Requirement for Ras/Rac1-mediated p38 and c-Jun N-terminal kinase signaling in Stat3 transcriptional activity induced by the Src oncoprotein

Molecular and Cellular Biology

Volumn 19, Issue 11, 1999, Pages 7519-7528

  Turkson, James ^a,b   Bowman, Tammy ^a,b   Adnane, Jalila ^a,b   Zhang, Yi ^a,b   Djeu, Julie Y ^a,b   Sekharam, Madhavi ^a,b   Frank, David A ^c   Holzman, Lawrence B ^d   Wu, Jie ^a,b   Sebti, Said ^a,b   Jove, Richard ^a,b  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GROWTH FACTOR; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE; RAC1 PROTEIN; RAS PROTEIN; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL STRAIN 3T3; CONTROLLED STUDY; FIBROBLAST; MOUSE; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0032746702     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.11.7519     Document Type: Article

References (79)

1. Aftab, D. T., J. Kwan, and G. S. Martin. 1997. Ras-independent transformation by v-Src. Proc. Natl. Acad. Sci. USA 94:3028-3033.
2. Alessandrini, A., H. Greulich, W. Huang, and R. L. Erikson. 1996. Mek1 phosphorylation site mutants activate Raf-1 in NIH 3T3 cells. J. Biol. Chem. 271:31612-31618.
3. Beadling, C., J. Ng, J. W. Babbage, and D. A. Cantrell. 1996. Interleukin-2 activation of STAT5 requires the convergent action of tyrosine kinases and a serine/threonine kinase pathway distinct from the Raf-1/ERK2 MAP kinase pathway.EMBO J. 15:1902-1913.
4. Besser, D., J. F. Bromberg, J. E. Darnell, Jr., and H. Hanafusa. 1999. A single amino acid substitution in the v-Eyk intracellular domain results in activation of Stat3 and enhances cellular transformation. Mol. Cell. Biol. 19: 1401-1409.
5. Boulton, T. G., Z. Zhong, Z. Wen, J. E. Darnell, Jr., N. Stahl, and G. D. Yancopoulos. 1995. STAT3 activation by cytokines utilizing gp130 and related transducers involves a secondary modification requiring H7-sensitive kinase. Proc. Natl. Acad. Sci. USA 92:6915-6919.
6. Bromberg, J. F., C. M. Horvath, D. Besser, W. W. Lathem, and J. E. Darnell, Jr. 1998. Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol. 18:2553-2558.
7. Bromberg, J. F., C. M. Horvath, Z. Wen, R. D. Schreiber, and J. E. Darnell, Jr. 1996. Transcriptionally active Stat1 is required for the antiproliferative effects of both interferon alpha and interferon gamma. Proc. Natl. Acad. Sci. USA 93:7673-7678.
8. Caldenhoven, E., T. B. van Dijk, R. Solari, J. Armstrong, J. A. M. Raaijmakers, J. W. J. Lammers, L. Koenderman, and R. P. de Groot. 1996. STAT3beta, a splice variant of transcription factor STAT3, is a dominant negative regulator of transcription. J. Biol. Chem. 271:13221-13227.
9. Cao, X., X. Tay, G. R. Guy, and Y. H. Tan. 1996. Activation and association of Stat3 with Src in v-Src-transformed cell lines. Mol. Cell. Biol. 16:1595-1603.
10. Catlett-Falcone, R., T. H. Landowski, M. M. Oshiro, J. Turkson, A. Levitzki, R. Savino, G. Ciliberto, L. Moscinski, J. L. Fernandez-Luna, G. Nunez, W. S. Dalton, and R. Jove. 1999. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10:105-115.
11. Ceresa, B. P., C. M. Horvath, and J. E. Pessin. 1997. Signal transducer and activator of transcription-3 serine phosphorylation by insulin is mediated by a Ras/Raf/MEK-dependent pathway. Endocrinology 138:4131-4137.
12. Chai, S. K., G. L. Nichols, and P. Rothman. 1997. Constitutive activation of JAKs and STATs in BCL-Abl-expressing cell lines and peripheral blood cells derived from leukemic patients. J. Immunol. 159:4720-4728.
13. Chaturvedi, P., S. Sharma, and E. P. Reddy. 1997. Abrogation of interleukin-3 dependence of myeloid cells by the v-src oncogene requires SH2 and SH3 domains which specify activation of STATs. Mol. Cell. Biol. 17:3295-3304.
14. Chung, J., E. Uchida, T. C. Grammer, and J. Blenis. 1997. STAT3 serine phosphorylation by ERK-dependent and -independent pathways negatively modulates its tyrosine phosphorylation. Mol. Cell. Biol. 17:6508-6515.
15. Cressman, D. E., L. E. Greenbaum, R. A. DeAngelis, G. Ciliberto, E. E. Furth, V. Poli, and R. Taub. 1996. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 274:1379-1383.
16. Danial, N. N., A. Pernis, and P. B. Rothman. 1995. Jak-STAT signaling induced by the v-abl oncogene. Science 269:1875-1877.
17. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
18. Darnell, J. E., Jr., I. M. Kerr, and G. R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421.
19. David, M., E. Petricoin III, C. Benjamin, R. Pine, M. J. Weber, and A. C. Larner. 1995. Requirement for MAP kinase (ERK2) activity in interferon alpha-and interferon beta-stimulated gene expression through STAT proteins. Science 269:1721-1723.
20. del Peso, L., M. Gonzalez-Garcia, C. Page, R. Herrera, and G. Nunez. 1997. Interleukin 3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689.
21. Dudley, D. T., L. Pang, S. J. Decker, A. J. Bridges, and A. R. Saltiel. 1995. A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92:7686-7689.
22. Enslen, H., J. Ralngeaud, and R. J. Davis. 1998. Selective activation of p38 mitogen-activated protein (MAP) kinase isoforms by MAP kinase kinases MKK3 and MKK6. J. Biol. Chem. 273:1741-1748.
23. Fan, G., S. E. Merritt, M. Kortenjann, P. E. Shaw, and L. B. Holzman. 1996. Dual leucine zipper-bearing kinase (DLK) activates p46sapk and p38mapk but not ERK2. J. Biol. Chem. 271:24788-24793.
24. Fanger, G. R., P. Gerwins, C. Widmann, M. B. Jarpe, and G. L. Johnson. 1997. MEKKs, GCKs, MLKs, PAKs, TAKs, and tpls: upstream regulators of the c-Jun amino-terminal kinases? Curr. Opin. Genet. Dev. 7:67-74.
25. Frank, D. A., S. Mahajan, and J. Ritz. 1997. B lymphocytes from patients with chronic lymphocytic leukemia contain signal transducer and activator of transcription (STAT) 1 and STAT3 constitutively phosphorylated on serine residues. J. Clin. Investig. 100:3140-3148.
26. Fukada, T., M. Hibi, Y. Yamanaka, M. Takahashi-Tezuka, Y. Fujitani, T. Yamaguchi, K. Nakajima, and T. Hirano. 1996. Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 5:449-460.
27. Fukui, Y., A. R. Saltiel, and H. Hanafusa. 1991. Phosphatidylinositol-3 kinase is activated in v-src, v-yes, and v-fps transformed chicken embryo fibroblasts. Oncogene 6:407-111.
28. Garcia, R., and R. Jove. 1998. Activation of STAT transcription factors in oncogenic tyrosine kinase signaling. J. Biomed. Sci. 5:79-85.
29. Garcia, R., C.-L. Yu, A. Hudnall, R. Catlett, K. L. Nelson, T. Smithgall, D. J. Fujita, S. P. Ethier, and R. Jove. 1997. Constitutive activation of Stat3 in fibroblasts transformed by diverse oncoproteins and in breast carcinoma cells. Cell Growth Differ. 8:1267-1276.
30. Gollob, J. A., C. P. Schnipper, E. A. Murphy, J. Ritz, and D. A. Frank. 1999. The functional synergy between IL-12 and IL-2 involves p38 MAP kinase and is associated with the augmentation of STAT serine phosphorylation. J. Immunol. 162:4472-4481.
