PTP-PEST controls motility, adherens junction assembly, and Rho GTPase activity in colon cancer cells

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 2, 2010, Pages

  Espejo, Rosario ^a   Rengifo Cam, William ^a   Schaller, Michael D ^c   Evers, B Mark ^d   Sastry, Sarita K ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c WEST VIRGINIA UNIVERSITY   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Colon carcinoma; E cadherin; Motility; Phosphatase

Indexed keywords

PROTEIN TYROSINE PHOSPHATASE; RAC1 PROTEIN; RECOMBINANT ENZYME; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UVOMORULIN; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 12;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL JUNCTION; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; COLON CANCER; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REPRESSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; CELL CULTURE; CELL MOTION; CELL STRAIN HCT116; COLON TUMOR; COMPARATIVE STUDY; DRUG ANTAGONISM; ENZYME ACTIVATION; ENZYMOLOGY; HUMAN; METABOLISM; MIGRATION INHIBITION; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ADHERENS JUNCTIONS; ANIMALS; CELL LINE, TUMOR; CELL MIGRATION INHIBITION; CELL MOVEMENT; CELLS, CULTURED; COLONIC NEOPLASMS; ENZYME ACTIVATION; HCT116 CELLS; HUMANS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 12; RATS; RHO GTP-BINDING PROTEINS;

EID: 77955861826     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00148.2010     Document Type: Article

References (50)

1. Akhtar N, Hotchin NA. RAC1 regulates adherens junctions through endocytosis of E-cadherin. Mol Biol Cell 12: 847-862, 2001.
2. Angers-Lousteau A, Cote J, Charest A, Dowbenko D, Spencer S, Lasky L, Tremblay M. Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J Cell Biol 144: 1019-1031, 1999.
3. Avizienyte E, Wyke AW, Jones RL, McLean GW, Westhoff MA, Brunton VG, Frame MC. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signaling. Nat Cell Biol 4: 632-638, 2002.
4. Blume-Jensen P, Hunter T. Oncogenic kinase signaling. Nature 411: 355-365, 2001.
5. Bradley WD, Koleske AJ. Regulation of cell migration and morphogenesis by abl-family kinases: emerging mechanisms and physiological contexts. J Cell Sci 122: 3441-3454, 2009.
6. Braga V, Yap AS. The challenges of abundance: epithelial junctions and small GTPase signaling. Curr Opin Cell Biol 17: 466-474, 2005.
7. Brunton V, Ozanne B, Paraskeva C, Frame M. A role for epidermal growth factor receptor, c-src and focal adhesion kinase in an in vitro model for the progression of colon cancer. Oncogene 14: 283-293, 1997.
8. Charest A, Wagner J, Kwan M, Tremblay ML. Coupling of the murine protein tyrosine phosphatase PEST to the epidermal growth factor (EGF) receptor through a Src homology 3 (SH3) domain-mediated association with Grb2. Oncogene 14: 1643-1651, 1997.
9. Chellaiah MA, Schaller MD. Activation of src kinase by protein-tyrosine phosphatase-PEST in osteoclasts: comparative analysis of the effects of bisphosphonate and protein-tyrosine phosphatase inhibitor on src activation in vitro. J Cell Physiol 220: 382-393, 2009.
10. Cong F, Spencer S, Cote JF, Wu Y, Tremblay ML, Lasky LA, Goff SP. Cytoskeletal protein PSTPIP1 directs the PEST-type protein tyrosine phosphatase to the c-Abl kinase to mediate Abl dephosphorylation. Molecular Cell 6: 1413-1423, 2000.
11. Cousin H, Alfandari D. A PTP-PEST-like protein affects α5β1-integrindependent matrix assembly, cell adhesion, and migration in Xenopus gastrula. Dev Biol 265: 416-432, 2004.
12. DeSeau V, Rosen N, Bolen J. Analysis of pp60-Src tyrosine kinase activity and phosphotyrosyl phosphatase activity in human colon carcinoma and normal human colon mucosal cells. J Cell Biochem 35: 113-128, 1987.
13. Garton A, Tonks N. Regulation of fibroblast motility by the protein tyrosine phosphatase PTP-PEST. J Biol Chem 274: 3811-3818, 1999.
14. Glaven J, Whitehead I, Bagrodia S, Kay R, Cerione R. The Dbl-related protein, Lfc, localizes to microtubules and mediates the activation of Rac signaling pathways in cells. J Biol Chem 274: 2279-2285, 1999.
15. Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6: 622-634, 2005.
16. Halle M, Liu YC, Hardy S, Theberge JF, Blanchetot C, Bourdeau A, Meng TC, Tremblay ML. Caspase-3 regulates catalytic activity and scaffolding functions of the protein tyrosine phosphatase PEST, a novel modulator of the apoptotic response. Mol Cell Biol 27: 1172-1190, 2007.
17. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 100: 57-70, 2000.
18. Irby R, Yeatman T. Role of Src expression and activation in human cancer. Oncogene 19: 5636-5642, 2000.
19. Kinch MS, Clark GJ, Der CJ, Burridge K. Tyrosine phosphorylation regulates the adhesions of ras-transformed breast epithelia. J Cell Biol 130: 461-471, 1995.
20. Laemmli U. Cleavage of the structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680-685, 1970.
21. Lozano E, Frasa M, Smolarczyk K, Knaus UG, Braga VM. PAK is required for the disruption of E-cadherin adhesion by the small GTPase Rac. J Cell Sci 121: 933-938, 2008.
22. Lyons P, Dunty J, Schaefer E, Schaller M. Inhibition of the catalytic activity of cell adhesion kinase beta by protein tyrosine phosphatase-PEST- mediated dephosporylation. J Biol Chem 276: 24422-24431, 2001.
23. Mariner DJ, Anastasiadis P, Keilhack H, Bohmer F, Wang J, Reynolds AB. Identification of src phosphorylation sites in the catenin p120catenin. J Biol Chem 276: 28006-28013, 2001.
24. Mathew S, George SP, Wang Y, Siddiqui MR, Srinivasan K, Tan L, Khurana S. Potential molecular mechanism for c-Src kinase-mediated regulation of intestinal cell migration. J Biol Chem 283: 22709-22722, 2008.
25. Morikawa K, Walker S, Jessup J, Fidler I. In vivo selection of highly metastatic cells from surgical specimens of different primary human colon carcinomas implanted into nude mice. Cancer Res 48: 1943-1948, 1988.
26. Morikawa K, Walker S, Nakajima M, Pathak S, Jessup M, Fidler I. Influence of organ environment on the growth, selection, and metastasis of human colon carcinoma cells in nude mice. Cancer Res 48: 6863-6871, 1988.
27. Nakagawa M, Fukata M, Yamaga M, Itoh N, Kaibuchi K. Recruitment and activation of Rac1 by the formation of E-cadherin-mediated cell-cell adhesion sites. J Cell Sci 114: 1829-1838, 2001.
28. Noren NK, Niessen CM, Gumbiner BM, Burridge K. Cadherin engagement regulates Rho family GTPases. J Biol Chem 276: 33305-33308, 2001.
29. Peinado H, Olmeda D, Cano A. Snail, zeb, and bHLH factors in tumor progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7: 415-428, 2007.
30. Playford MP, Lyons PD, Sastry SK, Schaller MD. Identification of a filamin docking site on PTP-PEST. J Biol Chem 281: 34104-34112, 2006.
31. Playford MP, Vadali K, Cai X, Burridge K, Schaller MD. Focal adhesion kinase regulates cell-cell contact formation in epithelial cells via modulation of Rho. Exp Cell Res 314: 3187-3197, 2008.
32. Pouliot N, Nice E, Burgess A. Laminin-10 mediates basal and EGF-stimulated motility of human colon carcinoma cells via α3β1 and α6β4 integrins. Exp Cell Res 266: 1-10, 2001.
33. Reinhold WC, Reimers MA, Lorenzi P, Ho J, Shankavaram UT, Ziegler MS, Bussey KJ, Nishizuka S, Ikediobi O, Pommier YG, Weinstein JN. Multifactorial regulation of E-cadherin expression: an integrative study. Mol Cancer Ther 9: 1-16, 2010.
34. Ren X, Kiosses W, Schwartz M. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J 18: 578-585, 1999.
35. Rengifo-Cam W, Konishi A, Morishita N, Matsuoka H, Yamori T, Nada S, Okada M. Csk defines the ability of integrin-mediated cell adhesion and migration in human colon cancer cells: implication for a potential role in cancer metastasis. Oncogene 23: 289-297, 2004.
36. Sahai E, Marshall CJ. Rho-GTPases and cancer. Nat Rev Cancer 2: 133-142, 2002.
37. Sastry S, Lyons P, Schaller M, Burridge K. PTP-PEST controls motility through regulation of Rac1. J Cell Sci 115: 4305-4316, 2002.
38. Sastry SK, Rajfur Z, Liu BP, Cote JF, Tremblay M, Burridge K. PTP-PEST couples membrane protrusion and tail retraction via VAV2 and p190RhoGAP. J Biol Chem 281: 11627-11636, 2006.
39. Sirois J, Cote JF, Charest A, Uetani N, Bourdeau A, Duncan SA, Daniels E, Tremblay ML. Essential function of PTP-PEST during mouse embryonic vascularization, mesenchyme formation, neurogenesis and early liver development. Mech Dev 123: 869-880, 2006.
40. Streit S, Ruhe JE, Knyazev P, Knyazeva T, Iacobelli S, Peter S, Hoefler H, Ullrich A. PTP-PEST phosphatase variations in human cancer. Cancer Genet Cytogenet 170: 48-53, 2006.
41. Taieb D, Roignot J, André F, Garcia S, Masson B, Pierres A, Iovanna JL, Soubeyran P. ArgBP2-dependent signaling regulates pancreatic cell migration, adhesion, and tumorigenicity. Cancer Res 68: 4588-4596, 2008.
42. Takekawa M, Itoh F, Hinoda Y, Adachi M, Ariyama T, Inazawa J, Imai K, Yachi A. Chromosomal localization of the protein tyrosine phosphatase G1 gene and characterization of the aberrant transcripts in human colon cancer cells. FEBS Lett 339: 222-228, 1994.
43. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454, 2002.
44. Tomar A, Schlaepfer DD. Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility. Curr Opin Cell Biol 21: 676-683, 2009.
45. Towbin H, Staehlin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354, 1979.
46. Warner SJ, Longmore GD. Distinct functions for Rho1 in maintaining adherens junctions and apical tension in remodeling epithelia. J Cell Biol 185: 1111-1125, 2009.
47. Yamada S, Nelson WJ. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 178: 517-527, 2007.
48. Yap AS, Kovacs EM. Direct cadherin-activated cell signaling: a view from the plasma membrane. J Cell Biol 160: 11-16, 2003.
49. Zandy NL, Playford M, Pendergast AM. Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc Natl Acad Sci 104: 17686-17691, 2007.
50. Zheng Y, Xia Y, Hawke D, Halle M, Tremblay ML, Gao X, Zhou XZ, Aldape K, Cobb MH, Xie K, He J, Lu Z. FAK phosphorylation by erk primes ras-induced tyrosine dephosphorylation of FAK mediated by PIN1 and PTP-PEST. Mol Cell 35: 11-25, 2009.