Ras-induced and extracellular signal-regulated kinase 1 and 2 phosphorylation-dependent isomerization of protein tyrosine phosphatase (PTP)-PEST by PIN1 promotes FAK dephosphorylation by PTP-PEST

Molecular and Cellular Biology

Volumn 31, Issue 21, 2011, Pages 4258-4269

  Zheng, Yanhua ^a   Yang, Weiwei ^a   Xia, Yan ^a   Hawke, David ^a   Liu, David X ^b   Lu, Zhimin ^a,c  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 12; PEPTIDYLPROLYL ISOMERASE PIN1; RAS PROTEIN;

ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ISOMERIZATION; METASTASIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL LINE, TRANSFORMED; CELL MOVEMENT; DISEASE PROGRESSION; FOCAL ADHESION KINASE 1; FOCAL ADHESIONS; GENES, RAS; HUMANS; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASMS; PEPTIDYLPROLYL ISOMERASE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 12; RAS PROTEINS;

EID: 83255187929     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05547-11     Document Type: Article

References (46)

1. Angers-Loustau, A., et al. 1999. Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J. Cell Biol. 144:1019-1031.
2. Antonyak, M. A., and R. A. Cerione. 2009. Ras and the FAK paradox. Mol. Cell 35:141-142.
3. Ayaki, M., et al. 2001. Reduced expression of focal adhesion kinase in liver metastases compared with matched primary human colorectal adenocarcinomas. Clin. Cancer Res. 7:3106-3112.
4. Bose, R., et al. 2006. Phosphoproteomic analysis of Her2/neu signaling and inhibition. Proc. Natl. Acad. Sci. U. S. A. 103:9773-9778.
5. Caceres, M., J. Guerrero, and J. Martinez. 2005. Overexpression of RhoAGTP induces activation of the epidermal growth factor receptor, dephosphorylation of focal adhesion kinase and increased motility in breast cancer cells. Exp. Cell Res. 309:229-238.
6. Campbell, P. M., and C. J. Der. 2004. Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin. Cancer Biol. 14:105-114.
7. Chambers, A. F., A. C. Groom, and I. C. MacDonald. 2002. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2:563-572.
8. Chin, L., et al. 1999. Essential role for oncogenic Ras in tumour maintenance. Nature 400:468-472.
9. Cui, Y., Y. C. Liao, and S. H. Lo. 2004. Epidermal growth factor modulates tyrosine phosphorylation of a novel tensin family member, tensin3. Mol. Cancer Res. 2:225-232.
10. Davidson, D., and A. Veillette. 2001. PTP-PEST, a scaffold protein tyrosine phosphatase, negatively regulates lymphocyte activation by targeting a unique set of substrates. EMBO J. 20:3414-3426.
11. Fang, D., et al. 2007. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J. Biol. Chem. 282:11221-11229.
12. Gabriel, B., et al. 2006. Weak expression of focal adhesion kinase (pp125FAK) in patients with cervical cancer is associated with poor disease outcome. Clin. Cancer Res. 12:2476-2483.
13. Garton, A. J., and N. K. Tonks. 1994. Ptp-Pest-a protein-tyrosine-phosphatase regulated by serine phosphorylation. EMBO J. 13:3763-3771.
14. Garton, A. J., and N. K. Tonks. 1999. Regulation of fibroblast motility by the protein tyrosine phosphatase PTP-PEST. J. Biol. Chem. 274:3811-3818.
15. Guo, H. B., M. Randolph, and M. Pierce. 2007. Inhibition of a specific N-glycosylation activity results in attenuation of breast carcinoma cell invasiveness- related phenotypes: inhibition of epidermal growth factor-induced dephosphorylation of focal adhesion kinase. J. Biol. Chem. 282:22150-22162.
16. Guvakova, M. A., and E. Surmacz. 1999. The activated insulin-like growth factor I receptor induces depolarization in breast epithelial cells characterized by actin filament disassembly and tyrosine dephosphorylation of FAK, Cas, and paxillin. Exp. Cell Res. 251:244-255.
17. Hanks, S. K., L. Ryzhova, N. Y. Shin, and J. Brabek. 2003. Focal adhesion kinase signaling activities and their implications in the control of cell survival and motility. Front. Biosci. 8:d982-d996.
18. Hunter, T. 1998. Prolyl isomerases and nuclear function. Cell 92:141-143.
19. Julien, S. G., N. Dube, S. Hardy, and M. L. Tremblay. 2011. Inside the human cancer tyrosine phosphatome. Nat. Rev. Cancer 11:35-49.
20. Lu, K. P., and X. Z. Zhou. 2007. The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat. Rev. Mol. Cell. Biol. 8:904-916.
21. Lu, Z., G. Jiang, P. Blume-Jensen, and T. Hunter. 2001. Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase. Mol. Cell. Biol. 21:4016-4031.
22. Lu, Z., et al. 1998. Activation of protein kinase C triggers its ubiquitination and degradation. Mol. Cell. Biol. 18:839-845.
23. Lu, Z., S. Xu, C. Joazeiro, M. H. Cobb, and T. Hunter. 2002. The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol. Cell 9:945-956.
24. Lynch, L., P. I. Vodyanik, D. Boettiger, and M. A. Guvakova. 2005. Insulinlike growth factor I controls adhesion strength mediated by alpha5beta1 integrins in motile carcinoma cells. Mol. Biol. Cell 16:51-63.
25. Manes, S., et al. 1999. Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol. Cell. Biol. 19:3125-3135.
26. McLean, G. W., et al. 2005. The role of focal-adhesion kinase in cancer. A new therapeutic opportunity. Nat. Rev. Cancer 5:505-515.
27. Mitra, S. K., D. A. Hanson, and D. D. Schlaepfer. 2005. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6:56-68.
28. Ohta, R., et al. 2006. Reduced expression of focal adhesion kinase in intrahepatic cholangiocarcinoma is associated with poor tumor differentiation. Oncology 71:417-422.
29. Parsons, J. T. 2003. Focal adhesion kinase: the first ten years. J. Cell Sci. 116:1409-1416.
30. Ridley, A. J., et al. 2003. Cell migration: integrating signals from front to back. Science 302:1704-1709.
31. Schaller, M. D. 2004. FAK and paxillin: regulators of N-cadherin adhesion and inhibitors of cell migration? J. Cell Biol. 166:157-159.
32. Schubbert, S., K. Shannon, and G. Bollag. 2007. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 7:295-308.
33. Sood, A. K., et al. 2004. Biological significance of focal adhesion kinase in ovarian cancer: role in migration and invasion. Am. J. Pathol. 165:1087-1095.
34. Streit, S., et al. 2006. PTP-PEST phosphatase variations in human cancer. Cancer Genet. Cytogenet. 170:48-53.
35. Takekawa, M., et al. 1992. Cloning and characterization of a human cDNA encoding a novel putative cytoplasmic protein-tyrosine-phosphatase. Biochem. Biophys. Res. Commun. 189:1223-1230.
36. Thelemann, A., et al. 2005. Phosphotyrosine signaling networks in epidermal growth factor receptor overexpressing squamous carcinoma cells. Mol. Cell Proteomics 4:356-376.
37. Tonks, N. K. 2006. Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7:833-846.
38. Vadlamudi, R. K., L. Adam, D. Nguyen, M. Santos, and R. Kumar. 2002. Differential regulation of components of the focal adhesion complex by heregulin: role of phosphatase SHP-2. J. Cell Physiol. 190:189-199.
39. Wang, F. M., et al. 2005. SHP-2 promoting migration and metastasis of MCF-7 with loss of E-cadherin, dephosphorylation of FAK and secretion of MMP-9 induced by IL-1 beta in vivo and in vitro. Breast Cancer Res. Treat. 89:5-14.
40. Yamanaka, I., et al. 2003. Epidermal growth factor increased the expression of alpha 2 beta 1-integrin and modulated integrin-mediated signaling in human cervical adenocarcinoma cells. Exp. Cell Res. 286:165-174.
41. Yang, Q., D. Co, J. Sommercorn, and N. K. Tonks. 1993. Cloning and expression of Ptp-Pest-a novel, human, nontransmembrane protein tyrosine phosphatase. J. Biol. Chem. 268:6622-6628.
42. Yi, T. L., J. L. Cleveland, and J. N. Ihle. 1991. Identification of novel protein tyrosine phosphatases of hematopoietic-cells by polymerase chain-reaction amplification. Blood 78:2222-2228.
43. Yu, D. H., C. K. Qu, O. Henegariu, X. Lu, and G. S. Feng. 1998. Proteintyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J. Biol. Chem. 273:21125-21131.
44. Zheng, Y., and Z. Lu. 2009. Paradoxical roles of FAK in tumor cell migration and metastasis. Cell Cycle 8:3474-3479.
45. Zheng, Y. H., et al. 2009. FAK phosphorylation by ERK primes Ras-induced tyrosine dephosphorylation of FAK mediated by PIN1 and PTP-PEST. Mol. Cell 35:11-25.
46. Zhou, X. Z., P. J. Lu, G. Wulf, and K. P. Lu. 1999. Phosphorylation-dependent prolyl isomerization: a novel signaling regulatory mechanism. Cell. Mol. Life Sci. 56:788-806.