S., Therrien, S. F., and Gross, J., 1979, Procollagen segment-long-spacing crystallites: Their role in collagen fibrillogenesis, Proc. Natl. Acad. Sci. USA 76:313–317.

    Article  PubMed  CAS  Google Scholar 

  • Burbelo, P., Martin, G., and Yamada, Y., 1988, ¦Á1(IV) and al(IV) collagen genes regulated by a bidirectional promoter and a shared enhancer, Proc. Natl. Acad. Sci. USA 85:9674–9682.

    Article  Google Scholar 

  • Burbelo, P., Killen, P. D., Ebihara, I., Sakurai, Y., and Yamada, Y., 1989, Structure and expression of collagen IV genes, in: Collagen—Molecular Biology, Vol. IV (B. R. Olsen and M. E. Nimni, eds.), pp. 51–64, CRC Press, Boca Raton, Fla.

    Google Scholar 

  • Butkowski, R. J., Langeveld, J. P. M., Wieslander, J., Hamilton, J., and Hudson, B. G., 1987, Localization of the Goodpasture epitope to a novel chain of basement membrane collagen, J. Biol. Chem. 262:7874–7877.

    PubMed  CAS  Google Scholar 

  • Byers, P. H., and Bonadio, J. F., 1989, The nature, characterization and phenotypic effects of mutations that affect collagen structure and processing, in: Collagen—Molecular Biology, Vol. IV (B. R. Olsen and M. E. Nimni, eds.), pp. 125–139, CRC Press, Boca Raton, Fla.

    Google Scholar 

  • Byers, P. H., Click, E. M., Harper, E., and Bornstein, P., 1975, Interchain disulfide bonds in pro-collagen are located in a large non-triple-helical COOH-terminal domain, Proc. Natl. Acad. Sci. USA 72:3009–3013.

    Article  CAS  Google Scholar 

  • Cassidy, K., Eikenberry, E. F., Olsen, B. R., and Brodsky, B., 1980, X-ray diffraction investigations of collagen fibril structure in dermatosparactic lamb tissues, Lab. Invest. 43:542–546.

    PubMed  CAS  Google Scholar 

  • Chapman, J. A., 1989, The regulation of size and form in assembly of collagen fibrils in vivo, Biopolymers 28:1367–1382.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, S.-Y., Gong, Q.-H., Parkinson, C., Robinson, E. A., Appella, E., Merlino, G. T., and Pastan, I., 1987, The nucleotide sequence of human cellular thyroid hormone binding protein present in endoplasmic reticulum, J. Biol. Chem. 257:11221–11227.

    Google Scholar 

  • Chen-Kiang, S., Cardinale, G. J., and Udenfriend, S., 1977, Homology between a prolyl hydroxylase subunit and a tissue protein that crossreacts immunologically with the enzyme, Proc. Natl. Acad. Sci. USA 74:4420–4424.

    Article  PubMed  CAS  Google Scholar 

  • Chu, M.-L., Pan, T.-C., Conway, D., Saitta, B., Stokes, D., Kuo, H.-J., Glanville, R. W., Timpl, R., Mann, K., and Deutzmann, R., 1990, The structure of type VI collagen, Ann. N.Y. Acad. Sci. 580:55–63.

    Article  PubMed  CAS  Google Scholar 

  • Clark, C. C., 1979, The distribution and initial characterization of oligosaccharide units on the COOH-terminal propeptide extensions of the pro-a1 and pro-a2 chains of type I procollagen, J. Biol. Chem. 254:10798–10802.

    PubMed  CAS  Google Scholar 

  • Deak, S. B. M., Pope, F. M., and Prockop, D. J., 1983, The molecular defect in a nonlethal variant of osteogenesis imperfecta, J. Biol. Chem. 258:15192–15197.

    PubMed  CAS  Google Scholar 

  • Diegelmann, R. F., Bernstein, L., and Peterkofsky, B., 1973, Cell-free synthesis on membrane-bound polysomes of chick embryo connective tissue and the localization of prolyl hydroxylase on the polysome¨Cmembrane complex, J. Biol. Chem. 248:6514–6521.

    PubMed  CAS  Google Scholar 

  • Dölz, E., and Engel, J., 1990, Nucleation, propagation, and direction of triple-helix formation in collagens, I, III, and IV and in gelatin as monitored by electron microscopy, Ann. N.Y. Acad. Sci. 580:421–424.

    Article  Google Scholar 

  • Dombrowski, K. E., Vogel, B. E., and Prockop, D. J., 1989, Mutations that alter the primary structure of type I procollagen have long-range effects on its cleavage by procollagen N-proteinase, Biochemistry 28:7107–7112.

    Article  PubMed  CAS  Google Scholar 

  • Duksin, D., and Bornstein, P., 1977, Impaired conversion of procollagen to collagen by fibroblasts and bone treated with tunicamycin, an inhibitor of protein glycosylation, J. Biol. Chem. 252:955–962.

    PubMed  CAS  Google Scholar 

  • Duksin, D., Davidson, M. M., and Bornstein, P., 1978, The role of glycosylation in the enzymatic conversion of procollagen to collagen: Studies using tunicamycin and concanavalin A, Arch. Biochem. Biophys. 185:326–332.

    Article  PubMed  CAS  Google Scholar 

  • Edman, J. C., Ellis, L., Blacher, R. W., Roth, R. A., and Rutter, W. J., 1985, Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin, Nature 317:267–270.

    Article  PubMed  CAS  Google Scholar 

  • Fessier, L. I., and Fessier, J. H., 1979, Characterization of type III procollagen from chick embryo blood vessels, J. Biol. Chem. 254:233–239.

    Google Scholar 

  • Fessier, L. I., Morris, N. P., and Fessier, J. H., 1975, Procollagen: Biological scission of amino and carboxyl extension peptides, Proc. Natl. Acad. Sci. USA 72:4905–4909.

    Article  Google Scholar 

  • Fjolstad, M., and Helle, O., 1974, A hereditary dysplasia of collagen tissues in sheep, J. Pathol. 112:183–188.

    Article  PubMed  CAS  Google Scholar 

  • Fleischmajer, R., Olsen, B. R., Timpl, R., Perlish, J. S., and Lovelace, O., 1983, Collagen fibril formation during embryogenesis, Proc. Natl. Acad. Sci. USA 80:3354–3358.

    Article  PubMed  CAS  Google Scholar 

  • Fleischmajer, R., Kühn, K., and Olsen, B. R. (eds), 1990, Structure, Molecular Biology, and Pathology of Collagen, Ann. N.Y. Acad. Sci. 580.

    Google Scholar 

  • Geetha-Habid, M., Noiva, R., Kaplan, H. A., and Lennarz, W. J., 1988, Glycosylation site binding protein, A component of oligosaccharyl transferase, is highly similar to three other 57 kd luminal proteins of the ER, Cell 54:1053–1060.

    Article  Google Scholar 

  • Goldberg, B., Taubman, M. B., and Radin, B., 1975, Procollagen peptidase: Its mode of action on the native substrate, Cell 4:45–50.

    Article  PubMed  CAS  Google Scholar 

  • Gong, Q.-H., Fukuda, T., Parkinson, C., and Cheng, S.-Y., 1988, Nucleotide sequence of a full-length cDNA clone encoding a mouse cellular thyroid hormone binding protein (p55) that is homologous to protein disulphide isomerase and the 3-subunit of prolyl 4-hydroxylase, Nucleic Acids Res. 16:1203.

    Article  PubMed  CAS  Google Scholar 

  • Gordon, M. K., Gerecke, D. R., Dublet, B., van der Rest, M., and Olsen, B. R., 1989, Type XII collagen—A large multidomain molecule with partial homology to type IX collagen, J. Biol. Chem. 264:19772–19778.

    PubMed  CAS  Google Scholar 

  • Halila, R., and Peltonen, L., 1984, Neutral protease cleaving the N-terminal propeptide of type III procollagen: Partial purification and characterization of the enzyme from smooth muscle cells of bovine aorta, Biochemistry 23:1254–1256.

    Article  Google Scholar 

  • Halila, R., and Peltonen, L., 1986, Purification of human procollagen type III N-proteinase from placenta and preparation of antiserum, Biochem. J. 239:47–52.

    PubMed  CAS  Google Scholar 

  • Harwood, R., Grant, M. E., and Jackson, D. S., 1974, Collagen biosynthesis: Characterization of subcellular fractions from embryonic chick fibroblasts and the intracellular localization of protocollagen prolyl and protocollagen lysyl hydroxylases, Biochem. J. 176:283–294.

    Google Scholar 

  • Harwood, R., Grant, M. E., and Jackson, D. S., 1976, The influence of a,a’-bipyridyl, colchicine and antimycin A on the secretory process in embryonic chick tendon and cartilage cells, Biochem. J. 176:283–294.

    Google Scholar 

  • Hatamochi, A., Golumbeck, P. T., van Schaftinger, E., and de Crombrugghe, B., 1988, A CCAAT DNA binding factor consisting of two different components that are both required for DNA binding, J. Biol. Chem. 263:5940–5947.

    PubMed  CAS  Google Scholar 

  • Hayashi, M., Ninomiya, Y., Parsons, T., Hayashi, K., Olsen, B. R., and Trelstad, R. L., 1986, Differential localization of mRNAs of collagen types I and II in chick fibroblasts, chondrocytes, and corneal cells by in situ hybridization using cDNA probes, J. Cell Biol. 102:2302–2309.

    Article  PubMed  CAS  Google Scholar 

  • Helaakoski, T., Vuori, K., Myllylä, R., and Kivirikko, K. I., 1989, Molecular cloning of the a-subunit of human prolyl 4-hydroxylase: The complete cDNA-derived amino acid sequence and evidence for alternative splicing of RNA transcripts, Proc. Natl. Acad. Sci. USA 86:4392–4396.

    Article  PubMed  CAS  Google Scholar 

  • Helle, O., and Ness, N. N., 1972, A hereditary skin defect in sheep, Acta Vet. Scand. 13:443–445.

    PubMed  CAS  Google Scholar 

  • Hoffmann, H.-P., Olsen, B. R., Chen, H.-T., and Prockop, D. J., 1976, Segment-long-spacing aggregates and isolation of COOH-terminal peptides from type I procollagen, Proc. Natl. Acad. Sci. USA 73:4304–4308.

    Article  PubMed  CAS  Google Scholar 

  • Hojima, Y., van der Rest, M., and Prockop, D. J., 1985, Type I procollagen carboxyl-terminal proteinase from chick embryo tendons, J. Biol. Chem. 260:15996–16003.

    PubMed  CAS  Google Scholar 

  • Hojima, Y., McKenzie, J. A., van der Rest, M., and Prockop, D. J., 1989, Type I procollagen Nproteinase from chick embryo tendons. Purification of a new 500-kDa form of the enzyme and identification of the catalytically active polypeptides J. Biol. Chem. 264:11336–11345.

    PubMed  CAS  Google Scholar 

  • Hörlein, D., Fietzek, P. P., Wachter, E., Lapière, C. M., and Kühn, K., 1979, Amino acid sequence of the aminoterminal segment of dermatosparactic calf skin procollagen type I, Eur. J. Biochem. 99:31–38.

    Article  PubMed  Google Scholar 

  • Horton, W., Miyashita, T., Kohno, K., Hassell, J. R., and Yamada, Y., 1987, Identification of a phenotype-specific enhancer in the first intron of the rat collagen II gene, Proc. Natl. Acad. Sci. USA 84:8864–8868.

    Article  CAS  Google Scholar 

  • Hostikka, S. L., Eddy, R. L., Byers, M. G., Höyhtyä, M., Schows, T. B., and Tryggvason, K., 1990, Identification of a distinct type IV collagen a chain with restricted kidney distribution and assignment of its gene to the locus of X chromosome-linked Alport syndrome, Proc. Natl. Acad. Sci. USA 87:1606–1610.

    Article  PubMed  CAS  Google Scholar 

  • Hously, T. J., Rowland, F. N., Ledger, P. W., Kaplan, J., and Tanzer, M. L., 1980, Effects of tunicamycin on the biosynthesis of procollagen by human fibroblasts, J. Biol. Chem. 255:121–128.

    Google Scholar 

  • Hulmes, D. J. S., Kadler, K. E., Mould, A. P., Hojima, Y., Holmes, D. F., Cummings, C., Chapman, J. A., and Prockop, D. J., 1989, Pleomorphism in type I collagen fibrils produced by persistence of the procollagen N-propeptide, J. Mol. Biol. 210:337–345.

    Article  PubMed  CAS  Google Scholar 

  • Iyama, K., Ninomiya, Y., Olsen, B. R., Linsenmayer, T. F., Trelstad, R. L., and Hayashi, M., 1991, Spatio-temporal pattern of type X collagen gene expression and collagen deposition in embryonic chick vertebrae undergoing endochondral ossification, Anat. Rec. 229: 462–472.

    Article  PubMed  CAS  Google Scholar 

  • Jaenisch, R., Harbers, K., Schnieke, A., Lohler, J., and Chumakov, I., 1983, Germline integration of Moloney murine leukemia virus at the Mov 13 locus leads to recessive lethal mutations and early embryonic death, Cell 32:209–216.

    Article  PubMed  CAS  Google Scholar 

  • Kao, W. W.-Y., Berg, R. A., and Prockop, D. J., 1977, Kinetics for the secretion of procollagen by freshly isolated tendon cells, J. Biol. Chem. 252:8391–8397.

    PubMed  CAS  Google Scholar 

  • Kao, W. W.-Y., Prockop, D. J., and Berg, R. A., 1979, Kinetics for the secretion of non-helical procollagen by freshly isolated tendon cellsJ. Biol. Chem. 254:2234–2243.

    PubMed  CAS  Google Scholar 

  • Kao, W. W.-Y., Nakazawa, M., Aida, T., Everson, W. V., Kao, C. W.-C., Seyer, J., and Hughes, S. H., 1988, Isolation of cDNA clones and genomic DNA clones of 3-subunit of chicken prolyl 4hydroxylase, Connect. Tissue Res. 18:157–174.

    Article  CAS  Google Scholar 

  • Kaplan, H. A., Naider, F., and Lennarz, W. J., 1988, Partial characterization and purification of the glycosylation site recognition component of oligosaccharyl-transferase, J. Biol. Chem. 263:7814–7820.

    PubMed  CAS  Google Scholar 

  • Karim, A., Cournil, I., and Leblond, C. P., 1979, Immunochemical localization of procollagens, J. Histochem. Cytochem. 27:1070.

    Article  PubMed  CAS  Google Scholar 

  • Kaytes, P., Wood, L., Theriault, N., Kurkinen, M., and Vogeli, G., 1988, Head-to-head arrangement of murine type IV collagen genesJ. Biol. Chem. 263:19274–19277.

    PubMed  CAS  Google Scholar 

  • Khillan, J. S., Schmidt, A., Overbeek, P. A., de Crombrugghe, B., and Westphal, H., 1986, Developmental and tissue-specific expression directed by the a2 type I collagen promoter in transgenic miceProc. Natl. Acad. Sci. USA 83:725–729.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, T., Cheah, K. S. E., Chan, S. D. H., Lui, V. C. H., Mattei, M.-G., van der Rest, M., Ono, K., Solomon, E., Ninomiya, Y., and Olsen, B. R., 1989a, The human a2(XI) collagen (COL11A2) chain, J. Biol. Chem. 264:13910–13916.

    CAS  Google Scholar 

  • Kimura, T., Mattei, M.-G., Stevens, J. W., Goldring, M. B., Ninomiya, Y., and Olsen, B. R., 1989b, Molecular cloning of rat and human type IX collagen cDNA and localization of the a1(IX) gene on the human chromosome 6, Eur. J. Biochem. 179:71–78.

    Article  CAS  Google Scholar 

  • Kivirikko, K. I., and Myllylä, R., 1979, Collagen glycosyltransferases, Int. Rev. Connect. Tissue Res. 8:23–72.

    PubMed  CAS  Google Scholar 

  • Kivirikko, K. I., and Myllylä, R., 1984, Biosynthesis of collagens, in: Extracellular Matrix Biochemistry, (K. A. Piez and A. H. Reddi, eds.), pp. 83–118, Elsevier, New York.

