Rapid phosphorylation of Ets-2 accompanies mitogen-activated protein kinase activation and the induction of heparin-binding epidermal growth factor gene expression by oncogenic Raf-1

Molecular and Cellular Biology

Volumn 17, Issue 5, 1997, Pages 2401-2412

  McCarthy, Sean A ^a,e   Chen, Dan ^a   Yang, Beom Seok ^b   Garcia Ramirez, Jose J ^c   Cherwinski, Holly ^a   Chen, Xiao Rong ^d   Klagsbrun, Michael ^d   Hauser, Craig A ^c   Ostrowski, Michael C ^b   McMahon, Martin ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c BURNHAM INSTITUTE   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; GENE PRODUCT; HEPARIN BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; THREONINE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INDUCTION; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALIA; MURINAE;

EID: 0030974039     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.5.2401     Document Type: Article

References (77)

1. Aaronson, S. A. 1991. Growth factors and cancer. Science 254:1146-1153.
2. Ambrosio, L., A. P. Mahowald, and N. Perrimon. 1989. Requirement of the Drosophila raf homologue for torso function. Nature 342:288-291.
3. Bishop, J. M. 1995. Cancer: the rise of the genetic paradigm. Genes Dev. 9:1309-1315.
4. Bortner, D. M., S. J. Langer, and M. C. Ostrowski. 1993. Non-nuclear oncogenes and the regulation of gene expression in transformed cells. Crit. Rev. Oncog. 4:137-160.
5. Bos, J. L. 1989. Ras oncogenes in human cancer: a review. Cancer Res. 49:4682-4689.
6. Bruder, J. T., G. Heidecker, and U. R. Rapp. 1992. Serum-, TPA-, and Ras-induced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase. Genes Dev. 6:545-556.
7. Chang, H. C., N. M. Solomon, D. A. Wassarman, F. D. Karim, M. Therrien, G. M. Rubin, and T. Wolf. 1995. phyllopod functions in the fate determination of a subset of photoreceptors in Drosophila. Cell 80:463-472.
8. Chen, X., G. Raab, U. Deutsch, J. Zhang, R. M. Ezzell, and M. Klagsbrun. 1995. Induction of heparin-binding EGF-like growth factor expression during myogenesis. Activation of the gene by MyoD and localization of the transmembrane form of the protein on the myotube surface. J. Biol. Chem. 270:18285-18294.
9. Chrivia, J. C., R. P. Kwok, N. Lamb, M. Hagiwara, M. R. Montminy, and R. H. Goodman. 1993. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365:855-859.
10. Coffer, P., M. de Jonge, A. Mettouchi, B. Binetruy, J. Ghysdael, and W. Kruijer. 1994. junB promoter regulation: Ras mediated transactivation by c-Ets-1 and c-Ets-2. Oncogene 9:911-921.
11. Coso, O. A., M. Chiariello, J. C. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J. S. Gutkind. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137-1146.
12. Cowley, S., H. Paterson, P. Kemp, and C. J. Marshall. 1994 Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77:841-852.
13. Derijard, B., M. Hibi, I. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-ras that binds and phosphorylates the c-jun activation domain. Cell 76:1025-1037.
14. Dickson, B., and E. Hafen. 1994. Genetics of signal transduction in invertebrates. Curr. Opin. Genet. Dev. 4:64-70.
15. Dickson, B., F. Sprenger, D. Morrison, and E. Hafen. 1992. Raf functions downstream of Ras1 in the Sevenless signal transduction pathway. Nature 360:600-602.
16. Dickson, B. J., M. Dominguez, D. S. A. Van, and E. Hafen. 1995. Control of Drosophila photoreceptor cell fates by phyllopod, a novel nuclear protein acting downstream of the Raf kinase. Cell 80:453-462.
