RNA-binding protein Csx1 mediates global control of gene expression in response to oxidative stress

EMBO Journal

Volumn 22, Issue 23, 2003, Pages 6256-6266

  Rodríguez Gabriel, Miguel A ^a   Burns, Gavin ^b   McDonald, W Hayes ^a   Martín, Victoria ^a   Yates III, John R ^a   Bähler, Jürg ^b   Russell, Paul ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Microarray; Oxidative stress; Post transcriptional control of gene expression; RNA binding protein; Schizosaccharomyces pombe

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN CSX1; PROTEIN SPC1; RNA BINDING PROTEIN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CYTOTOXICITY; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; OSMOSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; SURVIVAL; YEAST;

FUNGAL PROTEINS; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; MUTAGENESIS, INSERTIONAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PHOSPHORYLATION; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; SCHIZOSACCHAROMYCES; TRANSCRIPTION FACTORS;

FUNGI; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 0347504851     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg597     Document Type: Article

References (71)

1. Bähler, J., Wu, J.Q., Longtine, M.S., Shah, N.G., McKenzie, A., 3rd, Steever, A.B., Wach, A., Philippsen, P. and Pringle, J.R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast, 14, 943-951.
2. Brennan, C.M. and Steitz, J.A. (2001) HuR and mRNA stability. Cell. Mol. Life Sci., 58, 266-277.
3. Buck, V., Quinn, J., Soto Pino, T., Martin, H., Saldanha, J., Makino, K., Morgan, B.A. and Millar, J.B. (2001) Peroxide sensors for the fission yeast stress-activated mitogen-activated protein kinase pathway. Mol. Biol. Cell, 12, 407-419.
4. Carballo, E., Lai, W.S. and Blackshear, P.J. (1998) Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science, 281, 1001-1005.
5. Carballo, E., Cao, H., Lai, W.S., Kennington, E.A., Campbell, D. and Blackshear, P.J. (2001) Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J. Biol. Chem., 276, 42580-42587.
6. Chang, L. and Karin, M. (2001) Mammalian MAP kinase signalling cascades. Nature, 410, 37-40.
7. Chen, C.Y. and Shyu, A.B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci., 20, 465-470.
8. Chen, C.Y. et al. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell, 107, 451-464.
9. Chen, D., Toone, W.M., Mata, J., Lyne, R., Bums, G., Kivinen, K., Brazma, A., Jones, N. and Bähler, J. (2003) Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell, 14, 214-229.
10. Chua, G., Taricani, L., Stangle, W. and Young, P.G. (2000) Insertional mutagenesis based on illegitimate recombination in Schizosaccharomyces pombe. Nucleic Acids Res., 28, e53.
11. Degols, G. and Russell, P. (1997) Discrete roles of the Spc1 kinase and the Atf1 transcription factor in the UV response of Schizosaccharomyces pombe. Mol. Cell. Biol., 17, 3356-3363.
12. Degols, G., Shiozaki, K. and Russell, P. (1996) Activation and regulation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol. Cell. Biol., 16, 2870-2877.
13. DeMaria, C.T. and Brewer, G. (1996) AUF1 binding affinity to A + U-rich elements correlates with rapid mRNA degradation. J. Biol. Chem., 271, 12179-12184.
14. Fan, J., Yang, X., Wang, W., Wood, W.H., 3rd, Becker, K.G. and Gorospe, M. (2002) Global analysis of stress-regulated mRNA turnover by using cDNA arrays. Proc. Natl Acad. Sci. USA, 99, 10611.
15. Finkel, T. and Holbrook, N.J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature, 408, 239-247.
16. Frevel, M.A., Bakheet, T., Silva, A.M., Hissong, J.G., Khabar, K.S. and Williams, B.R. (2003) p38 Mitogen-activated protein kinase-dependent and -independent signaling of mRNA stability of AU-rich element-containing transcripts. Mol. Cell. Biol., 23, 425-436.
17. Fuchs, S.Y., Tappin, I. and Ronai, Z. (2000) Stability of the ATF2 transcription factor is regulated by phosphorylation and dephosphorylation. J. Biol. Chem., 275, 12560-12564.
18. Gaits, F. and Russell, P. (1999) Active nucleocytoplasmic shuttling required for function and regulation of stress-activated kinase Spc1/StyI in fission yeast. Mol. Biol. Cell, 10, 1395-1407.
19. Gaits, F., Degols, G., Shiozaki, K. and Russell, P. (1998) Phosphorylation and association with the transcription factor Atf1 regulate localization of Spc1/Sty1 stress-activated kinase in fission yeast. Genes Dev., 12, 1464-1473.
20. Gallagher, J., Perrin D.M., Chan L., Kwong E. and Sigman D. (1996). Recognition of tetrahedral 1, 10-phenanthroline-cuprous chelates by transcriptionally active complexes does not depend on the sequence of the promoter. Chem. Biol. 3, 739-746.
21. Gallouzi, I.E., Brennan, C.M., Stenberg, M.G., Swanson, M.S., Eversole, A., Maizels, N. and Steitz, J.A. (2000) HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl Acad. Sci. USA, 97, 3073-3078.
22. 1 cyclin CLN3 to modulate cell fate in budding yeast. Genes Dev., 15, 2803-2808.
23. Gueydan, C., Droogmans, L., Chalon, P., Huez, G., Caput, D. and Kruys, V. (1999) Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor α mRNA. J. Biol. Chem., 274, 2322-2326.
24. Guhaniyogi, J. and Brewer, G. (2001) Regulation of mRNA stability in mammalian cells. Gene, 265, 11-23.
25. Habelhah, H., Shah, K., Huang, L., Ostareck-Lederer, A., Burlingame, A.L., Shokat, K.M., Hentze, M.W. and Ronai, Z. (2001) ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nature Cell Biol., 3, 325-330.
26. Kato, T., Jr, Okazaki, K., Murakami, H., Stettler, S., Fantes, P.A. and Okayama, H. (1996) Stress signal, mediated by a Hog1-like MAP kinase, controls sexual development in fission yeast. FEBS Lett., 378, 207-212.
27. Kawasaki, H., Schiltz, L., Chiu, R., Itakura, K., Taira, K., Nakatani, Y. and Yokoyama, K.K. (2000) ATF-2 has intrinsic histone acetyltransferase activity which is modulated by phosphorylation. Nature, 405, 195-200.
28. Kedersha, N., Cho, M.R., Li, W., Yacono, P.W., Chen, S., Gilks, N., Golan, D.E. and Anderson, P. (2000) Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J. Cell Biol., 151, 1257-1268.
29. Kontoyiannis, D., Kotlyarov, A., Carballo, E., Alexopoulou, L., Blackshear, P.J., Gaestel, M., Davis, R., Flavell, R. and Kollias, G. (2001) Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J., 20, 3760-3770.
30. Kyriakis, J.M. and Avruch, J. (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev., 81, 807-869.
31. Lai, W.S., Carballo, E., Strum, J.R., Kennington, E.A., Phillips, R.S. and Blackshear, P.J. (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor α mRNA. Mol. Cell. Biol., 19, 4311-4323.
32. Lasa, M., Mahtani, K.R., Finch, A., Brewer, G., Saklatvala, J. and Clark, A.R. (2000) Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol., 20, 4265-4274.
33. Lyne, R., Burns G., Mata J., Penkett C.J., Rustici G., Chen D., Langford C., Vetrie D. and Bähler J. (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility and processing of array data. BMC Genomics, 4, 27
34. MacCoss, M.J. et al. (2002) Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl Acad. Sci. USA, 99, 7900-7905.
35. Mahtani, K.R., Brook, M., Dean, J.L., Sully, G., Saklatvala, J. and Clark, A.R. (2001) Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor α mRNA stability. Mol. Cell. Biol., 21, 6461-6469.
36. Martindale, J.L. and Holbrook, N.J. (2002) Cellular response to oxidative stress: signaling for suicide and survival. J. Cell. Physiol., 192, 1-15.
37. Millar, J.B., Buck, V. and Wilkinson, M.G. (1995) Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev., 9, 2117-2130.
38. Ming, X.F., Stoecklin, G., Lu, M., Looser, R. and Moroni, C. (2001) Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol. Cell. Biol., 21, 5778-5789.
39. Mitchell, P. and Tollervey, D. (2000) mRNA stability in eukaryotes. Curr. Opin. Genet. Dev., 10, 193-198.
40. Moreno, S., Klar, A. and Nurse, P. (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 795-823.
41. Mukherjee, D., Gao, M., O'Connor, J.P., Raijmakers, R., Pruijn, G., Lutz, C.S. and Wilusz, J. (2002) The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J., 21, 165-174.
42. Nguyen, A.N., Lee, A., Place, W. and Shiozaki, K. (2000) Multistep phosphorelay proteins transmit oxidative stress signals to the fission yeast stress-activated protein kinase. Mol. Biol. Cell, 11, 1169-1181.
43. Parker, R., Herrick, D., Peltz, S.W. and Jacobson, A. (1991) Measurement of mRNA decay rates in Saccharomyces cerevisiae. Methods Enzymol., 194, 415-423.
44. Piecyk, M. et al. (2000) TIA-1 is a translational silencer that selectively regulates the expression of TNF-α. EMBO J., 19, 4154-4163.
45. 2 levels in fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell, 13, 805-816.
46. Robinson, M.J. and Cobb, M.H. (1997) Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol., 9, 180-186.
47. Saitoh, S., Takahashi, K., Nabeshima, K., Yamashita, Y., Nakaseko, Y., Hirata, A. and Yanagida, M. (1996) Aberrant mitosis in fission yeast mutants defective in fatty acid synthetase and acetyl CoA carboxylase. J. Cell Biol., 134, 949-961.
48. Saitoh, S., Chabes, A., McDonald, W.H., Thelander, L., Yates, J.R. and Russell, P. (2002) Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell, 109, 563-573.
49. Samejima, I., Mackie, S. and Fantes, P.A. (1997) Multiple modes of activation of the stress-responsive MAP kinase pathway in fission yeast. EMBO J., 16, 6162-6170.
50. Shieh, J.C., Wilkinson, M.G., Buck, V., Morgan, B.A., Makino, K. and Millar, J.B. (1997) The Mcs4 response regulator coordinately controls the stress-activated Wak1-Wis1-Sty1 MAP kinase pathway and fission yeast cell cycle. Genes Dev., 11, 1008-1022.
51. Shieh, J.C., Wilkinson, M.G. and Millar, J.B. (1998) The Win1 mitotic regulator is a component of the fission yeast stress-activated Sty1 MAPK pathway. Mol. Biol. Cell, 9, 311-322.
52. Shiozaki, K. and Russell, P. (1995) Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast. Nature, 378, 739-743.
53. Shiozaki, K. and Russell, P. (1996) Conjugation, meiosis and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev., 10, 2276-2288.
54. Shiozaki, K., Shiozaki, M. and Russell, P. (1997) Mcs4 mitotic catastrophe suppressor regulates the fission yeast cell cycle through the Wik1-Wis1-Spc1 kinase cascade. Mol. Biol. Cell, 8, 409-419.
55. Shiozaki, K., Shiozaki, M. and Russell, P. (1998) Heat stress activates fission yeast Spc1/StyI MAPK by a MEKK-independent mechanism. Mol. Biol. Cell, 9, 1339-1349.
56. Stoecklin, G., Stoeckle, P., Lu, M., Muehlemann, O. and Moroni, C. (2001) Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements. RNA, 7, 1578-1588.
57. Sugiura, R., Kita, A., Shimizu, Y., Shuntoh, H., Sio, S.O. and Kuno, T. (2003) Feedback regulation of MAPK signalling by an RNA-binding protein. Nature, 424, 961-965.
58. + encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J., 14, 6193-6208.
59. Tanaka, K. and Russell, P. (2001) Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nature Cell Biol., 3, 966-972.
60. Toda, T., Shimanuki, M. and Yanagida, M. (1991) Fission yeast genes that confer resistance to staurosporine encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev., 5, 60-73.
61. Toone, W.M., Kuge, S., Samuels, M., Morgan, B.A., Toda, T. and Jones, N. (1998) Regulation of the fission yeast transcription factor Pap1 by oxidative stress: requirement for the nuclear export factor Crm1 (exportin) and the stress-activated MAP kinase Sty1/Spc1. Genes Dev., 12, 1453-1463.
62. vanDam, 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.
63. Vasudevan, S. and Peltz, S.W. (2001) Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol. Cell, 7, 1191-1200.
64. Wang, W., Fumeaux, H., Cheng, H., Caldwell, M.C., Hutter, D., Liu, Y., Holbrook, N. and Gorospe, M. (2000) HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol., 20, 760-769.
65. Wang, Y., Liu, C.L., Storey, J.D., Tibshirani, R.J., Herschlag, D. and Brown, P.O. (2002) Precision and functional specificity in mRNA decay. Proc. Natl Acad. Sci. USA, 99, 5860.
66. Widmann, C., Gibson, S., Jarpe, M.B. and Johnson, G.L. (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev., 79, 143-180.
67. Wilkinson, M.G., Samuels, M., Takeda, T., Toone, W.M., Shieh, J.C., Toda, T., Millar, J.B. and Jones, N. (1996) The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev., 10, 2289-2301.
68. Wilusz, C.J., Wormington, M. and Peltz, S.W. (2001) The cap-to-tail guide to mRNA turnover. Nature Rev. Mol. Cell. Biol., 2, 237-246.
69. Winzen, R. et al. (1999) The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J., 18, 4969-4980.
70. Yang, C., Maiguel, D.A. and Carrier, F. (2002) Identification of nucleolin and nucleophosmin as genotoxic stress-responsive RNA-binding proteins. Nucleic Acids Res., 30, 2251-2260.
71. Zhang, W., Wagner, B.J., Ehrenman, K., Schaefer, A.W., DeMaria, C.T., Crater, D., DeHaven, K., Long, L. and Brewer, G. (1993) Purification, characterization and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol., 13, 7652-7665.