Human Ind1, an iron-sulfur cluster assembly factor for respiratory complex I

Molecular and Cellular Biology

Volumn 29, Issue 22, 2009, Pages 6059-6073

  Sheftel, Alex D ^a   Stehling, Oliver ^a   Pierik, Antonio J ^a   Netz, Daili J A ^a   Kerscher, Stefan ^b   Elsässer, Hans Peter ^a   Wittig, Ilka ^b   Balk, Janneke ^c   Brandt, Ulrich ^b   Lill, Roland ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; IRON SULFUR PROTEIN; PROTEIN HUMAN IND1; RESPIRATORY COMPLEX 1; UNCLASSIFIED DRUG;

ARTICLE; CELL STRUCTURE; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; RNA INTERFERENCE;

AMINO ACID MOTIFS; ANIMALS; CATTLE; CELL RESPIRATION; CONSERVED SEQUENCE; CYSTEINE; ELECTRON TRANSPORT COMPLEX I; HELA CELLS; HUMANS; IRON-SULFUR PROTEINS; LACTIC ACID; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NADH DEHYDROGENASE; NUCLEOSIDE-TRIPHOSPHATASE; PROTEIN BINDING; PROTEIN SUBUNITS; RNA INTERFERENCE;

EID: 71949116823     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00817-09     Document Type: Article

References (81)

1. Antonicka, H., I. Ogilvie, T. Taivassalo, R. P. Anitori, R. G. Haller, J. Vissing, N. G. Kennaway, and E. A. Shoubridge. 2003. Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. J. Biol. Chem. 278:43081-43088.
2. Balk, J., D. J. Aguilar Netz, K. Tepper, A. J. Pierik, and R. Lill. 2005. The essential WD40 protein Cia1 is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly. Mol. Cell. Biol. 25:10833-10841.
3. Balk, J., A. J. Pierik, D. J. Netz, U. Mühlenhoff, and R. Lill. 2004. The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J. 23:2105-2115. (Pubitemid 38737737)
4. Benit, P., S. Goncalves, E. P. Dassa, J. J. Briere, and P. Rustin. 2008. The variability of the harlequin mouse phenotype resembles that of human mitochondrial- complex I-deficiency syndromes. PLoS ONE 3:e3208.
5. Biederbick, A., O. Stehling, R. Rösser, B. Niggemeyer, Y. Nakai, H. P. Elsässer, and R. Lill. 2006. Role of human mitochondrial Nfs1 in cytosolic iron-sulfur protein biogenesis and iron regulation. Mol. Cell. Biol. 26:5675-5687.
6. Boyd, J. M., A. J. Pierik, D. J. Netz, R. Lill, and D. M. Downs. 2008. Bacterial ApbC can bind and effectively transfer iron-sulfur clusters. Biochemistry 47:8195-8202.
7. Brandt, U. 2006. Energy converting NADH:quinone oxidoreductase (complex I). Annu. Rev. Biochem. 75:69-92.
8. Bych, K., S. Kerscher, D. J. Netz, A. J. Pierik, K. Zwicker, M. A. Huynen, R. Lill, U. Brandt, and J. Balk. 2008. The iron-sulphur protein Ind1 is required for effective complex I assembly. EMBO J. 27:1736-1746.
9. Bych, K., D. J. Netz, G. Vigani, E. Bill, R. Lill, A. J. Pierik, and J. Balk. 2008. The essential cytosolic iron-sulfur protein Nbp35 acts without Cfd1 partner in the green lineage. J. Biol. Chem. 283:35797-35804.
10. Cavadini, P., G. Biasiotto, M. Poli, S. Levi, R. Verardi, I. Zanella, M. Derosas, R. Ingrassia, M. Corrado, and P. Arosio. 2007. RNA silencing of the mitochondrial ABCB7 transporter in HeLa cells causes an iron-deficient phenotype with mitochondrial iron overload. Blood 109:3552-3559. (Pubitemid 46572549)
11. Detmer, S. A., and D. C. Chan. 2007. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8:870-879.
12. Drapier, J. C., and J. B. Hibbs, Jr. 1996. Aconitases: a class of metalloproteins highly sensitive to nitric oxide synthesis. Methods Enzymol. 269:26-36.
13. Dudkina, N. V., H. Eubel, W. Keegstra, E. J. Boekema, and H. P. Braun. 2005. Structure of a mitochondrial supercomplex formed by respiratorychain complexes I and III. Proc. Natl. Acad. Sci. USA 102:3225-3229.
14. Dunning, C. J., M. McKenzie, C. Sugiana, M. Lazarou, J. Silke, A. Connelly, J. M. Fletcher, D. M. Kirby, D. R. Thorburn, and M. T. Ryan. 2007. Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J. 26:3227-3237.
15. Elsässer, H. P., U. Lehr, B. Agricola, and H. F. Kern. 1993. Structural analysis of a new highly metastatic cell line PaTu 8902 from a primary human pancreatic adenocarcinoma. Virchows Arch. B 64:201-207.
16. Folgero, T., K. Bertheussen, S. Lindal, T. Torbergsen, and P. Oian. 1993. Mitochondrial disease and reduced sperm motility. Hum. Reprod. 8:1863-1868.
17. Fukui, H., and C. T. Moraes. 2008. The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci. 31:251-256.
18. Gelling, C., I. W. Dawes, N. Richhardt, R. Lill, and U. Mühlenhoff. 2008. Mitochondrial Iba57p is required for Fe/S cluster formation on aconitase and activation of radical SAM enzymes. Mol. Cell. Biol. 28:1851-1861.
19. Gilkerson, R. W., D. H. Margineantu, R. A. Capaldi, and J. M. Selker. 2000. Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells. FEBS Lett. 474:1-4.
20. Hackenbrock, C. R. 1966. Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J. Cell Biol. 30:269-297.
21. Hales, K. G., and M. T. Fuller. 1997. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90:121-129.
22. Harlow, E., and D. Lane. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
23. Hatefi, Y., and D. L. Stiggall. 1978. Preparation and properties of succinate: ubiquinone oxidoreductase (complex II). Methods Enzymol. 53:21-27.
24. Hausmann, A., D. J. Aguilar Netz, J. Balk, A. J. Pierik, U. Mühlenhoff, and R. Lill. 2005. The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc. Natl. Acad. Sci. USA 102:3266-3271.
25. Hollingworth, R. M., K. I. Ahammadsahib, G. Gadelhak, and J. L. McLaughlin. 1994. New inhibitors of complex I of the mitochondrial electron transport chain with activity as pesticides. Biochem. Soc. Trans. 22:230-233.
26. Howell, B. F., S. McCune, and R. Schaffer. 1979. Lactate-to-pyruvate or pyruvate-to-lactate assay for lactate dehydrogenase: a re-examination. Clin. Chem. 25:269-272.
27. Janssen, R., J. Smeitink, R. Smeets, and L. van den Heuvel. 2002. CIA30 complex I assembly factor: a candidate for human complex I deficiency? Hum. Genet. 110:264-270. (Pubitemid 36067447)
28. Kirby, D. M., M. Crawford, M. A. Cleary, H. H. Dahl, X. Dennett, and D. R. Thorburn. 1999. Respiratory chain complex I deficiency: an underdiagnosed energy generation disorder. Neurology 52:1255-1264. (Pubitemid 29177931)
29. Kispal, G., P. Csere, C. Prohl, and R. Lill. 1999. The mitochondrial proteins Atm1p and Nfs1p are essential for biogenesis of cytosolic Fe/S proteins. EMBO J. 18:3981-3989. (Pubitemid 29335851)
30. Lazarou, M., D. R. Thorburn, M. T. Ryan, and M. McKenzie. 2009. Assembly of mitochondrial complex I and defects in disease. Biochim. Biophys. Acta 1793:78-88.
31. Leipe, D. D., Y. I. Wolf, E. V. Koonin, and L. Aravind. 2002. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 317:41-72.