17. Egan, S. E., and R. A. Weinberg. 1993. The pathway to signal achievement. Nature 365:781-783.
18. Galang, C. K., C. J. Der, and C. A. Hauser. 1994. Oncogenic Ras can induce transcriptional activation through a variety of promoter elements, including tandem c-Ets-2 binding sites. Oncogene 9:2913-2921.
19. Galang, C. K., R. J. Garcia, P. A. Solski, J. K. Westwick, C. J. Der, N. N. Neznanov, R. G. Oshima, and C. A. Hauser. 1996. Oncogenic Neu/ErbB-2 increases ets, AP-1, and NF-kappaB-dependent gene expression, and inhibiting ets activation blocks Neu-mediated cellular transformation. J. Biol. Chem. 271:7992-7998.
20. Garcia-Ramirez, J., and C. Hauser. Unpublished observations.
21. Garrity, P. A., D. Chen, E. V. Rothenberg, and B. J. Wold. 1994. Interleukin-2 transcription is regulated in vivo at the level of coordinated binding of both constitutive and regulated factors. Mol. Cell. Biol. 14:2159-2169.
22. Garrity, P. A., and B. J. Wold. 1992. Effects of different DNA polymerases in ligation-mediated PCR: enhanced genomic sequencing and in vivo footprinting. Proc. Natl. Acad. Sci. USA 89:1021-1025.
23. Gille, H., T. Strahl, and P. E. Shaw. 1995. Activation of ternary complex factor Elk-1 by stress-activated protein kinases. Curr. Biol. 5:1191-1200.
24. Gotoh, Y., E. Nishida, T. Yamashita, M. Hoshi, M. Kawakami, and H. Sakai. 1990. Microtubule-associated-protein (MAP) kinase activated by nerve growth factor and epidermal growth factor in PC12 cells. Identity with the mitogen-activated MAP kinase of fibroblastic cells. Eur. J. Biochem. 193: 661-669.
25. Grant, P. A., C. B. Thompson, and S. Pettersson. 1995. IgM receptor-mediated transactivation of the IgH 3′ enhancer couples a novel Elf-1-AP-1 protein complex to the developmental control of enhancer function. EMBO J. 14:4501-4513.
26. Gutman, A., and B. Wasylyk. 1990. The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites. EMBO J. 7:2241-2246.
27. Han, M., A. Golden, Y. Han, and P. W. Sternberg. 1993. C. elegans lin-45 raf gene participates in let-60 ras-stimulated vulval differentiation. Nature 363: 133-139.
28. Hauser, C. Unpublished observations.
29. Hauser, C., J. K. Westwick, and C. J. Der. 1995. Ras-mediated transcription activation: analysis by transient cotransfection assay. Methods Enzymol. 255: 412-425.
30. Herskowitz, I. 1995. MAP kinase pathways in yeast: for mating and more. Cell 80:187-197.
31. Hibi, M., A. Lin, T. Smeal, A. Minden, and M. Karin. 1993. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7:2135-2148.
32. Hill, C. S., R. Marais, S. John, J. Wynne, S. Dalton, and R. Treisman. 1993. Functional analysis of a growth factor-responsive transcription factor complex. Cell 73:395-406.
33. Hill, C. S., and R. Treisman. 1995. Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 80:199-211.
34. 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.
35. Janknecht, R. 1996. Analysis of the ERK-stimulated transcription factor ER81. Mol. Cell. Biol. 16:1550-1556.
36. Johnson, R., B. Spiegelman, D. Hanahan, and R. Wisdom. 1996. Cellular transformation and malignancy induced by ras require c-jun. Mol. Cell. Biol. 16:4504-4511.
37. Karin, M. 1991. Signal transduction and gene control. Curr. Opin. Cell Biol. 3:467-473.
38. Karin, M. 1994. Signal transduction from the cell surface to the nucleus through the phosphorylation of transcription factors. Curr. Opin. Cell Biol. 6:415-424.
39. Karin, M. 1990. Transcriptional control and the integration of cell-autonomous and environmental cues during development. Curr. Opin. Cell Biol. 2:996-1002.
