Deficient E-cadherin adhesion in C57BL/6J-Min/+ mice is associated with increased tyrosine kinase activity and RhoA-dependent actomyosin contractility

Experimental Cell Research

Volumn 312, Issue 4, 2006, Pages 387-400

  Carothers, Adelaide M ^a   Javid, Sara H ^a   Moran, Amy E ^a   Hunt, Daniel H ^b   Redston, Mark ^a   Bertagnolli, Monica M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Actomyosin contractility; APC dependent colon cancer; E cadherin mediated cell cell adhesion; MAP kinase; RhoA

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; MYOSIN ADENOSINE TRIPHOSPHATASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; COLORECTAL CARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENETIC TRANSCRIPTION; INTESTINE; LIGAND BINDING; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

ANIMALIA;

EID: 29144502281     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2005.11.019     Document Type: Article

References (75)

1. P. Polakis Wnt signaling and cancer Genes Dev. 14 2000 1837 1851
2. E. Sancho, E. Batlle, and H. Clevers Live and let die in the intestinal epithelium Curr. Opin. Cell Biol. 15 2003 763 770
3. S. Ichii, S. Takeda, A. Horii, S. Nakatsuru, Y. Miyoshi, M. Emi, Y. Fujiwara, K. Koyama, J. Furuyama, J. Utsunomiya, and Y. Nakamura Detailed analysis of genetic alterations in colorectal tumors from patients with and without familial adenomatous polyposis (FAP) Oncogene 8 1993 2399 2405
4. K.M. Haigis, J.G. Caya, M. Reichelderfer, and W.F. Dove Tumor regionality in the mouse intestine reflects the mechanism of loss of Apc function Proc. Natl. Acad. Sci. U. S. A. 99 2002 2931 8927
5. I.S. Näthke The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium Annu. Rev. Cell Dev. Biol. 20 2004 366 377
6. M. Bienz, and F. Hamada Adenomatous polyposis coli proteins and cell adhesion Curr. Opin. Cell Biol. 16 2004 528 535
7. M.C. Faux, J.L. Ross, C. Meeker, T. Johns, J.-i. Hing, R.J. Simpson, M.J. Layton, and A.W. Burgess Restoration of full-length adenomatous polyposis coli (APC) protein in a colon cancer cell line enhances cell adhesion J. Cell Sci. 117 2003 427 439
8. B.M. Gumbiner Regulation of cadherin adhesive activity J. Cell Biol. 148 2000 399 404
9. J. Hulsken, W. Birchmeier, and J. Behrens E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton J. Cell Biol. 127 1994 2061 2069
10. B. Rubinfeld, B. Souza, I. Albert, S. Munemitsu, and P. Polakis The APC protein and E-cadherin form similar but independent complexes with α-catenin, β-catenin, and plakoglobin J. Biol. Chem. 270 1995 5549 5555
11. M.L. Hermiston, M.H. Wong, and J.I. Gordon 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 1996 985 996
12. R. Smits, P. Ruiz, S. Diaz-Cano, A. Luz, S. Jagmohan-Changur, C. Breukel, C. Birchmeier, W. Birchmeier, and R. Fodde Gastroenterology 119 2000 1045 1053
13. L.K. Su, K.W. Kinzler, B. Vogelstein, A.C. Preisinger, A.R. Moser, C. Luongo, K.A. Goukld, and W.F. Dove Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene Science 256 1992 668 670
14. N.N. Mahmoud, S.K. Boolbol, R.T. Bilinski, C. Martucci, A. Chadburn, and M.M. Bertagnolli Apc gene mutation is associated with a dominant-negative effect upon intestinal cell migration Cancer Res. 57 1997 5045 5050
15. N.N. Mahmoud, R.T. Bilinski, M.R. Churchill, W. Edelmann, R. Kucherlapati, and M.M. Bertagnolli Genotype-phenotype correlation in murine Apc mutation: differences in enterocyte migration and response to sulindac Cancer Res. 59 1999 353 359
16. A.M. Carothers, K.A. Melstrom Jr., J.D. Mueller, M.J. Weyant, and M.M. Bertagnolli Progressive changes in adherens junction structure during intestinal adenoma formation in Apc mutant mice J. Biol. Chem. 276 2001 39094 39102
