Role of the cytoskeletal protein paxillin in oncogenesis

Critical Reviews in Oncogenesis

Volumn 11, Issue 1, 2000, Pages 63-76

  Sattler, Martin ^a   Pisick, Evan ^a   Morrison, Paul T ^b   Salgia, Ravi ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

BCR ABL; Cell motility; E6; Focal adhesion; Lung cancer; Paxillin

Indexed keywords

ASPARTIC ACID; BCR ABL PROTEIN; CYTOKINE; CYTOSKELETON PROTEIN; GROWTH FACTOR RECEPTOR; INTEGRIN; LEUCINE; ONCOPROTEIN; PAXILLIN;

AMINO ACID SEQUENCE; BREAST CANCER; CANCER; CARCINOGENESIS; CELL MOTILITY; HUMAN; KAPOSI SARCOMA; LUNG CANCER; MALIGNANT TRANSFORMATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; UTERINE CERVIX CARCINOMA;

EID: 0033999335     PISSN: 08939675     EISSN: None     Source Type: Journal    
DOI: 10.1615/critrevoncog.v11.i1.30     Document Type: Review

References (72)

1. Abedi, H., K. E. Dawes, and I. Zachary: Differential effects of platelet-derived growth factor BB on p125 focal adhesion kinase and paxillin tyrosine phosphorylation and on cell migration in rabbit aortic vascular smooth muscle cells and Swiss 3T3 fibroblasts. J. Biol. Chem., 270:11367-11376 (1995).
2. Alani, R. M. and K. Munger: Human papillomaviruses and associated malignancies. J. Clin. Oncol., 16:330-337 (1998).
3. Bellis, S. L., J. T. Miller, and C. E. Turner: Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J. Biol. Chem., 270:17437-17441 (1995).
4. Bellis, S. L., J. A. Perrotta, M. S. Curtis, and C. E. Turner: Adhesion of fibroblasts to fibronectin stimulates both serine and tyrosine phosphorylation of paxillin. Biochem. J., 325:375-381 (1997).
5. Birge, R. B., J. E. Fajardo, C. Reichman, S. E. Shoelson, Z. Songyang, L. C. Cantley, and H. Hanafusa: Identification and characterization of a high-affinity interaction between v-Crk and tyrosine-phosphorylated paxillin in CT10-transformed fibroblasts. Mol. Cell. Biol., 13:4648-4656 (1993).
6. Brown, M. C., J. A. Perrotta, and C. E. Turner: Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol., 135:1109-1123 (1996).
7. Brown, M. C., J. A. Perrotta, and C. E. Turner: Serine and threonine phosphorylation of the paxillin LIM domains regulates paxillin focal adhesion localization and cell adhesion to fibronectin. Mol. Biol. Cell, 9:1803-1816 (1998).
8. Brown, M. C. and C. E. Turner: Characterization of paxillin LIM domain-associated serine threonine kinases: activation by angiotensin II in vascular smooth muscle cells. J. Cell. Biochem., 76:99-108 (1999).
9. Burridge, K., C. E. Turner, and L. H. Romer: Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol., 119:893-903 (1992).
10. Casamassima, A. and E. Rozengurt: Insulin-like growth factor I stimulates tyrosine phosphorylation of p130(Cas), focal adhesion kinase, and paxillin. J. Biol. Chem., 273:26149-26156 (1998).
11. Chellappan, S., V. B. Kraus, B. Kroger, K. Munger, P. M. Howley, W. C. Phelps, and J. R. Nevins: Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. U.S.A., 89:4549-4553 (1992).
12. De Nichilo, M. O. and K. M. Yamada: Integrin alpha v beta 5-dependent serine phosphorylation of paxillin in cultured human macrophages adherent to vitronectin. J. Biol. Chem., 271:11016-11022 (1996).
13. Druker, B., M. Talpaz, D. Resta, B. Peng, E. Buchdunger, J. Ford, and C. Sawyers: Clinical efficacy and safety of an abl specific tyrosine kinase inhibitor as targeted therapy for chronic myelogenous leukemia. Blood Abst., (1999).
14. Dyson, N., P. M. Howley, K. Munger, and E. Harlow: The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science, 243:934-937 (1989).
15. Fujita, H., K. Kamiguchi, D. Cho, M. Shibanuma, C. Morimoto, and K. Tachibana: Interaction of Hic-5, A senescence-related protein, with focal adhesion kinase. J. Biol. Chem., 273:26516-26521 (1998).
16. Ganju, R. K., N. Munshi, B. C. Nair, Z. Y. Liu, P. Gill, and J. E. Groopman: Human immunodeficiency virus tat modulates the Flk-1/KDR receptor, mitogen-activated protein kinases, and components of focal adhesion in Kaposi's sarcoma cells. J. Virol., 72:6131-6137 (1998).
17. Glenney, J. R., Jr. and L. Zokas: Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J. Cell. Biol., 108:2401-2408 (1989).
18. Greenberg, S., P. Chang, and S. C. Silverstein: Tyrosine phosphorylation of the gamma subunit of Fc gamma receptors, p72syk, and paxillin during Fc receptor-mediated phagocytosis in macrophages. J. Biol. Chem., 269:3897-3902 (1994).
19. Hempstead, B. L., R. B. Birge, J. E. Fajardo, R. Glassman, D. Mahadeo, R. Kraemer, and H. Hanafusa: Expression of the v-crk oncogene product in PC12 cells results in rapid differentiation by both nerve growth factor- and epidermal growth factor-dependent pathways. Mol. Cell. Biol., 14:1964-1971 (1994).
20. Howley, P. M., D. Ganem, and E. Kieff: DNA viruses. In: (V. T. Devita, Jr., S. Hellman, and S. A. Rosenberg, Eds.) Lippincott-Raven, Philadelphia, PA (1997).
21. Huibregtse, J. M., M. Scheffner, and P. M. Howley: A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J., 10:4129-4135 (1991).
22. Huibregtse, J. M., M. Scheffner, and P. M. Howley: Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papilloma-virus E6 oncoprotein with p53. Mol. Cell. Biol., 13:775-784 (1993a).
23. Huibregtse, J. M., M. Scheffner, and P. M. Howley: Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol. Cell. Biol., 13:4918-1927 (1993b).
24. Huibregtse, J. M., M. Scheffner, and P. M. Howley: E6-AP directs the HPV E6-dependent inactivation of p53 and is representative of a family of structurally and functionally related proteins. Cold Spring Harb. Symp. Quant. Biol., 59:237-245 (1994).
25. Khan, M. A., N. Okumura, M. Okada, S. Kobayashi, and H. Nakagawa: Nerve growth factor stimulates tyrosine phosphorylation of paxillin in PC12h cells. FEBS Lett., 362:201-204 (1995).
26. Leduc, I. and S. Meloche: Angiotensin II stimulates tyrosine phosphorylation of the focal adhesion-associated protein paxillin in aortic smooth muscle cells. J. Biol. Chem., 270:4401-4404 (1995).
27. Lewis, J. M. and M. A. Schwartz: Integrins regulate the association and phosphorylation of paxillin by c-Abl. J. Biol. Chem., 273:14225-14230 (1998).
28. Lipsky, B. P., C. R. Beals, and D. E. Staunton: Leupaxin is a novel LIM domain protein that forms a complex with PYK2. J. Biol. Chem., 273:11709-11713 (1998).
29. Liu, S., S. M. Thomas, D. G. Woodside, D. M. Rose, W. B. Kiosses, M. Pfaff, and M. H. Ginsberg: Binding of paxillin to alpha4 integrins modifies integrin-dependent biological responses. Nature, 402:676-681 (1999).
30. Lo, S. H., E. Weisberg, and L. B. Chen: Tensin: a potential link between the cytoskeleton and signal transduction. Bioessays, 16:817-823 (1994).
31. Mazaki, Y., S. Hashimoto, and H. Sabe: Monocyte cells and cancer cells express novel paxillin isoforms with different binding properties to focal adhesion proteins. J. Biol. Chem., 272:7437-7444 (1997).
32. Mazaki, Y., H. Uchida, O. Hino, S. Hashimoto, and H. Sabe: Paxillin isoforms in mouse. Lack of the gamma isoform and developmentally specific beta isoform expression. J. Biol. Chem., 273:22435-22441 (1998).
33. Melo, J. V.: BCR-ABL gene variants. Baillieres Clin. Haematol., 10:203-222 (1997).
34. Miyamoto, S., H. Teramoto, O. A. Coso, J. S. Gutkind, P. D. Burbelo, S. K. Akiyama, and K. M. Yamada: Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J. Cell. Biol., 131:791-805 (1995).
35. Qian, F., D. L. Vaux, and I. L. Weissman: Expression of the integrin alpha 4 beta 1 on melanoma cells can inhibit the invasive stage of metastasis formation. Cell, 77:335-347 (1994).
36. Richardson, A., R. K. Malik, J. D. Hildebrand, and J. T. Parsons: Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol. Cell. Biol., 17:6906-6914 (1997).
