His-87 ligand in mitoNEET is crucial for the transfer of iron sulfur clusters from mitochondria to cytosolic aconitase

Biochemical and Biophysical Research Communications

Volumn 470, Issue 1, 2016, Pages 226-232

  Tan, Guoqiang ^a   Liu, Danhui ^a   Pan, Feiyan ^a   Zhao, Jin ^a   Li, Tang ^a   Ma, Yin ^a   Shen, Bo ^a   Lyu, Jianxin ^a  

^a WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Aconitase; His 87 ligand mutations; Iron sulfur cluster; MitoNEET

Indexed keywords

ACONITATE HYDRATASE; HISTIDINE; IRON SULFUR PROTEIN; MITONEET PROTEIN; UNCLASSIFIED DRUG; CISD1 PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; PROTEIN BINDING;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSFECTION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; WILD TYPE; ACTIVE TRANSPORT; BINDING SITE; CHEMISTRY; CYTOSOL; METABOLISM; PHYSIOLOGY;

ACONITATE HYDRATASE; BINDING SITES; BIOLOGICAL TRANSPORT, ACTIVE; CYTOSOL; HEP G2 CELLS; HISTIDINE; HUMANS; IRON-SULFUR PROTEINS; MCF-7 CELLS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEIN BINDING;

EID: 84956574430     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2016.01.040     Document Type: Article

References (35)

1. S. Tamir, M.L. Paddock, M. Darash-Yahana-Baram, S.H. Holt, Y.S. Sohn, L. Agranat, D. Michaeli, J.T. Stofleth, C.H. Lipper, F. Morcos, I.Z. Cabantchik, J.N. Onuchic, P.A. Jennings, R. Mittler, and R. Nechushtai Structure-function analysis of NEET proteins uncovers their role as key regulators of iron and ROS homeostasis in health and disease Biochim. Biophys. Acta 1853 2015 1294 1315
2. R. Lill, and U. Muhlenhoff Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases Annu. Rev. Biochem. 77 2008 669 700
3. A. Sheftel, O. Stehling, and R. Lill Iron-sulfur proteins in health and disease Trends Endocrinol. Metab. 21 2010 302 314
4. S. Adinolfi, C. Iannuzzi, F. Prischi, C. Pastore, S. Iametti, S.R. Martin, F. Bonomi, and A. Pastore Bacterial frataxin CyaY is the gatekeeper of iron-sulfur cluster formation catalyzed by IscS Nat. Struct. Mol. Biol. 16 2009 390 396
5. W. Wang, H. Huang, G. Tan, F. Si, M. Liu, A.P. Landry, J. Lu, and H. Ding In vivo evidence for the iron-binding activity of an iron-sulfur cluster assembly protein IscA in Escherichia coli Biochem. J. 432 2010 429 436
6. T. Zhou, J. Lin, Y. Feng, and J. Wang Binding of reduced nicotinamide adenine dinucleotide phosphate destabilizes the iron-sulfur clusters of human mitoNEET Biochemistry 49 2010 9604 9612
7. R. Lill Function and biogenesis of iron-sulphur proteins Nature 460 2009 831 838
8. C. Kumar, A. Igbaria, B. D'Autreaux, A.G. Planson, C. Junot, E. Godat, A.K. Bachhawat, A. Delaunay-Moisan, and M.B. Toledano Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control EMBO J. 30 2011 2044 2056
9. M.L. Paddock, S.E. Wiley, H.L. Axelrod, A.E. Cohen, M. Roy, E.C. Abresch, D. Capraro, A.N. Murphy, R. Nechushtai, J.E. Dixon, and P.A. Jennings MitoNEET is a uniquely folded 2Fe 2S outer mitochondrial membrane protein stabilized by pioglitazone Proc. Natl. Acad. Sci. U. S. A. 104 2007 14342 14347
10. J.R. Colca, W.G. McDonald, D.J. Waldon, J.W. Leone, J.M. Lull, C.A. Bannow, E.T. Lund, and W.R. Mathews Identification of a novel mitochondrial protein ("mitoNEET") cross-linked specifically by a thiazolidinedione photoprobe Am. J. Physiol. Endocrinol. Metab. 49 2004 E252 E260
11. S.E. Wiley, A.N. Murphy, S.A. Ross, P. van der Geer, and J.E. Dixon MitoNEET is an iron-containing outer mitochondrial membrane protein that regulates oxidative capacity Proc. Natl. Acad. Sci. U. S. A. 104 2007 5318 5323
12. S.E. Wiley, M.L. Paddock, E.C. Abresch, L. Gross, P. van der Geer, R. Nechushtai, A.N. Murphy, P.A. Jennings, and J.E. Dixon The outer mitochondrial membrane protein mitoNEET contains a novel redox-active 2Fe-2S cluster J. Biol. Chem. 282 2007 23745 23749
13. A.R. Conlan, M.L. Paddock, C. Homer, H.L. Axelrod, A.E. Cohen, E.C. Abresch, J.A. Zuris, R. Nechushtai, and P.A. Jennings 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 2011 516 523
14. A.R. Conlan, M.L. Paddock, H.L. Axelrod, A.E. Cohen, E.C. Abresch, S. Wiley, M. Roy, R. Nechushtai, and P.A. Jennings The novel 2Fe-2S outer mitochondrial protein mitoNEET displays conformational flexibility in its N-terminal cytoplasmic tethering domain Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 65 2009 654 659
15. A. Kounosu, T. Iwasaki, S. Baba, Y. Hayashi-Iwasaki, T. Oshima, and T. Kumasaka Crystallization and preliminary X-ray diffraction studies of the prototypal homologue of mitoNEET (Tth-NEET0026) from the extreme thermophile Thermus thermophilus HB8 Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 64 2008 1146 1148
16. J. Lin, T. Zhou, K. Ye, and J. Wang Crystal structure of human mitoNEET reveals distinct groups of iron sulfur proteins Proc. Natl. Acad. Sci. U. S. A. 104 2007 14640 14645
17. X. Hou, R. Liu, S. Ross, E.J. Smart, H. Zhu, and W. Gong Crystallographic studies of human MitoNEET J. Biol. Chem. 282 2007 33242 33246
18. J.A. Zuris, D.A. Halim, A.R. Conlan, E.C. Abresch, R. Nechushtai, M.L. Paddock, and P.A. Jennings Engineering the redox potential over a wide range within a new class of FeS proteins J. Am. Chem. Soc. 132 2010 13120 13122
19. M.M. Dicus, A. Conlan, R. Nechushtai, P.A. Jennings, M.L. Paddock, R.D. Britt, and S. Stoll Binding of histidine in the (Cys)3(His)1-coordinated [2Fe-2S] cluster of human mitoNEET J. Am. Chem. Soc. 132 2010 2037 2049
