Localization of collagen types I, III and V during tendon development. Changes in collagen types I and III are correlated with changes in fibril diameter

European Journal of Cell Biology

Volumn 72, Issue 4, 1997, Pages 352-361

  Birk, David E ^a   Mayne, Richard ^b  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Collagen fibrils; Collagen types I, III and V; Diameter; Fibrillogenesis; Matrix assembly; Tendon development

Indexed keywords

COLLAGEN FIBRIL; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE 5;

ANIMAL TISSUE; ARTICLE; CONNECTIVE TISSUE; DEVELOPMENT; EMBRYO; NONHUMAN; PRIORITY JOURNAL; TENDON;

EID: 0030945384     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Birk, D. E., J. M. Fitch, J. P. Babiarz, K. J. Doane, T. F. Linsenmayer: Collagen fibrillogenesis in vitro: interaction of types I and V collagen regulates fibril diameter. J. Cell Sci. 95, 649-657 (1990).
2. Birk, D. E., J. M. Fitch, J. P. Babiarz, T. F. Linsenmayer: Collagen type I and type V are present in the same fibril in the avian corneal stoma. J. Cell Biol. 106, 999-1008 (1988).
3. Birk, D. E., T. F. Linsenmayer: Collagen fibril assembly, deposition, and organization into tissue-specific matrices. In: P. D. Yurchenco, D. E. Birk, R. P. Mecham (eds): Extracellular Matrix Assembly and Structure. pp. 91-128. Academic Press. New York 1994.
4. Birk, D. E., M. V. Nurminskaya, E. I. Zycband: Collagen fibrillogenesis in situ: fibril segments undergo post-depositional modifications resulting in linear and lateral growth during matrix development. Dev. Dyn. 202, 229-243 (1995).
5. Birk, D. E., F. H. Silver: Collagen fibrillogenesis in vitro: comparison of types I, II, and III. Arch. Biochem. Biophys. 235, 178-185 (1984)
6. Birk, D. E., J. F. Southern, E. I. Zycband, J. T. Fallon, R. L. Trelstad: Collagen fibril bundles: a branching assembly unit in tendon morphogenesis. Development 107, 437-443 (1989).
7. Birk, D. E., R. L. Trelstad: Extracellular compartments in tendon morphogenesis: collagen fibril, bundle, and macroaggregate formation. J. Cell Biol. 103, 231-240 (1986).
8. Birk, D. E., E. I. Zycband, D. A. Winkelmann, R. L. Trelstad: Collagen fibrillogenesis in situ: fibril segments are intermediates in matrix assembly. Proc. Natl. Acad. Sci. USA 86, 4549-4553 (1989).
9. Birk, D. E., E. I. Zycband, D. A. Winkelmann, R. L. Trelstad: Collagen fibrillogenesis in situ. Discontinuous segmental assembly in extracellular compartments. Ann. N.Y. Acad. Sci. 580, 176-194 (1990).
10. Bland, Y. S., D. E. Ashhurst: Changes in the distribution of fibrillar collagens in the collateral and cruciate ligaments of the rabbit knee joint during fetal and postnatal development. Histochem. J. 28, 325-334 (1996).
11. Brewton, R. G., R. Mayne: Heterotypic type II, IX, and XI fibrils: comparison of vitreous and cartilage forms. In: P. D. Yurchenco, D. E. Birk, R. P. Mecham (eds.): Extracellular Matrix Assembly and Structure. pp. 129-170. Academic Press. New York 1994.
12. Doane, K. J., J. P. Babiarz, J. M. Fitch, T. F. Linsenmayer, D. E. Birk: Collagen fibril assembly by corneal fibroblasts in three-dimensional collagen gel cultures: small-diameter heterotypic fibrils are deposited in the absence of keratan sulfate proteoglycan. Exp. Cell Res. 202, 113-124 (1992).
13. Fichard, A., J.-P. Kleman, F. Ruggiero: Another look at collagen V and XI molecules. Matrix Biol. 14, 515-531 (1994).
14. Fitch, J. M., D. E. Birk, A. Mentzer, K. A. Hasty, C. Mainardi, T. F. Linsenmayer: Corneal collagen fibrils: dissection with specific collagenases and monoclonal antibodies. Invest. Ophthalmol. Visual Sci. 29, 1125-1136 (1988).
15. Fitch, J. M., E. Gibney, R. D. Sanderson, R. Mayne, T. F. Linsenmayer: Domain and basement membrane specificity of a monoclonal antibody against chicken type IV collagen. J. Cell Biol. 95, 641-647 (1982).
16. Fitch, J. M., J. Gross, R. Mayne, B. Johnson Wint, T. F. Linsenmayer: Organization of collagen types I and V in the embryonic chicken cornea: monoclonal antibody studies. Proc. Natl. Acad. Sci. USA 81, 2791-2795 (1984).
17. Fleischmajer, R. S., S. Gay, J. S. Perlish, J. P. Cesarini: Immuno-electron microscopy of type III collagen in normal and sclerodermal skin. J. Invest. Dermatol. 75, 189-191 (1980).
18. Fleischmajer, R., B. R. Olsen, R. Timpl, J. S. Perlish, O. Lovelace: Collagen fibril formation during embryogenesis. Proc. Natl. Acad. Sci. USA 80, 3354-3358 (1983).
19. Fleischmajer, R., R. Timpl, L. Tuderman, L. Raisher, M. Wiestner, J. S. Perlish, P. N. Graves: Ultrastructural identification of extension aminopropeptides of type I and III collagens in human skin. Proc. Natl. Acad. Sci. USA 78, 7360-7364 (1981).
20. Hamburger, V., H. L. Hamilton: A series of normal stages in development of the chick embryo. J. Morphol. 88, 49-92 (1951).
21. Hendrix, M. J., E. D. Hay, K. von der Mark, T. F. Linsenmayer: Immunohistochemical localization of collagen types I and II in the developing chick cornea and tibia by electron microscopy. Invest. Ophthalmol. Visual Sci. 22, 359-375 (1982).
22. Herrmann, H., W. Dessau, L. I. Fessier, K. von der Mark: Synthesis of types I, III and AB2 collagen by chick tendon fibroblasts in vitro. Eur. J. Biochem. 105, 63-74 (1980).
23. Jimenez, S. A., R. Yankowski, R. I. Bashey: Identification of two new collagen α-chains in extracts of lathyritic chicken embryo tendons. Biochem. Biophys. Res. Commun. 81, 1298-1306 (1978).
24. Keene, D. R., L. Y. Sakai, H. P. Bachinger, R. E. Burgeson: Type III collagen can be present on banded collagen fibrils regardless of fibril diameter. J. Cell Biol. 105, 2393-2402 (1987).
25. Lapiere, C. M., B. Nusgens, G. E. Pierard: Interaction between collagen type I and type III in conditioning bundles organization. Connect. Tissue Res. 5, 21-29 (1977).
26. Linsenmayer, T. F., J. M. Fitch, D. E. Birk: Heterotypic collagen fibrils and stabilizing collagens. Controlling elements in corneal morphogenesis? Ann. N. Y. Acad. Sci. 580, 143-160 (1990).
27. Linsenmayer, T. F., J. M. Fitch, T. M. Schmid, R. D. Sanderson, R. Mayne: Monoclonal antibodies against chicken type V collagen: production, specificity, and use for immunocytochemical localization in embryonic cornea and other organs. J. Cell Biol. 96. 124-132 (1983).
28. Linsenmayer, T. F., E. Gibney, F. Igoe, M. K. Gordon, J. M. Fitch, L. I. Fessler, D. E. Birk: Type V collagen: molecular structure and fibrillar organization of the chicken α1(V) NH2-terminal domain, a putative regulator of corneal fibrillogenesis. J. Cell Biol. 121, 1181-1189 (1993).
29. Linsenmayer, T. F., M. J. Hendrix, C. D. Little: Production and characterization of a monoclonal antibody to chicken type I collagen. Proc. Natl. Acad. Sci. USA 76, 3703-3707 (1979).
30. Mayne, R., R. G. Brewton: New members of the collagen super-family (Review). Curr. Opin. Cell Biol. 5, 883-890 (1993).
31. Mayne, R., P. M. Mayne, B. M. Wood, S. K. Justice, N. I. Zhidkova, J. R. Baker: Characterization of type V/XI collagen present in the embryonic chick tendon. Matrix Biol. (abst) 15, 161 (1996).
32. Mayne, R., R. D. Sanderson, H. Wiedemann, J. M. Fitch, T. F. Linsenmayer: The use of monoclonal antibodies to fragments of chicken type IV collagen in structural and localization studies. J. Biol. Chem. 258, 5794-5797 (1983).
33. McBride, D. J., R. L. Trelstad, F. H. Silver: Structural and mechanical assessment of developing chick tendon. Int. J. Biol. Macromol. 10, 194-200 (1988).
34. McLaughlin, J. S., T. F. Linsenmayer, D. E. Birk: Type V collagen synthesis and deposition by chicken embryo corneal fibroblasts in vitro. J. Cell Sci. 94, 371-379 (1989).
35. Mendler, M., S. G. Eich-Bender, L. Vaughan, K. H. Winterhalter, P. Bruckner: Cartilage contains mixed fibrils of collagen types II, IX, and XI. J. Cell Biol. 108, 191-197 (1989).
36. Nurminskaya, M. V., D. E. Birk: Differential expression of fibro-modulin mRNA associated with tendon fibril growth: isolation and characterization of a chicken fibromodulin cDNA. Biochem. J. 317, 785-789 (1996).
37. Peltonen, L., R. Halila, L. Ryhanen: Enzymes converting procollagens to collagens. J. Cell. Biochem. 28, 15-21 (1985).
38. Prockop, D. J., K. I. Kivirikko: Collagens: molecular biology, diseases, and potentials for therapy. Annu. Rev. Biochem. 64, 403-434 (1995).
39. Romanic, A. M., E. Adachi, Y. Hojima, J. Engel, D. J. Prockop: Polymerization of pNcollagen I and copolymerization of pNcollagen I with collagen I. A kinetic, thermodynamic, and morphologic study. J. Biol. Chem. 267, 22265-22271 (1992).
40. Romanic, A. M., E. Adachi, K. E. Kadler, Y. Hojima, D. J. Prockop: Copolymerization of pNcollagen III and collagen I. pNcollagen III decreases the rate of incorporation of collagen I into fibrils, the amount of collagen I incorporated, and the diameter of the fibrils formed. J. Biol. Chem. 266, 12703-12709 (1991).
41. Ros, M. A., F. B. Rivero, J. R. Hinchliffe, J. M. Hurle: Immunohistological and ultrastructural study of the developing tendons of the avian foot. Anat. Embryol. (Berl) 192, 483-496 (1995).
42. Swasdison, S., P. M. Mayne, D. W. Wright, M. A. Accavitti, J. M. Fitch, T. F. Linsenmayer, R. Mayne: Monoclonal antibodies that distinguish avian type I and type III collagens: isolation, characterization and immunolocalization in various tissues. Matrix 12, 56-65 (1992).
43. Tsuzaki, M., M. Yamauchi, A. J. Banes: Tendon collagens: extracellular matrix composition in shear stress and tensile components of flexor tendons. Connect. Tissue Res. 29, 141-152 (1993).
44. Vogel, K. G.: Glycosaminoglycans and proteoglycans. In: P. D. Yurchenco, D. E. Birk, R. P. Mecham (eds): Extracellular Matrix Assembly and Structure. pp. 243-280. Academic Press. New York 1994.
45. Yang, G. C., D. E. Birk: Topographics of extracytoplasmic compartments in developing chick tendon fibroblasts. J. Ultrastruct. Mol. Struct. Res. 97, 238-248 (1986).