37. Sabe, H., A. Hata, M. Okada, H. Nakagawa, and H. Hanafusa: Analysis of the binding of the Src homology 2 domain of Csk to tyrosine-phosphorylated proteins in the suppression and mitotic activation of c-Src. Proc. Natl. Acad. Sci. U.S.A., 91:3984-3988 (1994).
38. Sakata, H., H. Takayama, R. Sharp, J. S. Rubin, G. Merlino, and W. J. LaRochelle: Hepatocyte growth factor/scatter factor overexpression induces growth, abnormal development, and tumor formation in transgenic mouse livers. Cell Growth Differ., 7:1513-1523 (1996).
39. Salgia, R., B. Brunkhorst, E. Pisick, J. L. Li, S. H. Lo, L. B. Chen, and J. D. Griffin: Increased tyrosine phosphorylation of focal adhesion proteins in myeloid cell lines expressing p210BCR/ABL. Oncogene, 11:1149-1155 (1995a).
40. Salgia, R., J. L. Li, S. H. Lo, B. Brunkhorst, G. S. Kansas, E. S. Sobhany, Y. Sun, E. Pisick, M. Hallek, T. Ernst et al.: Molecular cloning of human paxillin, a focal adhesion protein phosphorylated by P210BCR/ABL. J. Biol. Chem., 270:5039-5047 (1995b).
41. Salgia, R., N. Uemura, K. Okuda, J. L. Li, E. Pisick, M. Sattler, R. de Jong, B. Druker, N. Heisterkamp, L. B. Chen et al.: CRKL links p210BCR/ABL with paxillin in chronic myelogenous leukemia cells. J. Biol. Chem., 270:29145-52910 (1995c).
42. Salgia, R., E. Pisick, M. Sattler, J. L. Li, N. Uemura, W. K. Wong, S. A. Burky, H. Hirai, L. B. Chen, and J. D. Griffin: p130CAS forms a signaling complex with the adapter protein CRKL in hematopoietic cells transformed by the BCR/ABL oncogene. J. Biol. Chem., 271:25198-25203 (1996a).
43. Salgia, R., M. Sattler, E. Pisick, J. L. Li, and J. D. Griffin: p210BCR/ABL induces formation of complexes containing focal adhesion proteins and the protooncogene product p 120c-Cbl. Exp. Hematol., 24:310-313 (1996b).
44. Salgia, R. and A. T. Skarin: Molecular abnormalities in lung cancer. J. Clin. Oncol., 16:1207-1217 (1998).
45. Salgia, R., J.-L. Li, D. Ewaniuk, Y.-B. Wang, M. Sattler, W.-C. Chen, W. Richards, E. Pisick, G. I. Shapiro, B. J. Rollins, L. B. Chen, J. D. Griffen, and D. J. Sugarbaker: Expression of the focal adhesion protein paxillin in lung cancer and its relation to cell motility. Oncogene, 18:67-77 (1999).
46. Sattler, M. and R. Salgia: Activation of hematopoietic growth factor signal transduction pathways by the human oncogene BCR/ABL. Cytokine Growth Factor Rev., 8:63-79 (1997).
47. Schaller, M. D. and J. T. Parsons: Focal adhesion kinase and associated proteins. Curr. Opin. Cell. Biol., 6:705-710 (1994).
48. Schaller, M. D. and J. T. Parsons: pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell Biol., 15:2635-2645 (1995).
49. Scheffner, M., J. M. Huibregtse, and P. M. Howley: Identification of a human ubiquitin-conjugating enzyme that mediates the E6-AP-dependent ubiquitination of p53. Proc. Natl. Acad. Sci. U.S.A., 91:8797-8801 (1994).
50. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley: The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of P53. Cell, 75:495-505 (1993).
51. Scheffner, M., B. A. Werness, J. M. Huibregtse, A. J. Levine, and P. M. Howley: The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell, 63:1129-1136 (1990).
52. Seckl, M. J., N. Morii, S. Narumiya, and E. Rozengurt: Guanosine 5′-3-O-(thio)triphosphate stimulates tyrosine phosphorylation of p125FAK and paxillin in permeabilized Swiss 3T3 cells. Role of p21rho. J. Biol. Chem., 270:6984-6990 (1995).
53. Seufferlein, T. and E. Rozengurt: Lysophosphatidic acid stimulates tyrosine phosphorylation of focal adhesion kinase, paxillin, and p130. Signaling pathways and cross-talk with platelet-derived growth factor. J. Biol. Chem., 269:9345-9351 (1994a).
54. Seufferlein, T. and E. Rozengurt: Sphingosine induces p125FAK and paxillin tyrosine phosphorylation, actin stress fiber formation, and focal contact assembly in Swiss 3T3 cells. J. Biol. Chem., 269:27610-27617 (1994b).
