UV-induced stabilization of c-fos and other short-lived mRNAs

Molecular and Cellular Biology

Volumn 20, Issue 10, 2000, Pages 3616-3625

  Blattner, Christine ^a,d   Kannouche, Patricia ^b,e   Litfin, Margarethe ^a   Bender, Klaus ^a,f   Rahmsdorf, Hans J ^a   Angulo, Jaime F ^b   Herrlich, Peter ^a,c  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^c UNIVERSITY OF KARLSRUHE   (Germany)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e UNIVERSITY OF SUSSEX   (United Kingdom)

^f Institut fur Rechtsmedizin   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DNA DAMAGE; GENE CONTROL; GENE EXPRESSION; GENE INDUCTION; GENETIC TRANSCRIPTION; IMMEDIATE EARLY GENE; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL;

ANIMALS; CELL DEATH; CELLS, CULTURED; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; FIBROBLASTS; GENES, FOS; GENES, IMMEDIATE-EARLY; GENES, P53; HALF-LIFE; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-MDM2; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RNA STABILITY; RNA, MESSENGER; TIME FACTORS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR AP-1; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

EID: 0034053967     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.10.3616-3625.2000     Document Type: Article

References (71)

1. Adler, V., S. Y. Fuchs, J. Kim, A. Kraft, M. P. King, J. Pelling, and Z. Ronai. 1995. Jun-NH2-terminal kinase activation mediated by UV-induced DNA lesions in melanoma and fibroblast cells. Cell Growth Differ. 6:1437-1446.
2. Angulo, J. F., P. L. Moreau, R. Maunoury, J. Laporte, A. M. Hill, R. Bertolotti, and R. Devoret. 1989. KIN, a mammalian nuclear protein immunologically related to E. coli RecA protein. Mutat. Res. 217:123-134.
3. Angulo, J. F., E. Rouer, A. Mazin, M. G. Mattei, A. Tissier, P. Horellou, R. Benarous, and R. Devoret. 1991. Identification and expression of the cDNA of KIN17, a zinc-finger gene located on mouse chromosome 2. encoding a new DNA-binding protein. Nucleic Acids Res. 19:5117-5123.
4. Aragane, Y., D. Kulms, D. Metze, C. Wilkes, B. Pöppelmann, T. A. Luger, and T. Schwarz. 1998. Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/Apo-1) independently of its ligand CD95L. J. Cell Biol. 140: 171-182.
5. Bates, S., and K. H. Vousden. 1999. Mechanisms of p53-mediated apoptosis. Cell. Mol. Life Sci. 55:28-37.
6. Bender, K., M. Göttlicher, S. Whiteside, H.-J. Rahmsdorf, and P. Herrlich. 1998. Sequential DNA damage-independent and -dependent activation of NF-kappaB by UV. EMBO J. 17:5170-5181.
7. Benson, F. E., A. Stasiak, and S. C. West. 1994. Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J. 13:5764-5771.
8. Blattner, C., A. Knebel, A. Radler-Pohl, C. Sachsenmaier, P. Herrlich, and H.-J. Rahmsdorf. 1994. DNA damaging agents and growth factors induce changes in the program of expressed gene products through common routes. Environ. Mol. Mutagen. 24:3-10.
9. Blattner, C., K. Bender, P. Herrlich, and H.-J. Rahmsdorf. 1998. Photoproducts in transcriptionally active DNA induce signal transduction to the delayed U.V.-responsive genes for collagenase and metallothionein. Oncogene 16:2827-2834.
10. Blattner, C., A. Sparks, and D. Lane. 1999. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol. Cell. Biol. 19:3704-3713.
11. Blattner, C., E. Tobiasch, M. Litfin, H.-J. Rahmsdorf, and P. Herrlich. 1999. DNA damage induced p53 stabilization: no indication for an involvement of p53 phosphorylation. Oncogene 18:1723-1732.
12. Brawerman, G. 1993. mRNA degradation in eukaryotic cells: an overview, p. 150-159. In J. Belasco and G. Brawerman (ed.), Control of messenger RNA stability. Academic Press, Inc., San Diego, Calif.
13. Brock, M. L., and D. J. Shapiro. 1983. Estrogen stabilizes vitellogenin mRNA against cytoplasmic degradation. Cell 34:207-214.
14. Brown, J. P., and M. Pagano. 1997. Mechanism of p53 degradation. Biochim. Biophys. Acta 1332:O1-O6.
15. Büscher, M., H.-J. Rahmsdorf, M. Litfin, M. Karin, and P. Herrlich. 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.
16. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
17. Chen, C. Y., F. Del Gatto-Konczak, Z. Wu, and M. Karin. 1998. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science 280:1945-1949.
18. Coffer, P. J., B. M. Burgering, M. P. Peppelenbosch, J. L. Bos, and W. Kruijer. 1995. UV activation of RTK activity. Oncogene 11:561-569.
19. Curran, T., G. Peters, C. Van Beveren, N. M. Teich, and I. M. Verma. 1982. FBJ murine osteosarcoma virus: identification and molecular cloning of biologically active proviral DNA. J. Virol. 44:674-682.
20. Curran, T., W. P. MacConnell, F. van Straaten, and I. M. Verma. 1983. Structure of the FBJ murine osteosarcoma virus genome: molecular cloning of its associated helper virus and the cellular homolog of the v-fos gene from mouse and human cells. Mol. Cell. Biol. 3:914-921.
21. de Vries, A., C. T. van Oostrom, F. M. Hofhuis, P. M. Dortant, R. J. Berg, F. R. de Gruijl, P. W. Wester, C. F. van Kreijl, P. J. Capel, H. van Steeg, and S. J. Verbeek. 1995. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377:169-173.
22. Donehower, L. A., M. Harvey, B. L. Slagle, M. J. McArthur, C. A. Montgomery, Jr., J. S. Butel, and A. Bradley. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356:215-221.
23. Elkeles, A., T. Juven-Gershon, D. Israeli, S. Wilder, A. Zalcenstein, and M. Oren. 1999. The c-fos proto-oncogene is a target for transactivation by the p53 tumor suppressor. Mol. Cell. Biol. 19:2594-2600.
24. Fornace, A. J., Jr. 1992. DNA-damage inducible genes in mammalian cells. Annu. Rev. Genet. 26:505-524.
25. Fort, P., L. Marty, M. Piecharzyk, S. el Sabrouty, C. Dani, P. Jeanteur, and J. M. Blanchard. 1985. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 13:1431-1442.
26. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis. ASM Press, Washington, D.C.
27. Gorospe, M., X. Wang, and H. J. Holbrook. 1998. p53-dependent elevation of p21Waf1 expression by UV light is mediated through mRNA stabilization and involves a vanadate-sensitive regulatory system. Mol. Cell. Biol. 18: 1400-1407.
28. Greenberg, M. E., and T. P. Bender. 1987. Preparation and analysis of RNA. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. John Wiley, New York, N.Y.
29. Herrlich, P., and F.-D. Böhmer. 2000. Redox regulation of signal transduction in mammalian cells. Biochem. Pharmacol. 59:35-41.
30. Herrlich, P., and H.-J. Rahmsdorf. 1994. Transcriptional and post-transcriptional responses to DNA-damaging agents. Curr. Opin. Cell Biol. 6:425-431.
31. Herrlich, P., C. Blattner, A. Knebel, K. Bender, and H.-J. Rahmsdorf. 1997. Nuclear and non-nuclear targets of genotoxic agents in the induction of gene expression. Shared principles in yeast, rodents, man and plants. Biol. Chem. 378:1217-1229.
32. Herrlich, P., H.-J. Rahmsdorf, K. Bender, C. Blattner, and A. Knebel. 1998. Signal transduction induced by adverse agents: activation by inhibition. The UV response 1997. p. 479-492. In A. Puga and K. B. Wallace (ed.), Molecular biology of the toxic response. Taylor & Francis, Philadelphia, Pa.
33. Iordanov, M., K. Bender, T. Ade, W. Schmid, C. Sachsenmaier, K. Engel, M. Gaestel, H.-J. Rahmsdorf, and P. Herrlich. 1997. CREB is activated by UVC through a p38/HOG-1-dependent protein kinase. EMBO J. 16:1009-1022.
34. Iordanov, M. S., D. Pribnow, J. L. Magun, T. H. Dinh, J. A. Pearson, and B. E. Magun. 1998. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J. Biol. Chem. 273:15794-15803.
35. Jackman, J., I. Alamo, Jr., and A. J. Fornace, Jr. 1994 Genotoxic stress confers preferential and coordinate messenger RNA stability on the five gadd genes. Cancer Res. 54:5656-5662.
36. Jacobson, A., and S. W. Peltz. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:693-739.
37. Kabnick, K. S., and D. E. Housman. 1988. Determinants that contribute to cytoplasmic stability of human c-fos and beta-globin mRNAs are located at several sites in each mRNA. Mol. Cell. Biol. 8:3244-3250.
38. Kannouche, P., G. Pinon-Lataillade, P. Mauffrey, C. Faucher, D. S. Biard, and J. F. Angulo. 1997. Overexpression of Kin17 protein forms intranuclear foci in mammalian cells. Biochimie 79:599-606.
39. Kannouche, P., G. Pinon-Lataillade, A. Tissier, O. Chevalier-Lagente, A. Sarasin, M. Mezzina, and J. F. Angulo. 1998. The nuclear concentration of Kin17, a mouse protein that binds to curved DNA, increases during cell proliferation and after UV irradiation. Carcinogenesis 19:781-789.
40. Kannouche, P., and J. F. Angulo. 1999. Overexpression of Kin17 protein disrupts nuclear morphology and inhibits the growth of mammalian cells. J. Cell Sci. 112:3215-3224.
41. Knebel, A., H.-J. Rahmsdorf, A. Ullrich, and P. Herrlich. 1996. Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J. 15:5314-5325.
42. Krämer, M., C. Sachsenmaier, P. Herrlich, and H.-J. Rahmsdorf. 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. Kurumizaka, H., H. Aihara, S. Ikawa, T. Kashima, L. R. Bazemore, K. Kawasaki, A. Sarai, C. M. Radding, and T. Shibata. 1996. A possible role of the C-terminal domain of the RecA protein. A gateway model for double-stranded DNA binding. J. Biol. Chem. 271:33515-33524.
44. Li, N., and M. Karin. 1998. Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc. Natl. Acad. Sci. USA 95:13012-13017.
45. Maltzman, W., and L. Czyzyk. 1984. UV irradiation stimulates levels of p53 cellular tumor antigen in nontransformed mouse cells. Mol. Cell. Biol. 4:1689-1694.
46. Miskin, R., and E. Reich. 1980. Plasminogen activator: induction of synthesis by DNA damage. Cell 19:217-224.
47. Miskin, R., and R. Benishai. 1981. Induction of plasminogen activator by UV light in normal and xeroderma pigmentosum fibroblasts. Proc. Natl. Acad. Sci. USA 78:6236-6240.
48. Paek, I., and R. Axel. 1987. Glucocorticoids enhance stability of human growth hormone mRNA. Mol. Cell. Biol. 7:1496-1507.
49. Peng, S., C. Chen, N. H. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein HuR, an ELAV protein. EMBO J. 17: 3461-3470.
50. Rahmsdorf, H.-J., A. Schönthal, P. Angel, M. Litfin, U. Rüther, and P. Herrlich. 1987. Posttranscriptional regulation of c-fos mRNA expression. Nucleic Acids Res. 15:1643-1659.
51. Raymond, V., J. A. Atwater, and I. M. Verma. 1989. Removal of a messenger-RNA destabilizing element correlates with the increased oncogenicity of proto-oncogene fos. Oncogene Res. 5:1-12.
52. Rosette, C., and M. Karin. 1996. Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274:1194-1197.
53. Ross, J. 1996. Control of messenger RNA stability in higher eukaryotes. Trends Genet. 12:171-175.
54. Rotem, N., J. H. Axelrod, and R. Miskin. 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.
55. Sachsenmaier, C., A. Radler-Pohl, R. Zinck, A. Nordheim, P. Herrlich, and H.-J. Rahmsdorf. 1994. Involvement of growth factor receptors in the mammalian UVC response. Cell 78:963-972.
56. Schiavi, S. C., C. L. Wellington, A. B. Shyu, C. Chen, M. E. Greenberg, and J. B. Belasco. 1994. Multiple elements in the c-fos protein-coding region facilitate messenger-RNA deadenylation and decay by a mechanism coupled to translation. J. Biol. Chem. 269:3441-3448.
57. Schönthal, A., P. Herrlich, H.-J. Rahmsdorf, and H. Ponta. 1988. Requirement for fos gene expression in the transcriptional activation of collagenase by other oncogenes and phorbol esters. Cell 54:325-334.
58. Schorpp, M., U. Mallick, H.-J. Rahmsdorf, and P. Herrlich. 1984. UV-induced extracellular factor from human fibroblasts communicates the UV response to non-irradiated cells. Cell 37:861-868.
59. Schreiber, M., B. Baumann, M. Cotten, P. Angel, and E. F. Wagner. 1995. Fos is an essential component of the mammalian UV response. EMBO J. 14:5338-5349.
60. Schreiber, M., A. Kolbus, F. Piu, A. Szabowski, U. Mohle-Steinlein, J. Tian, M. Karin, P. Angel, and E. F. Wagner. 1999. Control of cell cycle progression by c-Jun is p53 dependent. Genes Dev. 13:607-619.
61. Sheikh, M. S., M. J. Antinore, Y. Huang, and A. J. Fornace, Jr. 1998. Ultraviolet-irradiation-induced apoptosis is mediated via ligand independent activation of tumor necrosis factor receptor 1. Oncogene 17:2555-2563.
62. Shinohara, A., H. Ogawa, Y. Matsuda, N. Ushio, K. Ikeo, and T. Ogawa. 1993. Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat. Genet. 4:239-243.
63. Shyu, A. B., J. G. Belasco, and M. E. Greenberg. 1991. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid messenger-RNA decay. Genes Dev. 5:221-231.
64. Timchenko, T., A. Bailone, and R. Devoret. 1996. Btcd, a mouse protein that binds to curved DNA, can substitute in Escherichia coli for H-NS, a bacterial nucleoid protein. EMBO J. 15:3986-3992.
65. Tissier, A., P. Kannouche, P. Mauffrey, I. Allemand, G. Frelat, R. Devoret, and J. F. Angulo. 1996. Molecular cloning and characterization of the mouse Kin17 gene coding for a Zn-finger protein that preferentially recognizes bent DNA. Genomics 38:238-242.
66. Tyrrell, R. M. 1996. Oxidant, antioxidant status and photocarcinogenesis: the role of gene activation. Photochem. Photobiol. 63:380-383.
67. Van Hoof, A., and R. Parker. 1999. The exosome: a proteasome for RNA. Cell 99:347-350.
68. Voloshin, O. N., L. J. Wang, and R. D. Camerini-Otero. 1996. Homologous DNA pairing promoted by a 20-amino-acid peptide derived from RecA. Science 272:868-872.
69. Walker, G. C. 1985. Inducible DNA repair systems. Annu. Rev. Biochem. 54:425-457.
70. Wu, L., and A. J. Levine. 1997. Differential regulation of the p21/WAF-1 and mdm2 genes after high-dose UV irradiation: p53-dependent and p53-independent regulation of the mdm2 gene. Mol. Med. 3:441-451.
71. Yamaizumi, M., and T. Sugano. 1994. UV-induced nuclear accumulation of p53 is evoked through DNA damage in actively transcribed genes independent of the cell cycle. Oncogene 9:2775-2784.