Oxidative stress and protease dysfunction in the yeast model of Friedreich ataxia

Free Radical Biology and Medicine

Volumn 42, Issue 10, 2007, Pages 1561-1570

  Bulteau, Anne Laure ^a   Dancis, Andrew ^b   Gareil, Monique ^a   Montagne, Jean Jacques ^c,d   Camadro, Jean Michel ^c,d   Lesuisse, Emmanuel ^c  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c Laboratoire d'Ingénierie des Protéines et Contrôle Métabolique   (France)

^d INSTITUT JACQUES MONOD   (France)

Author keywords

Frataxin; Free radicals; Friedreich ataxia; Iron; Oxidative stress; Proteases; Yeast

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; FRATAXIN; IRON; IRON SULFUR PROTEIN; MUTANT PROTEIN; OXYGEN; PROTEASOME; PROTEIN KINASE PIM 1; PROTEINASE;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME INACTIVATION; FRIEDREICH ATAXIA; FUNGAL CELL CULTURE; GENOTYPE PHENOTYPE CORRELATION; MITOCHONDRION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; SACCHAROMYCES CEREVISIAE;

ENZYME ACTIVATION; FRIEDREICH ATAXIA; GENE DELETION; IRON; IRON-BINDING PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; OXIDATIVE STRESS; OXYGEN; PHENOTYPE; PROTEASOME ENDOPEPTIDASE COMPLEX; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SERINE ENDOPEPTIDASES;

SACCHAROMYCES CEREVISIAE;

EID: 34247188143     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.02.014     Document Type: Article

References (46)

1. Campuzano V., Montermini L., Molto M.D., Pianese L., Cossee M., Cavalcanti F., Monros E., Rodius F., Duclos F., Monticelli A., Zara F., Canizares J., Koutnikova H., Bidichandani S.I., Gellera C., Brice A., Trouillas P., De Michele G., Filla A., De Frutos R., Palau F., Patel P.I., Di Donato S., Mandel J.L., Cocozza S., Koenig M., and Pandolfo M. Friedreich's ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science 271 (1996) 1423-1427
2. Bencze K.Z., Kondapalli K.C., Cook J.D., McMahon S., Millan-Pacheco C., Pastor N., and Stemmler T.L. The structure and function of frataxin. Crit. Rev. Biochem. Mol. Biol. 41 (2006) 269-291
3. Calabrese V., Lodi R., Tonon C., D'Agata V., Sapienza M., Scapagnini G., Mangiameli A., Pennisi G., Stella A.M., and Butterfield D.A. Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich's ataxia. J. Neurol. Sci. 233 (2005) 145-162
4. Babcock M., de Silva D., Oaks R., Davis-Kaplan S., Jiralerspong S., Montermini L., Pandolfo M., and Kaplan J. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 276 (1997) 1709-1712
5. O'Neill H.A., Gakh O., Park S., Cui J., Mooney S.M., Sampson M., Ferreira G.C., and Isaya G. Assembly of human frataxin is a mechanism for detoxifying redox-active iron. Biochemistry 44 (2005) 537-545
6. Puccio H., Simon D., Cossee M., Criqui-Filipe P., Tiziano F., Melki J., Hindelang C., Matyas R., Rustin P., and Koenig M. Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet. 27 (2001) 181-186
7. Muhlenhoff U., Richhardt N., Ristow M., Kispal G., and Lill R. The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet. 11 (2002) 2025-2036
8. Gerber J., Muhlenhoff U., and Lill R. An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep. 4 (2003) 906-911
9. Zhang Y., Lyver E.R., Knight S.A., Pain D., Lesuisse E., and Dancis A. Mrs3p, Mrs4p, and frataxin provide iron for Fe-S cluster synthesis in mitochondria. J. Biol. Chem. 281 (2006) 22493-22502
10. Shoichet S.A., Baumer A.T., Stamenkovic D., Sauer H., Pfeiffer A.F., Kahn C.R., Muller-Wieland D., Richter C., and Ristow M. Frataxin promotes antioxidant defense in a thiol-dependent manner resulting in diminished malignant transformation in vitro. Hum. Mol. Genet. 11 (2002) 815-821
11. Bulteau A.L., O'Neill H.A., Kennedy M.C., Ikeda-Saito M., Isaya G., and Szweda L.I. Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science 305 (2004) 242-245
12. Lesuisse E., Santos R., Matzanke B.F., Knight S.A., Camadro J.M., and Dancis A. Iron use for haem synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet. 12 (2003) 879-889
13. Zhang Y., Lyver E.R., Knight S.A., Lesuisse E., and Dancis A. Frataxin and mitochondrial carrier proteins, Mrs3p and Mrs4p, cooperate in providing iron for heme synthesis. J. Biol. Chem. 281 (2006) 22493-22502
14. Santos R., Buisson N., Knight S.A., Dancis A., Camadro J.M., and Lesuisse E. Candida albicans lacking the frataxin homologue: a relevant yeast model for studying the role of frataxin. Mol. Microbiol. 54 (2004) 507-519
15. Chantrel-Groussard K., Geromel V., Puccio H., Koenig M., Munnich A., Rotig A., and Rustin P. Disabled early recruitment of antioxidant defenses in Friedreich's ataxia. Hum. Mol. Genet. 10 (2001) 2061-2067
16. Seznec H., Simon D., Bouton C., Reutenauer L., Hertzog A., Golik P., Procaccio V., Patel M., Drapier J.C., Koenig M., and Puccio H. Friedreich ataxia: the oxidative stress paradox. Hum. Mol. Genet. 14 (2005) 463-474
17. Anderson P.R., Kirby K., Hilliker A.J., and Phillips J.P. RNAi-mediated suppression of the mitochondrial iron chaperone, frataxin, in Drosophila. Hum. Mol. Genet. 14 (2005) 3397-3405
18. Gonzalez-Cabo P., Vazquez-Manrique R.P., Garcia-Gimeno M.A., Sanz P., and Palau F. Frataxin interacts functionally with mitochondrial electron transport chain proteins. Hum. Mol. Genet. 14 (2005) 2091-2098
19. Gordon D.M., Kogan M., Knight S.A., Dancis A., and Pain D. Distinct roles for two N-terminal cleaved domains in mitochondrial import of the yeast frataxin homolog, Yfh1p. Hum. Mol. Genet. 10 (2001) 259-269
20. Raguzzi F., Lesuisse E., and Crichton R.R. Iron storage in Saccharomyces cerevisiae. FEBS Lett. 231 (1988) 253-258
21. Liu T., Lu B., Lee I., Ondrovicova G., Kutejova E., and Suzuki C.K. DNA and RNA binding by the mitochondrial lon protease is regulated by nucleotide and protein substrate. J. Biol. Chem. 279 (2004) 13902-13910
22. Li J., Saxena S., Pain D., and Dancis A. Adrenodoxin reductase homolog (Arh1p) of yeast mitochondria required for iron homeostasis. J. Biol. Chem. 276 (2001) 1503-1509
23. Bulteau A.L., Lundberg K.C., Humphries K.M., Sadek H.A., Szweda P.A., Friguet B., and Szweda L.I. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J. Biol. Chem. 276 (2001) 30057-30063
24. Bulteau A.L., Moreau M., Nizard C., and Friguet B. Impairment of proteasome function upon UVA- and UVB-irradiation of human keratinocytes. Free Radic. Biol. Med. 32 (2002) 1157-1170
25. Groll M., and Huber R. Purification, crystallization, and X-ray analysis of the yeast 20S proteasome. Methods Enzymol. 398 (2005) 329-336
26. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
27. Reiner S., Micolod D., Zellnig G., and Schneiter R. A genomewide screen reveals a role of mitochondria in anaerobic uptake of sterols in yeast. Mol. Biol. Cell 17 (2006) 90-103
28. Poppek D., and Grune T. Proteasomal defense of oxidative protein modifications. Antioxid. Redox Signaling 8 (2006) 173-184
29. Major T., von Janowsky B., Ruppert T., Mogk A., and Voos W. Proteomic analysis of mitochondrial protein turnover: identification of novel substrate proteins of the matrix protease pim1. Mol. Cell. Biol. 26 (2006) 762-776
30. Bulteau A.L., Szweda L.I., and Friguet B. Mitochondrial protein oxidation and degradation in response to oxidative stress and aging. Exp. Gerontol. 41 (2006) 653-657
31. Sullivan P.G., Dragicevic N.B., Deng J.H., Bai Y., Dimayuga E., Ding Q., Chen Q., Bruce-Keller A.J., and Keller J.N. Proteasome inhibition alters neural mitochondrial homeostasis and mitochondria turnover. J. Biol. Chem. 279 (2004) 20699-20707
32. Conconi M., Petropoulos I., Emod I., Turlin E., Biville F., and Friguet B. Protection from oxidative inactivation of the 20S proteasome by heat-shock protein 90. Biochem. J. 333 Pt 2 (1998) 407-415
33. Bulteau A.L., Verbeke P., Petropoulos I., Chaffotte A.F., and Friguet B. Proteasome inhibition in glyoxal-treated fibroblasts and resistance of glycated glucose-6-phosphate dehydrogenase to 20 S proteasome degradation in vitro. J. Biol. Chem. 276 (2001) 45662-45668
34. Vozza A., Blanco E., Palmieri L., and Palmieri F. Identification of the mitochondrial GTP/GDP transporter in Saccharomyces cerevisiae. J. Biol. Chem. 279 (2004) 20850-20857
35. Lesuisse E., Lyver E.R., Knight S.A., and Dancis A. Role of YHM1, encoding a mitochondrial carrier protein, in iron distribution of yeast. Biochem. J. 378 (2004) 599-607
36. Knight S.A., Kim R., Pain D., and Dancis A. The yeast connection to Friedreich ataxia. Am. J. Hum. Genet. 64 (1999) 365-371
37. Desmyter L., Dewaele S., Reekmans R., Nystrom T., Contreras R., and Chen C. Expression of the human ferritin light chain in a frataxin mutant yeast affects ageing and cell death. Exp. Gerontol. 39 (2004) 707-715
38. Nystrom T. Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 24 (2005) 1311-1317
39. Ding Q., Dimayuga E., and Keller J.N. Proteasome regulation of oxidative stress in aging and age-related diseases of the CNS. Antioxid. Redox Signaling 8 (2006) 163-172
40. Chen X.J., Wang X., Kaufman B.A., and Butow R.A. Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 307 (2005) 714-717
41. Bateman J.M., Iacovino M., Perlman P.S., and Butow R.A. Mitochondrial DNA instability mutants of the bifunctional protein Ilv5p have altered organization in mitochondria and are targeted for degradation by Hsp78 and the Pim1p protease. J. Biol. Chem. 277 (2002) 47946-47953
42. Squier T.C. Redox modulation of cellular metabolism through targeted degradation of signaling proteins by the proteasome. Antioxid. Redox Signaling 8 (2006) 217-228
43. Grune T., and Davies K.J. The proteasomal system and HNE-modified proteins. Mol. Aspects Med. 24 (2003) 195-204
44. Chen Q., Thorpe J., Dohmen J.R., Li F., and Keller J.N. Ump1 extends yeast lifespan and enhances viability during oxidative stress: central role for the proteasome?. Free Radic. Biol. Med. 40 (2006) 120-126
45. Keller J.N. The many nuances of oxidative stress and proteolysis. Antioxid. Redox Signaling 8 (2006) 119-120
46. Sturm B., Bistrich U., Schranzhofer M., Sarsero J.P., Rauen U., Scheiber-Mojdehkar B., de Groot H., Ioannou P., and Petrat F. Friedreich's ataxia, no changes in mitochondrial labile iron in human lymphoblasts and fibroblasts: a decrease in antioxidative capacity?. J. Biol. Chem. 280 (2005) 6701-6708