Down-Regulation of MEK/ERK Signaling by E-Cadherin-Dependent PI3K/Akt Pathway in Differentiating Intestinal Epithelial Cells

Journal of Cellular Physiology

Volumn 199, Issue 1, 2004, Pages 32-39

  Laprise, Patrick ^a   Langlois, Marie Josée ^a   Boucher, Marie Josée ^a   Jobin, Christian ^b   Rivard, Nathalie ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CALCIUM; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; PROTEIN P21; UVOMORULIN;

ADENOVIRUS; ARTICLE; CELL CONTACT; CELL CYCLE; CELL DIFFERENTIATION; CELL JUNCTION; CELL STRAIN CACO 2; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TIGHT JUNCTION;

CACO-2 CELLS; CADHERINS; CALCIUM; CELL COMMUNICATION; CELL DIFFERENTIATION; CHELATING AGENTS; DOWN-REGULATION; EGTAZIC ACID; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; IMMUNOBLOTTING; INTESTINAL MUCOSA; MAP KINASE KINASE KINASE 1; MAP KINASE KINASE KINASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 1042291164     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.10432     Document Type: Article

References (48)

1. Aliaga JC, Deschênes C, Beaulieu JF, Calvo EL, Rivard N. 1999. Requirement of the MAP kinase cascade for cell cycle progression and differentiation of human intestinal cells. Am J Physiol 277: G631-G641.
2. Birchmeier W, Behrens J. 1994. Cadherin expression in carcinomas: Role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta 1198:11-26.
3. Chang L, Karin M. 2001. Mammalian MAP kinase signaling cascades. Nature 410:37-40.
4. Chiu T, Wu SS, Santiskulvong C, Tangkijvanich P, Yee HF Jr, Rozengurt E. 2002. Vasopressin-mediated mitogenic signaling in intestinal epithelial cells. Am J Physiol Cell Physiol 282:C434-C450.
5. Christofori G, Semb H. 1999. The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci 24:73-76.
6. Deschenes C, Vezina A, Beaulieu JF, Rivard N. 2001. Role of p27(Kip1) in human intestinal cell differentiation. Gastroenterology 120:423-438.
7. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Lochner D, Birchmeier W. 1991. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113:173-185.
8. Gumbiner BM. 1996. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 84:345-357.
9. Haller D, Russo MP, Sartor RB, Jobin C. 2002. IKKβ and phophatidylinositol 3-kinase/Akt participate in non-pathogenic gram-negative enteric bacteria-induced RelA phosphorylation and NFκB activation in both primary and intestinal epithelial cell lines. J Biol Chem 277:38168-38178.
10. Hermiston ML, Gordon JI. 1995a. In vivo analysis of cadherin function in the mouse intestinal epithelium: Essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J Cell Biol 129:489-506.
11. Hermiston ML, Gordon JI. 1995b. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270:1203-1207.
12. Hermiston ML, Wong MH, Gordon JI. 1996. 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 Dev 10:985-996.
13. Herrmann C, Martin GA, Wittinghofer A. 1995. Quantitative analysis of the complex between p21ras and the Ras-binding domain of the human Raf-1 protein kinase. J Biol Chem 270:2901-2905.
14. Houde M, Laprise P, Jean D, Blais M, Asselin C, Rivard N. 2001. Intestinal epithelial cell differentiation involves activation of p38 mitogen-activated protein kinase that regulates the homeobox transcription factor CDX2. J Biol Chem 276:21885-21894.
15. Ilyas M, Tomlinson IP, Handy A, Talbot IC, Bodmer WF. 1997. Allele loss, replication errors, and loss of expression of E-cadherin in colorectal cancers. Gut 40:654-659.
16. Jasleen J, Shimoda N, Shen ER, Tavakkolizadeh A, Whang EE, Jacobs DO, Zinner MJ, Ashley SW. 2000. Signaling mechanisms of glucagon-like peptide 2-induced intestinal epithelial cell proliferation. J Surg Res 90:13-18.
17. Jou TS, Stewart DB, Stappert J, Nelson WJ, Marrs JA. 1995. Genetic and biochemical dissection of protein linkages in the cadherin-catenin complex. Proc Natl Acad Sci USA 92:5067-5071.
18. Karam SM. 1999. Lineage commitment and maturation of epithelial cells in the gut. Front Biosci 4:D286-D298.
19. Kermorgant S, Aparicio T, Dessirier V, Lewin MJ, Lehy T. 2001. Hepatocyte growth factor induces colonic cancer cell invasiveness via enhanced motility and protease overproduction. Evidence for PI3 kinase and PKC involvement. Carcinogenesis 22:1035-1042.
20. Kinch MS, Petch L, Zhong C, Burridge K. 1997. E-cadherin engagement stimulates tyrosine phosphorylation. Cell Adhes Commun 4:425-437.
