The presence of multiple cellular defects associated with a novel G50E iron-sulfur cluster scaffold protein (ISCU) mutation leads to development of mitochondrial myopathy

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10359-10377

  Prasad Saha, Prasenjit ^a   Praveen, Kumar S K ^a   Srivastava, Shubhi ^a   Sinha, Devanjan ^a   Pareek, Gautam ^a   D'Silva, Patrick ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOSYNTHESIS; CELL CULTURE; DEFECTS; IRON; IRON COMPOUNDS; MITOCHONDRIA; PHYSIOLOGY; PROTEINS; SULFUR;

CELLULAR RESPIRATION; ELECTRON TRANSPORT CHAIN; IRON-SULFUR CLUSTERS; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL MYOPATHY; MOLECULAR MECHANISM; PHYSIOLOGICAL ACTIVITY; REACTIVE OXYGEN SPECIES;

SCAFFOLDS (BIOLOGY);

CYSTATHIONINE GAMMA LYASE; CYTOCHROME C OXIDASE; GLYCINE; GLYCINE 50; IRON SULFUR CLUSTER SCAFFOLD PROTEIN; IRON SULFUR PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN NFS1; REACTIVE OXYGEN METABOLITE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IRON CELL LEVEL; MISSENSE MUTATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL MYOPATHY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; SEQUENCE HOMOLOGY;

ELECTRON TRANSPORT SYSTEM (ETS); HSP70; IRON-SULFUR CLUSTER; IRON-SULFUR PROTEIN; J-PROTEIN; MITOCHONDRIAL DISEASES; MOLECULAR CHAPERONE; MYOPATHY; REACTIVE OXYGEN SPECIES (ROS);

AMINO ACID SEQUENCE; CELL RESPIRATION; ESCHERICHIA COLI; HELA CELLS; HETEROZYGOTE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; IRON; IRON-SULFUR PROTEINS; MEMBRANE POTENTIALS; MITOCHONDRIAL MYOPATHIES; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION, MISSENSE; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; SULFUR;

EID: 84898618402     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526665     Document Type: Article

References (64)

1. Craig, E. A., and Marszalek, J. (2002) A specialized mitochondrial molecular chaperone system: a role in formation of Fe/S centers. Cell. Mol. Life Sci. 59, 1658-1665
2. Craig, E. A., Voisine, C., and Schilke, B. (1999) Mitochondrial iron metabolism in the yeast Saccharomyces cerevisiae. Biol. Chem. 380, 1167-1173
3. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831-838
4. Meyer, J. (2008) Iron-sulfur protein folds, iron-sulfur chemistry, and evolution. J. Biol. Inorg. Chem. 13, 157-170
5. Hinchliffe, P., and Sazanov, L. A. (2005) Organization of iron-sulfur clus- ters in respiratory complex I. Science 309, 771-774
6. Sazanov, L. A. (2007) Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46, 2275-2288
7. Sun, F., Huo, X., Zhai, Y., Wang, A., Xu, J., Su, D., Bartlam, M., and Rao, Z. (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043-1057
8. Beinert, H., Kennedy, M. C., and Stout, C. D. (1996) Aconitase as ironsulfur protein, enzyme, and iron-regulatory protein. Chem. Rev. 96, 2335-2374
9. King, A., Selak, M. A., and Gottlieb, E. (2006) Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25, 4675-4682
10. Lill, R., Dutkiewicz, R., Elsässer, H. P., Hausmann, A., Netz, D. J., Pierik, A. J., Stehling, O., Urzica, E., and Mühlenhoff, U. (2006) Mechanisms of iron-sulfur protein maturation in mitochondria, cytosol and nucleus of eukaryotes. Biochim. Biophys. Acta 1763, 652-667
11. 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
12. Garland, S. A., Hoff, K., Vickery, L. E., and Culotta, V. C. (1999) Saccharomyces cerevisiae ISU1 and ISU2: members of a well-conserved gene family for iron-sulfur cluster assembly. J. Mol. Biol. 294, 897-907
13. Fontecave, M., and Ollagnier-de-Choudens, S. (2008) Iron-sulfur cluster biosynthesis in bacteria: mechanisms of cluster assembly and transfer. Arch. Biochem. Biophys. 474, 226-237
14. Biederbick, A., Stehling, O., Rösser, R., Niggemeyer, B., Nakai, Y., Elsässer, 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
15. Majewska, J., Ciesielski, S. J., Schilke, B., Kominek, J., Blenska, A., Delewski, W., Song, J. Y., Marszalek, J., Craig, E. A., and Dutkiewicz, R. (2013) Binding of the chaperone Jac1 protein and cysteine desulfurase Nfs1 to the iron-sulfur cluster scaffold Isu protein is mutually exclusive. J. Biol. Chem. 288, 29134-29142
16. Johnson, D. C., Dean, D. R., Smith, A. D., and Johnson, M. K. (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74, 247-281
17. Bencze, K. Z., Kondapalli, K. C., Cook, J. D., McMahon, S., Millán-Pacheco, C., Pastor, N., and Stemmler, T. L. (2006) The structure and function of frataxin. Crit. Rev. Biochem. Mol. Biol. 41, 269-291
18. Craig, E. A., Huang, P., Aron, R., and Andrew, A. (2006) The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. Rev. Physiol. Biochem. Pharmacol. 156, 1-21
19. Schilke, B., Williams, B., Knieszner, H., Pukszta, S., D'Silva, P., Craig, E. A., and Marszalek, J. (2006) Evolution of mitochondrial chaperones utilized in Fe-S cluster biogenesis. Curr. Biol. 16, 1660-1665
20. Ciesielski, S. J., Schilke, B. A., Osipiuk, J., Bigelow, L., Mulligan, R., Majewska, J., Joachimiak, A., Marszalek, J., Craig, E. A., and Dutkiewicz, R. (2012) Interaction of J-protein co-chaperone Jac1 with Fe-S scaffold Isu is indispensable in vivo and conserved in evolution. J. Mol. Biol. 417, 1-12
21. Andrew, A. J., Dutkiewicz, R., Knieszner, H., Craig, E. A., and Marszalek, J. (2006) Characterization of the interaction between the J-protein Jac1p and the scaffold for Fe-S cluster biogenesis, Isu1p. J. Biol. Chem. 281, 14580-14587
22. Mochel, F., Knight, M. A., Tong, W. H., Hernandez, D., Ayyad, K., Taivassalo, T., Andersen, P. M., Singleton, A., Rouault, T. A., Fischbeck, K. H., and Haller, R. G. (2008) Splice mutation in the iron-sulfur cluster scaffold protein ISCU causes myopathy with exercise intolerance. Am. J. Hum. Genet. 82, 652-660
23. Olsson, A., Lind, L., Thornell, L. E., and Holmberg, M. (2008) 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, 1666-1672
24. Kollberg, G., Melberg, A., Holme, E., and Oldfors, A. (2011) Transient restoration of succinate dehydrogenase activity after rhabdomyolysis in iron-sulphur cluster deficiency myopathy. Neuromuscul. Disord. 21, 115-120
25. Larsson, L. E., Linderholm, H., Mueller, R., Ringqvist, T., and Soernaes, R. (1964) Hereditary metabolic myopathy with paroxysmal myoglobinuria due to abnormal glycolysis. J. Neurol. Neurosurg. Psychiatry 27, 361-380
26. Kollberg, G., and Holme, E. (2009) Antisense oligonucleotide therapeutics for iron-sulphur cluster deficiency myopathy. Neuromuscul. Disord. 19, 833-836
27. Sanaker, P. S., Toompuu, M., Hogan, V. E., He, L., Tzoulis, C., Chrzanowska- Lightowlers, Z. M., Taylor, R. W., and Bindoff, L. A. (2010) Differences inRNAprocessing underlie the tissue specific phenotype of ISCU myopathy. Biochim. Biophys. Acta 1802, 539-544
28. Kollberg, G., Tulinius, M., Melberg, A., Darin, N., Andersen, O., Holmgren, D., Oldfors, A., and Holme, E. (2009) Clinical manifestation and a new ISCU mutation in iron-sulphur cluster deficiency myopathy. Brain 132, 2170-2179
29. Goswami, A. V., Samaddar, M., Sinha, D., Purushotham, J., and D'Silva, P. (2012) Enhanced J-protein interaction and compromised protein stability of mtHsp70 variants lead to mitochondrial dysfunction in Parkinson's disease. Hum. Mol. Genet. 21, 3317-3332
30. Uchiyama, A., Kim, J. S., Kon, K., Jaeschke, H., Ikejima, K., Watanabe, S., and Lemasters, J. J. (2008) Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury. Hepatology 48, 1644-1654
31. Spinazzi, M., Casarin, A., Pertegato, V., Salviati, L., and Angelini, C. (2012) Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat. Protoc. 7, 1235-1246
32. Pierik, A. J., Netz, D. J., and Lill, R. (2009) Analysis of iron-sulfur protein maturation in eukaryotes. Nat. Protoc. 4, 753-766
33. Schilke, B., Voisine, C., Beinert, H., and Craig, E. (1999) Evidence for a conserved system for iron metabolism in the mitochondria of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 96, 10206-10211
34. Meisinger, C., Ryan, M. T., Hill, K., Model, K., Lim, J. H., Sickmann, A., Müller, H., Meyer, H. E., Wagner, R., and Pfanner, N. (2001) Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors. Mol. Cell. Biol. 21, 2337-2348
35. Lee, S., Sheck, L., Crowston, J. G., Van Bergen, N. J., O'Neill, E. C., O'Hare, F., Kong, Y. X., Chrysostomou, V., Vincent, A. L., and Trounce, I. A. (2012) Impaired complex-I-linked respiration and ATP synthesis in primary open-angle glaucoma patient lymphoblasts. Invest. Ophthalmol Vis. Sci. 53, 2431-2437
36. Wen, J. J., and Garg, N. J. (2010) Mitochondrial complex III defects contribute to inefficient respiration and ATP synthesis in the myocardium of Trypanosoma cruzi-infected mice. Antioxid. Redox Signal. 12, 27-37
37. Sheftel, A., Stehling, O., and Lill, R. (2010) Iron-sulfur proteins in health and disease. Trends Endocrinol. Metab. 21, 302-314
38. + exchange activity, osmotic swelling and mitophagy. Cell Death Differ. 14, 1647-1656
39. Johnson, L. V., Walsh, M. L., Bockus, B. J., and Chen, L. B. (1981) Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J. Cell Biol. 88, 526-535
40. Gallet, P. F., Maftah, A., Petit, J. M., Denis-Gay, M., and Julien, R. (1995) Direct cardiolipin assay in yeast using the red fluorescence emission of 10-N-nonyl acridine orange. Eur. J. Biochem. 228, 113-119
41. Delatycki, M. B., Camakaris, J., Brooks, H., Evans-Whipp, T., Thorburn, D. R., Williamson, R., and Forrest, S. M. (1999) Direct evidence that mitochondrial iron accumulation occurs in Friedreich ataxia. Ann. Neurol. 45, 673-675
42. Kakhlon, O., and Cabantchik, Z. I. (2002) The labile iron pool: characterization, measurement, and participation in cellular processes(1). Free Radic. Biol. Med. 33, 1037-1046
43. Devireddy, L. R., Hart, D. O., Goetz, D. H., and Green, M. R. (2010) A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 141, 1006-1017
44. Gutteridge, J. M., Maidt, L., and Poyer, L. (1990) Superoxide dismutase and Fenton chemistry. Reaction of ferric-EDTA complex and ferric-bipyridyl complex with hydrogen peroxide without the apparent formation of iron(II). Biochem. J. 269, 169-174
45. Py, B., and Barras, F. (2010) Building Fe-S proteins: bacterial strategies. Nat. Rev. Microbiol. 8, 436-446
46. Jang, S., and Imlay, J. A. (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J. Biol. Chem. 282, 929-937
47. Dixon, S. J., and Stockwell, B. R. (2014) The role of iron and reactive oxygen species in cell death. Nat. Chem. Biol. 10, 9-17
48. Uhrigshardt, H., Singh, A., Kovtunovych, G., Ghosh, M., and Rouault, T. A. (2010) Characterization of the human HSC20, an unusual DnaJ type III protein, involved in iron-sulfur cluster biogenesis. Hum. Mol. Genet. 19, 3816-3834
49. Adinolfi, S., Rizzo, F., Masino, L., Nair, M., Martin, S. R., Pastore, A., and Temussi, P. A. (2004) Bacterial IscU is a well folded and functional single domain protein. Eur. J. Biochem. 271, 2093-2100
50. Kato, S., Mihara, H., Kurihara, T., Takahashi, Y., Tokumoto, U., Yoshimura, T., and Esaki, N. (2002) Cys-328 of IscS and Cys-63 of IscU are the sites of disulfide bridge formation in a covalently bound IscS/IscU complex: implications for the mechanism of iron-sulfur cluster assembly. Proc. Natl. Acad. Sci. U.S.A. 99, 5948-5952
51. Agar, J. N., Krebs, C., Frazzon, J., Huynh, B. H., Dean, D. R., and Johnson, M. K. (2000) IscU as a scaffold for iron-sulfur cluster biosynthesis: sequential assembly of [2Fe-2S] and [4Fe-4S] clusters in IscU. Biochemistry 39, 7856-7862
52. Wu, G., Mansy, S. S., Wu Sp, S. P., Surerus, K. K., Foster, M. W., and Cowan, J. A. (2002) Characterization of an iron-sulfur cluster assembly protein (ISU1) from Schizosaccharomyces pombe. Biochemistry 41, 5024-5032
53. Shimomura, Y., Kamikubo, H., Nishi, Y., Masako, T., Kataoka, M., Kobayashi, Y., Fukuyama, K., and Takahashi, Y. (2007) Characterization and crystallization of an IscU-type scaffold protein with bound [2Fe-2S] cluster from the hyperthermophile, Aquifex aeolicus. J. Biochem. 142, 577-586
54. Hall, R. E., Henriksson, K. G., Lewis, S. F., Haller, R. G., and Kennaway, N. G. (1993) Mitochondrial myopathy with succinate dehydrogenase and aconitase deficiency. Abnormalities of several iron-sulfur proteins. J. Clin. Invest. 92, 2660-2666
55. Richardson, D. R., Lane, D. J., Becker, E. M., Huang, M. L., Whitnall, M., Suryo Rahmanto, Y., Sheftel, A. D., and Ponka, P. (2010) Mitochondrial iron trafficking and the integration of iron metabolism between the mitochondrion and cytosol. Proc. Natl. Acad. Sci. U.S.A. 107, 10775-10782
56. Batandier, C., Fontaine, E., Kériel, C., and Leverve, X. M. (2002) Determination of mitochondrial reactive oxygen species: methodological aspects. J. Cell Mol. Med. 6, 175-187
57. Kudin, A. P., Bimpong-Buta, N. Y., Vielhaber, S., Elger, C. E., and Kunz, W. S. (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 279, 4127-4135
58. Liu, Y., Fiskum, G., and Schubert, D. (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780-787
59. Trachootham, D., Lu, W., Ogasawara, M. A., Nilsa, R. D., and Huang, P. (2008) Redox regulation of cell survival. Antioxid. Redox Signal. 10, 1343-1374
60. De Moura, M. B., Dos Santos, L. S., and Van Houten, B. (2010) Mitochondrial dysfunction in neurodegenerative diseases and cancer. Environ. Mol. Mutagen. 51, 391-405
61. Kirkinezos, I. G., and Moraes, C. T. (2001) Reactive oxygen species and mitochondrial diseases. Semin. Cell Dev. Biol. 12, 449-457
62. Levi, S., and Rovida, E. (2009) The role of iron in mitochondrial function. Biochim. Biophys. Acta 1790, 629-636
63. Dutkiewicz, R., Schilke, B., Cheng, S., Knieszner, H., Craig, E. A., and Marszalek, J. (2004) Sequence-specific interaction between mitochondrial Fe-S scaffold protein Isu and Hsp70 Ssq1 is essential for their in vivo function. J. Biol. Chem. 279, 29167-29174
64. Shimomura, Y., Wada, K., Fukuyama, K., and Takahashi, Y. (2008) The asymmetric trimeric architecture of [2Fe-2S] IscU: implications for its scaffolding during iron-sulfur cluster biosynthesis. J. Mol. Biol. 383, 133-143