40. Karin, M., and T. Hunter. 1995. Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr. Biol. 5:747-757.
41. Kyriakis, J. M., P. Banerjee, E. Nikolakaki, T. Dai, E. A. Rubie, M. F. Ahmad, J. Avruch, and J. R. Woodgett. 1994. The stress activated protein kinase subfamily of c-jun kinases. Nature 369:156-160.
42. Langer, S. J., D. M. Bortner, M. F. Roussel, C. J. Sherr, and M. C. Ostrowski. 1992. Mitogenic signaling by colony-stimulating factor 1 and ras is suppressed by the ets-2 DNA-binding domain and restored by myc overexpression. Mol. Cell. Biol. 12:5355-5362.
43. MacNicol, A. M., A. J. Muslin, and L. T. Williams. 1993. Raf-1 kinase is essential for early Xenopus development and mediates the induction of mesoderm by FGF. Cell 73:571-583.
44. Mahony, D., and E. Lees. Unpublished observations.
45. Mansour, S. J., W. T. Matten, A. S. Hermann, J. M. Candia, S. Rong, K. Fukasawa, W. G. Vande, and N. G. Ahn. 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265:966-970.
46. Marais, R., J. Wynne, and R. Treisman. 1993. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell 73:381-394.
47. Marshall, C. J. 1994. MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4:82-89.
48. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
49. McCarthy, S. A., M. L. Samuels, C. A. Pritchard, J. A. Abraham, and M. McMahon. 1995. Rapid induction of heparin binding epidermal growth factor/diphtheria toxin receptor by Ras and Raf oncogenes. Genes Dev. 9:1953-1964.
50. 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.
51. 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 GTPases Rac and Cdc42Hs. Cell 81:1147-1157.
52. Monte, D., L. Coutte, J. L. Baert, I. Angeli, D. Stehelin, and Y. de Launoit. 1995. Molecular characterization of the ets-related human transcription factor ER81. Oncogene 11:771-779.
53. Nishida, E., and Y. Gotoh. 1993. The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci. 18:128-131.
54. Nishida, Y., M. Hata, T. Ayaki, H. Ryo, M. Yamagata, K. Shimizu, and Y. Nishizuka. 1988. Proliferation of both somatic and germ cells is affected in the Drosophila mutants of raf proto-oncogene. EMBO J. 7:775-781.
55. O'Neill, E. M., I. Rebay, R. Tjian, and G. M. Rubin. 1994. The activities of two ets-related transcription factors required for Drosophila eye development are modulated by the ras/MAPK pathway. Cell 78:137-147.
56. Ostrowski, M. Unpublished observations.
57. Pankov, R., A. Umezawa, R. Maki, C. J. Der, C. A. Hauser, and R. G. Oshima. 1994. Oncogene activation of human keratin 18 transcription via the Ras signal transduction pathway. Proc. Natl. Acad. Sci. USA 91:873-877.
58. Parker, D., K. Ferreri, T. Nakajima, V. J. La Morte, R. Evans, S. C. Koerber, C. Hoeger, and M. R. Montminy. 1996. Phosphorylation of CREB at Ser-133 induces complex formation with CREB-binding protein via a direct mechanism. Mol. Cell. Biol. 16:694-703.
59. Pritchard, C. A., L. Bolin, R. Slattery, R. L. Murray, and M. McMahon. 1996. Post-natal lethality and neurological and gastrointestinal defects in mice with targeted disruption of the A-Raf protein kinase. Curr. Biol. 6:614-617.
60. Rebay, I., and G. M. Robin. 1995. Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras/MAPK pathway. Cell 81:857-866.
61. Reddy, M. A., S. J. Langer, M. S. Colman, and M. C. Ostrowski. 1992. An enhancer element responsive to ras and fms signaling pathways is composed of two distinct nuclear factor binding sites. Mol. Endocrinol. 6:1051-1060.
