Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1989 Jun;8(6):1711–1717. doi: 10.1002/j.1460-2075.1989.tb03563.x

The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species.

M Ozawa 1, H Baribault 1, R Kemler 1
PMCID: PMC401013  PMID: 2788574

Abstract

Uvomorulin belongs to the group of Ca2+-dependent cell adhesion molecules, which are integral membrane proteins with several structural features in common. In particular, the cytoplasmic part of these proteins is highly conserved in different species, suggesting a common biological function. To test this assumption we transfected a uvomorulin full-length cDNA into uvomorulin-negative mouse NIH 3T3 and L cells. Immunoprecipitations with anti-uvomorulin antibodies detected, in addition to uvomorulin, three independent proteins of 102, 88 and 80 kd which are of host origin and which form complexes with uvomorulin. Using cDNA constructs coding for uvomorulin with cytoplasmic or extracellular deletions it is shown that the 102, 88 and 80 kd proteins complex with the cytoplasmic domain of uvomorulin. Peptide pattern analysis revealed that these three proteins are identical in different mouse cells. When uvomorulin cDNA was introduced into cell lines from other species, such as human HeLa and avian fibroblasts, the expressed uvomorulin was also associated with endogenous 102, 88 and 80 kd proteins and, moreover, each of these proteins showed structural similarities to the respective mouse molecule. A panel of antibodies specific for known cytoplasmic proteins of mol. wts similar to those of the three proteins did not react with any of the described components. This suggests that the 102, 88 and 80 kd proteins constitute a new group of proteins for which we propose the nomenclature of catenin alpha, beta and gamma respectively. The characterization of these proteins provides a first molecular basis for a possible cytoplasmic anchorage of uvomorulin to the cytoskeleton.

Full text

PDF
1711

Images in this article

1712Image
on p.1712
1712Image
on p.1712
1713Image
on p.1713
1713Image
on p.1713
1714Image
on p.1714
1714Image
on p.1714
1715Image
on p.1715
1715Image
on p.1715
1715Image
on p.1715

Selected References

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

  1. Artzt K., Dubois P., Bennett D., Condamine H., Babinet C., Jacob F. Surface antigens common to mouse cleavage embryos and primitive teratocarcinoma cells in culture. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2988–2992. doi: 10.1073/pnas.70.10.2988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Behrens J., Birchmeier W., Goodman S. L., Imhof B. A. Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin. J Cell Biol. 1985 Oct;101(4):1307–1315. doi: 10.1083/jcb.101.4.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boller K., Vestweber D., Kemler R. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J Cell Biol. 1985 Jan;100(1):327–332. doi: 10.1083/jcb.100.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burgess D. R. Reactivation of intestinal epithelial cell brush border motility: ATP-dependent contraction via a terminal web contractile ring. J Cell Biol. 1982 Dec;95(3):853–863. doi: 10.1083/jcb.95.3.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  6. Copeland C. S., Zimmer K. P., Wagner K. R., Healey G. A., Mellman I., Helenius A. Folding, trimerization, and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell. 1988 Apr 22;53(2):197–209. doi: 10.1016/0092-8674(88)90381-9. [DOI] [PubMed] [Google Scholar]
  7. Cunningham B. A., Hemperly J. J., Murray B. A., Prediger E. A., Brackenbury R., Edelman G. M. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. doi: 10.1126/science.3576199. [DOI] [PubMed] [Google Scholar]
  8. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  9. Ekblom P., Vestweber D., Kemler R. Cell-matrix interactions and cell adhesion during development. Annu Rev Cell Biol. 1986;2:27–47. doi: 10.1146/annurev.cb.02.110186.000331. [DOI] [PubMed] [Google Scholar]
  10. Gallin W. J., Sorkin B. C., Edelman G. M., Cunningham B. A. Sequence analysis of a cDNA clone encoding the liver cell adhesion molecule, L-CAM. Proc Natl Acad Sci U S A. 1987 May;84(9):2808–2812. doi: 10.1073/pnas.84.9.2808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gumbiner B. Cadherins: a family of Ca2+-dependent adhesion molecules. Trends Biochem Sci. 1988 Mar;13(3):75–76. doi: 10.1016/0968-0004(88)90040-0. [DOI] [PubMed] [Google Scholar]
  12. Gumbiner B., Simons K. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J Cell Biol. 1986 Feb;102(2):457–468. doi: 10.1083/jcb.102.2.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hatta K., Nose A., Nagafuchi A., Takeichi M. Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J Cell Biol. 1988 Mar;106(3):873–881. doi: 10.1083/jcb.106.3.873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  15. Hirano S., Nose A., Hatta K., Kawakami A., Takeichi M. Calcium-dependent cell-cell adhesion molecules (cadherins): subclass specificities and possible involvement of actin bundles. J Cell Biol. 1987 Dec;105(6 Pt 1):2501–2510. doi: 10.1083/jcb.105.6.2501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kaaden O. R., Lange S., Stiburek B. Establishment and characterization of chicken embryo fibroblast clone LSCC-H32. In Vitro. 1982 Oct;18(10):827–834. doi: 10.1007/BF02796323. [DOI] [PubMed] [Google Scholar]
  17. Mansouri A., Spurr N., Goodfellow P. N., Kemler R. Characterization and chromosomal localization of the gene encoding the human cell adhesion molecule uvomorulin. Differentiation. 1988 Jun;38(1):67–71. doi: 10.1111/j.1432-0436.1988.tb00593.x. [DOI] [PubMed] [Google Scholar]
  18. Moscovici C., Moscovici M. G., Jimenez H., Lai M. M., Hayman M. J., Vogt P. K. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell. 1977 May;11(1):95–103. doi: 10.1016/0092-8674(77)90320-8. [DOI] [PubMed] [Google Scholar]
  19. Nagafuchi A., Shirayoshi Y., Okazaki K., Yasuda K., Takeichi M. Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature. 1987 Sep 24;329(6137):341–343. doi: 10.1038/329341a0. [DOI] [PubMed] [Google Scholar]
  20. Nagafuchi A., Takeichi M. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J. 1988 Dec 1;7(12):3679–3684. doi: 10.1002/j.1460-2075.1988.tb03249.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nose A., Nagafuchi A., Takeichi M. Isolation of placental cadherin cDNA: identification of a novel gene family of cell-cell adhesion molecules. EMBO J. 1987 Dec 1;6(12):3655–3661. doi: 10.1002/j.1460-2075.1987.tb02698.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Peyriéras N., Louvard D., Jacob F. Characterization of antigens recognized by monoclonal and polyclonal antibodies directed against uvomorulin. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8067–8071. doi: 10.1073/pnas.82.23.8067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ringwald M., Schuh R., Vestweber D., Eistetter H., Lottspeich F., Engel J., Dölz R., Jähnig F., Epplen J., Mayer S. The structure of cell adhesion molecule uvomorulin. Insights into the molecular mechanism of Ca2+-dependent cell adhesion. EMBO J. 1987 Dec 1;6(12):3647–3653. doi: 10.1002/j.1460-2075.1987.tb02697.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sussman J. J., Bonifacino J. S., Lippincott-Schwartz J., Weissman A. M., Saito T., Klausner R. D., Ashwell J. D. Failure to synthesize the T cell CD3-zeta chain: structure and function of a partial T cell receptor complex. Cell. 1988 Jan 15;52(1):85–95. doi: 10.1016/0092-8674(88)90533-8. [DOI] [PubMed] [Google Scholar]
  25. Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development. 1988 Apr;102(4):639–655. doi: 10.1242/dev.102.4.639. [DOI] [PubMed] [Google Scholar]
  26. Vestweber D., Gossler A., Boller K., Kemler R. Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol. 1987 Dec;124(2):451–456. doi: 10.1016/0012-1606(87)90498-2. [DOI] [PubMed] [Google Scholar]
  27. Vestweber D., Kemler R. Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 1985 Dec 16;4(13A):3393–3398. doi: 10.1002/j.1460-2075.1985.tb04095.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vestweber D., Kemler R. Rabbit antiserum against a purified surface glycoprotein decompacts mouse preimplantation embryos and reacts with specific adult tissues. Exp Cell Res. 1984 May;152(1):169–178. doi: 10.1016/0014-4827(84)90241-6. [DOI] [PubMed] [Google Scholar]
  29. Vestweber D., Kemler R. Some structural and functional aspects of the cell adhesion molecule uvomorulin. Cell Differ. 1984 Dec;15(2-4):269–273. doi: 10.1016/0045-6039(84)90084-8. [DOI] [PubMed] [Google Scholar]
  30. Volk T., Geiger B. A-CAM: a 135-kD receptor of intercellular adherens junctions. II. Antibody-mediated modulation of junction formation. J Cell Biol. 1986 Oct;103(4):1451–1464. doi: 10.1083/jcb.103.4.1451. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES