Reactive oxygen species and yeast apoptosis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 7, 2008, Pages 1354-1368

  Perrone, Gabriel G ^a   Tan, Shi Xiong ^a   Dawes, Ian W ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Actin; Apoptosis; Endoplasmic reticulum; Mitochondria; Oxidative stress; Programmed cell death; Reactive oxygen species; Saccharomyces cerevisiae; Stress responses; Yeast

Indexed keywords

ACTIN; ALLOGRAFT INFLAMMATORY FACTOR 1; METAL; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; CELL DAMAGE; CELL DEATH; CELL DISRUPTION; CELL FUNCTION; CELL STRUCTURE; CYTOSKELETON; DEFENSE MECHANISM; ENDOPLASMIC RETICULUM STRESS; MITOCHONDRION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SACCHAROMYCES CEREVISIAE; YEAST;

ACTINS; ANTIOXIDANTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CYTOSKELETON; DNA DAMAGE; ENDOPLASMIC RETICULUM; METALS; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 46549088173     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.01.023     Document Type: Review

References (179)

1. Temple M.D., Perrone G.G., and Dawes I.W. Complex cellular responses to reactive oxygen species. Trends Cell Biol. 15 (2005) 319-326
2. Collinson L.P., and Dawes I.W. Inducibility of the response of yeast cells to peroxide stress. J. Gen. Microbiol. 138 (1992) 329-335
3. Jamieson D.J. Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione. J. Bacteriol. 174 (1992) 6678-6681
4. Gasch A.P., Spellman P.T., Kao C.M., Carmel-Harel O., Eisen M.B., Storz G., Botstein D., and Brown P.O. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11 (2000) 4241-4257
5. Flattery-O'Brien J.A., and Dawes I.W. Hydrogen peroxide causes RAD9-dependent cell cycle arrest in G2 in Saccharomyces cerevisiae whereas menadione causes G1 arrest independent of RAD9 function. J. Biol. Chem. 273 (1998) 8564-8571
6. Lee J., Romeo A., and Kosman D.J. Transcriptional remodeling and G1 arrest in dioxygen stress in Saccharomyces cerevisiae. J. Biol. Chem. 271 (1996) 24885-24893
7. Fabrizio P., Battistella L., Vardavas R., Gattazzo C., Liou L.L., Diaspro A., Dossen J.W., Gralla E.B., and Longo V.D. Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J. Cell Biol. 166 (2004) 1055-1067
8. Laun P., Pichova A., Madeo F., Fuchs J., Ellinger A., Kohlwein S., Dawes I., Frohlich K.U., and Breitenbach M. Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol. Microbiol. 39 (2001) 1166-1173
9. Breitenbach M., Laun P., Heeren G., Jarolim S., and Pichova A. Mother cell-specific ageing. In: Dickinson J.R., and Schweizer M. (Eds). The Metabolism and Molecular Physiology of Saccharomyces cerevisiae (2004), CRC, Boca Raton 20-41
10. Longo V.D., Mitteldorf J., and Skulachev V.P. Programmed and altruistic ageing. Nat. Rev. Genet. 6 (2005) 866-872
11. Madeo F., Frohlich E., and Frohlich K.U. A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell Biol. 139 (1997) 729-734
12. Madeo F., Frohlich E., Ligr M., Grey M., Sigrist S.J., Wolf D.H., and Frohlich K.U. Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145 (1999) 757-767
13. Wadskog I., Maldener C., Proksch A., Madeo F., and Adler L. Yeast lacking the SRO7/SOP1-encoded tumor suppressor homologue show increased susceptibility to apoptosis-like cell death on exposure to NaCl stress. Mol. Biol. Cell 15 (2004) 1436-1444
14. Ludovico P., Sousa M.J., Silva M.T., Leao C., and Corte-Real M. Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147 (2001) 2409-2415
15. King D.A., Hannum D.M., Qi J.S., and Hurst J.K. HOCl-mediated cell death and metabolic dysfunction in the yeast Saccharomyces cerevisiae. Arch. Biochem. Biophys. 423 (2004) 170-181
16. Granot D., Levine A., and Dor-Hefetz E. Sugar-induced apoptosis in yeast cells. FEMS Yeast Res. 4 (2003) 7-13
17. Herker E., Jungwirth H., Lehmann K.A., Maldener C., Frohlich K.U., Wissing S., Buttner S., Fehr M., Sigrist S., and Madeo F. Chronological aging leads to apoptosis in yeast. J. Cell Biol. 164 (2004) 501-507
18. Mazzoni C., Mancini P., Madeo F., Palermo V., and Falcone C. A Kluyveromyces lactis mutant in the essential gene KlLSM4 shows phenotypic markers of apoptosis. FEMS Yeast. Res. 4 (2003) 29-35