    Google Scholar 

  • Kivirikko, K. I., and Myllylä, R., 1985, Post-translational processing of procollagens, Ann. N.Y. Acad. Sci. 460:187–201.

    Article  PubMed  CAS  Google Scholar 

  • Kivirikko, K. I., Myllylä, R., and Pihlajaniemi, T., 1989, Protein hydroxylation: Prolyl 4-hydroxylase, an enzyme with four cosubstrates and a multifunctional subunit, FASEB J. 3:1609–1617.

    PubMed  CAS  Google Scholar 

  • Kivirikko, K. I., Helaakoski, T., Tasanen, K., Vuori, K., Myllylä, R., Parkkonen, T., and Pihlajaniemi, T., 1990, Molecular biology of prolyl 4-hydroxylase, Ann. N.Y. Acad. Sci. 580:132–142.

    Article  PubMed  CAS  Google Scholar 

  • Kohn, L. D., Isersky, C., Zupnik, J., Lenaers, A., Lee, G., and Lapiere, C. M., 1974, Calf tendon procollagen peptidase: Its purification and endopeptidase mode of action, Proc. Natl. Acad. Sci. USA 71:40–44.

    Article  PubMed  CAS  Google Scholar 

  • Koivu, J., Myllylä, R., Helaakoski, T., Pihlajaniemi, T., Tasanen, K., and Kivirikko, K. I., 1987, A single polypeptide acts both as the 13 subunit of prolyl 4-hydroxylase and as a protein disulphide-isomerase, J. Biol. Chem. 262:6447–6449.

    PubMed  CAS  Google Scholar 

  • Kratochwil, K., von der Mark, K., Kollar, E. J., Jaenisch, R., Mooslehner, K., Schwarz, M., Haase, K., Gmachl, I., and Harbers, K., 1989, Retrovirus-induced insertional mutation of Mov 13 mice affects collagen I expression in a tissue-specific manner, Cell 57:807–816.

    Article  PubMed  CAS  Google Scholar 

  • Lee, B., Vissing, H., Ramirez, F., Rogers, D., and Rimoin, D., 1989, Identification of the molecular defect in a family with spondyloepiphyseal dysplasia, Science 244:978–980.

    Article  PubMed  CAS  Google Scholar 

  • Lenaers, A., Ansay, M., Nusgens, B. V., and Lapiere, C. M., 1971, Collagen made of extended a-chains, procollagen, in genetically-defective dermatosparaxic calves, Eur. J. Biochem. 23:533–543.

    Article  PubMed  CAS  Google Scholar 

  • Leung, M. K., Fessier, L. I., Greenberg, D. B., and Fessier, J. H., 1979, Separate amino and carboxyl procollagen peptidases in chick embryo tendon, J. Biol. Chem. 254:224–232.

    PubMed  CAS  Google Scholar 

  • LuValle, P., Ninomiya, Y., Rosenblum, N. D., and Olsen, B. R., 1988, The type X collagen gene: Intron sequences split the 5’ untranslated region and separate the coding regions for the non-collagenous amino-terminal and triple-helical domains, J. Biol. Chem. 263: 18378–18385.

    PubMed  CAS  Google Scholar 

  • LuValle, P., Hayashi, M., and Olsen, B. R., 1989, Transcriptional regulation of type X collagen during chondrocyte maturation, Dev. Biol. 133:613–616.

    Article  PubMed  CAS  Google Scholar 

  • Maity, S. N., Golumbeck, P. T., Karsenty, G., and de Crombrugghe, B., 1988, Selective activation of transcription by a novel CCAAT binding factor, Science 241:582–585.

    Article  PubMed  CAS  Google Scholar 

  • Mayne, R., and Burgeson, R. E. (eds.), 1987, Structure and Function of Collagen Types, Academic Press, New York.

    Google Scholar 

  • Miller, E. J., 1985, The structure of fibril-forming collagens, Ann. N.Y. Acad. Sci. 460:1–13.

    Article  PubMed  CAS  Google Scholar 

  • Morikawa, T., Tuderman, L., and Prockop, D. J., 1980, Inhibitors of procollagen N-protease. Synthetic peptides with sequences similar to the cleavage site in the pro¦Á1(I) chain, Biochemistry 19:2646–2650.

    Article  PubMed  CAS  Google Scholar 

  • Munro, S., and Pelham, H R B, 1987, A C-terminal signal prevents secretion of luminal ER proteins, Cell 48:899–907.

    Article  PubMed  CAS  Google Scholar 

  • Muragaki, Y., Jacenko, O., Apte, S., Mattei, M.-G., Ninomiya, Y., and Olsen, B. R., 1991, The a2(VIII) collagen gene¡ªa novel member of the short-chain collagen family located on the human chromosome 1, J. Biol. Chem. 266: 7721–7727.

    PubMed  CAS  Google Scholar 

  • Nicholls, A. C., Pope, F. M., and Schloon, H., 1979, Biochemical heterogeneity of osteogenesis imperfecta: New variant, Lancet,1:1193.

    Article  PubMed  CAS  Google Scholar 

  • Nicholls, A. C., Osse, G., Schloon, H. G., Lenard, H. G., Deak, S., Myers, J. C., Prockop, D. J., Weigel, W. R. F., Fryer, P., and Pope, F. M., 1984, The clinical features of homozygous a2(I) deficient osteogenesis imperfecta, J. Med. Genet. 21:257–262.

