Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system

Genes and Development

Volumn 10, Issue 8, 1996, Pages 985-996

  Hermiston, Michelle L ^a   Wong, Melissa H ^a   Gordon, Jeffrey I ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

adhesion; Cadherins; catenins; chimeric transgenic mice; differentiation; intestinal epithelium; migration

Indexed keywords

UVOMORULIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; INTESTINE CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM; INTESTINE VILLUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

EID: 0029964159     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.8.985     Document Type: Article

References (51)

1. Bradley, R.S , P. Cowin, and A.M. Brown. 1993. Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J. Cell Biol. 123: 1857-1865.
2. Bry, L., P. Falk, K. Huttner, A. Ouellette, T. Midtvedt, and J.I. Gordon. 1994. Paneth cell differentiation in the developing intestine of normal and transgenic mice. Proc. Natl. Acad. Sci. 91: 10335-10339.
3. Calvert, R. and P. Pothier. 1990. Migration of fetal intestinal intervillous cells in neonatal mice. Anat. Rec. 227: 199-206.
4. Cheng, H. 1974. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. IV. Paneth cells. Am. J. Anat. 141: 521-536.
5. Cohn, S. M., T C Simon, K.A. Roth, E.H. Birkenmeier, and J.I. Gordon. 1992. Use of transgenic mice to map cis-acting elements in the intestinal fatty acid binding protein gene [Fabpi] that control its cell lineage-specific and regional patterns of expression along the duodenal-colonic and cryptvillus axes of the gut epithelium. J. Cell Biol. 119: 27-44.
6. Crossman, M.W., S M. Hauft, and J.I. Gordon. 1994. The mouse ileal lipid binding protein gene: A model for studying axial patterning during gut morphogenesis. J. Cell Biol. 126: 1547-1564.
7. Dickinson, M.E., R. Krumlauf, and A.P. McMahon. 1994. Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system. Development 120: 1453-1471.
8. Falk, P., K.A. Roth, and J.I Gordon. 1994. Lectins are sensitive tools for defining the differentiation programs of mouse gut epithelial cell lineages. Am. J. Physiol. [Gastrointest Liver Physiol] 266: G987-G1003.
9. Funayama, N., F Fagotto, P. McCrea, and B.M. Gumbiner. 1995. Embryonic axis induction by the armadillo repeat domain of β-catenin: Evidence for intracellular signaling. J. Cell Biol. 128: 959-968.
10. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol 119: 493-501.
11. Haegel, H., L. Larue, M. Ohsugi, L. Fedorov, K. Herrenknecht, and R. Kemler. 1995. Lack of β-catenin affects mouse development at gastrulation. Development 121: 3529-3537.
12. Hall, P A., P J. Coates, B. Ansari, and D. Hopwood. 1994. Regulation of cell number in mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci. 107: 3569-3577.
13. Heasman, J , A. Crawford, K. Goldstone, P. Garner-Hamrick, B. Gumbiner, P McCrea, C. Kintner, C.Y. Noro, and C. Wylie. 1994. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79: 791-803
14. Hermiston, M.L. and J.I. Gordon. 1995a. In vivo analysis of cadherin function in mouse small intestinal enterocytes: Essential role in adhesion, maintenance of differentation, and regulation of programmed cell death. J. Cell Biol. 129: 489-506.
15. _. 1995b. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270: 1203-1207.
16. Hermiston, M.L., R.P. Green, and J.I. Gordon. 1993. Chimeric-transgenic mice represent a powerful tool for studying how the proliferation and differentiation programs of intestinal epithelial cell lineages are regulated. Proc. Natl. Acad. Sci. 90: 8866-8870.
17. Hinck, L., I.S. Näthke, J. Papkoff, and W.J. Nelson. 1994. Dynamics of cadherin/catenin complex formation: Novel protein interactions and pathways of complex assembly. J. Cell Biol. 125: 1327-1340.
18. Hoschuetzky, H., H. Aberle, and R. Kemler. 1994. β-Catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127: 1375-1380.
19. Huttenlocher, A., R.R. Sandborg, and A.F. Horwitz. 1995. Adhesion in cell migration. Curr. Opin. Cell Biol. 7: 697-706.
20. Jou, T.-S., D.E. Stewart, J. Stappert, W.J. Nelson, and J.A. Marrs. 1995. Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc. Natl. Acad. Sci. 92: 5067-5071.
21. Kim, S.H., K.A. Roth, A R. Moser, and J.I. Gordon. 1993. Transgenic mouse models that explore the multistep hypothesis of intestinal neoplasia J. Cell Biol. 123: 877-893.
22. Kintner, C. 1992. Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell 69: 225-236.
23. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
24. Larue, L., M. Ohsugi, J. Hirchenhain, and R. Kemler. 1994. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl. Acad. Sci. 91: 8263-8267.