19. Mazzoni C., Mancini P., Verdone L., Madeo F., Serafini A., Herker E., and Falcone C. A truncated form of KlLsm4p and the absence of factors involved in mRNA decapping trigger apoptosis in yeast. Mol. Biol. Cell 14 (2003) 721-729
20. Phillips A.J., Sudbery I., and Ramsdale M. Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 14327-14332
21. Zhang Q., Chieu H.K., Low C.P., Zhang S., Heng C.K., and Yang H. Schizosaccharomyces pombe cells deficient in triacylglycerols synthesis undergo apoptosis upon entry into the stationary phase. J. Biol. Chem. 278 (2003) 47145-47155
22. Poliakova D., Sokolikova B., Kolarov J., and Sabova L. The antiapoptotic protein Bcl-x(L) prevents the cytotoxic effect of Bax, but not Bax-induced formation of reactive oxygen species, in Kluyveromyces lactis. Microbiology 148 (2002) 2789-2795
23. Thorpe G.W., Fong C.S., Alic N., Higgins V.J., and Dawes I.W. Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 6564-6569
24. Halliwell B., and Gutteridge J.M. Lipid peroxidation, oxygen radicals, cell damage, and antioxidant therapy. Lancet 1 (1984) 1396-1397
25. Halliwell B. Free radicals and metal ions in health and disease. Proc. Nutr. Soc. 46 (1987) 13-26
26. Dawes I.W. Yeast stress responses. In: Dickinson J.R., and Schweizer M. (Eds). The Metabolism and Molecular Physiology of Saccharomyces cerevisiae (2004), CRC Press, Boca Raton 376-438
27. Bouveris A., and Cadenas E. Production of superoxide radicals and hydrogen peroxide in mitochondria. In: Oberely L.W. (Ed). Superoxide Dismutases (1982), CRC press, Boca Raton, Florida 15-30
28. Gardner P.R., and Fridovich I. Superoxide sensitivity of the Escherichia coli aconitase. J. Biol. Chem. 266 (1991) 19328-19333
29. Halliwell B., and Gutteridge J.M. Free Radicals in Biology and Medicine. 4th (2007), Oxford University press, Oxford
30. Gross E., Sevier C.S., Heldman N., Vitu E., Bentzur M., Kaiser C.A., Thorpe C., and Fass D. Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 299-304
31. Tu B.P., Ho-Schleyer S.C., Travers K.J., and Weissman J.S. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290 (2000) 1571-1574
32. Tu B.P., and Weissman J.S. Oxidative protein folding in eukaryotes: mechanisms and consequences. J. Cell Biol. 164 (2004) 341-346
33. Halliwell B., and Aruoma O.I. DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett. 281 (1991) 9-19
34. Halliwell B. The biological significant of oxygen-derived species. In: Valentine J.S., Foote C.S., Greenberg A., and Liebman J.F. (Eds). Active Oxygen in Biochemistry (1995), Blackie Academic and Professional, Glasgow 313-335
35. Buchczyk D.P., Briviba K., Hartl F.U., and Sies H. Responses to peroxynitrite in yeast: glyceraldehyde-3-phosphate dehydrogenase (GAPDH) as a sensitive intracellular target for nitration and enhancement of chaperone expression and ubiquitination. Biol. Chem. 381 (2000) 121-126
36. Castello P.R., David P.S., McClure T., Crook Z., and Poyton R.O. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell. Metab. 3 (2006) 277-287
37. Almeida B., Buttner S., Ohlmeier S., Silva A., Mesquita A., Sampaio-Marques B., Osorio N.S., Kollau A., Mayer B., Leao C., Laranjinha J., Rodrigues F., Madeo F., and Ludovico P. NO-mediated apoptosis in yeast. J. Cell Sci. 120 (2007) 3279-3288
38. Evans M.V., Turton H.E., Grant C.M., and Dawes I.W. Toxicity of linoleic acid hydroperoxide to Saccharomyces cerevisiae: involvement of a respiration-related process for maximal sensitivity and adaptive response. J. Bacteriol. 180 (1998) 483-490
39. Gunstone F.D. Fatty Acid and Lipid Chemistry (1996), Blackie Academic and Professional, London
40. Requena J.R., Levine R.L., and Stadtman E.R. Recent advances in the analysis of oxidized proteins. Amino Acids 25 (2003) 221-226
41. Aguilaniu H., Gustafsson L., Rigoulet M., and Nystrom T. Protein oxidation in G0 cells of Saccharomyces cerevisiae depends on the state rather than rate of respiration and is enhanced in pos9 but not yap1 mutants. J. Biol. Chem. 276 (2001) 35396-35404
42. Aguilaniu H., Gustafsson L., Rigoulet M., and Nystrom T. Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299 (2003) 1751-1753
43. Santoro N., and Thiele D.J. Oxidative stress responses in the yeast. In: Mager S.H.W.H. (Ed). Yeast Stress Responses (1997), Springer 171-211
44. Jamieson D.J. Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14 (1998) 1511-1527
45. Le Moan N., Clement G., Le Maout S., Tacnet F., and Toledano M.B. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J. Biol. Chem. 281 (2006) 10420-10430
46. Shenton D., and Grant C.M. Protein S-thiolation targets glycolysis and protein synthesis in response to oxidative stress in the yeast Saccharomyces cerevisiae. Biochem. J. 374 (2003) 513-519
47. Cabiscol E., Piulats E., Echave P., Herrero E., and Ros J. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem. 275 (2000) 27393-27398
48. Costa V.M., Amorim M.A., Quintanilha A., and Moradas-Ferreira P. Hydrogen peroxide-induced carbonylation of key metabolic enzymes in Saccharomyces cerevisiae: the involvement of the oxidative stress response regulators Yap1 and Skn7. Free Radic. Biol. Med. 33 (2002) 1507-1515
49. Erjavec N., Larsson L., Grantham J., and Nystrom T. Accelerated aging and failure to segregate damaged proteins in Sir2 mutants can be suppressed by overproducing the protein aggregation-remodeling factor Hsp104p. Genes Dev. 21 (2007) 2410-2421
50. Reverter-Branchat G., Cabiscol E., Tamarit J., and Ros J. Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae: common targets and prevention by calorie restriction. J. Biol. Chem. 279 (2004) 31983-31989
51. Wolff S.P., and Dean R.T. Fragmentation of proteins by free radicals and its effect on their susceptibility to enzymic hydrolysis. Biochem. J. 234 (1986) 399-403
52. Stadtman E.R. Protein oxidation and aging. Science 257 (1992) 1220-1224
53. Gebicki S., Gill K.H., Dean R.T., and Gebicki J.M. Action of peroxidases on protein hydroperoxides. Redox Rep. 7 (2002) 235-242
54. Aeschbach R., Amado R., and Neukom H. Formation of dityrosine cross-links in proteins by oxidation of tyrosine residues. Biochim. Biophys. Acta 439 (1976) 292-301
55. Fu S., Hick L.A., Sheil M.M., and Dean R.T. Structural identification of valine hydroperoxides and hydroxides on radical-damaged amino acid, peptide, and protein molecules. Free Radic. Biol. Med. 19 (1995) 281-292
56. Ames B.N., and Gold L.S. Endogenous mutagens and the causes of aging and cancer. Mutat. Res. 250 (1991) 3-16
57. Lafleur M.V., and Retel J. Contrasting effects of SH-compounds on oxidative DNA damage: repair and increase of damage. Mutat. Res. 295 (1993) 1-10
58. Burhans W.C., Weinberger M., Marchetti M.A., Ramachandran L., D'Urso G., and Huberman J.A. Apoptosis-like yeast cell death in response to DNA damage and replication defects. Mutat. Res. 532 (2003) 227-243
59. Marchetti M.A., Weinberger M., Murakami Y., Burhans W.C., and Huberman J.A. Production of reactive oxygen species in response to replication stress and inappropriate mitosis in fission yeast. J. Cell Sci. 119 (2006) 124-131
60. Tucker C.L., and Fields S. Quantitative genome-wide analysis of yeast deletion sensitivities to oxidative and chemical stress. Comp. Funct. Genomics 5 (2004) 216-224
61. Gralla E.B., and Kosman D.J. Molecular genetics of superoxide dismutases in yeasts and related fungi. Adv. Genet. 30 (1992) 251-319
62. Gasch A.P. Comparative genomics of the environmental stress response in ascomycete fungi. Yeast 24 (2007) 961-976
63. Hertle K., Haase E., and Brendel M. The SNQ3 gene of Saccharomyces cerevisiae confers hyper-resistance to several functionally unrelated chemicals. Curr. Genet. 19 (1991) 429-433
64. Kuge S., and Jones N. YAP1 dependent activation of TRX2 is essential for the response of Saccharomyces cerevisiae to oxidative stress by hydroperoxides. EMBO J. 13 (1994) 655-664
65. 2 receptor and redox-transducer in gene activation. Cell 111 (2002) 471-481
66. Okazaki S., Naganuma A., and Kuge S. Peroxiredoxin-mediated redox regulation of the nuclear localization of Yap1, a transcription factor in budding yeast. Antioxid. Redox Signal. 7 (2005) 327-334
