Persulfide formation on mitochondrial cysteine desulfurase: Enzyme activation by a eukaryote-specific interacting protein and Fe-S cluster synthesis

Biochemical Journal

Volumn 448, Issue 2, 2012, Pages 171-187

  Pandey, Alok ^a   Golla, Ramesh ^b   Yoon, Heeyong ^b   Dancis, Andrew ^b   Pain, Debkumar ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cysteine desulfurase; Fe S cluster; Mitochondrion; Nfs1p Isd11p complex; Persulfide; Yeast

Indexed keywords

BACTERIAL ENZYME; CYSTATHIONINE GAMMA LYASE; CYSTEINE; FUNGAL PROTEIN; IRON; MITOCHONDRIAL ENZYME; PROTEIN ISD11P; PROTEIN NFS1P; SULFIDE; SULFUR; UNCLASSIFIED DRUG;

ARTICLE; CELL ISOLATION; CONFORMATIONAL TRANSITION; COVALENT BOND; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; EUKARYOTE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE;

ALLELES; CARBON-SULFUR LYASES; ENZYME ACTIVATION; GENES, FUNGAL; IRON-SULFUR PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MULTIENZYME COMPLEXES; MUTATION; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SULFIDES; SULFURTRANSFERASES;

BACTERIA (MICROORGANISMS); EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84869029429     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120951     Document Type: Article

References (41)

1. Kiley, P. J. and Beinert, H. (2003) The role of Fe-S proteins in sensing and regulation in bacteria. Curr. Opin. Microbiol. 6, 181-185
2. Imlay, J. A. (2006) Iron-sulphur clusters and the problem with oxygen. Mol. Microbiol. 59, 1073-1082
3. Rouault, T. A. (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2, 406-414
4. Stemmler, T. L., Lesuisse, E., Pain, D. and Dancis, A. (2010) Frataxin and mitochondrial Fe-S cluster biogenesis. J. Biol. Chem. 285, 26737-26743
5. Lill, R. (2009) Function and biogenesis of iron-sulphur proteins. Nature 460, 831-838
6. Kessler, D. (2006) Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30, 825-840
7. Mueller, E. G. (2006) Trafficking in persulfides: delivering sulfur in biosynthetic pathways. Nat. Chem. Biol. 2, 185-194
8. 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
9. Cupp-Vickery, J. R., Urbina, H. and Vickery, L. E. (2003) Crystal structure of IscS, a cysteine desulfurase from Escherichia coli. J. Mol. Biol. 330, 1049-1059
10. Kaiser, J. T., Clausen, T., Bourenkow, G. P., Bartunik, H.-D., Steinbacher, S. and Huber, R. (2000) Crystal structure of a NifS-like protein from Thermotoga maritima : implications for iron sulphur cluster assembly. J. Mol. Biol. 297, 451-464
11. Shi, R., Proteau, A., Villarroya, M., Moukadiri, I., Zhang, L., Trempe, J. F., Matte, A., Armengod, M. E. and Cygler, M. (2010) Structural basis for Fe-S cluster assembly and tRNA thiolation mediated by IscS protein-protein interactions. PLoS Biol. 8, e1000354
12. Zheng, L., White, R. H., Cash, V. L., Jack, R. F. and Dean, D. R. (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 90, 2754-2758
13. Zheng, L., White, R. H., Cash, V. L. and Dean, D. R. (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33, 4714-4720
14. Rouault, T. A. and Tong, W. H. (2008) Iron-sulfur cluster biogenesis and human disease. Trends Genet. 24, 398-407
15. Li, J., Kogan, M., Knight, S. A. B., Pain, D. and Dancis, A. (1999) Yeast mitochondrial protein, Nfs1p, coordinately regulates iron-sulfur cluster proteins, cellular iron uptake, and iron distribution. J. Biol. Chem. 274, 33025-33034
16. Kolman, C. and Söll, D. (1993) SPL1-1, a Saccharomyces cerevisiae mutation affecting tRNA splicing. J. Bacteriol. 175, 1433-1442
17. Land, T. and Rouault, T. A. (1998) Targeting of a human iron-sulfur cluster assembly enzyme, nifs, to different subcellular compartments is regulated through alternative AUG utilization. Mol. Cell 2, 807-815
18. Naamati, A., Regev-Rudzki, N., Galperin, S., Lill, R. and Pines, O. (2009) Dual targeting of Nfs1 and discovery of its novel processing enzyme, Icp55. J. Biol. Chem. 284, 30200-30208
19. Amutha, B., Gordon, D. M., Gu, Y., Lyver, E. R., Dancis, A. and Pain, D. (2008) GTP is required for iron-sulfur cluster biogenesis in mitochondria. J. Biol. Chem. 283, 1362-1371
20. Amutha, B., Gordon, D. M., Dancis, A. and Pain, D. (2009) Nucleotide-dependent iron-sulfur cluster biogenesis of endogenous and imported apoproteins in isolated intact mitochondria. Methods Enzymol. 456, 247-266
21. Pain, J., Balamurali, M. M., Dancis, A. and Pain, D. (2010) Mitochondrial NADH kinase, Pos5p, is required for efficient iron-sulfur cluster biogenesis in Saccharomyces cerevisiae. J. Biol. Chem. 285, 39409-39424
22. Yoon, H., Zhang, Y., Pain, J., Lyver, E. R., Lesuisse, E., Pain, D. and Dancis, A. (2011) Rim2, a pyrimidine nucleotide exchanger, is needed for iron utilization in mitochondria. Biochem. J. 440, 137-146
23. Wiedemann, N., Urzica, E., Guiard, B., Müller, H., Lohaus, C., Meyer, H. E., Ryan, M. T., Meisinger, C., Mühlenhoff, U., Lill, R. and Pfanner, N. (2006) Essential role of Isd11 in mitochondrial iron-sulfur cluster synthesis on Isu scaffold proteins. EMBO J. 25, 184-195
24. Adam, A. C., Bornhövd, C., Prokisch, H., Neupert, W. and Hell, K. (2006) The Nfs1 interacting protein Isd11 has an essential role in Fe/S cluster biogenesis in mitochondria. EMBO J. 25, 174-183
25. Shi, Y., Ghosh, M. C., Tong, W.-H. and Rouault, T. A. (2009) Human ISD11 is essential for both iron-sulfur cluster assembly and maintenance of normal cellular iron homeostasis. Hum. Mol. Genet. 18, 3014-3025
26. Pandey, A., Yoon, H., Lyver, E. R., Dancis, A. and Pain, D. (2012) Identification of a Nfs1p-bound persulfide intermediate in Fe-S cluster synthesis by intact mitochondria. Mitochondrion 12, 539-549
27. Longtine, M. S., McKenzie, III, A., Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J. R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961
28. Sepuri, N. B. V., Gordon, D. M. and Pain, D. (1998) A GTP-dependent "push" is generally required for efficient protein translocation across the mitochondrial inner membrane into the matrix. J. Biol. Chem. 273, 20941-20950
29. Gu, Y., Gordon, D. M., Amutha, B. and Pain, D. (2005) A GTP:AMP phosphotransferase, Adk2p, in Saccharomyces cerevisiae: role of the C-terminus in protein folding/stabilization, thermal tolerance, and enzymatic activity. J. Biol. Chem. 280, 18604-18609
30. Siegel, L. M. (1965) A direct microdetermination for sulfide. Anal. Biochem. 11, 126-132
31. 2 - of aconitase during cluster interconversions and removal. J. Biol. Chem. 263, 8194-8198
32. Munujos, P., Coll-Canti, J., Gonzalez-Sastre, F. and Gella, F. J. (1993) Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor. Anal. Biochem. 212, 506-509
33. Siegel, L. and Englard, S. (1962) Beef heart malic dehydrogenases. III. Comparative studies of some properties of M-malic dehydrogenase and S-malic dehydrogenase. Biochim. Biophys. Acta 64, 101-110
34. Chouchani, E. T., James, A. M., Fearnley, I. M., Lilley, K. S. and Murphy, M. P. (2011) Proteomic approaches to the characterization of protein thiol modification. Curr. Opin. Chem. Biol. 15, 120-128
35. Hochgräfe, F., Mostertz, J., Pöther, D.-C., Becher, D., Helmann, J. D. and Hecker, M. (2007) S-Cysteinylation is a general mechanism for thiol protection of Bacillus subtilis proteins after oxidative stress. J. Biol. Chem. 282, 25981-25985
36. 2S signals through protein S-sulfhydration. Sci. Signaling 2, ra72
37. Ghezzi, D., Goffrini, P., Uziel, G., Horvath, R., Klopstock, T., Lochmüller, H., D'Adamo, P., Gasparini, P., Strom, T. M., Prokisch, H. et al. (2009) SDHAF1, encoding a LYR complex-II specific assembly factor, is mutated in SDH-defective infantile leukoencephalopathy. Nat. Genet. 6, 654-656
38. Atkinson, A., Smith, P., Fox, J. L., Cui, T.-Z., Khalimonchuk, O. and Winge, D. R. (2011) The LYR protein Mzm1 functions in the insertion of the Rieske Fe/S protein in yeast mitochondria. Mol. Cell. Biol. 31, 3988-3996
39. Mihara, H. and Esaki, N. (2002) Bacterial cysteine desulfurases: their function and mechanisms. Appl. Microbiol. Biotechnol. 60, 12-23
40. Tsai, C.-L. and Barondeau, D. P. (2010) Human frataxin is an allosteric switch that activates the Fe-S cluster biosynthetic complex. Biochemistry 49, 9132-9139
41. Schmucker, S., Martelli, A., Colin, F., Page, A., Wattenhofer- Donzé, M., Reutenauer, L. and Puccio, H. (2011) Mammalian frataxin: an essential function for cellular viability through an interaction with a preformed ISCU/NFS1/ISD11 iron-sulfur assembly complex. PLoS ONE 6, e16199