Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Jul 29;355(1399):885–890. doi: 10.1098/rstb.2000.0624

Patterning of cell assemblies regulated by adhesion receptors of the cadherin superfamily.

M Takeichi 1, S Nakagawa 1, S Aono 1, T Usui 1, T Uemura 1
PMCID: PMC1692800  PMID: 11128982

Abstract

During morphogenesis, cell-cell association patterns are dynamically altered. We are interested in how cell adhesion molecules can regulate the patterning of cellular assemblies. Cadherins, a group of cell-cell adhesion receptors, are crucial for the organized assembly of many cell types, but they also regulate dynamic aspects of cell association. For example, during neural crest emigration from the neural tube, the cadherin subtypes expressed by crest cells are switched from one subtype to another. Artificial perturbation of this switch results in blocking of their escape from the neural tube. Intracellular modulations of cadherin activity also seem to play a role in regulation of cell adhesion. We identified p120ctn as a regulator of cadherin function in carcinoma cells. With such regulators, cells may make a choice as to whether they should maintain stable cell contacts or disrupt their association. Finally, we found another type of cadherin-mediated cell patterning: Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity in Drosophila imaginal discs. Thus, the cadherin superfamily receptors control the patterning of cell assemblies through a variety of mechanisms.

Full Text

The Full Text of this article is available as a PDF (350.8 KB).