67. Veal E.A., Ross S.J., Malakasi P., Peacock E., and Morgan B.A. Ybp1 is required for the hydrogen peroxide-induced oxidation of the Yap1 transcription factor. J. Biol. Chem. 278 (2003) 30896-30904
68. Izawa S., Maeda K., Sugiyama K., Mano J., Inoue Y., and Kimura A. Thioredoxin deficiency causes the constitutive activation of Yap1, an AP-1-like transcription factor in Saccharomyces cerevisiae. J. Biol. Chem. 274 (1999) 28459-28465
69. Kuge S., Toda T., Iizuka N., and Nomoto A. Crm1 (XpoI) dependent nuclear export of the budding yeast transcription factor yAP-1 is sensitive to oxidative stress. Genes Cells 3 (1998) 521-532
70. Wood M.J., Storz G., and Tjandra N. Structural basis for redox regulation of Yap1 transcription factor localization. Nature 430 (2004) 917-921
71. 2 stress signal. Mol. Cell 27 (2007) 675-688
72. Davies J.M., Lowry C.V., and Davies K.J. Transient adaptation to oxidative stress in yeast. Arch. Biochem. Biophys. 317 (1995) 1-6
73. Wiese A.G., Pacifici R.E., and Davies K.J. Transient adaptation of oxidative stress in mammalian cells. Arch. Biochem. Biophys. 318 (1995) 231-240
74. C.H. Ng, S.X. Tan, G.G. Perrone, G.W. Thorpe, V.J. Higgins, I. Dawes, Adaptation to hydrogen peroxide in Saccaromyces cerevisiae: the role of NADPH-generating systems and the Skn7 transcription factor, Free Radic. Biol. Med. (in press), doi:10.1016/j.freeradbiomed.2007.12.008.
75. Alic N., Felder T., Temple M.D., Gloeckner C., Higgins V.J., Briza P., and Dawes I.W. Genome-wide transcriptional responses to a lipid hydroperoxide: adaptation occurs without induction of oxidant defenses. Free Radic. Biol. Med. 37 (2004) 23-35
76. Brookes P.S., Yoon Y., Robotham J.L., Anders M.W., and Sheu S.S. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol., Cell Physiol. 287 (2004) C817-C833
77. Andreyev A.Y., Kushnareva Y.E., and Starkov A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc). 70 (2005) 200-214
78. Cadenas E., and Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29 (2000) 222-230
79. Sedensky M.M., and Morgan P.G. Mitochondrial respiration and reactive oxygen species in mitochondrial aging mutants. Exp. Gerontol. 41 (2006) 237-245
80. Drakulic T., Temple M.D., Guido R., Jarolim S., Breitenbach M., Attfield P.V., and Dawes I.W. Involvement of oxidative stress response genes in redox homeostasis, the level of reactive oxygen species, and ageing in Saccharomyces cerevisiae. FEMS Yeast Res. 5 (2005) 1215-1228
81. Bonawitz N.D., Chatenay-Lapointe M., Pan Y., and Shadel G.S. Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell. Metab. 5 (2007) 265-277
82. Schieke S.M., and Finkel T. TOR and aging: less is more. Cell. Metab. 5 (2007) 233-235
83. Jazwinski S.M. Yeast longevity and aging-the mitochondrial connection. Mech. Ageing. Dev. 126 (2005) 243-248
84. Liu Z., and Butow R.A. Mitochondrial retrograde signaling. Annu. Rev. Genet. 40 (2006) 159-185
85. Barros M.H., Bandy B., Tahara E.B., and Kowaltowski A.J. Higher respiratory activity decreases mitochondrial reactive oxygen release and increases life span in Saccharomyces cerevisiae. J. Biol. Chem. 279 (2004) 49883-49888
86. Passos J.F., Saretzki G., Ahmed S., Nelson G., Richter T., Peters H., Wappler I., Birket M.J., Harold G., Schaeuble K., Birch-Machin M.A., Kirkwood T.B., and von Zglinicki T. Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol. 5 (2007) e110
87. Stockl P., Zankl C., Hutter E., Unterluggauer H., Laun P., Heeren G., Bogengruber E., Herndler-Brandstetter D., Breitenbach M., and Jansen-Durr P. Partial uncoupling of oxidative phosphorylation induces premature senescence in human fibroblasts and yeast mother cells. Free Radic. Biol. Med. 43 (2007) 947-958
88. Barros M.H., Netto L.E., and Kowaltowski A.J. H(2)O(2) generation in Saccharomyces cerevisiae respiratory pet mutants: effect of cytochrome c. Free Radic. Biol. Med. 35 (2003) 179-188
89. L. Hlavata, L. Nachin, P. Jezek, T. Nystrom, Elevated Ras/PKA activity in Saccharomyces cerevisiae reduces proliferation rate and lifespan by two different ROS-dependent routes, Aging Cell (in press), doi:10.1111/j.1474-9726.2007.00361.x.
90. Heeren G., Jarolim S., Laun P., Rinnerthaler M., Stolze K., Perrone G.G., Kohlwein S.D., Nohl H., Dawes I.W., and Breitenbach M. The role of respiration, reactive oxygen species and oxidative stress in mother cell-specific ageing of yeast strains defective in the RAS signalling pathway. FEMS Yeast Res. 5 (2004) 157-167
91. Machida K., and Tanaka T. Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F(0)F(1)-ATPase in yeast. FEBS Lett. 462 (1999) 108-112
92. Lee Y.J., Hoe K.L., and Maeng P.J. Yeast cells lacking the CIT1-encoded mitochondrial citrate synthase are hypersusceptible to heat- or aging-induced apoptosis. Mol. Biol. Cell 18 (2007) 3556-3567
93. Kakkar P., and Singh B.K. Mitochondria: a hub of redox activities and cellular distress control. Mol. Cell. Biochem. 305 (2007) 235-253
94. Eisenberg T., Buttner S., Kroemer G., and Madeo F. The mitochondrial pathway in yeast apoptosis. Apoptosis 12 (2007) 1011-1023
95. Tao W., Kurschner C., and Morgan J.I. Bcl-xS and Bad potentiate the death suppressing activities of Bcl-xL, Bcl-2, and A1 in yeast. J. Biol. Chem. 273 (1998) 23704-23708
96. Zhang H., Cowan-Jacob S.W., Simonen M., Greenhalf W., Heim J., and Meyhack B. Structural basis of BFL-1 for its interaction with BAX and its anti-apoptotic action in mammalian and yeast cells. J. Biol. Chem. 275 (2000) 11092-11099
97. Priault M., Chaudhuri B., Clow A., Camougrand N., and Manon S. Investigation of bax-induced release of cytochrome c from yeast mitochondria permeability of mitochondrial membranes, role of VDAC and ATP requirement. Eur. J. Biochem. 260 (1999) 684-691
98. Gross A., Pilcher K., Blachly-Dyson E., Basso E., Jockel J., Bassik M.C., Korsmeyer S.J., and Forte M. Biochemical and genetic analysis of the mitochondrial response of yeast to BAX and BCL-X(L). Mol. Cell. Biol. 20 (2000) 3125-3136
99. Ott M., Norberg E., Walter K.M., Schreiner P., Kemper C., Rapaport D., Zhivotovsky B., and Orrenius S. The mitochondrial TOM complex is required for tBid/Bax-induced cytochrome c release. J. Biol. Chem. 282 (2007) 27633-27639
100. Sanjuan Szklarz L.K., Kozjak-Pavlovic V., Vogtle F.N., Chacinska A., Milenkovic D., Vogel S., Durr M., Westermann B., Guiard B., Martinou J.C., Borner C., Pfanner N., and Meisinger C. Preprotein transport machineries of yeast mitochondrial outer membrane are not required for Bax-induced release of intermembrane space proteins. J. Mol. Biol. 368 (2007) 44-54
101. Chen S.R., Dunigan D.D., and Dickman M.B. Bcl-2 family members inhibit oxidative stress-induced programmed cell death in Saccharomyces cerevisiae. Free Radic. Biol. Med. 34 (2003) 1315-1325
102. Polcic P., and Forte M. Response of yeast to the regulated expression of proteins in the Bcl-2 family. Biochem. J. 374 (2003) 393-402
103. Pizzo P., and Pozzan T. Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol. 17 (2007) 511-517
104. Scheckhuber C.Q., Erjavec N., Tinazli A., Hamann A., Nystrom T., and Osiewacz H.D. Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat. Cell Biol. 9 (2007) 99-105
105. Fannjiang Y., Cheng W.C., Lee S.J., Qi B., Pevsner J., McCaffery J.M., Hill R.B., Basanez G., and Hardwick J.M. Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev. 18 (2004) 2785-2797
106. Kitagaki H., Araki Y., Funato K., and Shimoi H. Ethanol-induced death in yeast exhibits features of apoptosis mediated by mitochondrial fission pathway. FEBS Lett. 581 (2007) 2935-2942
107. Boyce M., and Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 13 (2006) 363-373
108. Kincaid M.M., and Cooper A.A. ERADicate ER stress or die trying. Antioxid. Redox Signal. 9 (2007) 2373-2387
109. Sevier C.S., and Kaiser C.A. Formation and transfer of disulphide bonds in living cells. Nat. Rev., Mol. Cell Biol. 3 (2002) 836-847
110. Tu B.P., and Weissman J.S. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol. Cell. 10 (2002) 983-994
111. Pollard M.G., Travers K.J., and Weissman J.S. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell. 1 (1998) 171-182
112. Cuozzo J.W., and Kaiser C.A. Competition between glutathione and protein thiols for disulphide-bond formation. Nat. Cell Biol. 1 (1999) 130-135
113. Frand A.R., and Kaiser C.A. Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol. Cell. 4 (1999) 469-477
114. Sevier C.S., Qu H., Heldman N., Gross E., Fass D., and Kaiser C.A. Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129 (2007) 333-344
115. Travers K.J., Patil C.K., Wodicka L., Lockhart D.J., Weissman J.S., and Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101 (2000) 249-258
116. Ellgaard L., and Helenius A. Quality control in the endoplasmic reticulum. Nat. Rev., Mol. Cell Biol. 4 (2003) 181-191
117. Rutkowski D.T., and Kaufman R.J. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem. Sci. 32 (2007) 469-476
118. Haynes C.M., Titus E.A., and Cooper A.A. Degradation of misfolded proteins prevents ER-derived oxidative stress and cell death. Mol. Cell. 15 (2004) 767-776
119. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., and Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11 (2003) 619-633
120. Sugiura M., and Takagi H. Yeast cell death caused by mutation of the OST2 gene encoding the epsilon-subunit of Saccharomyces cerevisiae oligosaccharyltransferase. Biosci. Biotechnol. Biochem. 70 (2006) 1234-1241
121. Silberstein S., Collins P.G., Kelleher D.J., and Gilmore R. The essential OST2 gene encodes the 16-kD subunit of the yeast oligosaccharyltransferase, a highly conserved protein expressed in diverse eukaryotic organisms. J. Cell Biol. 131 (1995) 371-383
122. Hauptmann P., Riel C., Kunz-Schughart L.A., Frohlich K.U., Madeo F., and Lehle L. Defects in N-glycosylation induce apoptosis in yeast. Mol. Microbiol. 59 (2006) 765-778
123. Rabinovich E., Kerem A., Frohlich K.U., Diamant N., and Bar-Nun S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22 (2002) 626-634
124. Ye Y., Meyer H.H., and Rapoport T.A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414 (2001) 652-656
125. Wojcik C., Rowicka M., Kudlicki A., Nowis D., McConnell E., Kujawa M., and DeMartino G.N. Valosin-containing protein (p97) is a regulator of endoplasmic reticulum stress and of the degradation of N-end rule and ubiquitin-fusion degradation pathway substrates in mammalian cells. Mol. Biol. Cell 17 (2006) 4606-4618
126. Braun R.J., Zischka H., Madeo F., Eisenberg T., Wissing S., Buttner S., Engelhardt S.M., Buringer D., and Ueffing M. Crucial mitochondrial impairment upon CDC48 mutation in apoptotic yeast. J. Biol. Chem. 281 (2006) 25757-25767
127. McCormack J.G., Halestrap A.P., and Denton R.M. Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol. Rev. 70 (1990) 391-425
128. Malhotra J.D., and Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid. Redox Signal. 9 (2007) 2277-2293
129. Strayle J., Pozzan T., and Rudolph H.K. Steady-state free Ca(2+) in the yeast endoplasmic reticulum reaches only 10 microM and is mainly controlled by the secretory pathway pump pmr1. EMBO J. 18 (1999) 4733-4743
130. Bonilla M., Nastase K.K., and Cunningham K.W. Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J. 21 (2002) 2343-2353
131. Pozniakovsky A.I., Knorre D.A., Markova O.V., Hyman A.A., Skulachev V.P., and Severin F.F. Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J. Cell Biol. 168 (2005) 257-269
132. Varbiro G., Toth A., Tapodi A., Veres B., Sumegi B., and Gallyas Jr. F. Concentration dependent mitochondrial effect of amiodarone. Biochem. Pharmacol. 65 (2003) 1115-1128
133. Varbiro G., Toth A., Tapodi A., Bognar Z., Veres B., Sumegi B., and Gallyas Jr. F. Protective effect of amiodarone but not N-desethylamiodarone on postischemic hearts through the inhibition of mitochondrial permeability transition. J. Pharmacol. Exp. Ther. 307 (2003) 615-625
134. Courchesne W.E., and Ozturk S. Amiodarone induces a caffeine-inhibited, MID1-depedent rise in free cytoplasmic calcium in Saccharomyces cerevisiae. Mol. Microbiol. 47 (2003) 223-234
135. Gupta S.S., Ton V.K., Beaudry V., Rulli S., Cunningham K., and Rao R. Antifungal activity of amiodarone is mediated by disruption of calcium homeostasis. J. Biol. Chem. 278 (2003) 28831-28839
136. Kowaltowski A.J., Vercesi A.E., Rhee S.G., and Netto L.E. Catalases and thioredoxin peroxidase protect Saccharomyces cerevisiae against Ca(2+)-induced mitochondrial membrane permeabilization and cell death. FEBS Lett. 473 (2000) 177-182
137. Monteiro G., Kowaltowski A.J., Barros M.H., and Netto L.E. Glutathione and thioredoxin peroxidases mediate susceptibility of yeast mitochondria to Ca(2+)-induced damage. Arch. Biochem. Biophys. 425 (2004) 14-24
138. Niederer K.E., Morrow D.K., Gettings J.L., Irick M., Krawiecki A., and Brewster J.L. Cypermethrin blocks a mitochondria-dependent apoptotic signal initiated by deficient N-linked glycosylation within the endoplasmic reticulum. Cell. Signal. 17 (2005) 177-186
139. Durr G., Strayle J., Plemper R., Elbs S., Klee S.K., Catty P., Wolf D.H., and Rudolph H.K. The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol. Biol. Cell 9 (1998) 1149-1162
140. Vashist S., Frank C.G., Jakob C.A., and Ng D.T. Two distinctly localized p-type ATPases collaborate to maintain organelle homeostasis required for glycoprotein processing and quality control. Mol. Biol. Cell 13 (2002) 3955-3966
141. Dimmer K.S., Fritz S., Fuchs F., Messerschmitt M., Weinbach N., Neupert W., and Westermann B. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol. Biol. Cell 13 (2002) 847-853
142. Kellermayer R., Aiello D.P., Miseta A., and Bedwell D.M. Extracellular Ca(2+) sensing contributes to excess Ca(2+) accumulation and vacuolar fragmentation in a pmr1Delta mutant of S. cerevisiae. J. Cell Sci. 116 (2003) 1637-1646
143. Lapinskas P.J., Cunningham K.W., Liu X.F., Fink G.R., and Culotta V.C. Mutations in PMR1 suppress oxidative damage in yeast cells lacking superoxide dismutase. Mol. Cell. Biol. 15 (1995) 1382-1388
144. Park S.Y., Seo S.B., Lee S.J., Na J.G., and Kim Y.J. Mutation in PMR1, a Ca(2+)-ATPase in Golgi, confers salt tolerance in Saccharomyces cerevisiae by inducing expression of PMR2, an Na(+)-ATPase in plasma membrane. J. Biol. Chem. 276 (2001) 28694-28699
145. Devasahayam G., Burke D.J., and Sturgill T.W. Golgi manganese transport is required for rapamycin signaling in Saccharomyces cerevisiae. Genetics 177 (2007) 231-238
146. Devasahayam G., Ritz D., Helliwell S.B., Burke D.J., and Sturgill T.W. Pmr1, a Golgi Ca2+/Mn2+-ATPase, is a regulator of the target of rapamycin (TOR) signaling pathway in yeast. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 17840-17845
147. Gourlay C.W., and Ayscough K.R. The actin cytoskeleton: a key regulator of apoptosis and ageing?. Nat. Rev., Mol. Cell Biol. 6 (2005) 583-589
148. Gourlay C.W., and Ayscough K.R. The actin cytoskeleton in ageing and apoptosis. FEMS Yeast Res. 5 (2005) 1193-1198
149. Haarer B.K., and Amberg D.C. Old yellow enzyme protects the actin cytoskeleton from oxidative stress. Mol. Biol. Cell 15 (2004) 4522-4531
150. Farah M.E., and Amberg D.C. Conserved actin cysteine residues are oxidative stress sensors that can regulate cell death in yeast. Mol. Biol. Cell 18 (2007) 1359-1365
151. Gourlay C.W., and Ayscough K.R. Actin-induced hyperactivation of the Ras signaling pathway leads to apoptosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 26 (2006) 6487-6501
152. Gourlay C.W., and Ayscough K.R. Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J. Cell Sci. 118 (2005) 2119-2132
153. Liang Q., and Zhou B. Copper and manganese induce yeast apoptosis via different pathways. Mol. Biol. Cell 18 (2007) 4741-4749
154. D.S. Gomes, M.D. Pereira, A.D. Panek, L.R. Andrade, E.C. Eleutherio, Apoptosis as a mechanism for removal of mutated cells of Saccharomyces cerevisiae: The role of Grx2 under cadmium exposure, Biochim. Biophys. Acta (in press), doi:10.1016/j.bbagen.2007.09.014.
155. Du L., Yu Y., Chen J., Liu Y., Xia Y., Chen Q., and Liu X. Arsenic induces caspase- and mitochondria-mediated apoptosis in Saccharomyces cerevisiae. FEMS Yeast Res. 7 (2007) 860-865
156. Jian W., Arora J.S., Oe T., Shuvaev V.V., and Blair I.A. Induction of endothelial cell apoptosis by lipid hydroperoxide-derived bifunctional electrophiles. Free Radic. Biol. Med. 39 (2005) 1162-1176
157. Reekmans R., De Smet K., Chen C., Van Hummelen P., and Contreras R. Old yellow enzyme interferes with Bax-induced NADPH loss and lipid peroxidation in yeast. FEMS Yeast Res. 5 (2005) 711-725
158. Zhivotovsky B., and Kroemer G. Apoptosis and genomic instability. Nat. Rev., Mol. Cell Biol. 5 (2004) 752-762
159. Thorsen M., Lagniel G., Kristiansson E., Junot C., Nerman O., Labarre J., and Tamas M.J. Quantitative transcriptome, proteome, and sulfur metabolite profiling of the Saccharomyces cerevisiae response to arsenite. Physiol. Genomics 30 (2007) 35-43
160. Wu A.L., and Moye-Rowley W.S. GSH1, which encodes gamma-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol. Cell. Biol. 14 (1994) 5832-5839
161. P.J. Dilda, G.G. Perrone, A. Philp, R.B. Lock, I.W. Dawes, P.J. Hogg, Insight into the selectivity or arsenic trioxide for acute promyelocytic leukemia cells by characterizing Saccharomyces cerevisiae deletion strains that are sensitive or resistant to the metalloid, Int. J. Biochem. Cell Biol. (in press), doi:10.1016/j.biocel.2007.11.002.
162. Schafer F.Q., and Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30 (2001) 1191-1212
163. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., and Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397 (1999) 441-446
164. Wissing S., Ludovico P., Herker E., Buttner S., Engelhardt S.M., Decker T., Link A., Proksch A., Rodrigues F., Corte-Real M., Frohlich K.U., Manns J., Cande C., Sigrist S.J., Kroemer G., and Madeo F. An AIF orthologue regulates apoptosis in yeast. J. Cell Biol. 166 (2004) 969-974
165. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., and Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419 (2002) 367-374
166. Miramar M.D., Costantini P., Ravagnan L., Saraiva L.M., Haouzi D., Brothers G., Penninger J.M., Peleato M.L., Kroemer G., and Susin S.A. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol. Chem. 276 (2001) 16391-16398
167. Lipton S.A., and Bossy-Wetzel E. Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111 (2002) 147-150
168. Krantic S., Mechawar N., Reix S., and Quirion R. Apoptosis-inducing factor: a matter of neuron life and death. Prog. Neurobiol. 81 (2007) 179-196
169. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schagger H., Rustin P., and Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 23 (2004) 4679-4689
170. Li W., Sun L., Liang Q., Wang J., Mo W., and Zhou B. Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol. Biol. Cell 17 (2006) 1802-1811
171. Madeo F., Herker E., Maldener C., Wissing S., Lachelt S., Herlan M., Fehr M., Lauber K., Sigrist S.J., Wesselborg S., and Frohlich K.U. A caspase-related protease regulates apoptosis in yeast. Mol. Cell. 9 (2002) 911-917
172. Mitsui K., Nakagawa D., Nakamura M., Okamoto T., and Tsurugi K. Valproic acid induces apoptosis dependent of Yca1p at concentrations that mildly affect the proliferation of yeast. FEBS Lett. 579 (2005) 723-727
173. Khan M.A., Chock P.B., and Stadtman E.R. Knockout of caspase-like gene, YCA1, abrogates apoptosis and elevates oxidized proteins in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 17326-17331
174. Fahrenkrog B., Sauder U., and Aebi U. The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J. Cell Sci. 117 (2004) 115-126
175. Madeo F., Herker E., Wissing S., Jungwirth H., Eisenberg T., and Frohlich K.U. Apoptosis in yeast. Curr. Opin. Microbiol. 7 (2004) 655-660
176. G.W. Thorpe, On the cellular mechanisms required for survival of oxidative stress in Saccharomyces cerevisiae, PhD thesis, University of New South Wales, Kensington, 2006, p. 172.
177. Izawa S., Inoue Y., and Kimura A. Oxidative stress response in yeast: effect of glutathione on adaptation to hydrogen peroxide stress in Saccharomyces cerevisiae. FEBS Lett. 368 (1995) 73-76
178. Grant C.M., Collinson L.P., Roe J.H., and Dawes I.W. Yeast glutathione reductase is required for protection against oxidative stress and is a target gene for yAP-1 transcriptional regulation. Mol. Microbiol. 21 (1996) 171-179
179. Grant C.M., MacIver F.H., and Dawes I.W. Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr. Genet. 29 (1996) 511-515