Loss of tafazzin in yeast leads to increased oxidative stress during respiratory growth

Molecular Microbiology

Volumn 68, Issue 4, 2008, Pages 1061-1072

  Chen, Shuliang ^a   He, Quan ^a   Greenberg, Miriam L ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CARDIOLIPIN; HYDROGEN PEROXIDE; MENADIONE; OLEIC ACID; PARAQUAT; REACTIVE OXYGEN METABOLITE;

ARTICLE; BARTH SYNDROME; CONTROLLED STUDY; FUNGAL GENE; FUNGUS GROWTH; GENETIC CONSERVATION; MICROBIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; SENSITIVITY ANALYSIS; TAFAZZIN GENE; TEMPERATURE; YEAST;

ACYLTRANSFERASES; CARDIOLIPINS; ETHANOL; HEAT; HYDROGEN PEROXIDE; OLEIC ACID; OXIDATIVE STRESS; PARAQUAT; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VITAMIN K 3;

EID: 42549160157     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06216.x     Document Type: Article

References (62)

1. Ames, B.N., Shigenaga, M.K. Hagen, T.M. (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90 : 7915 7922.
2. Bailey, S.M., Pietsch, E.C. Cunningham, C.C. (1999) Ethanol stimulates the production of reactive oxygen species at mitochondrial complexes I and III. Free Radic Biol Med 27 : 891 900.
3. Barros, M.H., Netto, L.E. Kowaltowski, A.J. (2003) H(2)O(2) generation in Saccharomyces cerevisiae respiratory pet mutants: effect of cytochrome c. Free Radic Biol Med 35 : 179 188.
4. Barth, P.G., Wanders, R.J. Vreken, P. (1999) X-linked cardioskeletal myopathy and neutropenia (Barth syndrome)-MIM 302060. J Pediatr 135 : 273 276.
5. Beyer, K. Nuscher, B. (1996) Specific cardiolipin binding interferes with labeling of sulfhydryl residues in the adenosine diphosphate/adenosine triphosphate carrier protein from beef heart mitochondria. Biochemistry 35 : 15784 15790.
6. Bione, S., D'Adamo, P., Maestrini, E., Gedeon, A.K., Bolhuis, P.A. Toniolo, D. (1996) A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat Genet 12 : 385 389.
7. Bolhuis, P.A., Hensels, G.W., Hulsebos, T.J., Baas, F. Barth, P.G. (1991) Mapping of the locus for X-linked cardioskeletal myopathy with neutropenia and abnormal mitochondria (Barth syndrome) to Xq28. Am J Hum Genet 48 : 481 485.
8. Brandner, K., Mick, D.U., Frazier, A.E., Taylor, R.D., Meisinger, C. Rehling, P. (2005) Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth Syndrome. Mol Biol Cell 16 : 5202 5214.
9. Brown, S.W., Oliver, S.G., Harrison, D.E.F. Righelato, R.C. (1981) Ethanol inhibition of yeast growth and fermentation: differences in the magnitude and complexity of the effect. Eur J Appl Microbiol Biotechnol 11 : 151 155.
10. Chance, B., Sies, H. Boveris, A. (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59 : 527 605.
11. Chang, S.C., Heacock, P.N., Mileykovskaya, E., Voelker, D.R. Dowhan, W. (1998) Isolation and characterization of the gene (CLS1) encoding cardiolipin synthase in Saccharomyces cerevisiae. J Biol Chem 273 : 14933 14941.
12. Chen, Q., Vazquez, E.J., Moghaddas, S., Hoppel, C.L. Lesnefsky, E.J. (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278 : 36027 36031.
13. Chi, Z. Arneborg, N. (1999) Relationship between lipid composition, frequency of ethanol-induced respiratory deficient mutants, and ethanol tolerance in Saccharomyces cerevisiae. J Appl Microbiol 86 : 1047 1052.
14. Costa, V., Amorim, M.A., Reis, E., Quintanilha, A. Moradas-Ferreira, P. (1997) Mitochondrial superoxide dismutase is essential for ethanol tolerance of Saccharomyces cerevisiae in the post-diauxic phase. Microbiology (Reading, England) 143 : 1649 1656.
15. Costa, V. Moradas-Ferreira, P. (2001) Oxidative stress and signal transduction in Saccharomyces cerevisiae: insights into ageing, apoptosis and diseases. Mol Aspects Med 22 : 217 246.
16. Costa, V., Reis, E., Quintanilha, A. Moradas-Ferreira, P. (1993) Acquisition of ethanol tolerance in Saccharomyces cerevisiae: the key role of the mitochondrial superoxide dismutase. Arch Biochem Biophys 300 : 608 614.
17. Dirmeier, R., O'Brien, K., Engle, M., Dodd, A., Spears, E. Poyton, R.O. (2004) Measurement of oxidative stress in cells exposed to hypoxia and other changes in oxygen concentration. Methods Enzymol 381 : 589 603.
18. Drees, M. Beyer, K. (1988) Interaction of phospholipids with the detergent-solubilized ADP/ATP carrier protein as studied by spin-label electron spin resonance. Biochemistry 27 : 8584 8591.
19. Du, X., Takagi (2007) N-Acetyltransferase Mpr1 confers ethanol tolerance on Saccharomyces cerevisiae by reducing reactive oxygen species. Appl Microbiol Biotechnol 75 : 1343 1351.
20. Gomez, B., Jr. Robinson, N.C. (1999) Phospholipase digestion of bound cardiolipin reversibly inactivates bovine cytochrome bc1. Biochemistry 38 : 9031 9038.
21. Grant, C.M., MacIver, F.H. Dawes, I.W. (1997) Mitochondrial function is required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. FEBS Lett 410 : 219 222.
22. Gu, Z., Valianpour, F., Chen, S., Vaz, F.M., Hakkaart, G.A., Wanders, R.J. Greenberg, M.L. (2004) Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome. Mol Microbiol 51 : 149 158.
23. Hayer-Hartl, M., Schagger, H., von Jagow, G. Beyer, K. (1992) Interactions of phospholipids with the mitochondrial cytochrome-c reductase studied by spin-label ESR and NMR spectroscopy. Eur J Biochem 209 : 423 430.
24. Hoch, F.L. (1992) Cardiolipins and biomembrane function. Biochimica Biophysica Acta 1113 : 71 133.
25. Ibeas, J.I. Jimenez, J. (1997) Mitochondrial DNA loss caused by ethanol in Saccharomyces flor yeasts. Appl Environ Microbiol 63 : 7 12.
26. Jamieson, D.J. (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14 : 1511 1527.
27. Jiang, F., Rizavi, H.S. Greenberg, M.L. (1997) Cardiolipin is not essential for the growth of Saccharomyces cerevisiae on fermentable or non-fermentable carbon sources. Mol Microbiol 26 : 481 491.
28. Jimenez, J. Benitez, T. (1988) Yeast cell viability under conditions of high temperature and ethanol concentrations depends on the mitochondrial genome. Curr Genet 13 : 461 469.
29. Jimenez, J., Longo, E. Benitez, T. (1988) Induction of petite yeast mutants by membrane-active agents. Appl Environ Microbiol 54 : 3126 3132.
30. Jones, R.P. Greenfield, P.F. (1985) Replicative inactivation and metabolic inhibition in yeast ethanol fermentations. Biotechnol Lett 7 : 223 228.
31. Koshkin, V. Greenberg, M.L. (2000) Oxidative phosphorylation in cardiolipin-lacking yeast mitochondria. Biochem J 347 (Part 3 687 691.
32. de Kroon, A.I. (2007) Metabolism of phosphatidylcholine and its implications for lipid acyl chain composition in Saccharomyces cerevisiae. Biochim Biophys Acta 1771 : 343 352.
33. Lushchak, V., Semchyshyn, H., Mandryk, S. Lushchak, O. (2005) Possible role of superoxide dismutases in the yeast Saccharomyces cerevisiae under respiratory conditions. Arch Biochem Biophys 441 : 35 40.
34. Ma, L., Vaz, F.M., Gu, Z., Wanders, R.J. Greenberg, M.L. (2004) The human TAZ gene complements mitochondrial dysfunction in the yeast taz1Delta mutant. Implications for Barth syndrome. J Biol Chem 279 : 44394 44399.
35. McKenzie, M., Lazarou, M., Thorburn, D.R. Ryan, M.T. (2006) Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J Mol Biol 361 : 462 469.
36. Mishra, P. Prasad, R. (1988) Role of phospholipid head groups in ethanol tolerance of Saccharomyces cerevisiae. J Gen Microbiol 134 : 3205 3211.
37. Nebot, C., Moutet, M., Huet, P., Xu, J.Z., Yadan, J.C. Chaudiere, J. (1993) Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Anal Biochem 214 : 442 451.
38. Neuwald, A.F. (1997) Barth syndrome may be due to an acyltransferase deficiency. Curr Biol 7 : R465 R466.
39. Pfeiffer, K., Gohil, V., Stuart, R.A., Hunte, C., Brandt, U., Greenberg, M.L. Schagger, H. (2003) Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 278 : 52873 52880.
40. Pilkington, B.J. Rose, A.H. (1991) Incorporation of unsaturated fatty acids by Saccharomyces cerevisiae: conservation of fatty-acyl saturation in phosphatidylinositol. Yeast 7 : 489 494.
41. Quintans, L.N., Castro, G.D. Castro, J.A. (2005) Oxidation of ethanol to acetaldehyde and free radicals by rat testicular microsomes. Arch Toxicol 79 : 25 30.
42. Reznick, A.Z. Packer, L. (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233 : 357 363.
43. Robinson, N.C., Zborowski, J. Talbert, L.H. (1990) Cardiolipin-depleted bovine heart cytochrome c oxidase: binding stoichiometry and affinity for cardiolipin derivatives. Biochemistry 29 : 8962 8969.
44. Schagger, H., Hagen, T., Roth, B., Brandt, U., Link, T.A. von Jagow, G. (1990) Phospholipid specificity of bovine heart bc1 complex. Eur J Biochem 190 : 123 130.
45. Schlame, M., Rua, D. Greenberg, M.L. (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39 : 257 288.
46. Schlame, M., Kelley, R.I., Feigenbaum, A., Towbin, J.A., Heerdt, P.M., Schieble, T., et al. (2003) Phospholipid abnormalities in children with Barth syndrome. J Am Coll Cardiol 42 : 1994 1999.
47. Schlame, M., Ren, M., Xu, Y., Greenberg, M.L. Haller, I. (2005) Molecular symmetry in mitochondrial cardiolipins. Chem Phys Lipids 138 : 38 49.
48. Sedlak, E. Robinson, N.C. (1999) Phospholipase A(2) digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure. Biochemistry 38 : 14966 14972.
49. Shigenaga, M.K., Hagen, T.M. Ames, B.N. (1994) Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA 91 : 10771 10778.
50. Tuller, G., Nemec, T., Hrastnik, C. Daum, G. (1999) Lipid composition of subcellular membranes of an FY1679-derived haploid yeast wild-type strain grown on different carbon sources. Yeast 15 : 1555 1564.
51. Turrens, J.F. (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552 : 335 344.
52. Vaden, D.L., Gohil, V.M., Gu, Z. Greenberg, M.L. (2005) Separation of yeast phospholipids using one-dimensional thin-layer chromatography. Anal Biochem 338 : 162 164.
53. Valianpour, F., Vreken, P., Nijtmans, L.G., van Roermund, C.W.T., Grivell, L.A., Wanders, R.J. Barth, P.G. (2001) Investigation of defective cardiolipin remodeling in Barth syndrome using yeast as study model (Abstract). J Inherit Metab Dis 24 : 83.
54. Valianpour, F., Mitsakos, V., Schlemmer, D., Towbin, J.A., Taylor, J.M., Ekert, P.G., et al. (2005) Monolysocardiolipins accumulate in Barth syndrome but do not lead to enhanced apoptosis. J Lipid Res 46 : 1182 1195.
55. Vaz, F.M., Houtkooper, R.H., Valianpour, F., Barth, P.G. Wanders, R.J. (2003) Only one splice variant of the human TAZ gene encodes a functional protein with a role in cardiolipin metabolism. J Biol Chem 278 : 43089 43094.
56. Vreken, P., Valianpour, F., Nijtmans, L.G., Grivell, L.A., Plecko, B., Wanders, R.J. Barth, P.G. (2000) Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem Biophys Res Commun 279 : 378 382.
57. Wills, C. (1990) Regulation of sugar and ethanol metabolism in Saccharomyces cerevisiae. Crit Rev Biochem Mol Biol 25 : 245 280.
58. Xu, Y., Sutachan, J.J., Plesken, H., Kelley, R.I. Schlame, M. (2005) Characterization of lymphoblast mitochondria from patients with Barth syndrome. Lab Invest 85 : 823 830.
59. You, K.M., Rosenfield, C.L. Knipple, D.C. (2003) Ethanol tolerance in the yeast Saccharomyces cerevisiae is dependent on cellular oleic acid content. Appl Environ Microbiol 69 : 1499 1503.
60. Yu, C.A. Yu, L. (1980) Structural role of phospholipids in ubiquinol-cytochrome c reductase. Biochemistry 19 : 5715 5720.
61. Zhang, M., Mileykovskaya, E. Dowhan, W. (2002) Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J Biol Chem 277 : 43553 43556.
62. Zhang, M., Mileykovskaya, E. Dowhan, W. (2005) Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem 280 : 29403 29408.