Characterization of the peroxide sensitivity of COX-deficient yeast strains reveals unexpected relationships between COX assembly proteins

Free Radical Biology and Medicine

Volumn 51, Issue 8, 2011, Pages 1589-1600

  Veniamin, Simona ^a   Sawatzky, Luanne G ^a   Banting, Graham S ^a   Glerum, D Moira ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

COX assembly; Cytochrome oxidase; Free radicals; Peroxide; Suppressors

Indexed keywords

CATALASE; COX11 PROTEIN; CYTOCHROME C OXIDASE; FUNGAL PROTEIN; PEROXIDE; SCO1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FUNGAL STRAIN; FUNGUS MUTANT; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; YEAST;

CATALASE; CELLS, CULTURED; COPPER; HYDROGEN PEROXIDE; MEMBRANE PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MULTIENZYME COMPLEXES; MUTATION; ORGANISMS, GENETICALLY MODIFIED; RESPIRATION; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSGENES; YEASTS;

EID: 80052715173     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.06.024     Document Type: Article

References (37)

1. N.J. Robinson, and D.R. Winge Copper metallochaperones Annu. Rev. Biochem. 79 2010 537 562
2. M. Schulze, and G. Rodel SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II Mol. Gen. Genet. 211 1988 492 498 (Pubitemid 18083405)
3. A. Tzagoloff, N. Capitanio, M.P. Nobrega, and D. Gatti Cytochrome oxidase assembly in yeast requires the product of COX11, a homolog of the P. denitrificans protein encoded by ORF3 EMBO J. 9 1990 2759 2764
4. D.M. Glerum, A. Shtanko, and A. Tzagoloff Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase J. Biol. Chem. 271 1996 14504 14509 (Pubitemid 26190352)
5. J. Beers, D.M. Glerum, and A. Tzagoloff Purification, characterization, and localization of yeast Cox17p, a mitochondrial copper shuttle J. Biol. Chem. 272 1997 33191 33196 (Pubitemid 28023665)
6. Y.-C. Horng, P.A. Cobine, A.B. Maxfield, H.S. Carr, and D.R. Winge Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome c oxidase J. Biol. Chem. 279 2004 35334 35340 (Pubitemid 39100532)
7. J.C. Williams, C. Sue, G.S. Banting, H. Yang, D.M. Glerum, W.A. Hendrickson, and E.A. Schon Crystal structure of human SCO1: implications for redox signaling by a mitochondrial cytochrome c oxidase "assembly" protein J. Biol. Chem. 280 2005 15202 15211 (Pubitemid 40562876)
8. L. Banci, I. Bertini, S. Ciofi-Baffoni, T. Hadjiloi, M. Martinelli, and P. Palumaa Mitochondrial copper(I) transfer from Cox17 to Sco1 is coupled to electron transfer Proc. Natl. Acad. Sci. U. S. A. 105 2008 6803 6808 (Pubitemid 351754485)
9. A assembly Nat. Chem. Biol. 4 2008 599 601
10. S.C. Leary, P.A. Cobine, B.A. Kaufman, G.H. Guercin, A. Mattman, J. Palaty, G. Lockitch, D.R. Winge, P. Rustin, R. Horvath, and E.A. Shoubridge The human cytochrome c oxidase assembly factors SCO1 and SCO2 have regulatory roles in the maintenance of cellular copper homeostasis Cell Metab. 5 2007 9 20 (Pubitemid 44933111)
11. S.C. Leary, F. Sasarman, T. Nishimura, and E.A. Shoubridge Human SCO2 is required for the synthesis of CO II and as a thiol-disulphide oxidoreductase for SCO1 Hum. Mol. Genet. 18 2009 2230 2240
12. L. Stiburek, K. Vesela, H. Hansikova, H. Hulkova, and J. Zeman Loss of function of Sco1 and its interaction with cytochrome c oxidase Am. J. Physiol. Cell Physiol. 296 2009 C1218 1226
13. H. Yang, S. Brosel, R. Acin-Perez, V. Slavkovich, I. Nishino, R. Khan, I.J. Goldberg, J. Graziano, G. Manfredi, and E.A. Schon Analysis of mouse models of cytochrome c oxidase deficiency owing to mutations in Sco2 Hum. Mol. Genet. 19 2010 170 180
14. L.C. Papadopoulou, C.M. Sue, M.M. Davidson, K. Tanji, I. Nishino, J.E. Sadlock, S. Krishna, W. Walker, J. Selby, D.M. Glerum, R.V. Coster, G. Lyon, E. Scalais, R. Lebel, P. Kaplan, S. Shanske, D.C. De Vivo, E. Bonilla, M. Hirano, S. DiMauro, and E.A. Schon Fatal infantile cardioencephalomyopathy with COX deficiency and mutations in SCO2, a COX assembly gene Nat. Genet. 23 1999 333 337 (Pubitemid 29526433)
15. I. Valnot, S. Osmond, N. Gigarel, B. Mehaye, J. Amiel, V. Cormier-Daire, A. Munnich, J.P. Bonnefont, P. Rustin, and A. Rotig Mutations of the SCO1 gene in mitochondrial cytochrome c oxidase deficiency with neonatal-onset hepatic failure and encephalopathy Am. J. Hum. Genet. 67 2000 1104 1109
16. B site formation of cytochrome c oxidase J. Biol. Chem. 279 2004 34833 34839 (Pubitemid 39318117)
17. K.L. Seib, M.P. Jennings, and A.G. McEwan A Sco homologue plays a role in defence against oxidative stress in pathogenic Neisseria FEBS Lett. 546 2003 411 415 (Pubitemid 36782449)
18. P. Saenkham, P. Vattanaviboon, and S. Mongkolsuk Mutation in sco affects cytochrome c assembly and alters oxidative stress resistance in Agrobacterium tumefaciens FEMS Microbiol. Lett. 293 2009 122 129
19. S. Brosel, H. Yang, K. Tanji, E. Bonilla, and E.A. Schon Unexpected vascular enrichment of SCO1 over SCO2 in mammalian tissues: implications for human mitochondrial disease Am. J. Pathol. 177 2010 2541 2548
20. C. Pungartnik, M.F. Kern, M. Brendel, and J.A. Henriques Mutant allele pso7-1, that sensitizes Saccharomyces cerevisiae to photoactivated psoralen, is allelic with COX11, encoding a protein indispensable for a functional cytochrome c oxidase Curr. Genet. 36 1999 124 129 (Pubitemid 29440494)
21. G.S. Banting, and D.M. Glerum Mutational analysis of the Saccharomyces cerevisiae cytochrome c oxidase assembly protein, Cox11p Eukaryot. Cell 5 2006 568 578
22. O. Khalimonchuk, A. Bird, and D.R. Winge Evidence for a pro-oxidant intermediate in the assembly of cytochrome oxidase J. Biol. Chem. 282 2007 17442 17449 (Pubitemid 47100294)
23. D.M. Glerum, A. Shtanko, and A. Tzagoloff SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae J. Biol. Chem. 271 1996 20531 20535 (Pubitemid 26281827)
24. Y. Wen, W. Li, E.C. Poteet, L. Xie, C. Tan, L.-J. Yan, X. Ju, R. Liu, H. Qian, M.A. Marvin, M.S. Goldberg, H. She, Z. Mao, J.W. Simpkins, and S.-H. Yang Alternative mitochondrial electron transfer as a novel strategy for neuroprotection J. Biol. Chem. 286 2011 16504 16515
25. H.S. Carr, A.B. Maxfield, Y.-C. Horng, and D.R. Winge Functional analysis of the domains in Cox11 J. Biol. Chem. 280 2005 22664 22669 (Pubitemid 40853170)
26. A.M. Vetrano, D.E. Heck, T.M. Mariano, V. Mishin, D.L. Laskin, and J.D. Laskin Characterization of the oxidase activity in mammalian catalase J. Biol. Chem. 280 2005 35372 35381 (Pubitemid 41532726)
27. M. Salvi, V. Battaglia, A.M. Brunati, N. La Rocca, E. Tibaldi, P. Pietrangeli, L. Marcocci, B. Mondovi, C.A. Rossi, and A. Toninello Catalase takes part in rat liver mitochondria oxidative stress defense J. Biol. Chem. 282 2007 24407 24415 (Pubitemid 47328021)
28. G.F. Sprague Jr., and S.C. Winans Eukaryotes learn how to count: quorum sensing by yeast Genes Dev. 20 2006 1045 1049
29. J.S. Finkel, and A.P. Mitchell Genetic control of Candida albicans biofilm development Nat. Rev. Microbiol. 9 2011 109 118
30. S. Melov, J. Ravenscroft, S. Malik, M.S. Gill, D.W. Walker, P.E. Clayton, D.C. Wallace, B. Malfroy, S.R. Doctrow, and G.J. Lithgow Extension of life-span with superoxide dismutase/catalase mimetics Science 289 2000 1567 1569
31. D.F. Dai, L.F. Santana, M. Vermulst, D.M. Tomazela, M.J. Emond, M.J. MacCoss, K. Gollahon, G.M. Martin, L.A. Loeb, W.C. Ladiges, and P.S. Rabinovitch Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging Circulation 119 2009 2789 2797
32. O.I. Petriv, and R.A. Rachubinski Lack of peroxisomal catalase causes a progeric phenotype in Caenorhabditis elegans J. Biol. Chem. 279 2004 19996 20001 (Pubitemid 38623442)
33. J.I. Koepke, K.A. Nakrieko, C.S. Wood, K.K. Boucher, L.J. Terlecky, P.A. Walton, and S.R. Terlecky Restoration of peroxisomal catalase import in a model of human cellular aging Traffic 8 2007 1590 1600 (Pubitemid 47578363)
34. E.J. Collinson, G.L. Wheeler, E.O. Garrido, A.M. Avery, S.V. Avery, and C.M. Grant The yeast glutaredoxins are active as glutathione peroxidases J. Biol. Chem. 277 2002 16712 16717 (Pubitemid 34967691)
35. T.V. Vygodina, and A.A. Konstantinov Peroxidase activity of mitochondrial cytochrome c oxidase Biochemistry (Moscow) 72 2007 1056 1064 (Pubitemid 350022589)
36. 2 removal in brain mitochondria via the thioredoxin/peroxiredoxin system J. Biol. Chem. 285 2010 27850 27858
37. D.E. Fomenko, A. Koc, N. Agisheva, M. Jacobsen, A. Kaya, M. Malinouski, J.C. Rutherford, K.-L. Siu, D.-Y. Jin, D.R. Winge, and V.N. Gladyshev Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide Proc. Natl. Acad. Sci. U. S. A. 108 2011 2729 2734