A role for iron-sulfur clusters in the regulation of transcription factor Yap5-dependent high iron transcriptional responses in yeast

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35709-35721

  Li, Liangtao ^a   Miao, Ren ^a   Bertram, Sophie ^a   Jia, Xuan ^a   Ward, Diane M ^a   Kaplan, Jerry ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSOLIC; GENETIC SCREENS; GENTISATE; IRON-SULFUR CLUSTERS; REGULATION OF TRANSCRIPTION; TARGET GENES; TRANSCRIPTIONAL RESPONSE;

ENCODING (SYMBOLS); GENES; IRON; SULFUR; TRANSCRIPTION; TRANSCRIPTION FACTORS; YEAST;

IRON COMPOUNDS;

CHAPERONE; GLUTAREDOXIN; HOMOGENTISATE 1,2 DIOXYGENASE; IRON; IRON SULFUR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR YAP5; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL GENE; FUNGAL GENETICS; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOSS; GENE MUTATION; GENE TARGETING; GENETIC PROCEDURES; GENETIC SCREENING; ISU1 GENE; MITOCHONDRION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PSEUDAMINOBACTER SALICYLATOXIDANS; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; SSQ1 GENE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; YEAST; YFH1 GENE;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, FUNGAL; HSP70 HEAT-SHOCK PROTEINS; IRON; MITOCHONDRIAL PROTEINS; MUTATION; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SULFUR; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84867415067     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.395533     Document Type: Article

References (38)

