Frataxin is essential for extramitochondrial Fe - S cluster proteins in mammalian tissues

Human Molecular Genetics

Volumn 16, Issue 22, 2007, Pages 2651-2658

  Martelli, Alain ^a   Wattenhofer donzé, Marie ^a,e   Schmucker, Stéphane ^a,d   Bouvet, Samuel ^a   Reutenauer, Laurence ^a,c   Puccio, Hélène ^a,b,c,d,e  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e l'alimentation et l'Environnement   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDOPHOSPHORIBOSYLTRANSFERASE; ENDONUCLEASE; FRATAXIN; IRON SULFUR PROTEIN; PROTEIN NTH 1; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; XANTHINE OXIDASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; GENE DELETION; MAMMAL; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; CYTOSOL; FRIEDREICH ATAXIA; IRON; IRON-BINDING PROTEINS; IRON-SULFUR PROTEINS; MICE; MICE, TRANSGENIC; MITOCHONDRIA; MUTATION; SULFUR;

MAMMALIA;

EID: 35449008450     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm163     Document Type: Article

References (41)

1. Harding, A.E. (1981) Friedreich's ataxia: A clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features. Brain, 104, 589-620.
2. 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.
3. Rotig, A., de Lonlay, P., Chretien, D., Foury, F., Koenig, M., Sidi, D., Munnich, A. and Rustin, P. (1997) Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia. Nat. Genet., 17, 215-217.
4. 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.
5. Muhlenhoff, U., Gerber, J., Richhardt, N. and Lill, R. (2003) Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isulp. Embo J., 22, 4815-4825.
6. Duby, G., Foury, F., Ramazzotti, A., Herrmann, J. and Lutz, T. (2002) A non-essential function for yeast frataxin in iron-sulfur cluster assembly. Hum. Mol. Genet., 11, 2635-2643.
7. 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.
8. 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.
9. 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.
10. Layer, G., Ollagnier-de Choudens, S., Sanakis, Y. and Fontecave, M. (2006) Iron-sulfur cluster biosynthesis: Characterization of Escherichia coli CYaY as an iron donor for the assembly of [2Fe-2S] clusters in the scaffold IscU. J Bio. Chem., 281, 16256-16263.
11. 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.
12. Lill, R., Dutkiewicz, R., Elsasser, H.P., Hausmann, A., Netz, D.J., Pierik, A.J., Stehling, O., Urzica, E. and Muhlenhoff, U. (2006) Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes. Biochim, Biophys. Acta, 1763, 652-667.
13. Lutz, T., Westermann, B., Neupert, W. and Herrmann, J.M. (2001) The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulfur clusters in mitochondria. J Mol Biol, 307, 815-825.
14. Kispal, G., Csere, P., Prohl, C. and Lill, R. (1999) The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J., 18, 3981-3989.
15. Li, K., Tong, W.H., Hughes, R.M. and Rouault, T.A. (2006) Roles of the mammalian cytosolic cysteine desulfurase, ISCS, and scaffold protein, ISCU, in iron-sulfur cluster assembly. J. Biol. Chem., 281, 12344-12351.
16. Acquaviva, F., De Biase, I., Nezi, L., Ruggiero, G., Tatangelo, F., Pisano, C., Monticelli, A., Garbi, C., Acquaviva, A.M. and Cocozza, S. (2005) Extra-mitochondrial localisation of frataxin and its association with IscU1 during enterocyte-like differentiation of the human colon adenocarcinoma cell line Caco-2. J. Cell. Sci., 118, 3917-3924.
17. Condo, I., Ventura, N., Malisan, F., Tomassini, B. and Testi, R. (2006) A pool of extramitochondrial frataxin that promotes cell survival. J. Biol. Chem., 281; 16750-16756.
18. Lu, C. and Cortopassi, G. (2007) Frataxin knockdown causes loss of cytoplasmic iron-sulfur cluster functions, redox alterations and induction of heme transcripts. Arch. Biochem. Biophys., 457, 111-122.
19. Fosset, C., Chauveau, M.J., Guillon, B., Canal, F., Drapier, J.C. and Bouton, C. (2006) RNA silencing of mitochondrial m-Nfs1 reduces Fe-S enzyme activity both in mitochondria and cytosol of mammalian cells. J. Biol. Chem., 281, 25398-25406.
20. Biederbick, A., Stehling, O., Rosser, R., Niggemeyer, B., Nakai, Y., Elsasser, H.P. and Lill, R. (2006) Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell. Biol., 26, 5675-5687.