    Article  PubMed  CAS  Google Scholar 

  • Ninomiya, Y., Gordon, M., van der Rest, M., Schmid, T., Linsenmayer, T., and Olsen, B. R., 1986, The developmentally regulated type X collagen gene contains a long open reading frame without introns, J. Biol. Chem. 261:5041–5050.

    PubMed  CAS  Google Scholar 

  • Ninomiya, Y., Castagnola, P., Gerecke, D., Gordon, M., Jacenko, O., LuValle, P., McCarthy, M., Muragaki, Y., Nishimura, I., Oh, S., Rosenblum, N., Sato, N., Sugrue, S., Taylor, R., Vasios, G., Yamaguchi, N., and Olsen, B. R., 1990, The molecular biology of collagens with short triple-helical domains, in: Collagen Genes: Extracellular Matrix Genes (L. J. Sandell and C. D. Boyd, eds.), pp. 79–114, Academic Press, New York.

    Google Scholar 

  • Nishimura, I., Muragaki, Y., and Olsen, B. R., 1989, Tissue-specific forms of type IX collagenproteoglycan arise from the use of two widely separated promoters, J. Biol. Chem. 264:20033–20041.

    PubMed  CAS  Google Scholar 

  • Nist, C., von der Mark, K., Hay, E. D., Olsen, B. R., Bornstein, P., Ross, R., and Dehm, P., 1975, Location of procollagen in chick corneal and tendon fibroblasts with ferritin-conjugated antibodies,J. Cell Biol. 65:75–87.

    Article  PubMed  CAS  Google Scholar 

  • Njieha, F. K., Morikawa, T., Tuderman, L., and Prockop, D. J., 1982, Partial purification of a pro-collagen C-proteinase. Inhibition by synthetic peptides and sequential cleavage of type I pro-collagen, Biochemistry 21:757–764.

    Article  PubMed  CAS  Google Scholar 

  • Nusgens, B., Goebels, Y., Shinkai, H., and Lapiere, C. M., 1980, Procollagen type III N-terminal endopeptidase in fibroblast culture, Biochem. J. 191:699–706.

    PubMed  CAS  Google Scholar 

  • O’Hara, P. J., Read, W. K., Romane, W. M., and Bridges, C. H., 1970, A collagenous tissue dysplasia of calves, Lab. Invest. 23:307–314.

    PubMed  Google Scholar 

  • Oikarinen, J., Hatamochi, A., and de Crombrugghe, B., 1987, Separate binding sites for nuclear factor 1 and a CCAAT DNA binding factor in the mouse a2(I) collagen promoter, J. Biol. Chem. 262:11064–11070.

    PubMed  CAS  Google Scholar 

  • Olsen, B. R., and Prockop, D. J., 1974, Ferritin-conjugated antibodies used for labeling of organelles involved in the cellular synthesis and transport of procollagen, Proc. Natl. Acad. Sci. USA 71:2033–2037.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, B. R., Berg, R. A., Kishida, Y., Prockop, D. J., 1975, Further characterization of embryonic tendon fibroblasts and the use of immuno-ferritin techniques to study collagen biosynthesis, J. Cell Biol. 64:340–355.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, B. R., Hoffman, H.-P., and Prockop, D. J., 1976, Interchain disulfide bonds at the COOHterminal end of procollagen synthesized by matrix-free cells from chick embryonic tendon and cartilage, Arch. Biochem. Biophys. 175:341–350.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, B. R., Guzman, N. A., Engel, J., Condit, C., and Aase, S., 1977, Purification and characterization of a peptide from the carboxy-terminal region of chick tendon procollagen type I, Biochemistry 16:3030–3036.

    Article  PubMed  CAS  Google Scholar 

  • Olsen, B. R., Gerecke, D., Gordon, M., Green, G., Kimura, T., Konomi, H., Muragaki, Y., Ninomiya, Y., Nishimura, I., and Sugrue, S., 1989, A new dimension in extracellular matrix, in: Collagen: Biochemistry, Biotechnology, and Molecular Biology, Vol. IV, (B. R. Olsen, and M. E. Nimni, eds.), pp. 2–19, CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Parkkonen, R., Kivirikko, K. I., and Pihlajaniemi, T., 1988, Molecular cloning of a multifunctional chicken protein acting as the prolyl 4-hydroxylase 0-subunit, protein disulphide isomerase and a cellular thyroid binding protein. Comparison of cDNA-deduced amino acid sequences with those in other species, Biochem. J. 256:1005–1011.

    PubMed  CAS  Google Scholar 

  • Peterkofsky, B., and Assad, R., 1976, Submicrosomal localization of prolyl hydroxylase from chick embryo limb bone, J. Biol. Chem. 251:4771–4777.

    Google Scholar 

  • Pihlajaniemi, T., Dickson, L. A., Pope, F. M., Korhonen, V. R., Nicholls, A., Prockop, D. J., and Myers, J. C., 1984, Osteogenesis imperfecta: Cloning of a proa2(I) collagen gene with a frame-shift mutation, J. Biol. Chem. 259:12941–12944.

    PubMed  CAS  Google Scholar 

  • Pihlajaniemi, T., Myllylä, R., Seyer, J., Kurkinen, M., and Prockop, D. J., 1987a, Partial characterization of a low molecular weight human collagen that undergoes alternative splicing, Proc. Natl. Acad. Sci. USA 84:940–944.

    Article  CAS  Google Scholar 

  • Pihlajaniemi, T., Helaakoshi, T., Tasanen, K., Myllylä, R., Huhtala, M.-L., Koivu, J., and Kivirikko, K. I., 1987b, Molecular cloning of the 13 subunit of human prolyl 4-hydroxylase. This subunit and protein disulphide isomerase are products of the same gene, EMBO J. 6:643–649.

    CAS  Google Scholar 

  • Pihlajaniemi, T., Tamminen, M., Sandberg, M., Hirvonen, H., and Vuorio, E., 1990, The al chain of type XIII collagen: Polypeptide structure, alternative splicing, and tissue distribution, Ann. N.Y. Acad. Sci. 580:440–443.

    Article  Google Scholar 

  • Poole, A. R., Pidoux, I., Reiner, A., Choi, H., and Rosenberg, L. C., 1984, Association of an extra-cellular protein (chondrocalcin) with the calcification of cartilage in endochondral bone formation, J. Cell Biol. 98:54–65.

    Article  PubMed  CAS  Google Scholar 

  • Pöschl, E., Pollner, R., and Kuhn, K., 1988, The genes for the a1(IV) and a2(IV) chains of human basement membrane collagen type IV are arranged head-to-head and separated by a bi-directional promoter of unique structure, EMBO J. 7:2687–2695.

    PubMed  Google Scholar 

  • Prockop, D. J., and Guzman, N. A., 1977, Collagen diseases and the biosynthesis of collagen, Hosp. Pract. December:61–68.

    Google Scholar 

  • Prockop, D. J., Kivirikko, K. I., Tuderman, L., and Guzman, N. A., 1979, The biosynthesis of collagen and its disorders, N. Engl. J. Med. 301(July 5 and July 12):13–24, 77–85.

    Google Scholar 

  • Prockop, D. J., Olsen, A., Kontusari, S., Hyland, J., Ala-Kokko, L., Vasan, N. S., Barton, E., Buck, D., Harrison, K., and Brent, R. L., 1990, Mutations in human procollagen genes. Consequences of the mutations in man and in transgenic mice, Ann. N.Y. Acad. Sci. 580:330–339.

    Article  PubMed  CAS  Google Scholar 

  • Quinn, R A, and Krane, S. M., 1976, Abnormal properties of collagen lysyl hydroxylase from skin fibroblasts of siblings with hydroxylysine-deficient collagen, J. Clin. Invest. 57:83–93.

    Article  PubMed  CAS  Google Scholar 

  • Ramirez, F., 1989, Organization and evolution of the fibrillar collagen genes, in: Collagen—Molecular Biology, Vol. IV (B. R. Olsen and M. E. Nimni, eds.), pp. 21–30, CRC Press, Boca Raton, Fla.

    Google Scholar 

  • Ramirez, F., and DiLiberto, M., 1990, Complex and diversified regulatory programs control the expression of vertebrate collagen genes, FASEB J. 4:1616–1623.

    PubMed  CAS  Google Scholar 

  • Ramirez, F., Bernard, M., Chu, M.-L., Dickson, L., Sangiorgi, F., Weil, D., de Wet, W., Junien, C., and Sobel, M., 1985, Isolation and characterization of the human fibrillar collagen genes, Ann. N.Y. Acad. Sci. 460:117–129.

    Article  PubMed  CAS  Google Scholar 

  • Revel, J.-P., and Hay, E. D., 1963, An autoradiographic and electron microscopic study of collagen synthesis in differentiating cartilage, Z. Zellforsch. Mikrosk. Anat. 61:110–114.

    Article  PubMed  CAS  Google Scholar 

  • Risteli, J., Tryggvason, K., and Kivirikko, K. I., 1977, Prolyl 3-hydroxylase: Partial characterization of the enzyme from rat kidney cortex, Eur. J. Biochem. 73:485–492.

    Article  PubMed  CAS  Google Scholar 

  • Rosenbloom, H., Harsch, M., and Jimenez, S. A., 1973, Hydroxyproline content determines the denaturation temperature of chick tendon procollagen, Arch. Biochem. Biophys. 158:478–484.

    Article  PubMed  CAS  Google Scholar 

  • Rosenbloom, J., Endo, R., and Harsch, M., 1976, Termination of procollagen chain synthesis by puromycin, J. Biol. Chem. 251:2070–2076.

    PubMed  CAS  Google Scholar 

  • Ross, R., 1975, Connective tissue cells, cell proliferation and synthesis of extracellular matrix—A review, Philos. Trans. R. Soc. London Ser. B 271:247–259.

    Article  CAS  Google Scholar 

  • Ross, D. W., and Benditt, E. P., 1965, Wound healing and collagen formation. V. Quantitative electron microscope autoradiographic observations of proline 3H utilization by fibroblasts, J. Cell Biol. 27:83–106.

    Article  PubMed  CAS  Google Scholar 

  • Rossi, P., and de Crombrugghe, B., 1987, Identification of a cell-specific transcriptional enhancer in the first intron of the mouse alpha 2 (type I) collagen gene, Proc. Natl. Acad. Sci. USA 84:5590–5594.

    Article  PubMed  CAS  Google Scholar 

  • Rossouw, C. M. S., Vergeer, W. P., du Plooy, S. J., Bernard, M P, Ramirez, F., and de Wet, W. J., 1987, DNA sequences in the first intron of the human pro-al (I) collagen gene enhance transcription, J. Biol. Chem. 262:15151–15157.