1. Kaplan, J., McVey Ward, D., Crisp, R. J., and Philpott, C. C. (2006) Iron-dependent metabolic remodeling in S. cerevisiae. Biochim. Biophys. Acta 1763, 646-651 (Pubitemid 44189539)
2. Ehrensberger, K. M., and Bird, A. J. (2011) Hammering out details: regulating metal levels in eukaryotes. Trends Biochem. Sci. 36, 524-531
3. Chen, O. S., Crisp, R. J., Valachovic, M., Bard, M., Winge, D. R., and Kaplan, J. (2004) Transcription of the yeast iron regulon does not respond directly to iron but rather to iron-sulfur cluster biosynthesis. J. Biol. Chem. 279, 29513-29518 (Pubitemid 38915831)
4. Rutherford, J. C., Ojeda, L., Balk, J., Mühlenhoff, U., Lill, R., and Winge, D. R. (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J. Biol. Chem. 280, 10135-10140 (Pubitemid 40395866)
5. Mühlenhoff, U., Molik, S., Godoy, J. R., Uzarska, M. A., Richter, N., Seubert, A., Zhang, Y., Stubbe, J., Pierrel, F., Herrero, E., Lillig, C. H., and Lill, R. (2010) Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell Metab. 12, 373-385
6. Ojeda, L., Keller, G., Muhlenhoff, U., Rutherford, J. C., Lill, R., and Winge, D. R. (2006) Role of glutaredoxin-3 and glutaredoxin-4 in the iron regulation of the Aft1 transcriptional activator in Saccharomyces cerevisiae. J. Biol. Chem. 281, 17661-17669 (Pubitemid 44035564)
7. Pujol-Carrion, N., Belli, G., Herrero, E., Nogues, A., and de la Torre-Ruiz, M. A. (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localization of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J. Cell Sci. 119, 4554-4564 (Pubitemid 44830654)
8. Li, L., Bagley, D., Ward, D. M., and Kaplan, J. (2008) Yap5 is an iron-responsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol. Cell Biol. 28, 1326-1337 (Pubitemid 351214134)
9. Li, L., Jia, X., Ward, D. M., and Kaplan, J. (2011) Yap5 protein-regulated transcription of the TYW1 gene protects yeast from high iron toxicity. J. Biol. Chem. 286, 38488-38497
10. Pimentel, C., Vicente, C., Menezes, R. A., Caetano, S., Carreto, L., and Rodrigues-Pousada, C. (2012) The role of the Yap5 transcription factor in remodeling gene expression in response to iron bioavailability. PLoS One 7, e37434
11. Chen, O. S., Hemenway, S., and Kaplan, J. (2002) Inhibition of Fe-S cluster biosynthesis decreases mitochondrial iron export: evidence that Yfh1p affects Fe-S cluster synthesis. Proc. Natl. Acad. Sci. U.S.A. 99, 12321-12326
12. Hintner, J. P., Lechner, C., Riegert, U., Kuhm, A. E., Storm, T., Reemtsma, T., and Stolz, A. (2001) Direct ring fission of salicylate by a salicylate 1,2-dioxygenase activity from Pseudaminobacter salicylatoxidans. J. Bacteriol. 183, 6936-6942 (Pubitemid 33064208)
13. Lutz, T., Westermann, B., Neupert, W., and Herrmann, J. M. (2001) The mitochondrial proteins Ssq1 and Jac1 are required for the assembly of iron sulfur clusters in mitochondria. J. Mol. Biol. 307, 815-825 (Pubitemid 33027661)
14. Dutkiewicz, R., Schilke, B., Knieszner, H., Walter, W., Craig, E. A., and Marszalek, J. (2003) Ssq1, a mitochondrial Hsp70 involved in iron-sulfur (Fe-S) center biogenesis: similarities to and differences from its bacterial counterpart. J. Biol. Chem. 278, 29719-29727 (Pubitemid 36962358)
15. Irazusta, V., Obis, E., Moreno-Cermeño, A., Cabiscol, E., Ros, J., and Tamarit, J. (2010) Yeast frataxin mutants display decreased superoxide dismutase activity crucial to promote protein oxidative damage. Free Rad. Biol. Med. 48, 411-420
16. Li, L., and Kaplan, J. (1996) Characterization of yeast methyl sterol oxidase (ERG25) and identification of a human homologue. J. Biol. Chem. 271, 16927-16933 (Pubitemid 26239063)
17. Hintner, J. P., Reemtsma, T., and Stolz, A. (2004) Biochemical and molecular characterization of a ring fission dioxygenase with the ability to oxidize (substituted) salicylate(s) from Pseudaminobacter salicylatoxidans. J. Biol. Chem. 279, 37250-37260 (Pubitemid 39195431)
18. Matera, I., Ferraroni, M., Bürger, S., Scozzafava, A., Stolz, A., and Briganti, F. (2008) Salicylate 1,2-dioxygenase from Pseudaminobacter salicylatoxidans: crystal structure of a peculiar ring-cleaving dioxygenase. J. Mol. Biol. 380, 856-868
19. Lah, M. S., Dixon, M. M., Pattridge, K. A., Stallings, W. C., Fee, J. A., and Ludwig, M. L. (1995) Structure-function in Escherichia coli iron superoxide dismutase: comparisons with the manganese enzyme from Thermus thermophilus. Biochemistry 34, 1646-1660
20. Harpel, M. R., and Lipscomb, J. D. (1990) Gentisate 1,2-dioxygenase from Pseudomonas: purification, characterization, and comparison of the enzymes from Pseudomonas testosteroni and Pseudomonas acidovorans. J. Biol. Chem. 265, 6301-6311
21. Stearman, R., Dancis, A., and Klausner, R. D. (1998) YIpDCE1: an integrating plasmid for dual constitutive expression in yeast. Gene 212, 197-202 (Pubitemid 28274464)
22. Mühlenhoff, U., Richhardt, N., Ristow, M., Kispal, G., and Lill, R. (2002) The yeast frataxin homologue Yfh1p plays a specific role in the maturation of cellular Fe-S proteins. Hum. Mol. Genet. 11, 2025-2036 (Pubitemid 34919277)
23. Radisky, D. C., Babcock, M. C., and Kaplan, J. (1999) The yeast frataxin homologue mediates mitochondrial iron efflux. Evidence for a mitochondrial iron cycle. J. Biol. Chem. 274, 4497-4499
24. 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 (Pubitemid 29422537)
25. Lill, R., and Mühlenhoff, U. (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu. Rev. Biochem. 77, 669-700
26. Balk, J., Pierik, A. J., Netz, D. J., Mühlenhoff, U., and Lill, R. (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulfur proteins. EMBO J. 23, 2105-2115 (Pubitemid 38737737)
27. Zhang, Y., Lyver, E. R., Nakamaru-Ogiso, E., Yoon, H., Amutha, B., Lee, D. W., Bi, E., Ohnishi, T., Daldal, F., Pain, D., and Dancis, A. (2008) Dre2, a conserved eukaryotic Fe-S cluster protein, functions in cytosolic Fe-S protein biogenesis. Mol. Cell Biol. 28, 5569-5582
28. Bellí, G., Molina, M. M., García-Martínez, J., Pérez-Ortín, J. E., and Herrero, E. (2004) Saccharomyces cerevisiae glutaredoxin 5-deficient cells subjected to continuous oxidizing conditions are affected in the expression of specific sets of genes. J. Biol. Chem. 279, 12386-12395 (Pubitemid 38445806)
29. Puig, S., Askeland, E., and Thiele, D. J. (2005) Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120, 99-110 (Pubitemid 40094606)
30. Miao, R., Kim, H., Koppolu, U. M., Ellis, E. A., Scott, R. A., and Lindahl, P. A. (2009) Biophysical characterization of the iron in mitochondria from Atm1p-depleted Saccharomyces cerevisiae . Biochemistry. 48, 9556 -9568
31. Rouault, T. A. (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol. 2, 406-414
32. Askwith, C., and Kaplan, J. (1997) An oxidase-permease-based iron transport system in Schizosaccharomyces pombe and its expression in Saccharomyces cerevisiae. J. Biol. Chem. 272, 401-405 (Pubitemid 27021172)
33. Yamaguchi-Iwai, Y., Stearman, R., Dancis, A., and Klausner, R. D. (1996) Iron-regulated DNA binding by the AFT1 protein controls the iron regulon in yeast. EMBO J. 15, 3377-3384 (Pubitemid 26231944)
34. Pelletier, B., Trott, A., Morano, K. A., and Labbé, S. (2005) Functional characterization of the iron regulatory transcription factor Fep1 from Schizosaccharomyces pombe. J. Biol. Chem. 280, 25146-25161 (Pubitemid 40934607)
35. Kim, K. D., Kim, H. J., Lee, K. C., and Roe, J. H. (2011) Multidomain CGFS-type glutaredoxin Grx4 regulates iron homeostasis via direct interaction with a repressor Fep1 in fission yeast. Biochem. Biophys. Res. Commun. 408, 609-614
36. Jbel, M., Mercier, A., and Labbé, S. (2011) Grx4 monothiol glutaredoxin is required for iron limitation-dependent inhibition of Fep1. Eukaryot. Cell 10, 629-645
37. Mercier, A., Pelletier, B., and Labbé, S. (2006) A transcription factor cascade involving Fep1 and the CCAAT-binding factor Php4 regulates gene expression in response to iron deficiency in the fission yeast Schizosaccharomyces pombe. Eukaryot. Cell 5, 1866-1881
38. Vachon, P., Mercier, A., Jbel, M., and Labbé, S. (2012) The monothiol glutaredoxin Grx4 exerts an iron-dependent inhibitory effect on Php4 function. Eukaryot. Cell 11, 806-819