31. Grandis, J. R., S. D. Drenning, A. Chakraborty, M.-Y. Zhou, Q. Zeng, A. S. Pitt, and D. J. Tweardy. 1998. Requirement of Stat3 but not Stat1 activation for epidermal growth factor receptor-mediated cell growth in vitro. J. Clin. Investig. 102:1385-1392.
32. Greulich, H., C. Reichman, and H. Hanafusa. 1996. Delay in serum stimulation of Erk activity caused by oncogenic transformation. Oncogene 12: 1689-1695.
33. Hauser, P. J., D. Agrawal, J. Hackney, and W. J. Pledger. 1998. STAT3 activation accompanies keratinocyte differentiation. Cell Growth Differ. 10:847-855.
34. Her, J.-H., S. Lakhani, K. Zu, J. Vila, P. Dent, T. W. Sturgill, and M. J. Weber. 1993. Dual phosphorylation and autophosphorylation in mitogen-activated protein (MAP) kinase activation. Biochem. J. 296:25-31.
35. Hill, C. S., and R. Treisman. 1995. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 80:199-211.
36. Hill, C. S., and R. Treisman. 1995. Differential activation of c-fos promoter elements by serum, lysophosphatidic acid, G proteins and polypeptide growth factors. EMBO J. 14:5037-5047.
37. Hill, C. S., J. Wynne, and R. Treisman. 1995. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81:1159-1170.
38. Holland, P. M., M. Suzanne, J. S. Campbell, S. Noselli, and J. A. Cooper. 1997. MKK7 is a stress-activated mitogen-activated protein kinase kinase functionally related to hemipterous. J. Biol. Chem. 272:24994-24998.
39. Holzman, L. Unpublished results.
40. Jain, N., T. Zhang, S. L. Fong, C. P. Lim, and X. Cao. 1998. Repression of Stat3 activity by mitogen-activated protein kinase (MAPK). Oncogene 17: 3157-3167.
41. c-src can induce focus formation without complete transformation of NIH 3T3 cells. Mol. Cell. Biol. 5:1073-1083.
42. Khosravi-Far, R., P. A. Solski, G. J. Clark, M. S. Kinch, and C. J. Der. 1995. Activation of Rac1, RhoA, and mitogen-activated protein kinases is required for Ras transformation. Mol. Cell. Biol. 15:6443-6453.
43. Li, J., and T. E. Smithgall. 1998. Fibroblasts transformation by Fps/Fes tyrosine kinases requires Ras, Rac, and Cdc42 and induces extracellular signal-regulated and c-Jun N-terminal kinase activation. J. Biol. Chem. 273:13828-13834.
44. Lim, L., E. Manser, T. Leung, and C. Hall. 1996. Regulation of phosphorylation pathways by p21 GTPases. The p21 Ras-related Rho subfamily and its role in phosphorylation signaling pathways. Eur. J. Biochem. 242:171-185.
45. Liu, A. X., J. R. Testa, T. C. Hamilton, R. Jove, S. V. Nicosia, and J. Q. Cheng. 1998. AKT2, a member of the protein kinase B family, is activated by growth factors, v-Ha-ras, and v-src through phosphatidylinositol 3-kinase in human ovarian epithelial cancer cells. Cancer Res. 58:2973-2977.
46. Lund, T. C., R. Garcia, M. M. Medveczky, R. Jove, and P. G. Medveczky. 1997. Activation of STAT transcription factors by herpesvirus saimiri Tip-484 requires p56lck. J. Virol. 71:6677-6682.
47. Migone, T. S., J. X. Lin, A. Cereseto, J. C. Mulloy, J. J. O'Shea, G. Franchini, and W. J. Leonard. 1995. Constitutively activated Jak-STAT pathway in T cells transformed with HTLV-I. Science 269:79-81.
48. Minden, A., A. Lin, F.-X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPase Rac and Cdc42Hs. Cell 81:1147-1157.
49. Minden, A., A. Lin, M. McMahon, C. Lange-Carter, B. Derijard, R. J. Davis, G. L. Johnson, and M. Karin. 1994. Differential activation of ERK and JNK mitogen-activated protein kinases by Raf-1 and MEKK. Science 266:1719-1723.