17. A.M. Moran, A.M. Carothers, M.J. Weyant, M. Redston, and M.M. Bertagnolli Carnosol inhibits β-catenin tyrosine phosphorylation and prevents adenoma formation in the C57BL/6J/Min/+ (Min/+) mouse Cancer Res. 65 2005 1097 1104
18. Y. Mosesson, and Y. Yarden Oncogenic growth factor receptors: implications for signal transduction therapy Semin. Cancer Biol. 14 2004 262 270
19. M. Majima, H. Amano, and I. Hayashi Prostanoid receptor signaling relevant to tumor growth and angiogenesis Trends Pharmacol. Sci. 24 2003 524 529
20. K. Takahashi, and K. Suzuki Density-dependent inhibition of growth involves prevention of EGF receptor activation by E-cadherin-mediated cell-cell adhesion Exp. Cell Res. 226 1996 214 222
21. X. Qian, T. Karpova, A.M. Sheppard, J. McNally, and D.R. Lowy E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases EMBO J. 23 2004 17739 17748
22. R.B. Hazan, and L. Norton The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton J. Biol. Chem. 273 1998 9078 9084
23. T. Müller, G. Bain, X. Wang, and J. Papkoff Regulation of epithelial cell migration and tumor formation by β-catenin signaling Exp. Cell Res. 280 2002 119 133
24. Z. Lu, S. Ghosh, Z. Wang, and T. Hunter Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of β-catenin, and enhanced tumor cell invasion Cancer Cell 4 2003 499 515
25. R. Pai, T. Nakamura, W.S. Moon, and A.S. Tarnawski Prostaglandins promote colon cancer cell invasion; signaling by cross-talk between two distinct growth factor receptors FASEB J. 17 2003 1640 1647
26. A.E. Moran, D.H. Hunt, S.H. Javid, M. Redston, A.M. Carothers, and M.M. Bertagnolli Apc deficiency is associated with increased Egfr activity in the intestinal enterocytes and adenomas of C57BL/6J-Min/+ mice J. Biol. Chem. 279 2004 43261 43272
27. R.B. Roberts, L. Min, M.K. Washington, S.J. Olsen, S.H. Settle, R.J. Coffey, and D.W. Threadgill Importance of epidermal growth factor receptor signaling in establishment of adenomas and maintenance of carcinomas during intestinal tumorigenesis Proc. Natl. Acad. Sci. U. S. A. 99 2001 1521 1526
28. 2 transactivates EGF receptor: a novel mechanism for promoting colon cancer growth and gastrointestinal hypertrophy Nat. Med. 8 2002 289 293
29. 2 regulates cell migration via the intracellular activation of the epidermal growth factor receptor J. Biol. Chem. 278 2003 35451
30. X.D. Ren, W.B. Kiosses, and M.A. Schwartz Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton EMBO J. 18 1999 578 585
31. R.F. Jacoby, K. Seiber, C.E. Cole, G. Kelloff, and R.A. Lubet The cyclooxygenase-2 inhibitor celecoxib is a potent preventive and therapeutic agent in the min mouse model of adenomatous polyposis Cancer Res. 60 2000 5040 5044
32. 2 receptor-evolved ERK activation J. Biol. Chem. 279 2004 29797 29804
33. P.L. Rice, M. Washington, S. Schleman, K.S. Beard, L.J. Driggers, and D.J. Ahnen Sulindac sulfide inhibits epidermal growth factor-induced phosphorylation of extracellular-regulated kinase 1/2 and Bad in human colon cancer cells Cancer Res. 63 2003 616 620
34. 2 enhances intestinal adenoma growth via activation of the Ras-mitogen-activated protein kinase cascade Cancer Res. 65 2005 1822 1829
35. T.L. Le, A.S. Yap, and J.L. Stow Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics J. Cell Biol. 146 1999 219 232
36. A.B. Jaffe, A. Hall, RHO GTPases: biochemistry and biology, Annu. Rev. Cell Dev. Biol. (in press).
37. N.K. Noren, C.M. Niessen, B.M. Gumbiner, and K. Burridge Cadherin engagement regulates Rho family GTPases J. Biol. Chem. 276 2001 33305 33308