20. C.M. Kusminski, W.L. Holland, K. Sun, J. Park, S.B. Spurgin, Y. Lin, G.R. Askew, J.A. Simcox, D.A. McClain, C. Li, and P.E. Scherer MitoNEET-driven alterations in adipocyte mitochondrial activity reveal a crucial adaptive process that preserves insulin sensitivity in obesity Nat. Med. 18 2012 1539 1549
21. R. Nechushtai, A.R. Conlan, Y. Harir, L. Song, O. Yogev, Y. Eisenberg-Domovich, O. Livnah, D. Michaeli, R. Rosen, V. Ma, Y. Luo, J.A. Zuris, M.L. Paddock, Z.I. Cabantchik, P.A. Jennings, and R. Mittler Characterization of arabidopsis NEET reveals an ancient role for NEET proteins in iron metabolism Plant Cell 24 2012 2139 2154
22. T. Takahashi, M. Yamamoto, K. Amikura, K. Kato, T. Serizawa, K. Serizawa, D. Akazawa, T. Aoki, K. Kawai, E. Ogasawara, J.I. Hayashi, K. Nakada, and M. Kainoh A novel MitoNEET ligand, TT01001, improves diabetes and ameliorates mitochondrial function in db/db mice J. Pharmacol. Exp. Ther. 352 2014 338 345
23. A.P. Landry, and H. Ding Redox control of human mitochondrial outer membrane protein MitoNEET [2Fe-2S] clusters by biological thiols and hydrogen peroxide J. Biol. Chem. 289 2014 4307 4315
24. B. Fang, F. Morcos, S. Yang-Sung, M. Darash-Yahana, C.O. Rezende, C.H. Lipper, M.L. Paddock, S. Luhua, L. Yuting, S.H. Holt, S. Tamir, E.A. Theodorakis, P.A. Jennings, J.N. Onuchic, R. Mittler, and R. Nechushtai The Fe-S cluster-containing NEET proteins mitoNEET and NAF-1 as chemotherapeutic targets in breast cancer Proc. Natl. Acad. Sci. U. S. A. 112 2015 3698 3703
25. J.A. Zuris, Y. Harir, A.R. Conlan, M. Shvartsman, D. Michaeli, S. Tamir, M.L. Paddock, J.N. Onuchic, R. Mittler, Z.I. Cabantchik, P.A. Jennings, and R. Nechushtai 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 2011 13047 13052
26. C.T. Saouma, M.M. Pinney, and J.M. Mayer Electron transfer and proton-coupled electron transfer reactivity and self-exchange of synthetic [2Fe-2S] complexes: models for Rieske and mitoNEET clusters Inorg. Chem. 53 2014 3153 3161
27. I. Ferecatu, S. Goncalves, M.P. Golinelli-Cohen, M. Clemancey, A. Martelli, S. Riquier, E. Guittet, J.M. Latour, H. Puccio, J.C. Drapier, E. Lescop, and C. Bouton The diabetes drug target MitoNEET governs a novel trafficking pathway to rebuild an Fe-S cluster into cytosolic aconitase/iron regulatory protein 1 J. Biol. Chem. 289 2014 28070 28086
28. J.A. Zuris, S.S. Ali, H. Yeh, T.A. Nguyen, R. Nechushtai, M.L. Paddock, and P.A. Jennings NADPH inhibits [2Fe-2S] cluster protein transfer from diabetes drug target MitoNEET to an apo-acceptor protein J. Biol. Chem. 287 2012 11649 11655
29. C.H. Lipper, M.L. Paddock, J.N. Onuchic, R. Mittler, R. Nechushtai, and P.A. Jennings Cancer-related NEET proteins transfer 2Fe-2S clusters to anamorsin, a protein required for cytosolic iron-sulfur cluster biogenesis PLoS One 10 2015 e0139699
30. C.D. Krause, L.S. Izotova, G. Ren, Z.R. Yuan, Y. Shi, C.C. Chen, Y. Ron, and S. Pestka Efficient co-expression of bicistronic proteins in mesenchymal stem cells by development and optimization of a multifunctional plasmid Stem Cell Res. Ther. 2 2011 15
31. M. Spinazzi, A. Casarin, V. Pertegato, L. Salviati, and C. Angelini Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells Nat. Protoc. 7 2012 1235 1246
32. N. Ajit Bolar, A.V. Vanlander, C. Wilbrecht, N. Van der Aa, J. Smet, B. De Paepe, G. Vandeweyer, F. Kooy, F. Eyskens, E. De Latter, G. Delanghe, P. Govaert, J.G. Leroy, B. Loeys, R. Lill, L. Van Laer, and R. Van Coster Mutation of the iron-sulfur cluster assembly gene IBA57 causes severe myopathy and encephalopathy Hum. Mol. Genet. 22 2013 2590 2602
33. K.D. Schnackerz, D. Dobritzsch, Y. Lindqvist, and P.F. Cook Dihydropyrimidine dehydrogenase: a flavoprotein with four iron-sulfur clusters Biochim. Biophys. Acta 1701 2004 61 74
34. D.W. Bak, J.A. Zuris, M.L. Paddock, P.A. Jennings, and S.J. Elliott Redox characterization of the FeS protein MitoNEET and impact of thiazolidinedione drug binding Biochemistry 48 2009 10193 10195
35. N. Shulga, and J.G. Pastorino Mitoneet mediates TNFalpha-induced necroptosis promoted by exposure to fructose and ethanol J. Cell Sci. 127 2014 896 907