Crossref journal-article
Cold Spring Harbor Laboratory
Genes & Development (246)
Abstract

The fission yeast Sty1 stress-activated MAP kinase is crucial for the cellular response to a variety of stress conditions. Accordingly,sty1− cells are defective in their response to nutrient limitation, lose viability in stationary phase, and are hypersensitive to osmotic stress, oxidative stress, and UV treatment. Some of these phenotypes are caused by Sty1-dependent regulation of the Atf1 transcription factor, which controls both meiosis-specific and osmotic stress-responsive genes. However, in this report we demonstrate that the cellular response to oxidative stress and to treatment with a variety of cytotoxic agents is the result of Sty1 regulation of the Pap1 transcription factor, a bZip protein with structural and DNA binding similarities to the mammalian c-Jun protein. We show that both Sty1 and Pap1 are required for the expression of a number of genes involved in the oxidative stress response and for the expression of two genes, hba2+/bfr1+ andpmd1+, which encode energy-dependent transport proteins involved in multidrug resistance. Furthermore, we demonstrate that Pap1 is regulated by stress-dependent changes in subcellular localization. On imposition of oxidative stress, the Pap1 protein relocalizes from the cytoplasm to the nucleus in a process that is dependent on the Sty1 kinase. This relocalization is the result of regulated protein export, rather than import, and involves the Crm1 (exportin) nuclear export factor and the dcd1+/pim1+ gene that encodes an Ran nucleotide exchange factor.

Bibliography

Toone, W. M., Kuge, S., Samuels, M., Morgan, B. A., Toda, T., & 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 & Development, 12(10), 1453–1463.

Authors 6
  1. W. Mark Toone (first)
  2. Shusuke Kuge (additional)
  3. Michael Samuels (additional)
  4. Brian A. Morgan (additional)
  5. Takashi Toda (additional)
  6. Nic Jones (additional)
References 71 Referenced 247
  1. 10.1083/jcb.108.4.1195
  2. Alfa C. Fantes P. Hyams J. McLeod M. Warbrick E. (1993) Experiments with fission yeast. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y).
  3. 10.1146/annurev.iy.12.040194.001041 / Annu. Rev. Immunol. / Function and activation of NFκB in the immune system. by Baeuerle (1994)
  4. 10.1126/science.7681220
  5. 10.1007/BF02172398
  6. 10.1016/S0021-9258(19)40219-6 / J. Biol. Chem. / Heat shock and arsenite increase expression of the multidrug resistance (MDR1) gene in human renal carcinoma cells. by Chin (1990)
  7. 10.1016/S0962-8924(97)01105-7 / Trends Cell Biol. / The search for physiological substrates of MAP and SAP kinases in mammalian cells. by Cohen (1997)
  8. 10.1128/MCB.17.6.3356 / Mol. Cell Biol. / Discrete roles of the Spc1 kinase and the Atf1 transcription factor in the UV response of Schizosaccharomyces pombe. by Degols (1997)
  9. 10.1128/MCB.16.6.2870 / Mol. Cell Biol. / Activation and regulation of the Spc1 stress- activated protein kinase in Schizosaccharomyces pombe. by Degols (1996)
  10. 10.1016/0092-8674(94)90380-8
  11. 10.1111/j.1432-1033.1992.tb17363.x / Eur. J. Biochem. / Thioredoxin regenerates proteins inactivated by oxidative stress in endothelial cells. by Fernando (1992)
  12. 10.1016/S0092-8674(00)80371-2
  13. 10.1038/36894
  14. Gaits, F.,G. Degols, K. Shiozaki, and P. Russell. 1998. Phosphorylation and association with the transcription factor Atf1 regulate localization of the Sty1/Spc1 stress-activated kinase in fission yeast. Genes & Dev. (this issue).. (10.1101/gad.12.10.1464)
  15. 10.1083/jcb.138.1.65
  16. 10.1146/annurev.bi.62.070193.002125
  17. 10.1126/science.7824938
  18. 10.1101/gad.7.11.2135
  19. 10.1046/j.1365-2443.1996.d01-247.x
  20. 10.1016/S0955-0674(97)80068-3
  21. 10.1016/0014-5793(95)01442-X
  22. 10.1083/jcb.133.6.1163
  23. 10.1002/j.1460-2075.1994.tb06304.x / EMBO J. / YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. by Kuge (1994)
  24. 10.1093/emboj/16.7.1710
  25. {'key': '2021111418531610000_12.10.1453.25', 'first-page': '59', 'article-title': 'Caffeine-resistance in fission yeast is caused by mutations in a single essential gene, crm1\n +.', 'volume': '250', 'author': 'Kumada', 'year': '1996', 'journal-title': 'Mol. Gen. Genet.'} / Mol. Gen. Genet. / Caffeine-resistance in fission yeast is caused by mutations in a single essential gene, crm1 +. by Kumada (1996)
  26. 10.1002/bies.950180708
  27. 10.1038/369156a0
  28. 10.1002/j.1460-2075.1995.tb07167.x / EMBO J. / ATF-2 contains a phosphorylation-dependent transcriptional activation domain by Livingstone (1995)
  29. 10.1016/0959-437X(94)90095-7
  30. 10.1016/0092-8674(91)90624-8
  31. 10.1016/0378-1119(93)90551-D
  32. 10.1002/j.1460-2075.1992.tb05601.x / EMBO J. / Negative regulation of mitosis by two functionally overlapping PTPases in fission yeast. by Millar (1992)
  33. 10.1101/gad.9.17.2117
  34. 10.1016/S0006-291X(05)81536-0
  35. 10.1016/0092-8674(91)90118-I
  36. 10.1016/0076-6879(91)94059-L
  37. 10.1093/emboj/16.5.1035
  38. 10.1128/jb.177.6.1536-1543.1995 / J. Bacteriol. / bfr1 +, a novel gene of Schizosaccharomyces pombe which confers brefeldin-a resistance, is structurally related to the ATP-binding cassette superfamily. by Nagao (1995)
  39. 10.1093/oxfordjournals.jbchem.a124864 / J. Biochem. / Transcriptional regulation of the catalase gene in the fission yeast Schizosaccharomyces pombe: Molecular cloning of the catalase gene and northern blot of the transcript. by Nakagawa (1995)
  40. 10.1172/JCI117768 / J. Clin. Invest. / Cross-resistance between cisplatin, antimony potassium tartrate, and arsenite in human tumor cells. by Naredi (1995)
  41. 10.1016/S0960-9822(06)00335-6
  42. 10.1038/386779a0
  43. 10.1111/j.1365-2958.1992.tb01526.x
  44. 10.1016/S0168-9525(97)01320-6
  45. 10.1126/science.274.5285.209
  46. 10.1126/science.278.5335.141
  47. 10.1074/jbc.272.22.14041
  48. 10.1074/jbc.270.13.7420
  49. 10.1101/gad.11.13.1717
  50. 10.1093/emboj/16.10.2634
  51. 10.1002/j.1460-2075.1994.tb06298.x / EMBO J. / A fission yeast RCC1-related protein is required for the mitosis to interphase transition. by Sazer (1994)
  52. 10.1038/378739a0
  53. 10.1101/gad.10.18.2276
  54. 10.1242/jcs.108.2.569 / J. Cell Sci. / A novel essential fission yeast gene pad1 + positively regulates pap1 +-dependent transcription and is implicated in the maintenance of chromosome structure. by Shimanuki (1995)
  55. 10.1101/gad.10.21.2745
  56. 10.1074/jbc.272.48.30470
  57. 10.1016/S0092-8674(00)80370-0
  58. 10.1002/j.1460-2075.1995.tb00310.x / EMBO J. / Schizosaccharomyces pombe atf1 + encodes a transcription factor required for sexual development and entry into stationary phase. by Takeda (1995)
  59. 10.1101/gad.5.1.60
  60. {'key': '2021111418531610000_12.10.1453.60', 'first-page': '5474', 'article-title': 'Fission yeast pap1-dependent transcription is negatively regulated by an essential nuclear protein, Crm1.', 'volume': '12', 'author': 'Toda', 'year': '1992', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Fission yeast pap1-dependent transcription is negatively regulated by an essential nuclear protein, Crm1. by Toda (1992)
  61. 10.1016/S0955-0674(96)80067-6
  62. 10.1006/bbrc.1995.2147
  63. 10.1074/jbc.271.15.9166
  64. {'key': '2021111418531610000_12.10.1453.64', 'first-page': '147', 'article-title': 'Enhanced expression of the human multidrug resistance 1 gene in response to UV light irradiation.', 'volume': '4', 'author': 'Uchiumi', 'year': '1993', 'journal-title': 'Cell Growth & Differ.'} / Cell Growth & Differ. / Enhanced expression of the human multidrug resistance 1 gene in response to UV light irradiation. by Uchiumi (1993)
  65. 10.1016/S0021-9258(18)45397-5 / J. Biol. Chem. / Isolation and sequence of the promoter region of the human multidrug resistance (P-glycoprotein) gene. by Ueda (1987)
  66. 10.1002/j.1460-2075.1995.tb07168.x / EMBO J. / ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. by van Dam (1995)
  67. 10.1002/j.1460-2075.1991.tb05007.x / EMBO J. / The Wis1 protein kinase is a dose-dependent regulator of mitosis in Schizosaccharomyces pombe. by Warbrick (1991)
  68. 10.1016/0955-0674(95)80063-8
  69. 10.1002/j.1460-2075.1986.tb04414.x / EMBO J. / Periodic transcription as a means of regulating gene expression during the cell cycle: Contrasting modes of expression of DNA ligase genes in budding and fission yeast. by White (1986)
  70. 10.1101/gad.10.18.2289
  71. 10.1016/S0968-0004(00)89095-7
Dates
Type When
Created 17 years, 6 months ago (Feb. 20, 2008, 5:52 p.m.)
Deposited 3 years, 9 months ago (Nov. 14, 2021, 10:13 p.m.)
Indexed 2 days, 12 hours ago (Aug. 24, 2025, 6:53 p.m.)
Issued 27 years, 3 months ago (May 15, 1998)
Published 27 years, 3 months ago (May 15, 1998)
Published Online 27 years, 3 months ago (May 15, 1998)
Published Print 27 years, 3 months ago (May 15, 1998)
Funders 0

None

@article{Toone_1998, title={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}, volume={12}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.12.10.1453}, DOI={10.1101/gad.12.10.1453}, number={10}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Toone, W. Mark and Kuge, Shusuke and Samuels, Michael and Morgan, Brian A. and Toda, Takashi and Jones, Nic}, year={1998}, month=may, pages={1453–1463} }