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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 Jun;86(12):4549–4553. doi: 10.1073/pnas.86.12.4549

Collagen fibrillogenesis in situ: fibril segments are intermediates in matrix assembly.

D E Birk 1, E I Zycband 1, D A Winkelmann 1, R L Trelstad 1
PMCID: PMC287308  PMID: 2734306

Abstract

The assembly of discontinuous fibril segments and bundles was studied in 14-day chicken embryo tendons by using serial sections, transmission electron microscopy, and computer-assisted image reconstruction. Fibril segments were first found in extracytoplasmic channels, the sites of their polymerization; they also were found within fibril bundles. Single fibril segments were followed over their entire length in consecutive sections, and their lengths ranged from 7 to 15 microns. Structural differences in the ends of the fibril segments were identified, suggesting that the amino/carboxyl polarity of the fibril segment is reflected in its architecture. Our data indicate that fibril segments are precursors in collagen fibril formation, and we suggest that postdepositional fusion of fibril segments may be an important process in tendon development and growth.

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Selected References

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  1. Birk D. E., Trelstad R. L. Extracellular compartments in matrix morphogenesis: collagen fibril, bundle, and lamellar formation by corneal fibroblasts. J Cell Biol. 1984 Dec;99(6):2024–2033. doi: 10.1083/jcb.99.6.2024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birk D. E., Trelstad R. L. Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J Cell Biol. 1986 Jul;103(1):231–240. doi: 10.1083/jcb.103.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birk D. E., Trelstad R. L. Fibroblasts create compartments in the extracellular space where collagen polymerizes into fibrils and fibrils associate into bundles. Ann N Y Acad Sci. 1985;460:258–266. doi: 10.1111/j.1749-6632.1985.tb51173.x. [DOI] [PubMed] [Google Scholar]
  4. Harris A. K., Stopak D., Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature. 1981 Mar 19;290(5803):249–251. doi: 10.1038/290249a0. [DOI] [PubMed] [Google Scholar]
  5. Haworth R. A., Chapman J. A. A study of the growth of normal and iodinated collagen fibrils in vitro using electron microscope autoradiography. Biopolymers. 1977 Sep;16(9):1895–1906. doi: 10.1002/bip.1977.360160906. [DOI] [PubMed] [Google Scholar]
  6. Holmes D. F., Chapman J. A. Axial mass distributions of collagen fibrils grown in vitro: results for the end regions of early fibrils. Biochem Biophys Res Commun. 1979 Apr 27;87(4):993–999. doi: 10.1016/s0006-291x(79)80005-4. [DOI] [PubMed] [Google Scholar]
  7. Krummel T. M., Nelson J. M., Diegelmann R. F., Lindblad W. J., Salzberg A. M., Greenfield L. J., Cohen I. K. Fetal response to injury in the rabbit. J Pediatr Surg. 1987 Jul;22(7):640–644. doi: 10.1016/s0022-3468(87)80117-3. [DOI] [PubMed] [Google Scholar]
  8. PORTER K. R., PAPPAS G. D. Collagen formation by fibroblasts of the chick embryo dermis. J Biophys Biochem Cytol. 1959 Jan 25;5(1):153–166. doi: 10.1083/jcb.5.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Scott J. E. Proteoglycan-fibrillar collagen interactions. Biochem J. 1988 Jun 1;252(2):313–323. doi: 10.1042/bj2520313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Stopak D., Wessells N. K., Harris A. K. Morphogenetic rearrangement of injected collagen in developing chicken limb buds. Proc Natl Acad Sci U S A. 1985 May;82(9):2804–2808. doi: 10.1073/pnas.82.9.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Trelstad R. L., Birk D. E., Silver F. H. Collagen fibrillogenesis in tissues, in a solution and from modeling: a synthesis. J Invest Dermatol. 1982 Jul;79 (Suppl 1):109s–112s. doi: 10.1111/1523-1747.ep12545945. [DOI] [PubMed] [Google Scholar]
  12. Trelstad R. L., Hayashi K. Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth. Dev Biol. 1979 Aug;71(2):228–242. doi: 10.1016/0012-1606(79)90166-0. [DOI] [PubMed] [Google Scholar]
  13. Trelstad R. L. Multistep assembly of type I collagen fibrils. Cell. 1982 Feb;28(2):197–198. doi: 10.1016/0092-8674(82)90334-8. [DOI] [PubMed] [Google Scholar]
  14. Yang G. C., Birk D. E. Topographies of extracytoplasmic compartments in developing chick tendon fibroblasts. J Ultrastruct Mol Struct Res. 1986 Oct-Dec;97(1-3):238–248. doi: 10.1016/s0889-1605(86)80023-4. [DOI] [PubMed] [Google Scholar]

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