50. Moodie, S. A., B. M. Willumsen, M. J. Weber, and A. Wolfman. 1993. Complexes of Ras-GTP with Raf-1 and mitogen-activated protein kinase kinase. Science 260:1658-1661.
51. Morooka, T., and E. Nishida. 1998. Requirement of p38 mitogen-activated protein kinase-activated protein kinase for neuronal differentiation in PC12 cells. J. Biol. Chem. 273:24285-24288.
52. Ng, J., and D. Cantrell. 1997. STAT3 is a serine kinase target in T lymphocytes. J. Biol. Chem. 272:24542-24549.
53. Pumiglia, K., Y.-H. Chow, J. Fabian, D. Morrison, S. Decker, and R. Jove. 1995. Raf-1 N-terminal sequences necessary for Ras-Raf interaction and signal transduction. Mol. Cell. Biol. 15:398-406.
54. Qureshi, S. A., K. Alexandropoulos, M. Rim, C. K. Joseph, J. T. Bruder, U. R. Rapp, and D. A. Foster. 1992. Evidence that Ha-Ras mediates two distinguishable intracellular signals activated by v-Src. J. Biol. Chem. 267: 17635-17639.
55. Rodriguez-Viciana, P., P. H. Warne, A. Khwaja, B. M. Marte, D. Pappin, P. Das, M. D. Waterfield, A. Ridley, and J. Downward. 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89:457-467.
56. Schindler, C., and J. E. Darnell, Jr. 1995. Transcriptional responses to polypeptide ligands: the Jak-STAT pathway. Annu. Rev. Biochem. 64:621-651.
57. Sengupta, T. K., E. S. Talbot, P. A. Scherle, and L. B. Ivashkiv. 1998. Rapid inhibition of interleukin-6 signaling and Stat3 activation mediated by mitogen-activated protein kinases. Proc. Natl. Acad. Sci. USA 95:11107-11112.
58. Stacey, D. W., M. Roudebush, R. Day, S. D. Mosser, J. B. Gibbs, and L. A. Feig. 1991. Dominant inhibitory Ras mutants demonstrate the requirement for Ras activity in the action of tyrosine kinase oncogenes. Oncogene 6: 2297-2304.
59. Stofega, M. R., C.-L. Yu, J. Wu, and R. Jove. 1997. Activation of extracellular signal-regulated kinase (ERK) by mitogenic stimuli is repressed in v-Src transformed cells. Cell Growth Differ. 8:113-119.
60. Symons, M. 1996. Rho family of GTPases: the cytoskeleton and beyond. Trends Biochem. Sci. 21:178-181.
61. Takeda, K., K. Noguchi, W. Shi, T. Tanaka, M. Matsumoto, N. Yoshida, T. Kishimoto, and S. Akira. 1997. Targeted disruption of the mouse Statj gene leads to early embryonic lethality. Proc. Natl. Acad. Sci. USA 94:3801-3804.
62. Takemoto, S., J. C. Mulloy, A. Cereseto, T. S. Migone, B. K. Patel, M. Matsuoka, K. Yamaguchi, K. Takatsuki, S. Kamihira, J. D. White, W. J. Leonard, T. Waldmann, and G. Franchini. 1997. Proliferation of adult T cell leukemia/lymphoma cells is associated with the constitutive activation of JAK/STAT proteins. Proc. Natl. Acad. Sci. USA 94:13897-13902.
63. Tibbles, L. A., Y. L. Ing, F. Kiefer, J. Chan, N. Iscove, J. R. Woodgett, and N. J. Lassam. 1996. MLK-3 activates the SAPK/JNK and p38 pathways via SEK1 and MKK3/6. EMBO J. 15:7026-7035.
64. Turkson, J., T. Bowman, R. Garcia, E. Caldenhoven, R. P. De Groot, and R. Jove. 1998. Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol. Cell. Biol. 18:2545-2552.
