CREB is activated by UVC through a p38/HOG-1-dependent protein kinase

EMBO Journal

Volumn 16, Issue 5, 1997, Pages 1009-1022

  Iordanov, M ^a,b   Bender, K ^a   Ade, T ^a   Schmid, W ^c   Sachsenmaier, C ^a,d   Engel, K ^e   Gaestel, M ^e   Rahmsdorf, H J ^a   Herrlich, P ^a,f  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d Fred Hutchinson Cancer Research Center   (United States)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f UNIVERSITY OF KARLSRUHE   (Germany)

Author keywords

c fos; CREB; MAPKAP kinase 2; p108 CREB kinase; UV

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GROWTH FACTOR RECEPTOR; PROTEIN KINASE; SERINE; SURAMIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; ULTRAVIOLET C RADIATION;

ACTIVATING TRANSCRIPTION FACTOR 1; BLOTTING, WESTERN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA-BINDING PROTEINS; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; FLUORESCENT ANTIBODY TECHNIQUE; FORSKOLIN; HELA CELLS; HUMANS; KINETICS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; RIBOSOMAL PROTEIN S6 KINASES; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SURAMIN; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; ULTRAVIOLET RAYS;

ANIMALIA;

EID: 0031041602     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.5.1009     Document Type: Article

References (81)

1. Angel, P., Baumann, I., Stein, B., Delius, H., Rahmsdorf, H.J. and Herrlich, P. (1987) 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol. Cell. Biol. 7, 2256-2266.
2. Bading, H. and Greenberg, M.E. (1991) Stimulation of protein tyrosine phosphorylation by NMDA receptor activation. Science, 253, 912-914.
3. Bading, H., Ginty, D.D. and Greenberg, M.E. (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science, 260, 181-186.
4. Berkowitz, L.A., Riabowol, K.T. and Gilman, M.Z. (1989) Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter. Mol. Cell. Biol., 9, 4272-4281.
5. Betsholtz, C., Johnsson, A., Heldin, C.-H. and Westermark, B. (1986) Efficient reversion of simian sarcoma virus-transformation and inhibition of growth factor-induced mitogenesis by suramin. Proc. Natl Acad. Sci. USA, 83, 6440-6444.
6. Blendy, J.A., Kaestner, K.H., Schmid, W., Gass, P. and Schütz, G. (1996) Targeting of the CREB gene leads to up-regulation of a novel CREB mRNA isoform. EMBO J., 15, 1098-1106.
7. Blenis, J. (1993) Signal transduction via the MAP kinases: proceed at your own RSK. Proc. Natl Acad. Sci. USA, 90, 5889-5892.
8. 133 kinase in human melanocytes. Cell Growth Differ., 6, 291-302.
9. Bonni, A., Ginty, D.D., Dudek, H. and Greenberg, M.E. (1995) Serine 133-phosphorylated CREB induces transcription via a cooperative mechanism that may confer specificity to neurotrophin signals. Mol. Cell. Neurosci., 6, 168-183.
10. Büscher, M., Rahmsdorf, H.J., Litfin, M., Karin, M. and Herrlich, P. (1988) Activation of the c-fos gene by UV and phorbol ester: different signal transduction pathways converge to the same enhancer element. Oncogene, 3, 301-311.
11. Cano, E. and Mahadevan, L.C. (1995) Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci., 20, 117-122.
12. Chao, T.-S., Byron, K., Lee, K.-M., Villereal, M. and Rosner, M. (1992) Activation of MAP kinases by calcium-dependent and calcium-independent pathways. J. Biol. Chem., 267, 19876-19883.
13. Chrivia, J.C., Kwok, R.P.S., Lamb, N., Hagiwara, M., Montminy, M. and Goodman, R.H. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature, 365, 855-859.
14. Coffer, P.J., Burgering, B.M.T., Peppelenbosch, M.P., Bos, J.L. and Kruijer, W. (1995) UV activation of receptor tyrosine kinase activity. Oncogene, 11, 561-569.
15. Coffey, R.J., Jr, Leof, E.B., Shipley, G.D. and Moses, H.L. (1987) Suramin inhibition of growth factor receptor binding and mitogenicity in AKR-2B cells. J. Cell. Physiol., 132, 143-148.
16. Cuenda, A., Rouse, J., Doza, Y.N., Meier, R., Cohen, R., Gallagher, T.F., Young, P.R. and Lee, J.C. (1995) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett., 364, 229-233.
17. 2+/calmodulin-as well as cAMP-dependent protein kinase. Proc. Natl Acad. Sci. USA, 88, 5061-5065.
18. Dérijard, B., Hibi, M., Wu, I.-H., Barrett, T., Su, B., Deng, T., Karin, M. and Davis, R. (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.
19. Dévary, Y., Gottlieb, R.A., Smeal, T. and Karin, M. (1992) The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell, 71, 1081-1091.
20. Dévary, Y., Rosette, C., DiDonato, J.A. and Karin, M. (1993) NF-κB activation by ultraviolet light not dependent on a nuclear signal. Science, 261, 1442-1445.
21. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
22. Engel, K., Schultz, H., Martin, F., Kotlyarov, A., Plath, K., Hahn, M., Heinemann, U. and Gaestel, M. (1995) Constitutive activation of mitogen-activated protein kinase-activated protein kinase 2 by mutation of phosphorylation sites and an A-helix motif. J Biol. Chem., 270, 27213-27221.
23. Fantini, J., Rognoni, J.B., Roccabianca, M., Pommier, G. and Marvaldi, J. (1989) Suramin inhibits cell growth and glycolytic activity and triggers differentiation of human colic adenocarcinoma cell clone HT29-D4. J. Biol. Chem., 264, 10282-10286.
24. Fiore, R., Murphhy, T., Sanghera, J., Pelech, S. and Baraban, J. (1993) Activation of p42 mitogen-activated protein kinase by glutamate receptor stimulation in rat primary cortical cultures. J. Neurochem., 61, 1626-1633.
25. Fornace, A.J., Jr, Zmudzka, B., Hollander, M.C. and Wilson, S.H. (1989) Induction of β-polymerase mRNA by DNA-damaging agents in Chinese hamster ovary cells. Mol. Cell. Biol., 9, 851-853.
26. Foulkes, N.S., Borrelli, E. and Sassone-Corsi, P. (1991) CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription. Cell, 64, 739-749.
27. Friedberg, E., Walker, G. and Siede, W. (1995) DNA Repair and Mutagenesis. ASM Press, Washington, DC.
28. Gaestel, M. et al. (1989) Molecular cloning, sequencing and expression in E.coli of the 25 kDa growth-related protein of Ehrlich ascites tumor and its homology to mammalian stress proteins. Eur. J. Biochem., 179, 209-213.
29. Gaestel, M., Schröder, W., Benndorf, R., Lippmann, C., Buchner, K., Hucho, F., Erdmann, V.A. and Bielka, H. (1991) Identification of the phosphorylation sites of the murine small heat shock protein hsp 25. J. Biol. Chem., 266, 14721-14724.
30. Ginty, D., Bonni, A. and Greenberg, M. (1994) Nerve growth factor activates a Ras-dependent protein kinase that stimulates c-fos transcription via phosphorylation of CREB. Cell, 77, 713-725.
31. Gonzalez, G.A. and Montminy, M.R. (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell, 59, 675-680.
32. Haas, S. and Kaina, B. (1995) c-Fos is involved in the cellular defence against the genotoxic effect of UV radiation. Carcinogenesis, 16, 985-991.
33. Hai, T., Liu, F., Coukos, W.J. and Green, M.R. (1989) Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev., 3, 2083-2090.
34. Härtig, E., Loncarevic, I.F., Büscher, M., Herrlich, P. and Rahmsdorf, H.J. (1991) A new cAMP response element in the transcribed region of the human c-fos gene. Nucleic Acids Res., 19, 4153-4159.
35. Herdegen, T., Gass, P., Brecht, S., Neiss, W.F. and Schmid, W. (1994) The transcription factor CREB is not phosphorylated at serine 133 in axotomized neurons: implications for the expression of AP-1 proteins. Mol. Brain Res., 26, 259-270.
36. Herrera, R.E., Shaw, P.E. and Nordheim, A. (1989) Occupation of the c-fos serum response element in vivo by a multi-protein complex is unaltered by growth factor induction. Nature, 340, 68-70.
37. Hibi, M., Lin, A., Smeal, T., Minden, A. and Karin, M. (1993) Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev., 7, 2135-2148.
38. Iordanov, M. (1995) The cAMP responsive element binding protein (CREB) as a participant in the mammalian UVC response and as a target for repression by the activated glucocorticoid receptor. Ph.D. thesis, Universität Karlsruhe.
39. 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.
40. Kedar, P.S., Widen, S.G., Englander, E.W., Fornace, A.J., Jr and Wilson, S.H. (1991) The ATF/CREB transcription factor-binding site in the polymerase β promoter mediates the positive effect of N-methyl-N′-nitro-N-nitrosoguanidine on transcription. Proc. Natl Acad. Sci. USA, 88, 3729-3733.
41. Knebel, A., Rahmsdorf, H.J., Ullrich, A. and Herrlich, P. (1996) Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J., 15, 5314-5325.
42. Krämer, M., Sachsenmaier, C., Herrlich, P. and Rahmsdorf, H.J. (1993) UV-irradiation-induced interleukin-1 and basic fibroblast growth factor synthesis and release mediate part of the UV response. J. Biol. Chem., 268, 6734-6741.
43. Kwok, R.P.S., Lundblad, J.R., Chrivia, J.C., Richards, J.P., Bächinger, H.P., Brennan, R.G., Roberts, S.G.E., Green, M.R. and Goodman, R.H. (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature, 370, 223-226.
44. Kyriakis, J.M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E.A., Ahmad, M.F., Avruch, J. and Woodgett, J.R. (1994) The stress-activated protein kinase subfamily of cJun kinases. Nature, 369, 156-160.
45. Lee, J.C. et al. (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature, 372, 739-746.
46. Lee, K.A. and Masson, N. (1993) Transcription regulation by CREB and its relatives. Biochim. Biophys. Acta, 1174, 221-233.
47. Levitzki, A. and Gazit, A. (1995) Tyrosine kinase inhibition: an approach to drug development. Science, 267, 1782-1788.
48. Lu, X. and Lane, D.P. (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell, 75, 765-778.
49. Mai, S. et al. (1989) Mechanisms of the ultraviolet light response in mammalian cells. J. Cell Sci., 94, 609-615.
50. Marshall, C. (1994) MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev., 4, 82-89.
51. Matthews, R.P., Guthrie, C.R., Wailes, L.M., Zhao, X., Means, A.R. and McKnight, G.S. (1994) Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell. Biol., 14, 6107-6116.
52. Miskin, R. and Ben-Ishai, R. (1981) Induction of plasminogen activator by UV light in normal and xeroderma pigmentosum fibroblasts. Proc. Natl Acad. Sci. USA, 78, 6236-6240.
53. Montminy, M.R. and Bilezikjian, L.M. (1987) Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature, 328, 175-178.
54. Montminy, M.R., Sevarino, K.A., Wagner, J.A., Mandel, G. and Goodman, R.H. (1986) Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc. Natl Acad. Sci. USA, 83, 6682-6686.
55. Nelson, W.G. and Kastan, M.B. (1994) DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol., 14, 1815-1823.
56. Plath, K., Engel, K., Schwedersky, G. and Gaestel, M. (1994) Characterization of the proline-rich region of mouse MAPKAP kinase 2: influence on catalytic properties and binding to the c-abl SH3 domain in vitro. Biochem. Biophys. Res. Commun., 203, 1188-1194.
57. Pressman, B.C. (1976) Biological applications of ionophores. Annu. Rev. Biochem., 45, 501-530.
58. Price, M.A., Cruzalegui, F.H. and Treisman,R. (1996) The p38 and ERK MAP kinase pathways cooperate to activate Ternary Complex Factors and c-fos transcription in response to UV light. EMBO J., 15, 6552-6563.
59. Radler-Pohl, A., Sachsenmaier, C., Gebel, S., Auer, H.-P., Bruder, J.T., Rapp, U., Angel, P., Rahmsdorf, H.J. and Herrlich, P. (1993) UV-induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase. EMBO J., 12, 1005-1012.
60. Raingeaud, J., Gupta, S., Rogers, J.S., Dickens, M., Han, J., Ulevitch, R.J. and Davis, R.J. (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem., 270, 7420-7426.
61. Robertson, L., Kerppola, T., Vendrell, M., Luk, D., Smeyne, R., Bocchiaro, C., Morgan, J. and Curran, T. (1995) Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron, 14, 241-252.
62. Rosen, L., Ginty, D.D., Weber, M.J. and Greenberg, M.E. (1994) Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron, 12, 1207-1221.
63. Rotem, N., Axelrod, J.H. and Miskin, R. (1987) Induction of urokinase-type plasminogen activator by UV light in human fetal fibroblasts is mediated through a UV-induced secreted protein. Mol. Cell. Biol., 7, 622-631.
64. Sachsenmaier, C., Radler-Pohl, A., Zinck, R., Nordheim, A., Herrlich, P. and Rahmsdorf, H.J. (1994) Involvement of growth factor receptors in the mammalian UVC response. Cell, 78, 963-972.
65. Sassone-Corsi, R., Visvader, J., Ferland, L., Mellon, P.L. and Verma, I.M. (1988) Induction of proto-oncogene fos transcription through the adenylate cyclase pathway: characterization of a cAMP-responsive element. Genes Dev., 2, 1529-1538.
66. Schorpp, M., Mallick, U., Rahmsdorf, H.J. and Herrlich, P. (1984) UV-induced extraceffufar factor from human fibroblasts communicates the UV response to nonirradiated cells. Cell, 37, 861-868.
67. Schreiber, M., Baumann, B., Cotten, M., Angel, P. and Wagner, E.F. (1995) Fos is an essential component of the mammalian UV response. EMBO J., 14, 5338-5349.
68. Sheng, M., McFadden, G. and Greenberg, M. (1990) Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron, 4, 571-582.
69. 2+-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science, 252, 1427-1430.
70. Stein, B., Rahmsdorf, H.J., Steffen, A., Liftin, M. and Herrlich, P. (1989) UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein. Mol. Cell. Biol., 9, 5169-5181.
71. Stokoe, D., Campbell, D.G., Nakielny, S., Hidaka, H., Leevers, S.J., Marshall, C. and Cohen, P. (1992) MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J., 11, 3985-3994.
72. Sturgill, T.W., Ray, L.B., Erikson, E. and Maller, J.L. (1988) Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature, 334, 715-718.
73. Sun, P. and Maurer, R.A. (1995) An inactivating point mutation demonstrates that interaction of cAMP response element binding protein (CREB) with the CREB binding protein is not sufficient for transcriptional activation. J. Biol. Chem. 270, 7041-7044.
74. 2+/calmodulin-dependent protein kinases type II and type IV involvesphosphorylation of a site that negatively regulates activity. Genes Dev., 8, 2527-2539.
75. Taylor, S.S., Buechler, J.A. and Yonemoto, W. (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem., 59, 971-1005.
76. Treisman, R. (1994) Ternary complex factors: growth factor regulated transcriptional activators. Curr. Opin. Genet. Dev., 4, 96-101.
77. Treisman, R. (1996) Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol., 8, 205-215.
78. van Dam, H., Wilhelm, D., Herr, I., Steffen, A., Herrlich, P. and Angel, P. (1995) ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J., 14, 1798-1811.
79. van den Berg, S., Kaina, B., Rahmsdorf, H.J., Ponta, H. and Herrlich, P. (1991) Involvement of Fos in spontaneous and ultraviolet light induced genetic changes. Mol. Carcinogen., 4, 460-466.
80. Wasylyk, B., Wasylyk, C., Flores, P., Begue, A., Leprince, D. and Stehelin, D. (1990) The c-ets proto-oncogenes encode transcription factors that cooperate with c-Fos and c-Jun for transcriptional activation. Nature, 346, 191-193.
81. Yamaizumi, M. and Sugano, T. (1994) UV-induced nuclear accumulation of p53 is evoked through DNA damage of actively transcribed genes independent of the cell cycle. Oncogene, 9, 2775-2784.