Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Jul 1;111(1):271–278. doi: 10.1083/jcb.111.1.271

Characterization of a maternal type VI collagen in Xenopus embryos suggests a role for collagen in gastrulation

PMCID: PMC2116162  PMID: 2164030

Abstract

We characterized a novel extracellular matrix element that is present in the earliest developmental stages of Xenopus laevis, and is recognized by an mAb 3D7. Based on amino acid composition, breakdown patterns by bacterial collagenases, and the molecular weights of the components of the antigen (240, 200, and 140 kD), we found it very similar to mammalian collagen type VI. The antigen is evenly distributed in unfertilized eggs. Shortly after fertilization, it becomes localized intracellularly in the periphery of the cleaving embryo as well as in the extracellular spaces. During gastrulation, the antigen was localized in the cells lining the blastopore and in the extracellular space between the two cell layers, in the presumptive archenteron. When Fab elements of the 3D7 antibody were added to the culture medium, gastrulation was blocked, suggesting a role for the antigen in gastrulation movements.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Selected References

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

  1. Boucaut J. C., Darribère T., Boulekbache H., Thiery J. P. Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. 1984 Jan 26-Feb 1Nature. 307(5949):364–367. doi: 10.1038/307364a0. [DOI] [PubMed] [Google Scholar]
  2. Boucaut J. C., Darribère T., Poole T. J., Aoyama H., Yamada K. M., Thiery J. P. Biologically active synthetic peptides as probes of embryonic development: a competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J Cell Biol. 1984 Nov;99(5):1822–1830. doi: 10.1083/jcb.99.5.1822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burgeson R. E. New collagens, new concepts. Annu Rev Cell Biol. 1988;4:551–577. doi: 10.1146/annurev.cb.04.110188.003003. [DOI] [PubMed] [Google Scholar]
  4. Carter W. G. The cooperative role of the transformation-sensitive glycoproteins, GP140 and fibronectin, in cell attachment and spreading. J Biol Chem. 1982 Mar 25;257(6):3249–3257. [PubMed] [Google Scholar]
  5. Carter W. G. Transformation-dependent alterations is glycoproteins of extracellular matrix of human fibroblasts. Characterization of GP250 and the collagen-like GP140. J Biol Chem. 1982 Nov 25;257(22):13805–13815. [PubMed] [Google Scholar]
  6. Chu M. L., Conway D., Pan T. C., Baldwin C., Mann K., Deutzmann R., Timpl R. Amino acid sequence of the triple-helical domain of human collagen type VI. J Biol Chem. 1988 Dec 15;263(35):18601–18606. [PubMed] [Google Scholar]
  7. Crawford S. W., Featherstone J. A., Holbrook K., Yong S. L., Bornstein P., Sage H. Characterization of a type VI collagen-related Mr-140 000 protein from cutis-laxa fibroblasts in culture. Biochem J. 1985 Apr 15;227(2):491–502. doi: 10.1042/bj2270491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Darribère T., Riou J. F., Shi D. L., Delarue M., Boucaut J. C. Synthesis and distribution of laminin-related polypeptides in early amphibian embryos. Cell Tissue Res. 1986;246(1):45–51. doi: 10.1007/BF00218997. [DOI] [PubMed] [Google Scholar]
  9. Darribère T., Yamada K. M., Johnson K. E., Boucaut J. C. The 140-kDa fibronectin receptor complex is required for mesodermal cell adhesion during gastrulation in the amphibian Pleurodeles waltlii. Dev Biol. 1988 Mar;126(1):182–194. doi: 10.1016/0012-1606(88)90252-7. [DOI] [PubMed] [Google Scholar]
  10. Duband J. L., Rocher S., Chen W. T., Yamada K. M., Thiery J. P. Cell adhesion and migration in the early vertebrate embryo: location and possible role of the putative fibronectin receptor complex. J Cell Biol. 1986 Jan;102(1):160–178. doi: 10.1083/jcb.102.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Engel J., Furthmayr H., Odermatt E., von der Mark H., Aumailley M., Fleischmajer R., Timpl R. Structure and macromolecular organization of type VI collagen. Ann N Y Acad Sci. 1985;460:25–37. doi: 10.1111/j.1749-6632.1985.tb51154.x. [DOI] [PubMed] [Google Scholar]
  12. Gerhart J., Keller R. Region-specific cell activities in amphibian gastrulation. Annu Rev Cell Biol. 1986;2:201–229. doi: 10.1146/annurev.cb.02.110186.001221. [DOI] [PubMed] [Google Scholar]
  13. Green H., Goldberg B., Schwartz M., Brown D. D. The synthesis of collagen during the development of Xenopus laevis. Dev Biol. 1968 Oct;18(4):391–400. doi: 10.1016/0012-1606(68)90048-1. [DOI] [PubMed] [Google Scholar]
  14. Heller-Harrison R. A., Carter W. G. Pepsin-generated type VI collagen is a degradation product of GP140. J Biol Chem. 1984 Jun 10;259(11):6858–6864. [PubMed] [Google Scholar]
  15. Hessle H., Engvall E. Type VI collagen. Studies on its localization, structure, and biosynthetic form with monoclonal antibodies. J Biol Chem. 1984 Mar 25;259(6):3955–3961. [PubMed] [Google Scholar]
  16. Keller R. E. The cellular basis of amphibian gastrulation. Dev Biol (N Y 1985) 1986;2:241–327. doi: 10.1007/978-1-4613-2141-5_7. [DOI] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Lee G., Hynes R., Kirschner M. Temporal and spatial regulation of fibronectin in early Xenopus development. Cell. 1984 Mar;36(3):729–740. doi: 10.1016/0092-8674(84)90353-2. [DOI] [PubMed] [Google Scholar]
  19. Matthew W. D., Reichardt L. F. Development and application of an efficient procedure for converting mouse IgM into small, active fragments. J Immunol Methods. 1982;50(3):239–253. doi: 10.1016/0022-1759(82)90162-4. [DOI] [PubMed] [Google Scholar]
  20. Merril C. R., Goldman D., Sedman S. A., Ebert M. H. Ultrasensitive stain for proteins in polyacrylamide gels shows regional variation in cerebrospinal fluid proteins. Science. 1981 Mar 27;211(4489):1437–1438. doi: 10.1126/science.6162199. [DOI] [PubMed] [Google Scholar]
  21. Nakatsuji N., Smolira M. A., Wylie C. C. Fibronectin visualized by scanning electron microscopy immunocytochemistry on the substratum for cell migration in Xenopus laevis gastrulae. Dev Biol. 1985 Jan;107(1):264–268. doi: 10.1016/0012-1606(85)90395-1. [DOI] [PubMed] [Google Scholar]
  22. Outenreath R. L., Roberson M. M., Barondes S. H. Endogenous lectin secretion into the extracellular matrix of early embryos of Xenopus laevis. Dev Biol. 1988 Jan;125(1):187–194. doi: 10.1016/0012-1606(88)90071-1. [DOI] [PubMed] [Google Scholar]
  23. Roberson M. M., Barondes S. H. Lectin from embryos and oocytes of Xenopus laevis. Purification and properties. J Biol Chem. 1982 Jul 10;257(13):7520–7524. [PubMed] [Google Scholar]
  24. Roberson M. M., Barondes S. H. Xenopus laevis lectin is localized at several sites in Xenopus oocytes, eggs, and embryos. J Cell Biol. 1983 Dec;97(6):1875–1881. doi: 10.1083/jcb.97.6.1875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sage H., Bornstein P. Preparation and characterization of procollagens and procollagen-collagen intermediates. Methods Enzymol. 1982;82(Pt A):96–127. doi: 10.1016/0076-6879(82)82061-2. [DOI] [PubMed] [Google Scholar]
  26. Shulman M., Wilde C. D., Köhler G. A better cell line for making hybridomas secreting specific antibodies. Nature. 1978 Nov 16;276(5685):269–270. doi: 10.1038/276269a0. [DOI] [PubMed] [Google Scholar]
  27. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Trüeb B., Bornstein P. Characterization of the precursor form of type VI collagen. J Biol Chem. 1984 Jul 10;259(13):8597–8604. [PubMed] [Google Scholar]
  29. Trüeb B., Lewis J. B., Carter W. G. Translatable mRNA for GP140 (a subunit of type VI collagen) is absent in SV40 transformed fibroblasts. J Cell Biol. 1985 Feb;100(2):638–641. doi: 10.1083/jcb.100.2.638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Trüeb B., Winterhalter K. H. Type VI collagen is composed of a 200 kd subunit and two 140 kd subunits. EMBO J. 1986 Nov;5(11):2815–2819. doi: 10.1002/j.1460-2075.1986.tb04573.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. de StGroth S. F., Scheidegger D. Production of monoclonal antibodies: strategy and tactics. J Immunol Methods. 1980;35(1-2):1–21. doi: 10.1016/0022-1759(80)90146-5. [DOI] [PubMed] [Google Scholar]

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

RESOURCES