Frataxin interacts functionally with mitochondrial electron transport chain proteins

Human Molecular Genetics

Volumn 14, Issue 15, 2005, Pages 2091-2098

  González Cabo, Pilar ^a   Vázquez Manrique, Rafael P ^a,b   García Gimeno, M Adelaida ^a   Sanz, Pascual ^a   Palau, Francesc ^a  

^a INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSFERRING FLAVOPROTEIN; FRATAXIN; MULTIENZYME COMPLEX; PROTEIN SUBUNIT; SUCCINATE DEHYDROGENASE;

ARTICLE; CONTROLLED STUDY; ENZYME SUBUNIT; EXPERIMENTATION; FRIEDREICH ATAXIA; FUNGAL GENE; GENETIC ANALYSIS; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; ORTHOLOGY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; SACCHAROMYCES CEREVISIAE;

ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; IRON-BINDING PROTEINS; MITOCHONDRIA; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SUCCINATE DEHYDROGENASE;

ATAXIA; SACCHAROMYCES CEREVISIAE;

EID: 26444566405     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddi214     Document Type: Article

References (52)

1. Pandolfo, M. (2002) The molecular basis of Friedreich ataxia. Adv. Exp. Med. Biol., 516, 99-118.
2. Palau, F. (2001) Friedreich's ataxia and frataxin: Molecular genetics, evolution and pathogenesis (Review). Int. J. Mol. Med., 7, 581-589.
3. Campuzano, V., Montermini, L., Molto, M.D., Pianese, L., Cossee, M., Cavalcanti, F., Monros, E., Rodius, F., Duclos, F., Monticelli, A. et al. (1996) Friedreich's ataxia: Autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science, 271, 1423-1427.
4. Campuzano, V., Montermini, L., Lutz, Y., Cova, L., Hindelang, C., Jiralerspong, S., Trottier, Y., Kish, S.J.. Faucheux, B., Trouillas, P. et al. (1997) Frataxin is reduced in Friedreich ataxia patients and is associated with mitochondrial membranes. Hum. Mol. Genet., 6, 1771-1780.
5. Babcock, M., de Silva, D., Oaks, R., Davis-Kaplan, S., Jiralerspong, S., Montermini, L., Pandolfo, M. and Kaplan, J. (1997) Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science, 276, 1709-1712.
6. Koutnikova, H., Campuzano, V., Foury, F., Dolle, P., Cazzalini, O. and Koenig, M. (1997) Studies of human, mouse and yeast homologues indicate a mitochondrial function for frataxin. Nat. Genet., 16, 345-351.
7. Priller, J., Scherzer, C.R., Faber, P.W., MacDonald, M.E. and Young, A.B. (1997) Frataxin gene of Friedreich's ataxia is targeted to mitochondria. Ann. Neurol., 42, 265-269.
8. Dhe-Paganon, S., Shigeta, R., Chi, Y.I., Ristow, M. and Shoelson, S.E. (2000) Crystal structure of human frataxin. J. Biol. Chem., 275 30753-30756.
9. Musco, G., Stier, G., Kolmerer, B., Adinolfi, S., Martin, S., Frenkiel, T., Gibson, T. and Pastore, A. (2000) Towards a structural understanding of Friedreich's ataxia: The solution structure of frataxin. Structure Fold Des., 8, 695-707.
10. Gibson, T.J., Koonin, E.V., Musco, G., Pastore, A. and Bork, P. (1996) Friedreich's ataxia protein: Phylogenetic evidence for mitochondrial dysfunction. Trends Neurosci., 19, 465-468.
11. Canizares, J., Blanca, J.M., Navarro, J.A., Monros, E., Palau, F. and Molto, M.D. (2000) dfh is a Drosophila homolog of the Friedreich' ataxia disease gene. Gene, 256, 35-42.
12. Wilson, R.B. and Roof, D.M. (1997) Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nat. Genet., 16, 352-357.
13. Foury, F. and Cazzalini, O. (1997) Deletion of the yeast homologue of the human gene associated with Friedreich' ataxia elicits iron accumulation in mitochondria. FEBS Lett., 411, 373-377.
14. Adamec, J., Rusnak, F., Owen, W.G., Naylor, S., Benson, L.M., Gacy, A.M. and Isaya, G. (2000) Iron-dependent self-assembly of recombinant yeast frataxin: Implications for Friedreich ataxia. Am. J. Hum. Genet., 67, 549-562.
15. Park, S., Gakh, O., O'Neill, H.A., Mangravita, A., Nichol, H., Ferreira, G.C. and Isaya, G. (2003) Yeast frataxin sequentially chaperones and stores iron by coupling protein assembly with iron oxidation. J. Biol. Chem., 278, 31340-31351.
16. Nichol, H., Gakh, O., O'Neill, H.A., Pickering, I.J., Isaya, G. and George, G.N. (2003) Structure of frataxin iron cores: An X-ray absorption spectroscopic study. Biochemistry, 42, 5971-5976.
17. Gerber, J., Muhlenhoff, U. and Lill, R. (2003) An interaction between frataxin and Isu1/Nfs1 that is crucial for Fe/S cluster synthesis on Isu1. EMBO Rep., 4, 906-911.
18. Ramazzotti, A., Vanmansart, V. and Foury, F. (2004) Mitochondrial functional interactions between frataxin and Isu1p, the iron-sulfur cluster scaffold protein in Saccharomyces cerevisiae. FEBS Lett., 557, 215-220.
19. Yoon, T. and Cowan, J.A. (2003) Iron-sulfur cluster biosynthesis. Characterization of frataxin as an iron donor for assembly of [2Fe-2S] clusters in ISU-type proteins. J. Am. Chem. Soc., 125, 6078-6084.
20. Lesuisse, E., Santos, R., Matzanke, B.F., Knight, S.A., Camadro, J.M. and Dancis, A. (2003) Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Hum. Mol. Genet., 12, 879-889.
21. Yoon, T. and Cowan, J.A. (2004) Frataxin-mediated iron delivery to ferrochelatase in the final step of heme biosynthesis. J. Biol. Chem. 279, 25943-25946.
22. Bulteau, A.L., O'Neill, H.A., Kennedy, M.C., Ikeda-Saito, M., Isaya, G. and Szweda, L.I. (2004) Frataxin acts as an iron chaperone protein to modulate mitochondrial aconitase activity. Science, 305, 242-245.
23. Lodi, R., Cooper, J.M., Bradley, J.L., Manners, D., Styles, P., Taylor, D.J. and Schapira, A.H. (1999) Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia. Proc. Natl Acad. Sci. USA, 96, 11492-11495.
24. Ristow, M., Pfister, M.F., Yee, A.J., Schubert, M., Michael, L., Zhang, C.Y., Ueki, K., Michael, M.D., II, Lowell, B.B. and Kahn, C.R. (2000) Frataxin activates mitochondrial energy conversion and oxidative phosphorylation. Proc. Natl Acad. Sci. USA, 97, 12239-12243.
25. Cavadini, P., Gellera, C., Patel, P.I. and Isaya, G. (2000) Human frataxin maintains mitochondrial iron homeostasis in Saccharomyces cerevisiae. Hum. Mol. Genet., 9, 2523-2530.
26. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
27. Buisson, N. and Labbe-Bois, R. (1998) Flavohemoglobin expression and function in Saccharomyces cerevisiae. No relationship with respiration and complex response to oxidative stress. J. Biol. Chem. 273, 9527-9533.
28. Zhao, X.J., Raitt, D., Burke, P.V., Clewell, A.S., Kwast, K.E. and Poylon, R.O. (1996) Function and expression of flavohemoglobin in Saccharomyces cerevisiae. Evidence for a role in the oxidative stress response. J. Biol. Chem., 271, 25131-25138.
29. Casanova, N., O'Brien, K.M., Stahl, B.T., McClure, T. and Poyton, R.O. (2005) Yeast flavohemoglobin, a nitric oxide oxidoreductase, is located in both the cytosol and the mitochondrial matrix. J. Biol. Chem., 280, 7645-7653.
30. Chen, O.S., Hemenway, S. and Kaplan, J. (2002) Inhibition of Fe-S cluster biosynthesis decreases mitochondrial iron export: Evidence that Yfh1p affects Fe-S cluster synthesis. Proc. Natl Acad. Sci. USA, 99, 12321-12326.
31. Muhlenhoff, U., Richhardt, N., Ristow, M., Kispal, G. and Lill, R. (2002) The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Hum. Mol. Genet., 11, 2025-2036.
32. Rotig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munich, A. and Rustin, P. (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet., 17, 215-217.
33. Lemire, B.D. and Oyedotun, K.S. (2002) The Saccharomyces cerevisiae mitochondrial succinate: Ubiquinone oxidoreductase. Biochim. Biophys. Acta, 1553, 102-116.
34. Foury, F. (1999) Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Lett., 456, 281-284.
35. Eaton, S. (2002) Control of mitochondrial beta-oxidation flux. Prog. Lipid Res., 41, 197-239.
36. Busi, M.V., Zabaleta, E.J., Araya, A. and Gomez-Casati, D.F. (2004) Functional and molecular characterization of the frataxin hamolog from Arabidopsis thaliana. FEBS Lett., 576, 141-144.
37. Santos, R., Buisson, N., Knight, S.A., Dancis, A., Camadro, J.M. and Lesuisse, E. (2004) Candida albicans lacking the frataxin homologue: A relevant yeast model for studying the role of frataxin. Mol. Microbiol., 54, 507-519.
38. Puccio, H., Simon, D., Cossee, M., Criqui-Filipe, P., Tiziano, F., Melki, J., Hindelang, C., Matyas, R., Rustin, P. and Koenig, M. (2001) Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nat. Genet., 27, 181-186.
39. Turrens, J.F., Alexandre, A. and Lehninger, A.L. (1985) Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys., 237, 408-414.
40. Senoo-Matsuda, N., Yasuda, K., Tsuda, M., Ohkubo, T., Yoshimura, S., Nakazawa, H., Hartman, P.S. and Ishii, N. (2001) A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J. Biol. Chem., 276, 41553-41558.
41. Wong, A., Yang, J., Cavadini, P., Gellera, C., Lonnerdal, B., Taroni, F. and Cortopassi, G. (1999) The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum. Mol. Genet., 8, 425-430.
42. Rothstein, R.J. (1983) One-step gene disruption in yeast. Methods Enzymol., 101, 202-211.
43. Berben, G., Dumont, J., Gilliquet, V., Bolle, P.A. and Hilger, F. (1991) The YDp plasmids: A uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae. Yeast, 7, 475-477.
44. Song, W. and Carlson, M. (1998) Srb/mediator proteins interact functionally and physically with transcriptional repressor Sfl1. EMBO J., 17, 5757-5765.
45. Mayordomo, I., Regelmann, J., Horak, J. and Sanz, P. (2003) Saccharomyces cerevisiae 14-3-3 proteins Bmh1 and Bmh2 participate in the process of catabolite inactivation of maltose permease. FEBS Lett., 544, 160-164.
46. Fields, S. and Song, O. (1989) A novel genetic system to detect protein-protein interactions. Nature, 340, 245-246.
47. Hollenberg, S.M., Sternglanz, R., Cheng, P.F. and Weintraub, H. (1995) Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell. Biol., 15, 3813-3822.
48. Elledge, S.J., Mulligan, J.T., Ramer, S.W., Spottswood, M. and Davis, R.W. (1991) Lambda YES: A multifunctional cDNA expression vector for the isolation of genes by complementation of yeast and Escherichia coli mutations. Proc. Natl Acad. Sci. USA, 88, 1731-1735.
49. Yang, X., Hubbard, E.J. and Carlson, M. (1992) A protein kinase substrate identified by the two-hybrid system. Science, 257, 680-682.
50. Sanz, P., Alms, G.R., Haystead, T.A. and Carlson, M. (2000) Regulatory interactions between the Reg1-Glc7 protein phosphatase and the Snf1 protein kinase. Mol. Cell Biol., 20, 1321-1328.
51. Daum, G., Bohni, P.C. and Schatz, G. (1982) Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem., 257, 13028-13033.
52. Maneiro, E., Martin, M.A., de Andres, M.C., Lopez-Armada, M.J., Fernandez-Sueiro, J.L., del Hoyo, P., Galdo, F., Arenas, J. and Blanco, F.J. (2003) Mitochondrial respiratory activity is altered in osteoarthritic human articular chondrocytes. Arthritis Rheum., 48, 700-708.