25. McCrea, P., W.M. Brieher, and B.M. Gumbiner. 1993. Induction of a secondary body axis in Xenopus embryos by antibodies to β-catenin. J. Cell Biol. 123: 477-485.
26. Munemitsu, S., I. Albert, B. Souza, B. Rubinfeld, and P. Polakis. 1995. Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. 92: 3046-3050.
27. Nagafuchi, A. and M. Takeichi. 1988. Cell binding function of E-cadherin is regulated by the cytoplasmic domain. EMBO J. 7: 3679-3684.
28. Näthke, I.S., L. Hinck, J.R. Swedlow, J. Papkoff, and W.J. Nelson. 1994. Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125: 1341-1352.
29. Overduin, M., T.S. Harvey, S. Bagby, K.I. Tong, P. Yau, M. Takeichi, and M. Ikura. 1995. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science 267: 386-389.
30. Ozawa, M., H. Baribault, and R. Kemler. 1989. The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 8: 1711-1717.
31. Ozawa, M., M. Ringwald, and R. Kemler. 1990. Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Natl. Acad. Sci. 87: 4246-4250.
32. Pfeifer, M. 1995. Cell adhesion and signal transduction: The Armadillo connection. Trends Cell Biol. 5: 224-229.
33. Pfeifer, M., D. Sweeton, M. Casey, and E. Wieschaus. 1994. Wingless signal and zeste-white 3 trigger opposing changes in the intracellular distribution of Armadillo. Development 120: 369-380.
34. Podolsky, D.K. and M.W. Babyatsky. 1991. Growth and development of the gastrointestinal tract. In Textbook of gastroenterology (ed. T. Yamada, D.H. Alpers, C. Owyang, D.W. Powell, and F.E. Silverstein), Vol. 1, p. 489. J.B. Lippincott, Philadelphia, PA.
35. Polakis, P. 1995. Mutations in the APC gene and their implications for protein structure and function. Curr. Opin. Genet. Devel 5: 66-71.
36. Potten, C.S. 1992. The significance of spontaneous and induced apoptosis in the gastrointestinal tract of mice. Cancer Metast. Rev. 11: 179-195.
37. Potten, C.S. and M. Loeffler. 1990. Stem cells: Attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110: 1001-1020.
38. Riethmacher, D., V. Brinkmann, and C. Birchmeier. 1995. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc. Natl. Acad. Sci. 92: 855-859.
39. Roskelley, C.D., A. Srebrow, and M.J. Bissell. 1995. A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr. Opin. Cell Biol. 7: 736-747.
40. Roth, K.A. and J.I. Gordon. 1990. Spatial differentiation of the intestinal epithelium: Analysis of enteroendocrine cells containing immunoreactive serotonin, secretin, and substance P in normal and transgenic mice. Proc. Natl. Acad. Sci. 87: 6408-6412.
41. Roth, K.A., J.M. Hertz, and J.I. Gordon. 1990. Mapping enteroendocrine cell populations in transgenic mice reveals an unexpected degree of complexity in cellular differentiation within the gastrointestinal tract. J. Cell. Biol. 110: 1791-1801.
42. Rubinfeld, B., B. Souza, I. Albert, O. Muller, S.H. Chamberlain, F.R. Masiarz, S. Munemitsu, and P. Polakis. 1993. Association of the APC gene product with β-catenin. Science 262: 1731-1734.
43. Rubinfeld, B , B Souza, I. Albert, S. Munemitsu, and P. Polakis. 1995 The APC protein and E-cadherin form similar but independent complexes with α-catenin, β-catenin, and plakoglobin. J Biol Chem. 270: 5549-5555.
44. Schmidt, G.H., D.J. Winton, and B.A.J. Ponder. 1988. Development of the pattern of cell renewal in the crypt villus unit of chimeric mouse intestine. Development 103: 785-790.
45. Shapiro, L., A M. Fannon, P.D. Kwong, A. Thompson, M.S. Lehmann, G. Grübel, J.-F. Legrand, J Als-Nielsen, D.R Colman, and W.A. Hendrickson 1995. Structural basis of cell-cell adhesion by cadherins. Nature 374: 327-386.
46. Shibamoto, S., M Hayakawa, K. Takeuchi, T. Hori, N. Oku, K. Mayazawa, N. Kitamura, M. Takeichi, and F. Ito. 1994. Tyrosine phosphorylation of β-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhesion Commun. 1: 295-305
47. Su, L.-K., B. Kinzler, B. Vogelstein, A.C Preisinger, A.R. Moser, C. Luongo, K.A. Gould, and W.F. Dove. 1992. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256: 668-670.
48. Su, L.-K., B. Vogelstein, and K.W. Kinzler. 1993. Association of the APC tumor suppressor protein with catenins. Science 262: 1734-1737.
49. Trahair, J., M. Neutra, and J.I. Gordon. 1989. Use of transgenic mice to study the routing of secretory proteins in intestinal epithelial cells: Analysis of human growth hormone compartmentation as a function of cell type and differentiation. J Cell Biol 19: 3231-3242.
50. Vestweber, D. and R. Kemler. 1985. Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 4: 3393-3398.
51. Wright, N.A. and M. Irwin. 1982. The kinetics of villus cell populations in the mouse small intestine: Normal villi - the steady state requirement. Cell Tiss. Kinet. 15: 595-609.