65. Wagner, B. J., T. E. Hayes, C. J. Hoban, and B. H. Cochran. 1990. The SIF binding elements confers sis/PDGF inducibiliry onto the c-fos promoter. EMBO J. 9:4477-4484.
66. Wang, Z., B. J. Canagarajah, J. C. Boehm, S. Kassisa, M. H. Cobb, P. R. Young, S. Abdel-Meguid, J. L. Adams, and E. J. Goldsmith. 1998. Structural basis of inhibitor selectivity in MAP kinases. Structure 6:1117-1128.
67. Weber-Nordt, R. M. C. Egen, J. Wehinger, W. Ludwig, V. Gouilleux-Gruart, R. Mertelsmann, and J. Finke. 1996. Constitutive activation of STAT proteins in primary lymphoid and myeloid leukemia cells and in Epstein-Barr virus (EBV)-related lymphoma cell lines. Blood 88:809-816.
68. Wen, Z., and J. E. Darnell, Jr. 1997. Mapping of Stat3 serine phosphorylation to a single residue (727) and evidence that serine phosphorylation has no influence on DNA binding of Stat1 and Stat3. Nucleic Acids Res. 25:2062-2067.
69. Wen, Z., Z. Zhong, and J. E. Darnell, Jr. 1995. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82:241-250.
70. Whalen, A. M., S. C. Galasinski, P. S. Shapiro, T. S. Nahreini, and N. G. Ahn. 1997. Megakaryocytic differentiation induced by constitutive activation of mitogen-activated protein kinase kinase. Mol. Cell. Biol. 17:1947-1958.
71. Whitmarsh, A. J., J. Cavanagh, C. Tournier, J. Yasuda, and R. J. Davis. 1998. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281:1671-1674.
72. Whitmarsh, A. J., S.-H. Yang, M. S.-S. Su, A. D. Sharrocks, and R. J. Davis. 1997. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol. Cell. Biol. 17:2360-2371.
73. Wu, J., J. K. Harrison, P. Dent, K. R. Lynch, M. J. Weber, and T. W. Sturgill. 1993. Identification and characterization of a new mammalian mitogen-activated protein kinase kinase, MKK2. Mol. Cell. Biol. 13:4539-4548.
74. Yamauchi, K., K. Holt, and J. E. Pessin. 1993. Phosphatidylinositol 3-kinase functions upstream of Ras and Raf in mediating insulin stimulation of c-fos transcription. J. Biol. Chem. 268:14597-14600.
75. Yano, H., S. Nakanishi, K. Kimura, N. Hanai, Y. Saitoh, Y. Fukui, Y. Nonomura, and Y. Matsuda. 1993. Inhibition of histamine secretion by wortmannin through the blockade of phosphatidylinositol 3-kinase in RBL-2H3 cells. J. Biol. Chem. 268:25846-25856.
76. Yao, Z., K. Diener, X. S. Wang, M. Zukowski, G. Matsumoto, G. Zhou, R. Mo, T. Sasaki, H. Nishina, C. C. Hui, T. H. Tan, J. P. Woodgett, and J. M. Penninger. 1997. Activation of stress-activated protein kinases/c-Jun N-terminal protein kinases (SAPK/JNKs) by a novel mitogen-activated protein kinase kinase (MKK7). J. Biol. Chem. 272:32378-32383.
77. Yu, C.-L., D. J. Meyer, G. S. Campbell, A. C. Larner, C. Carter-Su, J. Schwartz, and R. Jove. 1995. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269:81-83.
78. Zhang, Q., I. Nowak, E. C. Vonderheid, A. H. Rook, M. E. Kadin, P. C. Nowell, L. M. Shaw, and M. A. Wasik. 1996. Activation of Jak/STAT proteins involved in signal transduction pathway mediated by receptor for interleukin 2 in malignant T lymphocytes derived from cutaneous anaplastic large T-cell lymphoma and Sezary syndrome. Proc. Natl. Acad. Sci. USA 93:9148-9153.
79. Zhong, Z., Z. Wen, and J. E. Darnell, Jr. 1994. Stat3: a STAT family member activated by tyrosine phosphorylation in response to epidermal growth factor and interleukin-6. Science 264:95-98.