Redox control of human mitochondrial outer membrane protein mitoneet [2FE-2S] clusters by biological thiols and hydrogen peroxide

Journal of Biological Chemistry

Volumn 289, Issue 7, 2014, Pages 4307-4315

  Landry, Aaron P ^a   Ding, Huangen ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIABETES; HYDROGEN PEROXIDE; IRON-SULFUR PROTEIN; REDOX REGULATION; THIOREDOXIN;

ESCHERICHIA COLI; HUMANS; HYDROGEN PEROXIDE; HYPOGLYCEMIC AGENTS; IRON-SULFUR PROTEINS; MITOCHONDRIAL PROTEINS; OXIDANTS; OXIDATION-REDUCTION; RECOMBINANT PROTEINS; THIAZOLIDINEDIONES;

EID: 84894188910     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.542050     Document Type: Article

References (57)

1. Colca, J. R., McDonald, W. G., Waldon, D. J., Leone, J. W., Lull, J. M., Bannow, C. A., Lund, E. T., and Mathews, W. R. (2004) Identification of a novel mitochondrial protein ("mitoNEET") cross-linked specifically by a thiazolidinedione photoprobe. Am. J. Physiol. Endocrinol. Metab. 286, E252-E260
2. Wiley, S. E., Murphy, A. N., Ross, S. A., van der Geer, P., and Dixon, J. E. (2007) MitoNEET is an iron-containing outer mitochondrial membrane protein that regulates oxidative capacity. Proc. Natl. Acad. Sci. U.S.A. 104, 5318-5323
3. Kusminski, C. M., Holland, W. L., Sun, K., Park, J., Spurgin, S. B., Lin, Y., Askew, G. R., Simcox, J. A., McClain, D. A., Li, C., and Scherer, P. E. (2012) MitoNEET-driven alterations in adipocyte mitochondrial activity reveal a crucial adaptive process that preserves insulin sensitivity in obesity. Nat. Med. 18, 1539-1549
4. Yonutas, H. M., and Sullivan, P. G. (2013) Targeting PPAR isoforms following CNS injury. Curr. Drug Targets 14, 733-742
5. Geldenhuys, W. J., and Van der Schyf, C. J. (2013) Rationally designed multi-targeted agents against neurodegenerative diseases. Curr. Med. Chem. 20, 1662-1672
6. Sohn, Y. S., Tamir, S., Song, L., Michaeli, D., Matouk, I., Conlan, A. R., Harir, Y., Holt, S. H., Shulaev, V., Paddock, M. L., Hochberg, A., Cabanchick, I. Z., Onuchic, J. N., Jennings, P. A., Nechushtai, R., and Mittler, R. (2013) NAF-1 and mitoNEET are central to human breast cancer proliferation by maintaining mitochondrial homeostasis and promoting tumor growth. Proc. Natl. Acad. Sci. U.S.A. 110, 14676-14681
7. Wiley, S. E., Paddock, M. L., Abresch, E. C., Gross, L., van der Geer, P., Nechushtai, R., Murphy, A. N., Jennings, P. A., and Dixon, J. E. (2007) The outer mitochondrial membrane protein mitoNEET contains a novel redox-active 2Fe-2S cluster. J. Biol. Chem. 282, 23745-23749
8. Hou, X., Liu, R., Ross, S., Smart, E. J., Zhu, H., and Gong, W. (2007) Crystallographic studies of human MitoNEET. J. Biol. Chem. 282, 33242-33246
9. Lin, J., Zhou, T., Ye, K., and Wang, J. (2007) Crystal structure of human mitoNEET reveals distinct groups of iron-sulfur proteins. Proc. Natl. Acad. Sci. U.S.A. 104, 14640-14645
10. Paddock, M. L., Wiley, S. E., Axelrod, H. L., Cohen, A. E., Roy, M., Abresch, E. C., Capraro, D., Murphy, A. N., Nechushtai, R., Dixon, J. E., and Jennings, P. A. (2007) MitoNEET is a uniquely folded 2Fe 2S outer mitochondrial membrane protein stabilized by pioglitazone. Proc. Natl. Acad. Sci. U.S.A. 104, 14342-14347