Selected References

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

  1. Adler P. N., Krasnow R. E., Liu J. Tissue polarity points from cells that have higher Frizzled levels towards cells that have lower Frizzled levels. Curr Biol. 1997 Dec 1;7(12):940–949. doi: 10.1016/s0960-9822(06)00413-1. [DOI] [PubMed] [Google Scholar]
  2. Aono S., Nakagawa S., Reynolds A. B., Takeichi M. p120(ctn) acts as an inhibitory regulator of cadherin function in colon carcinoma cells. J Cell Biol. 1999 May 3;145(3):551–562. doi: 10.1083/jcb.145.3.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barth A. I., Näthke I. S., Nelson W. J. Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr Opin Cell Biol. 1997 Oct;9(5):683–690. doi: 10.1016/s0955-0674(97)80122-6. [DOI] [PubMed] [Google Scholar]
  4. Burden-Gulley S. M., Brady-Kalnay S. M. PTPmu regulates N-cadherin-dependent neurite outgrowth. J Cell Biol. 1999 Mar 22;144(6):1323–1336. doi: 10.1083/jcb.144.6.1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chen H., Paradies N. E., Fedor-Chaiken M., Brackenbury R. E-cadherin mediates adhesion and suppresses cell motility via distinct mechanisms. J Cell Sci. 1997 Feb;110(Pt 3):345–356. doi: 10.1242/jcs.110.3.345. [DOI] [PubMed] [Google Scholar]
  6. Daniel J. M., Reynolds A. B. Tyrosine phosphorylation and cadherin/catenin function. Bioessays. 1997 Oct;19(10):883–891. doi: 10.1002/bies.950191008. [DOI] [PubMed] [Google Scholar]
  7. Eaton S., Wepf R., Simons K. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J Cell Biol. 1996 Dec;135(5):1277–1289. doi: 10.1083/jcb.135.5.1277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Geis K., Aberle H., Kühl M., Kemler R., Wedlich D. Expression of the Armadillo family member p120cas1B in Xenopus embryos affects head differentiation but not axis formation. Dev Genes Evol. 1998 Jan;207(7):471–481. doi: 10.1007/s004270050138. [DOI] [PubMed] [Google Scholar]
  9. Godt D., Tepass U. Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature. 1998 Sep 24;395(6700):387–391. doi: 10.1038/26493. [DOI] [PubMed] [Google Scholar]
  10. Guilford P., Hopkins J., Harraway J., McLeod M., McLeod N., Harawira P., Taite H., Scoular R., Miller A., Reeve A. E. E-cadherin germline mutations in familial gastric cancer. Nature. 1998 Mar 26;392(6674):402–405. doi: 10.1038/32918. [DOI] [PubMed] [Google Scholar]
  11. Hatta K., Takeichi M. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature. 1986 Apr 3;320(6061):447–449. doi: 10.1038/320447a0. [DOI] [PubMed] [Google Scholar]
  12. Hirano S., Kimoto N., Shimoyama Y., Hirohashi S., Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell. 1992 Jul 24;70(2):293–301. doi: 10.1016/0092-8674(92)90103-j. [DOI] [PubMed] [Google Scholar]
  13. Jawhari A. U., Farthing M. J., Pignatelli M. The E-cadherin/epidermal growth factor receptor interaction: a hypothesis of reciprocal and reversible control of intercellular adhesion and cell proliferation. J Pathol. 1999 Jan;187(2):155–157. doi: 10.1002/(SICI)1096-9896(199901)187:2<155::AID-PATH193>3.0.CO;2-E. [DOI] [PubMed] [Google Scholar]
  14. Mitchell H. K., Roach J., Petersen N. S. The morphogenesis of cell hairs on Drosophila wings. Dev Biol. 1983 Feb;95(2):387–398. doi: 10.1016/0012-1606(83)90040-4. [DOI] [PubMed] [Google Scholar]
  15. Nakagawa S., Takeichi M. Neural crest cell-cell adhesion controlled by sequential and subpopulation-specific expression of novel cadherins. Development. 1995 May;121(5):1321–1332. doi: 10.1242/dev.121.5.1321. [DOI] [PubMed] [Google Scholar]
  16. Nakagawa S., Takeichi M. Neural crest emigration from the neural tube depends on regulated cadherin expression. Development. 1998 Aug;125(15):2963–2971. doi: 10.1242/dev.125.15.2963. [DOI] [PubMed] [Google Scholar]
  17. Ozawa M., Kemler R. Altered cell adhesion activity by pervanadate due to the dissociation of alpha-catenin from the E-cadherin.catenin complex. J Biol Chem. 1998 Mar 13;273(11):6166–6170. doi: 10.1074/jbc.273.11.6166. [DOI] [PubMed] [Google Scholar]
  18. Paulson A. F., Fang X., Ji H., Reynolds A. B., McCrea P. D. Misexpression of the catenin p120(ctn)1A perturbs Xenopus gastrulation but does not elicit Wnt-directed axis specification. Dev Biol. 1999 Mar 15;207(2):350–363. doi: 10.1006/dbio.1998.9158. [DOI] [PubMed] [Google Scholar]
  19. Peifer M., Berg S., Reynolds A. B. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell. 1994 Mar 11;76(5):789–791. doi: 10.1016/0092-8674(94)90353-0. [DOI] [PubMed] [Google Scholar]
  20. Radice G. L., Ferreira-Cornwell M. C., Robinson S. D., Rayburn H., Chodosh L. A., Takeichi M., Hynes R. O. Precocious mammary gland development in P-cadherin-deficient mice. J Cell Biol. 1997 Nov 17;139(4):1025–1032. doi: 10.1083/jcb.139.4.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Riehl R., Johnson K., Bradley R., Grunwald G. B., Cornel E., Lilienbaum A., Holt C. E. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron. 1996 Nov;17(5):837–848. doi: 10.1016/s0896-6273(00)80216-0. [DOI] [PubMed] [Google Scholar]
  22. Steinberg M. S., Takeichi M. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):206–209. doi: 10.1073/pnas.91.1.206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Takeichi M. Morphogenetic roles of classic cadherins. Curr Opin Cell Biol. 1995 Oct;7(5):619–627. doi: 10.1016/0955-0674(95)80102-2. [DOI] [PubMed] [Google Scholar]
  24. Thiery J. P., Delouvée A., Gallin W. J., Cunningham B. A., Edelman G. M. Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol. 1984 Mar;102(1):61–78. doi: 10.1016/0012-1606(84)90175-1. [DOI] [PubMed] [Google Scholar]
  25. Turner C. M., Adler P. N. Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila. Mech Dev. 1998 Jan;70(1-2):181–192. doi: 10.1016/s0925-4773(97)00194-9. [DOI] [PubMed] [Google Scholar]
  26. Uemura T. The cadherin superfamily at the synapse: more members, more missions. Cell. 1998 Jun 26;93(7):1095–1098. doi: 10.1016/s0092-8674(00)81452-x. [DOI] [PubMed] [Google Scholar]
  27. Usui T., Shima Y., Shimada Y., Hirano S., Burgess R. W., Schwarz T. L., Takeichi M., Uemura T. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell. 1999 Sep 3;98(5):585–595. doi: 10.1016/s0092-8674(00)80046-x. [DOI] [PubMed] [Google Scholar]
  28. Watabe-Uchida M., Uchida N., Imamura Y., Nagafuchi A., Fujimoto K., Uemura T., Vermeulen S., van Roy F., Adamson E. D., Takeichi M. alpha-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J Cell Biol. 1998 Aug 10;142(3):847–857. doi: 10.1083/jcb.142.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wong L. L., Adler P. N. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J Cell Biol. 1993 Oct;123(1):209–221. doi: 10.1083/jcb.123.1.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Yap A. S., Niessen C. M., Gumbiner B. M. The juxtamembrane region of the cadherin cytoplasmic tail supports lateral clustering, adhesive strengthening, and interaction with p120ctn. J Cell Biol. 1998 May 4;141(3):779–789. doi: 10.1083/jcb.141.3.779. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES