A fatal mitochondrial disease is associated with defective NFU1 function in the maturation of a subset of mitochondrial Fe-S proteins

American Journal of Human Genetics

Volumn 89, Issue 5, 2011, Pages 656-667

  Navarro Sastre, Aleix ^a,b   Tort, Frederic ^a,b   Stehling, Oliver ^c   Uzarska, Marta A ^c   Arranz, José Antonio ^d   Del Toro, Mireia ^d   Labayru, M Teresa ^e   Landa, Joseba ^f   Font, Aida ^a,b   Garcia Villoria, Judit ^a,b   Merinero, Begoña ^b,g   Ugarte, Magdalena ^b,g   Gutierrez Solana, Luis Gonzalez ^h   Campistol, Jaume ^b,i   Garcia Cazorla, Angels ^b,i   Vaquerizo, Julian ^j   Riudor, Encarnació ^d   Briones, Paz ^a,b,k   Elpeleg, Orly ^l   Ribes, Antonia ^a,b   Lill, Roland ^c   more..

^a HOSPITAL CLÍNIC   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

^d HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^e HOSPITAL DE CRUCES   (Spain)

^f Hospital Nuestra Senora de Aranzazu   (Spain)

^g UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^h HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

ⁱ HOSPITAL SANT JOAN DE DÉU   (Spain)

^j HOSPITAL INFANTA CRISTINA   (Spain)

^k CSIC   (Spain)

^l HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE CLEAVAGE SYSTEM; IRON SULFUR PROTEIN; MITOCHONDRIAL PROTEIN; NFU1 PROTEIN; PYRUVATE DEHYDROGENASE COMPLEX; THIOCTIC ACID; THIOCTIC ACID SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CAUSE OF DEATH; CELL CULTURE; CHROMOSOME 2; CLINICAL ARTICLE; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE IDENTIFICATION; GENE MAPPING; GENETIC CODE; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HYPERGLYCINEMIA; INFANT; LACTIC ACIDOSIS; LIPOYLATION; MALE; MISSENSE MUTATION; MITOCHONDRIAL ENCEPHALOPATHY; MITOCHONDRIAL PULMONARY HYPERTENSION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PULMONARY HYPERTENSION; RNA INTERFERENCE; SACCHAROMYCES CEREVISIAE; SPLICING DEFECT;

AMINO ACID OXIDOREDUCTASES; CARRIER PROTEINS; CHROMOSOMES, HUMAN, PAIR 2; FEMALE; HELA CELLS; HOMOZYGOTE; HUMANS; HYPERTENSION; INFANT; IRON-SULFUR PROTEINS; MALE; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL PROTEINS; MULTIENZYME COMPLEXES; MUTATION, MISSENSE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SUCCINATE DEHYDROGENASE; SULFURTRANSFERASES; THIOCTIC ACID; TRANSFERASES;

SACCHAROMYCES CEREVISIAE;

EID: 80955133245     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2011.10.005     Document Type: Article

References (38)

1. R. Lill Function and biogenesis of iron-sulphur proteins Nature 460 2009 831 838
2. H. Ye, and T.A. Rouault Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease Biochemistry 49 2010 4945 4956
3. A. Sheftel, O. Stehling, and R. Lill Iron-sulfur proteins in health and disease Trends Endocrinol. Metab. 21 2010 302 314
4. B. Schilke, C. Voisine, H. Beinert, and E. Craig Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 96 1999 10206 10211
5. W.H. Tong, G.N. Jameson, B.H. Huynh, and T.A. Rouault Subcellular compartmentalization of human Nfu, an iron-sulfur cluster scaffold protein, and its ability to assemble a [4Fe-4S] cluster Proc. Natl. Acad. Sci. USA 100 2003 9762 9767
6. J.K. Hiltunen, K.J. Autio, M.S. Schonauer, V.A. Kursu, C.L. Dieckmann, and A.J. Kastaniotis Mitochondrial fatty acid synthesis and respiration Biochim. Biophys. Acta 1797 2010 1195 1202
7. M. Duran, F.A. Beemer, S.K. Wadman, U. Wendel, and B. Janssen A patient with alpha-ketoadipic and alpha-aminoadipic aciduria J. Inherit. Metab. Dis. 7 1984 61
8. N. Rodríguez-Ezpeleta, J. Alvarez-Busto, L. Imaz, M. Regueiro, M.N. Azcárate, R. Bilbao, M. Iriondo, A. Gil, A. Estonba, and A.M. Aransay High-density SNP genotyping detects homogeneity of Spanish and French Basques, and confirms their genomic distinctiveness from other European populations Hum. Genet. 128 2010 113 117
9. D.C. Johnson, D.R. Dean, A.D. Smith, and M.K. Johnson Structure, function, and formation of biological iron-sulfur clusters Annu. Rev. Biochem. 74 2005 247 281
10. H. Beinert A tribute to sulfur Eur. J. Biochem. 267 2000 5657 5664
11. P. Yuvaniyama, J.N. Agar, V.L. Cash, M.K. Johnson, and D.R. Dean NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein Proc. Natl. Acad. Sci. USA 97 2000 599 604
12. B. Touraine, J.P. Boutin, A. Marion-Poll, J.F. Briat, G. Peltier, and S. Lobréaux Nfu2: A scaffold protein required for [4Fe-4S] and ferredoxin iron-sulphur cluster assembly in Arabidopsis chloroplasts Plant J. 40 2004 101 111
13. T. Yabe, K. Morimoto, S. Kikuchi, K. Nishio, I. Terashima, and M. Nakai The Arabidopsis chloroplastic NifU-like protein CnfU, which can act as an iron-sulfur cluster scaffold protein, is required for biogenesis of ferredoxin and photosystem I Plant Cell 16 2004 993 1007
14. R. Balasubramanian, G. Shen, D.A. Bryant, and J.H. Golbeck Regulatory roles for IscA and SufA in iron homeostasis and redox stress responses in the cyanobacterium Synechococcus sp. strain PCC 7002 J. Bacteriol. 188 2006 3182 3191
15. S. Angelini, C. Gerez, S. Ollagnier-de Choudens, Y. Sanakis, M. Fontecave, F. Barras, and B. Py NfuA, a new factor required for maturing Fe/S proteins in Escherichia coli under oxidative stress and iron starvation conditions J. Biol. Chem. 283 2008 14084 14091
16. S. Bandyopadhyay, S.G. Naik, I.P. O'Carroll, B.H. Huynh, D.R. Dean, M.K. Johnson, and P.C. Dos Santos A proposed role for the Azotobacter vinelandii NfuA protein as an intermediate iron-sulfur cluster carrier J. Biol. Chem. 283 2008 14092 14099
17. S.J. Booker, R.M. Cicchillo, and T.L. Grove Self-sacrifice in radical S-adenosylmethionine proteins Curr. Opin. Chem. Biol. 11 2007 543 552
18. I. Padmalayam, S. Hasham, U. Saxena, and S. Pillarisetti Lipoic acid synthase (LASY): A novel role in inflammation, mitochondrial function, and insulin resistance Diabetes 58 2009 600 608
19. O. Stehling, D.J. Netz, B. Niggemeyer, R. Rösser, R.S. Eisenstein, H. Puccio, A.J. Pierik, and R. Lill Human Nbp35 is essential for both cytosolic iron-sulfur protein assembly and iron homeostasis Mol. Cell. Biol. 28 2008 5517 5528
20. O. Stehling, A.D. Sheftel, and R. Lill Chapter 12 Controlled expression of iron-sulfur cluster assembly components for respiratory chain complexes in mammalian cells Methods Enzymol. 456 2009 209 231
21. A.D. Sheftel, O. Stehling, A.J. Pierik, H.P. Elsässer, U. Mühlenhoff, H. Webert, A. Hobler, F. Hannemann, R. Bernhardt, and R. Lill Humans possess two mitochondrial ferredoxins, Fdx1 and Fdx2, with distinct roles in steroidogenesis, heme, and Fe/S cluster biosynthesis Proc. Natl. Acad. Sci. USA 107 2010 11775 11780
22. W.H. Tong, and T.A. Rouault Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis Cell Metab. 3 2006 199 210
23. A. Olsson, L. Lind, L.E. Thornell, and M. Holmberg Myopathy with lactic acidosis is linked to chromosome 12q23.3-24.11 and caused by an intron mutation in the ISCU gene resulting in a splicing defect Hum. Mol. Genet. 17 2008 1666 1672
24. F. Mochel, M.A. Knight, W.H. Tong, D. Hernandez, K. Ayyad, T. Taivassalo, P.M. Andersen, A. Singleton, T.A. Rouault, K.H. Fischbeck, and R.G. Haller Splice mutation in the iron-sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance Am. J. Hum. Genet. 82 2008 652 660
25. A.J. Pierik, D.J. Netz, and R. Lill Analysis of iron-sulfur protein maturation in eukaryotes Nat. Protoc. 4 2009 753 766
26. A.P. Yeh, C. Chatelet, S.M. Soltis, P. Kuhn, J. Meyer, and D.C. Rees Structure of a thioredoxin-like [2Fe-2S] ferredoxin from Aquifex aeolicus J. Mol. Biol. 300 2000 587 595
27. M.C. Unciuleac, K. Chandramouli, S. Naik, S. Mayer, B.H. Huynh, M.K. Johnson, and D.R. Dean In vitro activation of apo-aconitase using a [4Fe-4S] cluster-loaded form of the IscU [Fe-S] cluster scaffolding protein Biochemistry 46 2007 6812 6821
28. U. Muhlenhoff, N. Richter, O. Pines, A.J. Pierik, and R. Lill Specialized function of yeast Isa1 and Isa2 in the maturation of mitochondrial [4Fe-4S] proteins J. Biol. Chem. 2011 10.1074/jbc.M111.296152 In Press. Published online October 10, 2011
29. U. Mühlenhoff, J. Gerber, N. Richhardt, and R. Lill Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p EMBO J. 22 2003 4815 4825
30. C. Gelling, I.W. Dawes, N. Richhardt, R. Lill, and U. Mühlenhoff Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes Mol. Cell. Biol. 28 2008 1851 1861
31. U. Mühlenhoff, M.J. Gerl, B. Flauger, H.M. Pirner, S. Balser, N. Richhardt, R. Lill, and J. Stolz The ISC [corrected] proteins Isa1 and Isa2 are required for the function but not for the de novo synthesis of the Fe/S clusters of biotin synthase in Saccharomyces cerevisiae Eukaryot. Cell 6 2007 495 504
32. K. Bych, S. Kerscher, D.J. Netz, A.J. Pierik, K. Zwicker, M.A. Huynen, R. Lill, U. Brandt, and J. Balk The iron-sulphur protein Ind1 is required for effective complex I assembly EMBO J. 27 2008 1736 1746
33. A.D. Sheftel, O. Stehling, A.J. Pierik, D.J. Netz, S. Kerscher, H.P. Elsässer, I. Wittig, J. Balk, U. Brandt, and R. Lill Human ind1, an iron-sulfur cluster assembly factor for respiratory complex I Mol. Cell. Biol. 29 2009 6059 6073
34. A. Seyda, R.F. Newbold, T.J. Hudson, A. Verner, N. MacKay, S. Winter, A. Feigenbaum, S. Malaney, D. Gonzalez-Halphen, A.P. Cuthbert, and B.H. Robinson A novel syndrome affecting multiple mitochondrial functions, located by microcell-mediated transfer to chromosome 2p14-2p13 Am. J. Hum. Genet. 68 2001 386 396
35. X. Yi, and N. Maeda Endogenous production of lipoic acid is essential for mouse development Mol. Cell. Biol. 25 2005 8387 8392
36. A. Rötig, P. de Lonlay, D. Chretien, F. Foury, M. Koenig, D. Sidi, A. Munnich, and P. Rustin Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich ataxia Nat. Genet. 17 1997 215 217
37. C. Camaschella, A. Campanella, L. De Falco, L. Boschetto, R. Merlini, L. Silvestri, S. Levi, and A. Iolascon The human counterpart of zebrafish shiraz shows sideroblastic-like microcytic anemia and iron overload Blood 110 2007 1353 1358
38. D. Song, Z. Tu, and F.S. Lee Human ISCA1 interacts with IOP1/NARFL and functions in both cytosolic and mitochondrial iron-sulfur protein biogenesis J. Biol. Chem. 284 2009 35297 35307