11. Bak, D. W., Zuris, J. A., Paddock, M. L., Jennings, P. A., and Elliott, S. J. (2009) Redox characterization of the FeS protein MitoNEET and impact of thiazolidinedione drug binding. Biochemistry 48, 10193-10195
12. Tirrell, T. F., Paddock, M. L., Conlan, A. R., Smoll, E. J., Jr., Nechushtai, R., Jennings, P. A., and Kim, J. E. (2009) Resonance Raman studies of the (His)(Cys)(3) 2Fe-2S cluster of MitoNEET. Comparison to the (Cys)(4) mutant and implications of the effects of pH on the labile metal center. Biochemistry 48, 4747-4752
13. Conlan, A. R., Paddock, M. L., Homer, C., Axelrod, H. L., Cohen, A. E., Abresch, E. C., Zuris, J. A., Nechushtai, R., and Jennings, P. A. (2011) Mutation of the His ligand in mitoNEET stabilizes the 2Fe-2S cluster despite conformational heterogeneity in the ligand environment. Acta Crystallogr. D. Biol. Crystallogr. 67, 516-523
14. Tan, G., Landry, A. P., Dai, R., Wang, L., Lu, J., and Ding, H. (2012) Competition of zinc ion for the [2Fe-2S] cluster binding site in the diabetes drug target protein mitoNEET. Biometals 25, 1177-1184
15. Arif, W., Xu, S., Isailovic, D., Geldenhuys, W. J., Carroll, R. T., and Funk, M. O. (2011) Complexes of the outer mitochondrial membrane protein mitoNEET with resveratrol-3-sulfate. Biochemistry 50, 5806-5811
16. Zhou, T., Lin, J., Feng, Y., and Wang, J. (2010) Binding of reduced nicotinamide adenine dinucleotide phosphate destabilizes the iron-sulfur clusters of human mitoNEET. Biochemistry 49, 9604-9612
17. Baxter, E. L., Jennings, P. A., and Onuchic, J. N. (2011) Interdomain communication revealed in the diabetes drug target mitoNEET. Proc. Natl. Acad. Sci. U.S.A. 108, 5266-5271
18. Baxter, E. L., Jennings, P. A., and Onuchic, J. N. (2012) Strand swapping regulates the iron-sulfur cluster in the diabetes drug target mitoNEET. Proc. Natl. Acad. Sci. U.S.A. 109, 1955-1960
19. Bak, D. W., and Elliott, S. J. (2013) Conserved hydrogen bonding networks of MitoNEET Tune Fe-S cluster binding and structural stability. Biochemistry 52, 4687-4696
20. Zuris, J. A., Harir, Y., Conlan, A. R., Shvartsman, M., Michaeli, D., Tamir, S., Paddock, M. L., Onuchic, J. N., Mittler, R., Cabantchik, Z. I., Jennings, P. A., and Nechushtai, R. (2011) Facile transfer of [2Fe-2S] clusters from the diabetes drug target mitoNEET to an apo-acceptor protein. Proc. Natl. Acad. Sci. U.S.A. 108, 13047-13052
21. Zuris, J. A., Ali, S. S., Yeh, H., Nguyen, T. A., Nechushtai, R., Paddock, M. L., and Jennings, P. A. (2012) NADPH inhibits [2Fe-2S] cluster protein transfer from diabetes drug target MitoNEET to an apo-acceptor protein. J. Biol. Chem. 287, 11649-11655
22. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831-838
23. Dooley, C. T., Dore, T. M., Hanson, G. T., Jackson, W. C., Remington, S. J., and Tsien, R. Y. (2004) Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J. Biol. Chem. 279, 22284-22293
24. Veine, D. M., Mulrooney, S. B., Wang, P. F., and Williams, C. H., Jr. (1998) Formation and properties of mixed disulfides between thioredoxin reductase from Escherichia coli and thioredoxin. Evidence that cysteine-138 functions to initiate dithiol-disulfide interchange and to accept the reducing equivalent from reduced flavin. Protein Sci. 7, 1441-1450
25. Mulrooney, S. B. (1997) Application of a single-plasmid vector for mutagenesis and high-level expression of thioredoxin reductase and its use to examine flavin cofactor incorporation. Protein Expr. Purif. 9, 372-378
26. Ding, H., Harrison, K., and Lu, J. (2005) Thioredoxin reductase system mediates iron binding in IscA and iron delivery for the iron-sulfur cluster assembly in IscU. J. Biol. Chem. 280, 30432-30437
27. Mayhew, S. G. (1978) The redox potential of dithionite and SO-2 from equilibrium reactions with flavodoxins, methyl viologen and hydrogen plus hydrogenase. Eur. J. Biochem. 85, 535-547
28. Dicus, M. M., Conlan, A., Nechushtai, R., Jennings, P. A., Paddock, M. L., Britt, R. D., and Stoll, S. (2010) Binding of histidine in the (Cys)(3)(His)(1)-coordinated [2Fe-2S] cluster of human mitoNEET. J. Am. Chem. Soc. 132, 2037-2049
29. Iwasaki, T., Samoilova, R. I., Kounosu, A., Ohmori, D., and Dikanov, S. A. (2009) Continuous-wave and pulsed EPR characterization of the [2Fe-2S](Cys)3(His)1 cluster in rat MitoNEET. J. Am. Chem. Soc. 131, 13659-13667
30. Ding, H., and Demple, B. (1997) In vivo kinetics of a redox-regulated transcriptional switch. Proc. Natl. Acad. Sci. U.S.A. 94, 8445-8449
31. Djaman, O., Outten, F. W., and Imlay, J. A. (2004) Repair of oxidized iron-sulfur clusters in Escherichia coli. J. Biol. Chem. 279, 44590-44599
32. Gaudu, P., and Weiss, B. (1996) SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form. Proc. Natl. Acad. Sci. U.S.A. 93, 10094-10098
33. Quijano, C., Alvarez, B., Gatti, R. M., Augusto, O., and Radi, R. (1997) Pathways of peroxynitrite oxidation of thiol groups. Biochem. J. 322, 167-173
34. Eaton, P. (2006) Protein thiol oxidation in health and disease. Techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radic. Biol. Med. 40, 1889-1899
35. Szajewski, R. P., and Whitesides, G. M. (1980) Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J. Am. Chem. Soc. 102, 2011-2026
36. Arnér, E. S., and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109
37. Krause, G., Lundström, J., Barea, J. L., Pueyo de la Cuesta, C., and Holmgren, A. (1991) Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin. J. Biol. Chem. 266, 9494-9500
38. Ding, H., Hidalgo, E., and Demple, B. (1996) The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J. Biol. Chem. 271, 33173-33175
39. Ren, B., Duan, X., and Ding, H. (2009) Redox control of the DNA damageinducible protein DinG helicase activity via its iron-sulfur cluster. J. Biol. Chem. 284, 4829-4835
40. Crack, J. C., Green, J., Thomson, A. J., and Le Brun, N. E. (2012) Iron-sulfur cluster sensor-regulators. Curr. Opin. Chem. Biol. 16, 35-44
41. Gu, M., and Imlay, J. A. (2011) The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol. Microbiol. 79, 1136-1150
42. Dai, S., Schwendtmayer, C., Schürmann, P., Ramaswamy, S., and Eklund, H. (2000) Redox signaling in chloroplasts. Cleavage of disulfides by an iron-sulfur cluster. Science 287, 655-658
43. Walters, E. M., Garcia-Serres, R., Naik, S. G., Bourquin, F., Glauser, D. A., Schürmann, P., Huynh, B. H., and Johnson, M. K. (2009) Role of histidine-86 in the catalytic mechanism of ferredoxin:thioredoxin reductase. Biochemistry 48, 1016-1024
44. Collet, J. F., and Messens, J. (2010) Structure, function, and mechanism of thioredoxin proteins. Antioxid. Redox Signal. 13, 1205-1216
45. Watson, W. H., Pohl, J., Montfort, W. R., Stuchlik, O., Reed, M. S., Powis, G., and Jones, D. P. (2003) Redox potential of human thioredoxin 1 and identification of a second dithiol/disulfide motif. J. Biol. Chem. 278, 33408-33415
46. Wondrak, G. T. (2009) Redox-directed cancer therapeutics. Molecular mechanisms and opportunities. Antioxid. Redox Signal. 11, 3013-3069
47. Zschauer, T. C., Matsushima, S., Altschmied, J., Shao, D., Sadoshima, J., and Haendeler, J. (2013) Interacting with thioredoxin-1. Disease or no disease? Antioxid. Redox Signal. 18, 1053-1062
48. Hanschmann, E. M., Godoy, J. R., Berndt, C., Hudemann, C., and Lillig, C. H. (2013) Thioredoxins, glutaredoxins, and peroxiredoxins-molecular mechanisms and health significance. From cofactors to antioxidants to redox signaling. Antioxid. Redox Signal. 19, 1539-1605
49. Feinstein, D. L., Spagnolo, A., Akar, C., Weinberg, G., Murphy, P., Gavrilyuk, V., and Dello Russo, C. (2005) Receptor-independent actions of PPAR thiazolidinedione agonists. Is mitochondrial function the key? Biochem. Pharmacol. 70, 177-188
50. Geldenhuys, W. J., Funk, M. O., Awale, P. S., Lin, L., and Carroll, R. T. (2011) A novel binding assay identifies high affinity ligands to the rosiglitazone binding site of mitoNEET. Bioorg. Med. Chem. Lett. 21, 5498-5501
51. Bieganski, R. M., and Yarmush, M. L. (2011) Novel ligands that target the mitochondrial membrane protein mitoNEET. J. Mol. Graph. Model. 29, 965-973
52. Conlan, A. R., Axelrod, H. L., Cohen, A. E., Abresch, E. C., Zuris, J., Yee, D., Nechushtai, R., Jennings, P. A., and Paddock, M. L. (2009) Crystal structure of Miner1. The redox-active 2Fe-2S protein causative in Wolfram syndrome 2. J. Mol. Biol. 392, 143-153
53. Lin, J., Zhang, L., Lai, S., and Ye, K. (2011) Structure and molecular evolution of CDGSH iron-sulfur domains. PLoS ONE 6, e24790
54. Amr, S., Heisey, C., Zhang, M., Xia, X. J., Shows, K. H., Ajlouni, K., Pandya, A., Satin, L. S., El-Shanti, H., and Shiang, R. (2007) A homozygous mutation in a novel zinc-finger protein, ERIS, is responsible for Wolfram syndrome2. Am. J. Hum. Genet. 81, 673-683
55. Chen, Y. F., Kao, C. H., Chen, Y. T., Wang, C. H., Wu, C. Y., Tsai, C. Y., Liu, F. C., Yang, C. W., Wei, Y. H., Hsu, M. T., Tsai, S. F., and Tsai, T. F. (2009) Cisd2 deficiency drives premature aging and causes mitochondria-mediated defects in mice. Genes Dev. 23, 1183-1194
56. Chang, N. C., Nguyen, M., and Shore, G. C. (2012) BCL2-CISD2. An ER complex at the nexus of autophagy and calcium homeostasis? Autophagy 8, 856-857
57. Wiley, S. E., Andreyev, A. Y., Divakaruni, A. S., Karisch, R., Perkins, G., Wall, E. A., van der Geer, P., Chen, Y. F., Tsai, T. F., Simon, M. I., Neel, B. G., Dixon, J. E., and Murphy, A. N. (2013) Wolfram syndrome protein, Miner1, regulates sulphydryl redox status, the unfolded protein response, and Ca homeostasis. EMBO Mol. Med. 5, 904-918