    PubMed  CAS  Google Scholar 

  • Rowe, D. W., Moen, R. C., Davidson, J. M., Byers, P. H., Bornstein, P., and Palmiter, R. D., 1978, Correlation of procollagen mRNA levels in normal and transformed chick embryo fibroblasts with different rates of procollagen synthesis, Biochemistry 17:1581–1590.

    Article  PubMed  CAS  Google Scholar 

  • Salpeter, M. M., 1968, H3-proline incorporation into cartilage: Electron microscope auto-radiographic observations, J. Morphol. 124:387–421.

    Article  PubMed  CAS  Google Scholar 

  • Saus, J., Wieslander, J., Langeveld, J. P. M., Quinones, S., and Hudson, B. G., 1988, Identification of the Goodpasture antigen as the a3(IV) chain of collagen IV, J. Biol. Chem. 263:13374–13380.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Schnieke, A., Harbers, K., and Jaenisch, R., 1983, Embryonic lethal mutation in mice induced by retrovirus insertion in the al(I) collagen gene, Nature 304:315–320.

    Article  PubMed  CAS  Google Scholar 

  • Soininen, R., Huotari, M., Hostikka, S. L., Prockop, D. J., and Tryggvason, K., 1988, The structural genes for al and a2 chains of human type IV collagen are divergently encoded on opposite DNA strands and have an overlapping promoter region, J. Biol. Chem. 263:17217–17220.

    PubMed  CAS  Google Scholar 

  • Speakman, P. T., 1971, Proposed mechanism for the biological assembly of collagen triple-helix, Nature 229:241–243.

    Article  PubMed  CAS  Google Scholar 

  • Superti-Furga, A., Steinmann, B., Ramirez, F., and Byers, P. H., 1989, Molecular defects of type III procollagen in Ehlers¨CDanlos syndrome type IV, Hum. Genet. 82:104–108.

    Article  PubMed  CAS  Google Scholar 

  • Svoboda, K. K., Nishimura, I., Sugrue, S. P., Ninomiya, Y., and Olsen, B. R., 1988, Embryonic chicken cornea and cartilage synthesize type IX collagen molecules with different amino-terminal domains, Proc. Natl. Acad. Sci. USA 85:7496–7500.

    Article  PubMed  CAS  Google Scholar 

  • Tanzawa, K., Berger, J., and Prockop, D. J., 1985, Type I procollagen N-proteinase from whole chick embryos, J. Biol. Chem. 260:1120–1126.

    PubMed  CAS  Google Scholar 

  • Tanzer, M. L., Church, R. L., Yaeger, J. A., Wampler, D. E., and Park, E.-D., 1974, Procollagen: Intermediate forms containing several types of peptide chains and noncollagen peptide extensions at NH2 and COOH ends, Proc. Natl. Acad. Sci. USA 71:3009–3019.

    Article  PubMed  CAS  Google Scholar 

  • Tanzer, M. L., Rowland, F. N., Murray, L. W., and Kaplan, J., 1977, Inhibitory effects of tunicamycin on procollagen biosynthesis and secretion, Biochim. Biophys. Acta 500:187–196.

    Article  PubMed  CAS  Google Scholar 

  • Tromp, G., Kuivaniemi, H., Shikata, H., and Prockop, D. J., 1989, A single base mutation that substitutes serine for glycine 790 of the al(III) chain of type III procollagen exposes an arginine and causes Ehlers¡ªDanlos syndrome IV, J. Biol. Chem. 264:1349–1352.

    PubMed  CAS  Google Scholar 

  • Tuderman, L., Puistola, U., Anttinen, H., and Kivirikko, K. I., 1977, Partial purification and characterization of a neutral protease which cleaves the N-terminal propeptides from procollagen, Biochemistry 17:2948–2954.

    Article  Google Scholar 

  • Tuderman, L., Kivirikko, K. I., and Prockop, D. J., 1978, Partial purification and characterization of a neutral protease which cleaves the N-terminal propeptides from procollagen, Biochemistry 17:2948–2954.

    Article  PubMed  CAS  Google Scholar 

  • Turpeenniemi, T. M., Puistola, U., Anttinen, H., and Kivirikko, K. I., 1977, Affinity chromatography of lysyl hydroxylase on concanavalin A-agarose, Biochim. Biophys. Acta 483:215–219.

    Article  PubMed  CAS  Google Scholar 

  • Upholt, W. B., 1989, The type II collagen gene, in: Collagen—Molecular Biology, Vol. IV (B. R. Olsen and M. E. Nimni, eds.), pp. 31–49, CRC Press, Boca Raton, Fla.

    Google Scholar 

  • Upholt, W. B., and Olsen, B. R., 1991, The active genes of cartilage, in: Cartilage: Molecular Aspects (B. Hall and S. A. Newman, eds.), pp. 1–57, CRC Press, Boca Raton, Fla.

    Google Scholar 

  • Upholt, W. B., Strom, C. M., and Sandell, L. J., 1985, Structure of the type II collagen gene, Ann. N.Y. Acad. Sci. 460:130–140.

    Article  PubMed  CAS  Google Scholar 

  • van der Rest, M., Rosenberg, L. C., Olsen, B. R., and Poole, A. R., 1986, Chondrocalcin is identical with the C-propeptide of type II procollagen, Biochem. J. 237:923–925.

    PubMed  Google Scholar 

  • Vaughan, L., Mendler, M., Huber, J., Bruckner, P., Winterhalter, K. H., Irwin, M. H., and Mayne, R., 1988, D-periodic distribution of collagen type IX along cartilage fibrils, J. Cell Biol. 106:991–997.