55. Seufferlein, T. and E. Rozengurt: Sphingosylphosphorylcholine rapidly induces tyrosine phosphorylation of p125FAK and paxillin, rearrangement of the actin cytoskeleton and focal contact assembly. Requirement of p21rho in the signaling pathway. J. Biol. Chem., 270:24343-24351 (1995).
56. Shen, Y., G. Schneider, J. F. Cloutier, A. Veillette, and M. D. Schaller: Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem., 273:6474-6481 (1998).
57. Thomas, J. W., M. A. Cooley, J. M. Broome, R. Salgia, J. D. Griffin, C. R. Lombardo, and M. D. Schaller: The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin [in process citation]. J. Biol. Chem., 274:36684-36692 (1999).
58. Tong, X. and P. M. Howley: The bovine papillomavirus E6 oncoprotein interacts with paxillin and disrupts the actin cytoskeleton. Proc. Natl. Acad. Sci. U.S.A., 94:4412-4417 (1997).
59. Tong, X., R. Salgia, J. L. Li, J. D. Griffin, and P. M. Howley: The bovine papillomavirus E6 protein binds to the LD motif repeats of paxillin and blocks its interaction with vinculin and the focal adhesion kinase. J. Biol. Chem., 272:33373-33376 (1997).
60. Turner, C. E.: Paxillin: a cytoskeletal target for tyrosine kinases. Bioessays, 16:47-52 (1994).
61. Turner, C. E., M. C. Brown, J. A. Perrotta, M. C. Riedy, S. N. Nikolopoulos, A. R. McDonald, S. Bagrodia, S. Thomas, and P. S. Leventhal: Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell. Biol., 145:851-863 (1999).
62. Turner, C. E., J. R. Glenney, Jr., and K. Burridge: Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell. Biol., 111:1059-1068 (1990).
63. Turner, C. E. and J. T. Miller: Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp125Fak-binding region. J. Cell Sci., 107:1583-1591 (1994).
64. Turner, C. E., K. M. Pietras, D. S. Taylor, and C. J. Molloy: Angiotensin II stimulation of rapid paxillin tyrosine phosphorylation correlates with the formation of focal adhesions in rat aortic smooth muscle cells. J. Cell Sci., 108:333-342 (1995).
65. Vadlamudi, R., L. Adam, A. Talukder, J. Mendelsohn, and R. Kumar: Serine phosphorylation of paxillin by heregulin-betal: role of p38 mitogen activated protein kinase. Oncogene, 18:7253-7264 (1999a).
66. Vadlamudi, R., L. Adam, B. Tseng, L. Costa, and R. Kumar: Transcriptional up-regulation of paxillin expression by heregulin in human breast cancer cells. Cancer Res., 59:2843-2846 (1999b).
67. Vande Pol, S. B., M. C. Brown, and C. E. Turner: Association of Bovine Papillomavirus Type 1 E6 oncoprotein with the focal adhesion protein paxillin through a conserved protein interaction motif. Oncogene, 16:43-52 (1998).
68. Weng, Z., J. A. Taylor, C. E. Turner, J. S. Brugge, and C. Seidel-Dugan: Detection of Src homology 3-binding proteins, including paxillin, in normal and v-Src-transformed Balb/c 3T3 cells. J. Biol. Chem., 268:14956-14963 (1993).
69. Yamaguchi, R., M. Maki, M. Hatanaka, and H. Sabe: Unphosphorylated and tyrosine-phosphorylated forms of a focal adhesion protein, paxillin, are substrates for calpain II in vitro: implications for the possible involvement of calpain II in mitosis-specific degradation of paxillin. FEBS Lett., 356:114-116 (1994).
70. Yamaguchi, R., Y. Mazaki, K. Hirota, S. Hashimoto, and H. Sabe: Mitosis specific serine phosphorylation and downregulation of one of the focal adhesion protein, paxillin. Oncogene, 15:1753-1761 (1997).
71. Zachary, I., J. Sinnett-Smith, C. E. Turner, and E. Rozengurt: Bombesin, vasopressin, and endothelin rapidly stimulate tyrosine phosphorylation of the focal adhesion-associated protein paxillin in Swiss 3T3 cells. J. Biol. Chem., 268:22060-22065 (1993).
72. Zhu, W. Y., C. S. Jones, S. Amin, K. Matsukuma, M. Haque, V. Vuligonda, R. A. Chandraratna, and L. M. De Luca: Retinoic acid increases tyrosine phosphorylation of focal adhesion kinase and paxillin in MCF-7 human breast cancer cells. Cancer Res., 59:85-90 (1999).