38. E. Manser, Z.S. Zhao, T. Leung, G.H. Michael, and L. Lim Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) family J. Biol. Chem. 270 1995 25070 25078
39. R.H. Daniels, P.S. Hall, and G.M. Bokoch Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells EMBO J. 17 1998 754 764
40. K. Burridge, and K. Wannerberg Rho and Rac take center stage Cell 116 2004 167 179
41. 13 negatively regulate the adhesive functions of cadherin J. Biol. Chem. 277 2002 24594 24600
42. A. Gohla, R. Harhammer, and G. Schultz The G-protein G13 but not G12 mediates signaling from lysophosphatidic acid receptor via epidermal growth factor receptor to Rho J. Biol. Chem. 273 1998 4653 4659
43. K. Kimura, M. Ito, M. Amano, K. Chihara, Y. Fukata, M. Nakafuku, B. Yamamori, J. Feng, T. Nakano, K. Okawa, A. Iwamatsu, and K. Kaibuchi Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase) Science 273 1996 245 248
44. S. Arber, F.A. Barbayannis, H. Hanser, C. Schneider, C.A. Stanyon, O. Bernard, and P. Caroni Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase Nature 393 1998 805 809
45. I. Dikic, G. Towiwa, S. Lev, S.A. Courtneidge, and J. Schlessinger A role for Pyk2 and Src in linking G-protein-coupled receptors to MAPK activation Nature 383 1996 547 550
46. 2+, PKC, and Rho kinase Am. J. Physiol.: Cell Physiol. 282 2002 C1432 C1444
47. M. Krendel, N.A. Gloushankova, E.M. Bonder, H.H. Feder, J.M. Vasiliew, and I.M. Gelfand Myosin-dependent contractile activity of the actin cytoskeleton modulates the spatial organization of cell-cell contacts in cultured epitheliocytes Proc. Natl. Acad. Sci. U. S. A. 96 1999 9666 9670
48. M.L. Coleman, E.A. Sahai, M. Yeo, M. Bosch, M. Dewar, and M.F. Olson Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I Nat. Cell Biol. 3 2001 339 345
49. J.-M. Lai, C.-L. Hsieh, and Z.-F. Chang Caspase activation during phorbol ester-induced apoptosis requires ROCK-dependent myosin-mediated contraction J. Cell Sci. 116 2003 3491 3501
50. B. Wójciak-Stothard, A. Entwistly, R. Garg, and A.J. Ridley Regulation of TNFα-induced reorganization of the actin cytoskeleton and cell-cell junctions by Rho, Rac, and Cdc42 in human endothelial cells J. Cell. Physiol. 176 1998 150 160
51. A. Malliri, M. Symons, R.F. Hennigan, A.F. Hurlstone, R.F. Lamb, T. Wheeler, and B.W. Ozanne The transcription factor AP-1 is required for EGF-induced activation of Rho-like GTPases, cytoskeletal rearrangements, motility, and in vitro invasion of A431 cells J. Cell Biol. 143 1998 1087 1099
52. M. Caceres, J. Guerrero, and J. Martinez Overexpression of RhoA-GTP induces activation of the epidermal growth factor receptor, dephosphorylation of focal adhesion kinase and increased motility in breast cancer cells Exp. Cell Res. 309 2005 229 238
53. J.P. Segain, D. Raigeard del la Bletiere, V. Sauzeau, A. Bourreille, G. Hilaret, C. Cario-Toumaniantz, P. Pacaud, J.P. Galmiche, and G. Loirand Rho kinase blockade prevents inflammation via NFκB inhibition: evidence in Crohn's disease and experimental colitis Gastroenterology 124 2003 1180 1187
54. T.S. Sappenbeck, and J.I. Gordon Rac1 mutations produce aberrant epithelial differentiation in the developing and adult mouse small intestine Development 127 2000 2629 2642
55. Y. Kawasaki, R. Sato, and T. Akiyama Mutated APC and Asef are involved in the migration of colorectal tumour cells Nat. Cell Biol. 5 2003 190 192
56. M. Innocenti, E. Frittoli, I. Ponzanelli, J.R. Falck, S.M. Brachmann, P.P. DiFiore, and G. Scita Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1 J. Cell Biol. 160 2003 17 23
57. P. Tamas, Z. Solti, P. Bauer, A. Illes, S. Sipeki, A. Bauer, A. Farago, J. Downward, and L. Bunday Mechanism of epidermal growth factor regulation of Vav2, a guanine nucleotide exchange factor for Rac J. Biol. Chem. 278 2003 5163 5171
