Phenyl hydroquinone, an Ames test-negative carcinogen, induces Hog1-dependent stress response signaling: Implication for aneuploidy development in Saccharomyces cerevisiae

FEBS Journal

Volumn 275, Issue 22, 2008, Pages 5733-5744

  Yamamoto, Ayumi ^a   Nunoshiba, Tatsuo ^a   Umezu, Keiko ^b   Enomoto, Takemi ^a   Yamamoto, Kazuo ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b FUKUOKA DENTAL COLLEGE   (Japan)

Author keywords

Aneuploidy; Checkpoint; G2 M transition; MAPK; Phenyl hydroquinone

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE P38; PHENYLHYDROQUINONE;

AMES TEST; ANEUPLOIDY; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ANEUPLOIDY; BIPHENYL COMPOUNDS; CARCINOGENS; CELL CYCLE; CELL CYCLE PROTEINS; G2 PHASE; HYDROQUINONES; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

SACCHAROMYCES CEREVISIAE;

EID: 54849438701     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06700.x     Document Type: Article

References (59)

1. Brusick D (2005) Analysis of genotoxicity and the carcinogenic mode of action for ortho-phenylphenol. Environ Mol Mutagen 45, 460 481.
2. Hiraga K Fujii T (1984) Induction of tumours of the urinary bladder in F344 rats by dietary administration of o-phenylphenol. Food Chem Toxicol 22, 865 870.
3. Nunoshiba T, Watanabe E, Takahashi T, Daigaku Y, Ishikawa S, Mochizuki M, Ui A, Enomoto T Yamamoto K (2007) Ames test-negative carcinogen, ortho-phenyl phenol, binds tubulin and causes aneuploidy in budding yeast. Mutat Res 617, 90 97.
4. Hassold TJ Jacobs PA (1984) Trisomy in man. Annu Rev Genet 18, 69 97.
5. Hoyt MA, Stearns T Botstein D (1990) Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes. Mol Cell Biol 10, 223 234.
6. Kouprina N, Tsouladze A, Koryabin M, Hieter P, Spencer F Larionov V (1993) Identification and genetic mapping of CHL genes controlling mitotic chromosome transmission in yeast. Yeast 9, 11 19.
7. Maine GT, Sinha P Tye BK (1984) Mutants of S. cerevisiae defective in the maintenance of minichromosomes. Genetics 106, 365 385.
8. Spencer F, Gerring SL, Connelly C Hieter P (1990) Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124, 237 249.
9. Xiao Z, McGrew JT, Schroeder AJ Fitzgerald-Hayes M (1993) CSE1 and CSE2, two new genes required for accurate mitotic chromosome segregation in Saccharomyces cerevisiae. Mol Cell Biol 13, 4691 4702.
10. Boulet A, Simon M, Faye G, Bauer GA Burgers PM (1989) Structure and function of the Saccharomyces cerevisiae CDC2 gene encoding the large subunit of DNA polymerase III. EMBO J 8, 1849 1854.
11. Hartwell LH Smith D (1985) Altered fidelity of mitotic chromosome transmission in cell cycle mutants of S. cerevisiae. Genetics 110, 381 395.
12. Burke D, Gasdaska P Hartwell L (1989) Dominant effects of tubulin overexpression in Saccharomyces cerevisiae. Mol Cell Biol 9, 1049 1059.
13. Doheny KF, Sorger PK, Hyman AA, Tugendreich S, Spencer F Hieter P (1993) Identification of essential components of the S. cerevisiae kinetochore. Cell 73, 761 774.
14. Hoyt MA, He L, Totis L Saunders WS (1993) Loss of function of Saccharomyces cerevisiae kinesin-related CIN8 and KIP1 is suppressed by KAR3 motor domain mutations. Genetics 135, 35 44.
15. Snyder M Davis RW (1988) SPA1: a gene important for chromosome segregation and other mitotic functions in S. cerevisiae. Cell 54, 743 754.
16. Hoyt MA, Totis L Roberts BT (1991) S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function. Cell 66, 507 517.
17. Li R Murray AW (1991) Feedback control of mitosis in budding yeast. Cell 66, 519 531.
18. Yamamoto A, Guacci V Koshland D (1996) Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae. J Cell Biol 133, 85 97.
19. Lew DJ (2000) Cell-cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae. Curr Opin Genet Dev 10, 47 53.
20. Lew DJ Reed SI (1995) A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J Cell Biol 129, 739 749.
21. Booher RN, Deshaies RJ Kirschner MW (1993) Properties of Saccharomyces cerevisiae wee1 and its differential regulation of p34CDC28 in response to G1 and G2 cyclins. EMBO J 12, 3417 3426.
22. Clotet J, Escoté X, Adrover MA, Yaakov G, Garí E, Aldea M, de Nadal E Posas F (2006) Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. EMBO J 25, 2338 2346.
23. Sia RA, Herald HA Lew DJ (1996) Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol Biol Cell 7, 1657 1666.
24. Shulewitz MJ, Inouye CJ Thorner J (1999) Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol Cell Biol 19, 7123 7137.
25. Kaiser P, Sia RA, Bardes EG, Lew DJ Reed SI (1998) Cdc34 and the F-box protein Met30 are required for degradation of the Cdk-inhibitory kinase Swe1. Genes Dev 12, 2587 2597.
26. Sia RA, Bardes ES Lew DJ (1998) Control of Swe1p degradation by the morphogenesis checkpoint. EMBO J 17, 6678 6688.
27. Thornton BR Toczyski DP (2003) Securin and B-cyclin/CDK are the only essential targets of the APC. Nat Cell Biol 5, 1090 1104.
28. Boutros R, Dozier C Ducommun B (2006) The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol 18, 185 191.
29. Enserink JM, Smolka MB, Zhou H Kolodner RD (2006) Checkpoint proteins control morphogenetic events during DNA replication stress in Saccharomyces cerevisiae. J Cell Biol 175, 729 741.
30. Hiraoka M, Watanabe K, Umezu K Maki H (2000) Spontaneous loss of heterozygosity in diploid Saccharomyces cerevisiae cells. Genetics 156, 1531 1548.
31. Alexander MR, Tyers M, Perret M, Craig BM, Fang KS Gustin MC (2001) Regulation of cell cycle progression by Swe1p and Hog1p following hypertonic stress. Mol Biol Cell 12, 53 62.
32. Bellí G, Garí E, Aldea M Herrero E (2001) Osmotic stress causes a G1 cell cycle delay and downregulation of Cln3/Cdc28 activity in Saccharomyces cerevisiae. Mol Microbiol 39, 1022 1035.
33. de Nadal E, Alepuz PM Posas F (2002) Dealing with osmostress through MAP kinase activation. EMBO Rep 3, 735 740.
34. Mendenhall MD Hodge AE (1998) Regulation of Cdc28 cyclin-dependent protein kinase activity during the cell cycle of the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62, 1191 1243.
35. Sreenivasan A Kellogg D (1999) The Elm1 kinase functions in a mitotic signaling network in budding yeast. Mol Cell Biol 19, 7983 7994.
36. McMillan JN, Theesfeld CL, Harrison JC, Bardes ES Lew DJ (2002) Determinants of Swe1p degradation in Saccharomyces cerevisiae. Mol Biol Cell 13, 3560 3575.
37. Barral Y, Parra M, Bidlingmaier S Snyder M (1999) Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev 13, 176 187.
38. McMillan JN, Longtine MS, Sia RA, Theesfeld CL, Bardes ES, Pringle JR Lew DJ (1999) The morphogenesis checkpoint in Saccharomyces cerevisiae: cell cycle control of Swe1p degradation by Hsl1p and Hsl7p. Mol Cell Biol 19, 6929 6939.
39. Lew DJ (2003) The morphogenesis checkpoint: how yeast cells watch their figures. Curr Opin Cell Biol 15, 648 653.
40. Kawasaki Y, Nagao K, Nakamura T Yanagida M (2006) Fission yeast MAP kinase is required for the increased securin-separase interaction that rescues separase mutants under stresses. Cell Cycle 5, 1831 1839.
41. McGowan CH Russell P (2004) The DNA damage response: sensing and signaling. Curr Opin Cell Biol 16, 629 633.
42. Reitz RH, Fox TR, Quast JF, Hermann EA Watanabe PG (1983) Molecular mechanisms involved in the toxicity of orthophenylphenol and its sodium salt. Chem Biol Interact 43, 99 119.
43. Murata M, Moriya K, Inoue S Kawanishi S (1990) Oxidative damage to cellular and isolated DNA by metabolites of a fungicide ortho-phenylphenol. Carcinogenesis 20, 851 857.
44. Tayama S Nakagawa Y (1994) Effect of scavengers of active oxygen species on cell damage caused in CHO-K1 cells by phenylhydroquinone, an o-phenylphenol metabolite. Mutat Res 324, 121 131.
45. Ochiai N, Fujimura M, Oshima M, Motoyama T, Ichiishi A, Yamada-Okabe H Yamaguchi I (2002) Effects of iprodione and fludioxonil on glycerol synthesis and hyphal development in Candida albicans. Biosci Biotechnol Biochem 66, 2209 2215.
46. Zhang Y, Lamm R, Pillonel C, Lam S Xu JR (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68, 532 538.
47. Escote X, Zapater M, Clotet J Posas F (2004) Hog1 mediates cell-cycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6, 997 1002.
48. Winkler A, Arkind C, Mattison CP, Burkholder A, Knoche K Ota I (2002) Heat stress activates the yeast high-osmolarity glycerol mitogen-activated protein kinase pathway, and protein tyrosine phosphatases are essential under heat stress. Eukaryot Cell 1, 163 173.
49. Bilsland E, Molin C, Swaminathan S, Ramne A Sunnerhagen P (2004) Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol 53, 1743 1756.
50. Marques JM, Rodrigues RJ, de Magalhães-Sant'ana AC Gonçalves T (2006) Saccharomyces cerevisiae Hog1 protein phosphorylation upon exposure to bacterial endotoxin. J Biol Chem 281, 24687 24694.
51. Lawrence CL, Botting CH, Antrobus R Coote PJ (2004) Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol 24, 3307 3323.
52. Posas F Saito H (1998) Activation of the yeast SSK2 MAP kinase kinase kinase by the SSK1 two-component response regulator. EMBO J 17, 1385 1394.
53. Maeda T, Wurgler-Murphy SM Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242 245.
54. Duesberg P Rasnick D (2000) Aneuploidy, the somatic mutation that makes cancer a species of its own. Cell Motil Cytoskeleton 47, 81 107.
55. Wach A, Brachat A, Pöhlmann R Philippsen P (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793 1808.
56. Longtine MS, McKenzie A III., Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P Pringle JR (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953 961.
57. Daigaku Y, Endo K, Watanabe E, Ono T Yamamoto K (2004) Loss of heterozygosity and DNA damage repair in Saccharomyces cerevisiae. Mutat Res 556, 183 191.
58. Ohnishi G, Endo K, Doi A, Fujita A, Daigaku Y, Nunoshiba T Yamamoto K (2004) Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae. Biochem Biophys Res Commun 325, 928 933.
59. Araki Y, Kawasaki Y, Sasanuma H, Tye BK Sugino A (2003) Budding yeast mcm10/dna43 mutant requires a novel repair pathway for viability. Genes Cells 8, 183 191.