Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1986 Jul 1;103(1):231–240. doi: 10.1083/jcb.103.1.231

Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation

PMCID: PMC2113791  PMID: 3722266

Abstract

The formation of collagen fibrils, fibril bundles, and tissue-specific collagen macroaggregates by chick embryo tendon fibroblasts was studied using conventional and high voltage electron microscopy. During chick tendon morphogenesis, there are at least three extracellular compartments responsible for three levels of matrix organization: collagen fibrils, bundles, and collagen macroaggregates. Our observations indicate that the initial extracellular events in collagen fibrillogenesis occur within narrow cytoplasmic recesses, presumably under close cellular regulation. Collagen fibrils are formed within these deep, narrow recesses, which are continuous with the extracellular space. Where these narrow recesses fuse with the cell surface, it becomes highly convoluted with folds and processes that envelope forming fibril bundles. The bundles laterally associate and coalesce, forming aggregates within a third cell-defined extracellular compartment. Our interpretation is that this third compartment forms as cell processes retract and cytoplasm is withdrawn between bundles. These studies define a hierarchical organization within the tendon, extending from fibril assembly to fascicle formation. Correlation of different levels of extracellular compartmentalization with tissue architecture provides insight into the cellular controls involved in collagen fibril and higher order assembly and a better understanding of how collagen fibrils are collected into structural groups, positioned, and woven into functional tissue-specific collagen macroaggregates.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  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. Bruns R. R. Beaded filaments and long-spacing fibrils: relation to type VI collagen. J Ultrastruct Res. 1984 Nov;89(2):136–145. doi: 10.1016/s0022-5320(84)80010-6. [DOI] [PubMed] [Google Scholar]
  3. Bruns R. R., Hulmes D. J., Therrien S. F., Gross J. Procollagen segment-long-spacing crystallites: their role in collagen fibrillogenesis. Proc Natl Acad Sci U S A. 1979 Jan;76(1):313–317. doi: 10.1073/pnas.76.1.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chaplin D. M., Greenlee T. K., Jr The development of human digital tendons. J Anat. 1975 Nov;120(Pt 2):253–274. [PMC free article] [PubMed] [Google Scholar]
  5. Creutz C. E., Pollard H. B. Development of a cell-free model for compound exocytosis using components of the chromaffin cell. J Auton Nerv Syst. 1983 Jan;7(1):13–18. doi: 10.1016/0165-1838(83)90065-6. [DOI] [PubMed] [Google Scholar]
  6. Dvorak A. M., Galli S. J., Schulman E. S., Lichtenstein L. M., Dvorak H. F. Basophil and mast cell degranulation: ultrastructural analysis of mechanisms of mediator release. Fed Proc. 1983 May 15;42(8):2510–2515. [PubMed] [Google Scholar]
  7. Fleischmajer R., Olsen B. R., Timpl R., Perlish J. S., Lovelace O. Collagen fibril formation during embryogenesis. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3354–3358. doi: 10.1073/pnas.80.11.3354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fleischmajer R., Timpl R., Tuderman L., Raisher L., Wiestner M., Perlish J. S., Graves P. N. Ultrastructural identification of extension aminopropeptides of type I and III collagens in human skin. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7360–7364. doi: 10.1073/pnas.78.12.7360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garant P. R., Cho M. I. Cytoplasmic polarization of periodontal ligament fibroblasts. Implications for cell migration and collagen secretion. J Periodontal Res. 1979 Mar;14(2):95–106. doi: 10.1111/j.1600-0765.1979.tb00778.x. [DOI] [PubMed] [Google Scholar]
  10. Greenlee T. K., Jr, Ross R. The development of the rat flexor digital tendon, a fine structure study. J Ultrastruct Res. 1967 May;18(3):354–376. doi: 10.1016/s0022-5320(67)80124-2. [DOI] [PubMed] [Google Scholar]
  11. Hong B. S., Davison P. F., Cannon D. J. Isolation and characterization of a distinct type of collagen from bovine fetal membranes and other tissues. Biochemistry. 1979 Oct 2;18(20):4278–4282. doi: 10.1021/bi00587a003. [DOI] [PubMed] [Google Scholar]
  12. JACKSON S. F. The morphogenesis of avian tendon. Proc R Soc Lond B Biol Sci. 1956 Mar 13;144(917):556–572. doi: 10.1098/rspb.1956.0011. [DOI] [PubMed] [Google Scholar]
  13. Kastelic J., Galeski A., Baer E. The multicomposite structure of tendon. Connect Tissue Res. 1978;6(1):11–23. doi: 10.3109/03008207809152283. [DOI] [PubMed] [Google Scholar]
  14. Mallory T. B., Lawson G. M. Chronic Typhoid Cholecystitis. Am J Pathol. 1931 Jan;7(1):71–76.1. [PMC free article] [PubMed] [Google Scholar]
  15. Marchi F., Leblond C. P. Collagen biogenesis and assembly into fibrils as shown by ultrastructural and 3H-proline radioautographic studies on the fibroblasts of the rat food pad. Am J Anat. 1983 Oct;168(2):167–197. doi: 10.1002/aja.1001680206. [DOI] [PubMed] [Google Scholar]
  16. Miyahara M., Hayashi K., Berger J., Tanzawa K., Njieha F. K., Trelstad R. L., Prockop D. J. Formation of collagen fibrils by enzymic cleavage of precursors of type I collagen in vitro. J Biol Chem. 1984 Aug 10;259(15):9891–9898. [PubMed] [Google Scholar]
  17. Miyahara M., Njieha F. K., Prockop D. J. Formation of collagen fibrils in vitro by cleavage of procollagen with procollagen proteinases. J Biol Chem. 1982 Jul 25;257(14):8442–8448. [PubMed] [Google Scholar]
  18. Scott J. E., Orford C. R., Hughes E. W. Proteoglycan-collagen arrangements in developing rat tail tendon. An electron microscopical and biochemical investigation. Biochem J. 1981 Jun 1;195(3):573–581. doi: 10.1042/bj1950573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Scott J. E. The periphery of the developing collagen fibril. Quantitative relationships with dermatan sulphate and other surface-associated species. Biochem J. 1984 Feb 15;218(1):229–233. doi: 10.1042/bj2180229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Siegel R. C. Lysyl oxidase. Int Rev Connect Tissue Res. 1979;8:73–118. doi: 10.1016/b978-0-12-363708-6.50009-6. [DOI] [PubMed] [Google Scholar]
  21. Silver F. H. Type I collagen fibrillogenesis in vitro. Additional evidence for the assembly mechanism. J Biol Chem. 1981 May 25;256(10):4973–4977. [PubMed] [Google Scholar]
  22. Squier C. A., Bausch W. H. Three-dimensional organization of fibroblasts and collagen fibrils in rat tail tendon. Cell Tissue Res. 1984;238(2):319–327. doi: 10.1007/BF00217304. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. 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]
  26. Vogel K. G., Paulsson M., Heinegård D. Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycan of tendon. Biochem J. 1984 Nov 1;223(3):587–597. doi: 10.1042/bj2230587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wiestner M., Krieg T., Hörlein D., Glanville R. W., Fietzek P., Müller P. K. Inhibiting effect of procollagen peptides on collagen biosynthesis in fibroblast cultures. J Biol Chem. 1979 Aug 10;254(15):7016–7023. [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES