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. 1976 Nov;73(11):4027–4031. doi: 10.1073/pnas.73.11.4027

Collagen fibrillogenesis: intermediate aggregates and suprafibrillar order.

R L Trelstad, K Hayashi, J Gross
PMCID: PMC431312  PMID: 1069288

Abstract

Polymerization of collagen in vitro has been studied with the electron microscope at early time points of fibril assembly. We have found morphologically distinct stages of aggregation, which we suggest represent successive steps in fibril formation. Linear growth of the fibril appears to occur by the tandem addition of aggregates to each other and subsequently to the ends of a subfibril; lateral growth occurs by the entwining, like a rope, of these subfibrils. Fibrillogenesis is also accompanied by extensive development of suprafibrillar order in which various patterns of parallel, spiral, and orthogonal sets of fibrils were frequently observed.

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Selected References

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  1. Bornstein P. The biosynthesis of collagen. Annu Rev Biochem. 1974;43(0):567–603. doi: 10.1146/annurev.bi.43.070174.003031. [DOI] [PubMed] [Google Scholar]
  2. Bouligand Y. Twisted fibrous arrangements in biological materials and cholesteric mesophases. Tissue Cell. 1972;4(2):189–217. doi: 10.1016/s0040-8166(72)80042-9. [DOI] [PubMed] [Google Scholar]
  3. Bruns R. R., Gross J. Band pattern of the segment-long-spacing form of collagen. Its use in the analysis of primary structure. Biochemistry. 1973 Feb 27;12(5):808–815. doi: 10.1021/bi00729a004. [DOI] [PubMed] [Google Scholar]
  4. Dick Y. P., Nordwig A. Effect of pH on the stability of the collagen fold. Arch Biochem Biophys. 1966 Nov;117(2):466–468. doi: 10.1016/0003-9861(66)90436-x. [DOI] [PubMed] [Google Scholar]
  5. Fessler L. I., Morris N. P., Fessler J. H. Procollagen: biological scission of amino and carboxyl extension peptides. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4905–4909. doi: 10.1073/pnas.72.12.4905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. GROSS J., KIRK D. The heat precipitation of collagen from neutral salt solutions: some rate-regulating factors. J Biol Chem. 1958 Aug;233(2):355–360. [PubMed] [Google Scholar]
  7. GROSS J. THERMAL DENATURATION OF COLLAGEN IN THE DISPERSED AND SOLID STATE. Science. 1964 Feb 28;143(3609):960–961. doi: 10.1126/science.143.3609.960. [DOI] [PubMed] [Google Scholar]
  8. GROSS J. The behavior of collagen units as a model in morphogenesis. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):261–274. doi: 10.1083/jcb.2.4.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hayashi T., Nagai Y. Effect of pH on the stability of collagen molecule in solution. J Biochem. 1973 May;73(5):999–1006. doi: 10.1093/oxfordjournals.jbchem.a130184. [DOI] [PubMed] [Google Scholar]
  10. Hayashi T., Nagai Y. Factors affecting the interactions of collagen molecules as observed by in vitro fibril formation. I. Effects of small molecules, especially saccharides. J Biochem. 1972 Sep;72(3):749–758. doi: 10.1093/oxfordjournals.jbchem.a129953. [DOI] [PubMed] [Google Scholar]
  11. Hulmes D. J., Miller A., Parry D. A., Piez K. A., Woodhead-Galloway J. Analysis of the primary structure of collagen for the origins of molecular packing. J Mol Biol. 1973 Sep 5;79(1):137–148. doi: 10.1016/0022-2836(73)90275-1. [DOI] [PubMed] [Google Scholar]
  12. Lapiere C. M., Nusgens B. Polymerization of procollagen in vitro. Biochim Biophys Acta. 1974 Apr 11;342(2):237–246. doi: 10.1016/0005-2795(74)90078-6. [DOI] [PubMed] [Google Scholar]
  13. Martin G. R., Byers P. H., Piez K. A. Procollagen. Adv Enzymol Relat Areas Mol Biol. 1975;42:167–191. doi: 10.1002/9780470122877.ch3. [DOI] [PubMed] [Google Scholar]
  14. Miller A., Parry D. A. Structure and packing of microfibrils in collagen. J Mol Biol. 1973 Apr 5;75(2):441–447. doi: 10.1016/0022-2836(73)90035-1. [DOI] [PubMed] [Google Scholar]
  15. Obrink B. Non-aggregated tropocollagen at physiological pH and ionic strength. A chemical and physico-chemical characterization of tropocollagen isolated from the skin of lathyritic rats. Eur J Biochem. 1972 Feb;25(3):563–572. doi: 10.1111/j.1432-1033.1972.tb01729.x. [DOI] [PubMed] [Google Scholar]
  16. Trelstad R. L., Coulombre A. J. Morphogenesis of the collagenous stroma in the chick cornea. J Cell Biol. 1971 Sep;50(3):840–858. doi: 10.1083/jcb.50.3.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Trelstad R. L., Hayashi K., Toole B. P. Epithelial collagens and glycosaminoglycans in the embryonic cornea. Macromolecular order and morphogenesis in the basement membrane. J Cell Biol. 1974 Sep;62(3):815–830. doi: 10.1083/jcb.62.3.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Trelstad R. L., Kang A. H., Toole B. P., Gross J. Collagen heterogeneity. High resolution separation of native ( 1(I) 2 2 and ( 1(II) 3 and their component chains. J Biol Chem. 1972 Oct 25;247(20):6469–6473. [PubMed] [Google Scholar]
  19. WOOD G. C., KEECH M. K. The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J. 1960 Jun;75:588–598. doi: 10.1042/bj0750588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Weinstock M., Leblond C. P. Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after (3H)proline administration. J Cell Biol. 1974 Jan;60(1):92–127. doi: 10.1083/jcb.60.1.92. [DOI] [PMC free article] [PubMed] [Google Scholar]

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