62. Robertson, L. M., T. K. Kerppola, M. Vendrell, D. Luk, R. J. Smeyne, C. Bocchiaro, J. I. Morgan, and T. Curran. 1995. Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron 14:241-252.
63. Samuels, M. L., and M. McMahon. 1994. Inhibition of platelet-derived growth factor- and epidermal growth factor-mediated mitogenesis and signaling in 3T3 cells expressing delta Raf-1:ER, an estradiol-regulated form of Raf-1. Mol. Cell. Biol. 14:7855-7866.
64. Samuels, M. L., M. J. Weber, J. M. Bishop, and M. McMahon. 1993. Conditional transformation of cells and rapid activation of the mitogen-activated protein kinase cascade by an estradiol-dependent human Raf-1 protein kinase. Mol. Cell. Biol. 13:6241-6252.
65. Sanchez, I., R. T. Hughes, B. J. Mayer, K. Yee, J. R. Woodgett, J. Avruch, J. M. Kyriakis, and L. I. Zon. 1994. Role of SAPK/ERK kinase-1 in the stress activated pathway regulating transcription factor c-jun. Nature 372:794-798.
66. Sgouras, D. N., M. A. Athanasiou, G. J. Beal, Jr., R. J. Fisher, D. G. Blair, and G. J. Mavrothalassitis. 1995. ERF, an ETS domain protein with strong transcriptional repressor activity, can suppress ets-associated tumorigenesis and is regulated by phosphorylation during cell cycle and mitogenic stimulation. EMBO J. 14:4781-4793.
67. Stacey, K. J., L. F. Fowles, M. S. Colman, M. C. Ostrowski, and D. A. Hume. 1995. Regulation of urokinase-type plasminogen activator gene transcription by macrophage colony-stimulating factor. Mol. Cell. Biol. 15:3430-3441.
68. Stanton, V. P., Jr., D. W. Nichols, A. P. Laudano, and G. M. Cooper. 1989. Definition of the human raf amino-terminal regulatory region by deletion mutagenesis. Mol. Cell. Biol. 9:639-647.
69. Sternberg, P. W., A. Golden, and M. Han. 1993. Role of a raf proto-oncogene during Caenorhabditis elegans vulval development. Phil. Trans. R. Soc. Lond. 340:259-265.
70. Treisman, R. 1996. Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8:205-215.
71. Wassarman, D. A., M. Therrien, and G. M. Rubin. 1995. The Ras signaling pathway in Drosophila. Curr. Opin. Genet. Dev. 5:44-50.
72. Wasylyk, B., S. L. Hahn, and A. Giovane. 1993. The Ets family of transcription factors. Eur. J. Biochem. 211:7-18.
73. Wasylyk, C., P. Flores, A. Gutman, and B. Wasylyk. 1989. PEA3 is a nuclear target for transcription activation by non-nuclear oncogenes. EMBO J. 8:3371-3378.
74. Wasylyk, C., A. Gutman, R. Nicholson, and B. Wasylyk. 1991. The c-Ets oncoprotein activates the stromelysin promoter through the same elements as several non-nuclear oncoproteins. EMBO J. 10:1127-1134.
75. Wasylyk, C., S. M. Maira, P. Sobieszczuk, and B. Wasylyk. 1994. Reversion of Ras transformed cells by Ets transdominant mutants. Oncogene 9:3665-3673.
76. Wasylyk, C., B. Wasylyk, G. Heidecker, M. Huleihel, and U. R. Rapp. 1989. Expression of raf oncogenes activates the PEA1 transcription factor motif. Mol. Cell. Biol. 9:2247-2250.
77. Yang, B.-S., C. A. Hauser, G. Henkel, M. S. Colman, C. Van Beveren, K. J. Stacey, D. A. Hume, R. A. Maki, and M. C. Ostrowski. 1996. Ras-mediated phosphorylation of a conserved threonine residue enhances the transactivation activities of c-Ets1 and c-Ets2. Mol. Cell. Biol. 16:538-547.