21. Pondarre, C., Antiochos, B.B., Campagna, D.R., Clarke, S.L., Greer, E.L., Deck, K.M., McDonald, A., Han, A.P., Medlock, A., Kutok, J.L. et al. (2006) The mitochondrial ATP-binding cassette transporter Abcb7 is essential in mice and participates in cytosolic iron-sulfur cluster biogenesis. Hum. Mol. Genet., 15, 953-964.
22. Seznec, H., Simon, D., Bouton, C., Reutenauer, L., Hertzog, A., Golik, P., Procaccio, V., Patel, M., Drapier, J.C., Koenig, M. et a. (2005) Friedreich ataxia: The oxidative stress paradox. Hum. Mol. Genet., 14, 463-474.
23. Stehling, O., Elsasser, H.P., Bruckel, B., Muhlenhoff, U. and Lill, R. (2004) Iron-sulfur protein maturation in human cells: Evidence for a function of frataxin. Hum. Mol. Genet., 13, 3007-3015.
24. Harrison, R. (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic. Biol. Med., 33, 774-797.
25. Zhou, G., Broyles, S.S., Dixon, J.E. and Zalkin, H. (1992) Avian glutamine phosphoribosylpyrophosphate amidotransferase propeptide processing and activity are dependent upon essential cysteine residues. J. Biol. Chem., 267, 7936-7942.
26. Ide, H. and Kotera, M. (2004) Human DNA glycosylases involved in the repair of oxidatively damaged DNA. Biol. Pharm. Bull., 27, 480-485.
27. Takao, M., Kanno, S., Kobayashi, K., Zhang, Q.M., Yonei, S., van der Horst, G.T. and Yasui, A. (2002) A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J. Biol. Chem., 277, 42205-42213.
28. Schoenfeld, R.A., Napoli, E., Wong, A., Zhan, S., Reutenauer, L., Morin, D., Buckpitt, A.R., Taroni, F., Lonnerdal, B., Ristow, M. et al. (2005) Frataxin deficiency alters heme pathway transcripts and decreases mitochondrial heme metabolites in mammalian cells. Hum. Mol. Genet. 14, 3787-3799.
29. 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.
30. Bulteau, A.L., Ikeda-Saito, M. and Szweda, L.I. (2003) Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42, 14846-14855.
31. Layer, G., Heinz, D.W., Jahn, D. and Schubert, W.D. (2004) Structure and function of radical SAM enzymes. Curr. Opin. Chem. Biol., 8, 468-476.
32. Hanzelmann, P., Hernandez, H.L., Menzel, C., Garcia-Serres, R., Huynh, B.H., Johnson, M.K., Mendel, R.R. and Schindelin, H. (2004) Characterization of MOCS1A, an oxygen-sensitive iron-sulfur protein involved in human molybdenum cofactor biosynthesis. J. Biol. Chem. 279, 34721-34732.
33. Tong, W.H. and Rouault, T. (2000) Distinct iron-sulfur cluster assembly complexes exist in the cytosol and mitochondria of human cells. EMBO J., 19, 5692-5700.
34. Tong, W.H. and Rouault, T.A. (2006) Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis. Cell. Metab., 3, 199-210.
35. Tan, G., Napoli, E., Taroni, F. and Cortopassi, G. (2003) Decreased expression of genes involved in sulfur amino acid metabolism in frataxin-deficient cells. Hum. Mol. Genet., 12, 1699-1711.
36. Rudolf, J., Makrantoni, V., Ingledew, W.J., Stark, M.J. and White, M.F. (2006) The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol. Cell. Biol., 23, 801-808.
37. Paulson, H.L. and Miller, V.M. (2005) Breaks in coordination: DNA repair in inherited ataxia. Neuron, 46, 845-848.
38. Postic, C., Shiota, M., Niswender, K.D., Jetton, T.L., Chen, Y., Moates, J.M., Shelton, K.D., Lindner, J., Cherrington, A.D. and Magnuson, M.A. (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem., 274, 305-315.
39. Takao, M., Kanno, S., Shiromoto, T., Hasegawa, R., Ide, H., Ikeda, S., Sarker, A.H., Seki, S., Xing, J.Z., Le, X.C. et al. (2002) Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse Nth1 gene encoding an endonuclease III homolog for repair of thymine glycols. EMBO J., 21, 3486-3493.
40. Beckman, J.S., Parks, D.A., Pearson, J.D., Marshall, P.A. and Freeman, B.A. (1989) A sensitive fluorometric assay for measuring xanthine dehydrogenase and oxidase in tissues. Free Radic. Biol. Med., 6 607-615.
41. Gray, E.G. and Whittaker, V.P. (1962) The isolation of nerve endings from brain: An electron-microscopic study of cell fragments derived by homogenization and centrifugation. J. Anat., 96, 79-88.