58. S. Potempa, and A.J. Ridley Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly Mol. Biol. Cell 9 1998 2185 2200
59. E. Avizienyte, A.W. Wyke, R.J. Jones, G.W. McLean, M.A. Westhoff, V.G. Brunton, and M.C. Frame Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signaling Nat. Cell Biol. 4 2002 632 638
60. M.J. Weyant, A.M. Carothers, A.J. Dannenberg, and M.M. Bertagnolli (+)-Catechin inhibits intestinal tumor formation and suppresses focal adhesion kinase activation in the Min/+ mouse Cancer Res. 61 2001 118 125
61. R.L. Klemke, S. Cai, A.L. Giannini, P.J. Gallagher, P. de Lanerolle, and D.A. Cheresh Regulation of cell motility by mitogen-activated protein kinase J. Cell Biol. 137 1997 481 492
62. L. Moro, M. Venturino, C. Bosso, L. Silengo, F. Altruda, L. Beguinot, G. Tarone, and P. Defilippi Integrins induce activation of EGF receptor: role in MAP kinase induction and adhesion-dependent cell survival EMBO J. 17 1998 6622 6632
63. Q. Shi, and D. Boettiger A novel mode for integrin-mediated signaling: tethering is required for phosphorylation of FAK Y397 Mol. Biol. Cell 14 2003 4306 4315
64. Q. Lu, M. Paredes, J. Zhang, and K.S. Kosik Basal extracellular signal-regulated kinase activity modulates cell-cell and cell-matrix interactions Mol. Cell. Biol. 18 1998 3257 3265
65. M.W. Renshaw, D. Toksoz, and M.A. Schwartz Involvement of the small GTPase Rho in integrin-mediated activation of mitogen-activated protein kinase J. Biol. Chem. 271 1996 21691 21694
66. J.M. Vasiliev, T. Omelchenko, I.M. Gelfand, H.H. Feder, and E.M. Bonder Rho overexpression leads to mitosis-associated detachment of cells from epithelial sheets: a link to the mechanism of cancer dissemination Proc. Natl. Acad. Sci. U. S. A. 101 2004 12526 12530
67. K.M. Haigis, J.G. Caya, M. Reichelderfer, and W.F. Dove Intestinal adenomas can develop with a stable karyotype and stable microsatellites Proc. Natl. Acad. Sci. U. S. A. 99 2002 8927 8931
68. T. Kusama, M. Mukai, M. Ayaki, F. Imamura, M. Tasuta, Y. Matsumoto, H. Nakamura, and M. Inoue Inhibition of lysophosphatidic acid-induced RhoA activation and tumor cell invasion by 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors Int. J. Oncol. 23 2003 1173 1178
69. A. Tokumura, Y. Kanaya, M. Kitahara, M. Miyake, Y. Yoshioka, and K. Fukuzawa Increased formation of lysophosphatidic acids by lysophospholipase D in serum of hypercholesterolemic rabbits J. Lipid Res. 43 2002 307 315
70. J.N. Poynter, S.B. Gruber, P.D.R. Higgins, R. Almog, J.D. Bonner, H.S. Rennert, M. Low, J.K. Greenson, and G. Rennert Statins and the risk of colorectal cancer N. Engl. J. Med. 352 2005 2184 2192
71. N.N. Mahmoud, S.K. Boolbol, A.J. Dannenberg, J.R. Mestre, R.T. Bilinshi, C. Martucci, H.L. Newmark, A. Chadburn, and M.M. Bertagnolli The sulfide metabolite of sulindac prevents tumors and restores enterocyte apoptosis in a murine model of familial adenomatous polyposis Carcinogenesis 19 1998 87 91
72. W.J. Thompson, G.A. Piazza, H. Li, L. Liu, J. Fetter, B. Zhu, G. Sperl, D. Ahnen, and R. Pamukcu Exisulind induction of apoptosis involves guanosine 3′,5′-cyclic monophosphate phosphodiesterase inhibition, protein kinase G activation, and attenuated β-catenin Cancer Res. 60 2000 3338 3342
73. 2+ sensitization of contraction in vascular smooth muscle J. Biol. Chem. 275 2000 21722 21729
74. 2+ desensitization in vascular smooth muscle by activating the myosin light chain phosphatase J. Biol. Chem. 272 1997 5063 5068
75. J.S. Sebolt-Leopold, and R. Herrera Targeting the mitogen-activated protein kinase cascade to treat cancer Nat. Rev., Cancer 4 2004 937 947