32. Lill, R. 2009. Function and biogenesis of iron-sulphur proteins. Nature 460:831-838.
33. Lill, R., and U. Mühlenhoff. 2008. Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem. 77:669-700.
34. Martelli, A., M. Wattenhofer-Donze, S. Schmucker, S. Bouvet, L. Reutenauer, and H. Puccio. 2007. Frataxin is essential for extramitochondrial Fe-S cluster proteins in mammalian tissues. Hum. Mol. Genet. 16:2651-2658.
35. Martinez-Medellin, J., and H. M. Schulman. 1972. The kinetics of iron and transferrin incorporation into rabbit erythroid cells and the nature of stromal- bound iron. Biochim. Biophys. Acta 264:272-274.
36. Moreadith, R. W., M. L. Batshaw, T. Ohnishi, D. Kerr, B. Knox, D. Jackson, R. Hruban, J. Olson, B. Reynafarje, and A. L. Lehninger. 1984. Deficiency of the iron-sulfur clusters of mitochondrial reduced nicotinamide-adenine dinucleotide-ubiquinone oxidoreductase (complex I) in an infant with congenital lactic acidosis. J. Clin. Investig. 74:685-697.
37. Netz, D. J., A. J. Pierik, M. Stümpfig, U. Mühlenhoff, and R. Lill. 2007. The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol. Nat. Chem. Biol. 3:278-286.
38. Ogilvie, I., N. G. Kennaway, and E. A. Shoubridge. 2005. A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. J. Clin. Investig. 115:2784-2792.
39. Okun, J. G., P. Lummen, and U. Brandt. 1999. Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH: ubiquinone oxidoreductase). J. Biol. Chem. 274:2625-2630.
40. Okun, J. G., V. Zickermann, K. Zwicker, H. Schagger, and U. Brandt. 2000. Binding of detergents and inhibitors to bovine complex I-a novel purification procedure for bovine complex I retaining full inhibitor sensitivity. Biochim. Biophys. Acta 1459:77-87.
41. Orme-Johnson, W. H., and N. R. Orme-Johnson. 1978. Overview of ironsulfur proteins. Methods Enzymol. 53:259-268.
42. Pagani, S., G. Vecchio, S. Iametti, R. Bianchi, and F. Bonomi. 1986. On the role of the 2Fe-2S cluster in the formation of the structure of spinach ferredoxin. Biochim. Biophys. Acta 870:538-544.
43. Pagliarini, D. J., S. E. Calvo, B. Chang, S. A. Sheth, S. B. Vafai, S. E. Ong, G. A. Walford, C. Sugiana, A. Boneh, W. K. Chen, D. E. Hill, M. Vidal, J. G. Evans, D. R. Thorburn, S. A. Carr, and V. K. Mootha. 2008. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112-123.
44. Pondarré, C., B. B. Antiochos, D. R. Campagna, S. L. Clarke, E. L. Greer, K. M. Deck, A. McDonald, A. P. Han, A. Medlock, J. L. Kutok, S. A. Anderson, R. S. Eisenstein, and M. D. Fleming. 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.
45. Richardson, D. R., P. Ponka, and D. Vyoral. 1996. Distribution of iron in reticulocytes after inhibition of heme synthesis with succinylacetone: examination of the intermediates involved in iron metabolism. Blood 87:3477-3488.
46. Rossignol, R., R. Gilkerson, R. Aggeler, K. Yamagata, S. J. Remington, and R. A. Capaldi. 2004. Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res. 64:985-993. (Pubitemid 38176901)
47. Rouault, T. A., and W. H. Tong. 2005. Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat. Rev. Mol. Cell Biol. 6:345-351.
48. Roy, A., N. Solodovnikova, T. Nicholson, W. Antholine, and W. E. Walden. 2003. A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J. 22:4826-4835. (Pubitemid 37162918)
49. Saada, A., S. Edvardson, M. Rapoport, A. Shaag, K. Amry, C. Miller, H. Lorberboum-Galski, and O. Elpeleg. 2008. C6ORF66 is an assembly factor of mitochondrial complex I. Am. J. Hum. Genet. 82:32-38.
50. Saada, A., R. O. Vogel, S. J. Hoefs, M. A. van den Brand, H. J. Wessels, P. H. Willems, H. Venselaar, A. Shaag, F. Barghuti, O. Reish, M. Shohat, M. A. Huynen, J. A. Smeitink, L. P. van den Heuvel, and L. G. Nijtmans. 2009. Mutations in NDUFAF3 (C3ORF60), encoding an NDUFAF4 (C6ORF66)-interacting complex I assembly protein, cause fatal neonatal mitochondrial disease. Am. J. Hum Genet. 84:718-727.
51. Sazanov, L. A., and P. Hinchliffe. 2006. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430-1436.
52. Schägger, H. 2003. Blue native electrophoresis, p. 105-130. In C. Hunte, G. von Jagow, and H. Schägger (ed.), Membrane protein purification and crystallization. A practical guide, 2nd ed. Academic Press, New York, NY.
53. Schägger, H. 2006. Tricine-SDS-PAGE. Nat. Protoc. 1:16-22.
54. Schägger, H., R. de Coo, M. F. Bauer, S. Hofmann, C. Godinot, and U. Brandt. 2004. Significance of respirasomes for the assembly/stability of human respiratory chain complex I. J. Biol. Chem. 279:36349-36353.
55. Schägger, H., and K. Pfeiffer. 2000. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J. 19:1777-1783. (Pubitemid 30204389)
56. Smeitink, J., L. van den Heuvel, and S. DiMauro. 2001. The genetics and pathology of oxidative phosphorylation. Nat. Rev. Genet. 2:342-352.
57. Smith, D. G., R. M. Gawryluk, D. F. Spencer, R. E. Pearlman, K. W. Siu, and M. W. Gray. 2007. Exploring the mitochondrial proteome of the ciliate protozoon Tetrahymena thermophila: direct analysis by tandem mass spectrometry. J. Mol. Biol. 374:837-863.
58. Song, D., and F. S. Lee. 2008. A role for IOP1 in mammalian cytosolic iron-sulfur protein biogenesis. J. Biol. Chem. 283:9231-9238.
59. Srere, P. A., H. Brazil, and L. Gonen. 1963. The citrate condensing enzyme of pigeon breast muscle and moth flight muscle. Acta Chem. Scand. 17(Suppl.):S129-S134.
60. Stehling, O., H. P. Elsässer, B. Brückel, U. Mühlenhoff, and R. Lill. 2004. Iron-sulfur protein maturation in human cells: evidence for a function of frataxin. Hum. Mol. Genet. 13:3007-3015.
61. Stehling, O., D. J. Netz, B. Niggemeyer, R. Rösser, R. S. Eisenstein, H. Puccio, A. J. Pierik, and R. Lill. 2008. Human Nbp35 is essential for both cytosolic iron-sulfur protein assembly and iron homeostasis. Mol. Cell. Biol. 28:5517-5528.
62. Stevens, B. 1981. Mitochondrial structure, p. 471-488. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces: life cycle and inheritance, 1st ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
63. Sugiana, C., D. J. Pagliarini, M. McKenzie, D. M. Kirby, R. Salemi, K. K. Abu-Amero, H. H. Dahl, W. M. Hutchison, K. A. Vascotto, S. M. Smith, R. F. Newbold, J. Christodoulou, S. Calvo, V. K. Mootha, M. T. Ryan, and D. R. Thorburn. 2008. Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am. J. Hum. Genet. 83:468-478.
64. Tan, G., J. Lu, J. P. Bitoun, H. Huang, and H. Ding. 2009. IscA/SufA paralogues are required for the [4Fe-4S] cluster assembly in enzymes of multiple physiological pathways in Escherichia coli under aerobic growth conditions. Biochem. J. 420:463-472.
65. Tong, W. H., and T. A. Rouault. 2006. Functions of mitochondrial ISCU and cytosolic ISCU in mammalian iron-sulfur cluster biogenesis and iron homeostasis. Cell Metab. 3:199-210.
66. Trounce, I. A., Y. L. Kim, A. S. Jun, and D. C. Wallace. 1996. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol. 264:484-509. (Pubitemid 26089333)
67. Vahsen, N., C. Cande, J. J. Briere, P. Benit, N. Joza, N. Larochette, P. G. Mastroberardino, M. O. Pequignot, N. Casares, V. Lazar, O. Feraud, N. Debili, S. Wissing, S. Engelhardt, F. Madeo, M. Piacentini, J. M. Penninger, H. Schagger, P. Rustin, and G. Kroemer. 2004. AIF deficiency compromises oxidative phosphorylation. EMBO J. 23:4679-4689. (Pubitemid 39657867)
68. Vogel, R. O., C. E. Dieteren, L. P. van den Heuvel, P. H. Willems, J. A. Smeitink, W. J. Koopman, and L. G. Nijtmans. 2007. Identification of mitochondrial complex I assembly intermediates by tracing tagged NDUFS3 demonstrates the entry point of mitochondrial subunits. J. Biol. Chem. 282:7582-7590.
69. Vogel, R. O., R. J. Janssen, C. Ugalde, M. Grovenstein, R. J. Huijbens, H. J. Visch, L. P. van den Heuvel, P. H. Willems, M. Zeviani, J. A. Smeitink, and L. G. Nijtmans. 2005. Human mitochondrial complex I assembly is mediated by NDUFAF1. FEBS J. 272:5317-5326. (Pubitemid 41503160)
70. Vogel, R. O., R. J. Janssen, M. A. van den Brand, C. E. Dieteren, S. Verkaart, W. J. Koopman, P. H. Willems, W. Pluk, L. P. van den Heuvel, J. A. Smeitink, and L. G. Nijtmans. 2007. Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Genes Dev. 21:615-624.
71. Vogel, R. O., J. A. Smeitink, and L. G. Nijtmans. 2007. Human mitochondrial complex I assembly: a dynamic and versatile process. Biochim. Biophys. Acta 1767:1215-1227.
72. Vyoral, D., and J. Petrak. 1998. Iron transport in K562 cells: a kinetic study using native gel electrophoresis and 59Fe autoradiography. Biochim. Biophys. Acta 1403:179-188.
73. Wittig, I., H. P. Braun, and H. Schägger. 2006. Blue native PAGE. Nat. Protoc. 1:418-428.
74. Wittig, I., R. Carrozzo, F. M. Santorelli, and H. Schägger. 2007. Functional assays in high-resolution clear native gels to quantify mitochondrial complexes in human biopsies and cell lines. Electrophoresis 28:3811-3820. (Pubitemid 350143117)
75. Wittig, I., M. Karas, and H. Schägger. 2007. High resolution clear native electrophoresis for in-gel functional assays and fluorescence studies of membrane protein complexes. Mol. Cell. Proteomics 6:1215-1225.
76. Wittung-Stafshede, P. 2002. Role of cofactors in protein folding. Acc. Chem. Res. 35:201-208.
77. Yano, T., V. D. Sled', T. Ohnishi, and T. Yagi. 1996. Expression and characterization of the flavoprotein subcomplex composed of 50-kDa (NQO1) and 25-kDa (NQO2) subunits of the proton-translocating NADH-quinone oxidoreductase of Paracoccus denitrificans. J. Biol. Chem. 271:5907-5913. (Pubitemid 26083934)
78. Yano, T., T. Yagi, V. D. Sled', and T. Ohnishi. 1995. Expression and characterization of the 66-kilodalton (NQO3) iron-sulfur subunit of the protontranslocating NADH-quinone oxidoreductase of Paracoccus denitrificans. J. Biol. Chem. 270:18264-18270.
79. Zhang, Y., E. R. Lyver, E. Nakamaru-Ogiso, H. Yoon, B. Amutha, D. W. Lee, E. Bi, T. Ohnishi, F. Daldal, D. Pain, and A. Dancis. 2008. Dre2, a conserved eukaryotic Fe/S cluster protein, functions in cytosolic Fe/S protein biogenesis. Mol. Cell. Biol. 28:5569-5582.
80. Zheng, L., U. Baumann, and J. L. Reymond. 2004. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 32:e115.
81. Zhou, G., S. S. Broyles, J. E. Dixon, and H. Zalkin. 1992. Avian glutamine phosphoribosylpyrophosphate amidotransferase propeptide processing and activity are dependent upon essential cysteine residues. J. Biol. Chem. 267:7936-7942.