21. Kolligs FT, Bommer G, Goke B. 2002. Wnt/beta-catenin/tcf signaling: A critical pathway in gastrointestinal tumorigenesis. Digestion 66:131-144.
22. Kotani K, Ogawa W, Hino Y, Kitamura T, Ueno H, Sano W, Sutherland C, Granner DK, Kasuga M. 1999. Dominant negative forms of Akt (protein kinase B) and atypical protein kinase Clambda do not prevent insulin inhibition of phosphoenolpyruvate carboxy-kinase gene transcription. J Biol Chem 74:21305-21312.
23. Laprise P, Chailler P, Houde M, Beaulieu JF, Boucher MJ, Rivard N. 2002. Phosphatidylinositol 3-kinase controls human intestinal epithelial cell differentiation by promoting adherens junction assembly and p38 MAPK activation. J Biol Chem 277:8226-8234.
24. Levy P, Robin H, Kornprobst M, Capeau J, Cherqui G. 1998. Enterocytic differentiation of the human Caco-2 cell line correlates with alterations in integrin signaling. J Cell Physiol 177:618-627.
25. Li W, Duzgun A, Sumpio BE, Basson MD. 2001. Integrin and FAK-mediated MAPK activation is required for cyclic strain mitogenic effects in Caco-2 cells. Am J Physiol Gastrointest Liver Physiol 280: G75-G87.
26. Licato LL, Keku TO, Wurzelmann JI, Murray SC, Woosley JT, Sandler RS, Brenner DA. 1997. In vivo activation of mitogen-activated protein kinase signaling pathway in rat intestinal neoplasia. Gastroenterology 113:1589-1598.
27. Luongo D, Mazzarella G, Della RF, Maurano F, Rossi M. 2002. Down-regulation of ERK1 and ERK2 activity during differentiation of the intestinal cell line HT-29. Mol Cell Biochem 231:43-50.
28. Mariadason JM, Bordonaro M, Aslam F, Shi L, Kuraguchi M, Velcich A, Augenlicht LH. 2001. Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res 61:3465-3471.
29. Parsons JT, Martin KH, Slack JK, Taylor JM, Weed SA. 2000. Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene 19:5606-5613.
30. Pece S, Chiariello M, Murga C, Gutkind JS. 1999. Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J Biol Chem 274:19347-19351.
31. Peterson GL. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346-356.
32. Prober DA, Edgar BA. 2001. Growth regulation by oncogenes-new insights from model organisms. Curr Opin Genet Dev 11(1):19-26.
33. Reusch HP, Zimmermann S, Schaefer M, Paul M, Moelling K. 2001. Regulation of Raf by Akt controls growth and differentiation in vascular smooth muscle cells. J Biol Chem 276:33630-33637.
34. Rivard N, Boucher MJ, Asselin C, L'Allemain G. 1999. MAP kinase cascade is required for p27 downregulation and S phase entry in fibroblasts and epithelial cells. Am J Physiol 277:C652-C664.
35. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, Glass DJ. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286:1738-1741.
36. Sebolt-Leopold JS, Dudley DT, Herrera R, Van Becelaere K, Wiland A, Gowan RC, Tecle H, Barrett ST, Bridges A, Przybranowski S, Leopold WR, Saltiel AR. 1999. Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat Med 5:810-816.
37. Simcha I, Kirkpatrick C, Sadot E, Shtutman M, Polevoy G, Geiger B, Peifer M, Ben-Ze'ev A. 2001. Cadherin sequences that inhibit beta-catenin signaling: A study in yeast and mammalian cells. Mol Biol Cell 12:1177-1188.
38. Stockinger A, Eger A, Wolf J, Beug H, Foisner R. 2001. E-cadherin regulates cell growth by modulating proliferation-dependent b-catenin transcriptional activity. J Cell Biol 154:1185-1196.
39. Takeichi M. 1993. Cadherins in cancer: Implications for invasion and metastasis. Curr Opin Cell Biol 5:806-811.
40. Vachon PH, Beaulieu JF. 1992. Transient mosaic patterns of morphological and functional differentiation in the Caco-2 cell line. Gastroenterology 103:414-423.
41. van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88(6):789-799.
42. Vleminckx K, Kemler R. 1999. Cadherins and tissue formation: Integrating adhesion and signaling. Bioessays 21:211-220.
43. Vojtek AB, Cooper JA. 1995. Rho family members: Activators of MAP kinase cascades. Cell 82:527-529.
44. 2+ ions. J Cell Biol 102:1832-1842.
45. Warne PH, Viciana PR, Downward J. 1993. Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro. Nature 364:1031-1034.
46. Watabe M, Nagafuchi A, Tsukita S, Takeichi M. 1994. Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line. J Cell Biol 127:247-256.
47. Yancopoulos GD, Glass DJ. 1999. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286:1738-1741.
48. Zimmermann S, Moelling K. 1999. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286:1741-1744.