    Article  PubMed  CAS  Google Scholar 

  • Veis, A., and Brownell, A. G., 1977, Triple-helix formation on ribosome-bound nascent chains of procollagen: Deuterium—hydrogen exchange studies, Proc. Natl. Acad. Sci. USA 74:215–219.

    Article  Google Scholar 

  • Vissing, H., D’Alessio, M., Lee, B., Ramirez, F., Godfrey, M., and Hollister, D. W., 1989, Glycine to serine substitution in the triple-helical domain of proal(II) collagen results in a lethal perinatal form of short-limbed dwarfism, J. Biol. Chem. 264:18265–18267.

    PubMed  CAS  Google Scholar 

  • Vogeli, G., Ohkubo, H., Avvedimento, V. E., Sullivan, M., Yamada, Y., Mudryj, M., Pastan, I., and de Crombrugghe, B., 1981, A repetitive structure in the chick a2 collagen gene, Cold Spring Harbor Symp. Quant. Biol. 45:777–783.

    Article  CAS  Google Scholar 

  • Vuorio, E., and de Crombrugghe, B., 1990, The family of collagen genes, Annu. Rev. Biochem. 59:837–872.

    Article  PubMed  CAS  Google Scholar 

  • Weil, D., Bernard, M., Gargano, S., and Ramirez, F., 1987, The proa2(V) collagen gene is evolu-tionarily related to the major fibrillar-forming collagens, Nucleic Acids Res. 15:181–198.

    Article  PubMed  CAS  Google Scholar 

  • Weinstock, M., and Leblond, C. P., 1974, Synthesis, migration and release of precursor collagen by odontoblasts as visualized by radioautography after [3H]proline administration, J. Cell Biol. 60:92–127.

    Article  PubMed  CAS  Google Scholar 

  • Wick, G., Olsen, B. R., and Timpl, R., 1978, Immunohistologic analysis of fetal and dermatosparactic calf and sheep skin with antisera to procollagen and collagen type I, Lab. Invest. 39:151–156.

    PubMed  CAS  Google Scholar 

  • Willing, M. C., Cohn, D. H., and Byers, P. H., 1990, Frameshift mutation near the 3’ end of the COL1A1 gene of type I collagen predicts an elongated proal(I) chain and results in osteogenesis imperfecta type I, J. Clin. Invest. 85:282–290.

    Article  PubMed  CAS  Google Scholar 

  • Wright, D. W., and Mayne, R., 1988, Vitreous humor of chicken contains two fibrillar systems: An analysis of their structure, J. Ultrastruct. Mol. Struct. Res. 100:224–234.

    Article  PubMed  CAS  Google Scholar 

  • Yada, T., Suzuki, S., Kobayashi, K., Kobayashi, M., Hoshino, T., Horie, K., and Kimata, K., 1990, Occurence in chick embryo vitreous humor of a type IX collagen proteoglycan with an extraordinary large chondroitin sulfate chain and short al polypeptide, J. Biol. Chem. 265:6992–6999.

    PubMed  CAS  Google Scholar 

  • Yamada, Y., Avvedimento, V. E., Mudryj, M., Ohkubo, H., Vogeli, G., Irani, M., Pastan, I., and 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 22:877–892.

    Article  Google Scholar 

  • Yamada, Y., Kühn, K., and de Crombrugghe, B., 1983, A conserved nucleotide sequence, coding for a segment of the C-propeptide, is found at the same location in different collagen genes, Nucleic Acids Res. 11:2733–2744.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi, N., Benya, P. D., van der Rest, M., and Ninomiya, Y., 1989, The cloning and sequencing of al (VIII) collagen cDNAs demonstrate that type VIII collagen is a short chain collagen and contains triple-helical and carboxyl-terminal non-triple-helical domains similar to those of type X collagen, J. Biol. Chem. 264:16022–16029.

    PubMed  CAS  Google Scholar 

  • Yamaguchi, N., Mayne, R., and Ninomiya, Y., 1991, The al(VIII) collagen gene is homologous to the al(X) collagen gene and contains a large exon encoding the entire triple-helical and carboxyl-terminal non-triple-helical domain of the a1(VIII) polypeptide J. Biol. Chem. 266:4508–4513.

    PubMed  CAS  Google Scholar 

  • Yamauchi, K., Yamamoto, T., Hayashi, H., Koya, S., Takikawa, H., Toyoshima, K., and Horiuchi, R., 1987, Sequence of membrane-associated thyroid hormone binding protein from bovine liver: Its identity with protein disulphide isomerase, Biochem. Biophys. Res. Commun. 146:1485–1492.

    Article  PubMed  CAS  Google Scholar 

  • Yoshioka, H., and Ramirez, F., 1990, Pro-a1(XI) collagen, J. Biol. Chem. 265:6423–6426.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cellular Biology, Harvard Medical School, Boston, Massachusetts, 02115, USA

    Bjorn Reino Olsen

Authors
  1. Bjorn Reino Olsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Anatomy and Cellular Biology, Harvard Medical School, Boston, Massachusetts, 02115, USA

    Elizabeth D. Hay

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Springer Science+Business Media New York

About this chapter

Cite this chapter

Olsen, B.R. (1991). Collagen Biosynthesis. In: Hay, E.D. (eds) Cell Biology of Extracellular Matrix. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3770-0_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-3770-0_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6680-5

  • Online ISBN: 978-1-4615-3770-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation