Protein tyrosine phosphatase α Phosphotyrosyl-789 binds BCAR3 to position cas for activation at integrin-mediated focal adhesions

Molecular and Cellular Biology

Volumn 32, Issue 18, 2012, Pages 3776-3789

  Sun, Guobin ^a,b   Cheng, Suzanne Y S ^a,b   Chen, Min ^a,b,c   Lim, Chinten James ^a,b   Pallen, Catherine J ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR APOPTOSIS SUSCEPTIBILITY PROTEIN; INTEGRIN; PROTEIN; PROTEIN BCAR3; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE ALPHA; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENZYME BINDING; ENZYME PHOSPHORYLATION; FOCAL ADHESION; MOUSE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CELL MOVEMENT; CRK-ASSOCIATED SUBSTRATE PROTEIN; CYTOSKELETON; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INTEGRINS; MICE; PHOSPHORYLATION; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 4; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84866405687     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00214-12     Document Type: Article

References (50)

1. Ballestrem C, et al. 2006. Molecular mapping of tyrosine-phosphorylated proteins in focal adhesions using fluorescence resonance energy transfer. J. Cell Sci. 119:866-875.
2. Bhandari V, Lim KL, Pallen CJ. 1998. Physical and functional interactions between receptor-like protein-tyrosine phosphatase alpha and p59fyn. J. Biol. Chem. 273:8691-8698.
3. Bouton AH, Riggins RB, Bruce-Staskal PJ. 2001. Functions of the adapter protein Cas: signal convergence and the determination of cellular responses. Oncogene 20:6448-6458.
4. Cabodi S, del Pilar Camacho-Leal M, Di Stefano P, Defilippi P. 2010. Integrin signalling adaptors: not only figurants in the cancer story. Nat. Rev. Cancer 10:858-870.
5. Cai D, Clayton LK, Smolyar A, Lerner A. 1999. AND-34, a novel p130Cas-binding thymic stromal cell protein regulated by adhesion and inflammatory cytokines. J. Immunol. 163:2104-2112.
6. Cai D, et al. 2003. AND-34/BCAR3, a GDP exchange factor whose overexpression confers antiestrogen resistance, activates Rac, PAK1, and the cyclin D1 promoter. Cancer Res. 63:6802-6808.
7. Cary LA, Han DC, Polte TR, Hanks SK, Guan JL. 1998. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J. Cell Biol. 140:211-221.
8. Chen M, Chen SC, Pallen CJ. 2006. Integrin-induced tyrosine phosphorylation of protein-tyrosine phosphatase-alpha is required for cytoskeletal reorganization and cell migration. J. Biol. Chem. 281:11972-11980.
9. Defilippi P, Di Stefano P, Cabodi S. 2006. p130Cas: a versatile scaffold in signaling networks. Trends Cell Biol. 16:257-263.
10. del Pozo MA, Price LS, Alderson NB, Ren XD, Schwartz MA. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008-2014.
11. den Hertog J, Tracy S, Hunter T. 1994. Phosphorylation of receptor protein-tyrosine phosphatase alpha on Tyr789, a binding site for the SH3-SH2-SH3 adaptor protein GRB-2 in vivo. EMBO J. 13:3020-3032.
12. Dodelet VC, Pazzagli C, Zisch AH, Hauser CA, Pasquale EB. 1999. A novel signaling intermediate, SHEP1, directly couples Eph receptors to R-Ras and Rap1A. J. Biol. Chem. 274:31941-31946.
13. Donato DM, Ryzhova LM, Meenderink LM, Kaverina I, Hanks SK. 2010. Dynamics and mechanism of p130Cas localization to focal adhesions. J. Biol. Chem. 285:20769-20779.
14. Felekkis KN, et al. 2005. AND-34 activates phosphatidylinositol 3-kinase and induces anti-estrogen resistance in a SH2 and GDP exchange factorlike domain-dependent manner. Mol. Cancer Res. 3:32-41.
15. Fonseca PM, et al. 2004. Regulation and localization of CAS substrate domain tyrosine phosphorylation. Cell Signal. 16:621-629.
16. Geiger B, Yamada KM. 2011. Molecular architecture and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 3:a005033.
17. Gotoh T, Cai D, Tian X, Feig LA, Lerner A. 2000. p130Cas regulates the activity of AND-34, a novel Ral, Rap1, and R-Ras guanine nucleotide exchange factor. J. Biol. Chem. 275:30118-30123.
18. Harte MT, Macklem M, Weidow CL, Parsons JT, Bouton AH. 2000. Identification of two focal adhesion targeting sequences in the adapter molecule p130(Cas). Biochim. Biophys. Acta 1499:34-48.
19. Herrera Abreu MT, et al. 2008. Tyrosine phosphatase PTPalpha regulates focal adhesion remodeling through Rac1 activation. Am. J. Physiol. Cell Physiol. 294:C931-C944.
20. Kaplan KB, et al. 1994. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13:4745-4756.
21. Klemke RL, et al. 1998. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J. Cell Biol. 140:961-972.
22. Kostic A, Sap J, Sheetz MP. 2007. RPTPalpha is required for rigiditydependent inhibition of extension and differentiation of hippocampal neurons. J. Cell Sci. 120:3895-3904.
23. Kostic A, Sheetz MP. 2006. Fibronectin rigidity response through Fyn and p130Cas recruitment to the leading edge. Mol. Biol. Cell 17:2684-2695.
24. Lammers R, Lerch MM, Ullrich A. 2000. The carboxyl-terminal tyrosine residue of protein-tyrosine phosphatase alpha mediates association with focal adhesion plaques. J. Biol. Chem. 275:3391-3396.
25. Liu BA, et al. 2006. The human and mouse complement of SH2 domain proteins- establishing the boundaries of phosphotyrosine signaling. Mol. Cell 22:851-868.
26. Lu Y, Brush J, Stewart TA. 1999. NSP1 defines a novel family of adaptor proteins linking integrin and tyrosine kinase receptors to the c-Jun N-terminal kinase/stress-activated protein kinase signaling pathway. J. Biol. Chem. 274:10047-10052.
27. Mitra SK, Schlaepfer DD. 2006. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18:516-523.
28. Nakamoto T, et al. 1997. Requirements for localization of p130cas to focal adhesions. Mol. Cell. Biol. 17:3884-3897.
29. Parsons JT, Horwitz AR, Schwartz MA. 2010. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11: 633-643.
30. Petch LA, Bockholt SM, Bouton A, Parsons JT, Burridge K. 1995. Adhesion-induced tyrosine phosphorylation of the p130 src substrate. J. Cell Sci. 108(Pt 4):1371-1379.
31. Ponniah S, Wang DZ, Lim KL, Pallen CJ. 1999. Targeted disruption of the tyrosine phosphatase PTPalpha leads to constitutive downregulation of the kinases Src and Fyn. Curr. Biol. 9:535-538.
32. Riggins RB, Quilliam LA, Bouton AH. 2003. Synergistic promotion of c-Src activation and cell migration by Cas and AND-34/BCAR3. J. Biol. Chem. 278:28264-28273.
33. Ruest PJ, Shin NY, Polte TR, Zhang X, Hanks SK. 2001. Mechanisms of CAS substrate domain tyrosine phosphorylation by FAK and Src. Mol. Cell. Biol. 21:7641-7652.
34. Sakai R, et al. 1994. A novel signaling molecule, p130, forms stable complexes in vivo with v-Crk and v-Src in a tyrosine phosphorylationdependent manner. EMBO J. 13:3748-3756.
35. Sakakibara A, Hattori S. 2000. Chat, a Cas/HEF1-associated adaptor protein that integrates multiple signaling pathways. J. Biol. Chem. 275: 6404-6410.
36. Sawada Y, et al. 2006. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127:1015-1026.
37. Schrecengost RS, Riggins RB, Thomas KS, Guerrero MS, Bouton AH. 2007. Breast cancer antiestrogen resistance-3 expression regulates breast cancer cell migration through promotion of p130Cas membrane localization and membrane ruffling. Cancer Res. 67:6174-6182.
38. Schuh NR, Guerrero MS, Schrecengost RS, Bouton AH. 2010. BCAR3 regulates Src/p130 Cas association, Src kinase activity, and breast cancer adhesion signaling. J. Biol. Chem. 285:2309-2317.
39. Su J, Batzer A, Sap J. 1994. Receptor tyrosine phosphatase R-PTP-alpha is tyrosine-phosphorylated and associated with the adaptor protein Grb2. J. Biol. Chem. 269:18731-18734.
40. Su J, Muranjan M, Sap J. 1999. Receptor protein tyrosine phosphatase alpha activates Src-family kinases and controls integrin-mediated responses in fibroblasts. Curr. Biol. 9:505-511.
41. Tonks NK. 2006. Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7:833-846.
42. van Agthoven T, et al. 1998. Identification of BCAR3 by a random search for genes involved in antiestrogen resistance of human breast cancer cells. EMBO J. 17:2799-2808.
43. Vanden Borre P, Near RI, Makkinje A, Mostoslavsky G, Lerner A. 2011. BCAR3/AND-34 can signal independent of complex formation with CAS family members or the presence of p130Cas. Cell Signal 23:1030-1040.
44. von Wichert G, et al. 2003. RPTP-alpha acts as a transducer of mechanical force on alphav/beta3-integrin-cytoskeleton linkages. J. Cell Biol. 161: 143-153.
45. Vuori K, Ruoslahti E. 1995. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 270:22259-22262.
46. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B. 2003. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116:4605-4613.
47. Zaidel-Bar R, Geiger B. 2010. The switchable integrin adhesome. J. Cell Sci. 123:1385-1388.
48. Zeng L, et al. 2003. PTP alpha regulates integrin-stimulated FAK autophosphorylation and cytoskeletal rearrangement in cell spreading and migration. J. Cell Biol. 160:137-146.
49. Zhao X, Guan JL. 2011. Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv. Drug Deliv. Rev. 63:610-615.
50. Zheng XM, Resnick RJ, Shalloway D. 2000. A phosphotyrosine displacement mechanism for activation of Src by PTPalpha.EMBOJ. 19:964-978.