Loss of vacuolar H+-ATPase (V-ATPase) activity in yeast generates an iron deprivation signal that is moderated by induction of the peroxiredoxin TSA2

Journal of Biological Chemistry

Volumn 288, Issue 16, 2013, Pages 11366-11377

  Diab, Heba I ^a   Kane, Patricia M ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IRON HOMEOSTASIS; IRON UPTAKE; PH CONTROL; UP-REGULATION; V-ATPASE;

PHYSIOLOGY;

IRON;

CONCANAMYCIN A; GREEN FLUORESCENT PROTEIN; IRON; MUTANT PROTEIN; PEROXIREDOXIN; PROTEIN TSA2P; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG;

ARTICLE; BIOSENSOR; CELL NUCLEUS; CELL ORGANELLE; CELL PH; CELL VACUOLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INHIBITION; EUKARYOTE; GENE; GENE CONTROL; GENE MUTATION; GENETIC TRANSCRIPTION; HOMEOSTASIS; IRON BALANCE; IRON DEFICIENCY; IRON DEPLETION; IRON THERAPY; IRON TRANSPORT; MUTANT; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULON; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TSA2 GENE; UPREGULATION; VMA2 GENE;

GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; HOMEOSTASIS; HYDROGEN-ION CONCENTRATION; IRON; OXIDATIVE STRESS; PEROXIDASES; PEROXIREDOXINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84876582502     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.419259     Document Type: Article

References (65)

1. Bali, P. K., and Aisen, P. (1992) Receptor-induced switch in site-site cooperativity during iron release by transferrin. Biochemistry 31, 3963-3967.
2. Cipriano, D. J., Wang, Y., Bond, S., Hinton, A., Jefferies, K. C., Qi, J., and Forgac, M. (2008) Structure and regulation of the vacuolar ATPases. Biochim. Biophys. Acta 1777, 599-604.
3. Dautry-Varsat, A., Ciechanover, A., and Lodish, H. F. (1983) pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Natl. Acad. Sci. U.S.A. 80, 2258-2262.
4. Sorkin, A., and Von Zastrow, M. (2002) Signal transduction and endocytosis. Close encounters of many kinds. Nat. Rev. Mol. Cell Biol. 3, 600-614.
5. Karmazyn, M., Gan, X. T., Humphreys, R. A., Yoshida, H., and Kusumoto, K. (1999) The myocardial Na+-H+ exchange. Structure, regulation, and its role in heart disease. Circ. Res. 85, 777-786.
6. Kinouchi, K., Ichihara, A., Sano, M., Sun-Wada, G. H., Wada, Y., Kurauchi-Mito, A., Bokuda, K., Narita, T., Oshima, Y., Sakoda, M., Tamai, Y., Sato, H., Fukuda, K., and Itoh, H. (2010) The (pro)renin receptor/ ATP6AP2 is essential for vacuolar H+-ATPase assembly in murine cardiomyocytes. Circ. Res. 107, 30-34.
7. Williamson, W. R., and Hiesinger, P. R. (2010) On the role of v-ATPase V0a1-dependent degradation in Alzheimer disease. Commun. Integr. Biol. 3, 604-607.
8. Williamson, W. R., Wang, D., Haberman, A. S., and Hiesinger, P. R. (2010) A dual function of V0-ATPase a1 provides an endolysosomal degradation mechanism in Drosophila melanogaster photoreceptors. J. Cell Biol. 189, 885-899.
9. Kane, P. M. (2006) The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol. Mol. Biol. Rev. 70, 177-191.
10. Nishi, T., and Forgac, M. (2002) The vacuolar (H+)-ATPases. Nature's most versatile proton pumps. Nat. Rev. Mol. Cell Biol. 3, 94-103.
11. Breton, S., and Brown, D. (2007) New insights into the regulation of VATPase-dependent proton secretion. Am. J. Physiol. Renal Physiol. 292, F1-F10.
12. Allan, A. K., Du, J., Davies, S. A., and Dow, J. A. (2005) Genome-wide survey of V-ATPase genes in Drosophila reveals a conserved renal phenotype for lethal alleles. Physiol. Genomics 22, 128-138.
13. Sun-Wada, G., Murata, Y., Yamamoto, A., Kanazawa, H., Wada, Y., and Futai, M. (2000) Acidic endomembrane organelles are required for mouse postimplantation development. Dev. Biol. 228, 315-325.
14. Martínez-Muñoz, G. A., and Kane, P. (2008) Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J. Biol. Chem. 283, 20309-20319.
15. Tarsio, M., Zheng, H., Smardon, A. M., Martínez-Muñoz, G. A., and Kane, P. M. (2011) Consequences of loss of Vph1 protein-containing vacuolar ATPases (V-ATPases) for overall cellular pH homeostasis. J. Biol. Chem. 286, 28089-28096.
16. Bañuelos, M. A., Sychrová, H., Bleykasten-Grosshans, C., Souciet, J. L., and Potier, S. (1998) The Nha1 antiporter of Saccharomyces cerevisiae mediates sodium and potassium efflux. Microbiology 144, 2749-2758.
17. Pardo, J. M., Cubero, B., Leidi, E. O., and Quintero, F. J. (2006) Alkali cation exchangers. Roles in cellular homeostasis and stress tolerance. J. Exp. Bot. 57, 1181-1199.
18. Beauvoit, B., Rigoulet, M., Raffard, G., Canioni, P., and Guérin, B. (1991) Differential sensitivity of the cellular compartments of Saccharomyces cerevisiae to protonophoric uncoupler under fermentative and respiratory energy supply. Biochemistry 30, 11212-11220.
19. Freimoser, F. M., Hürlimann, H. C., Jakob, C. A., Werner, T. P., and Amrhein, N. (2006) Systematic screening of polyphosphate (poly P) levels in yeast mutant cells reveals strong interdependence with primary metabolism. Genome Biol. 7, R109.
20. Milgrom, E., Diab, H., Middleton, F., and Kane, P. M. (2007) Loss of vacuolar proton-translocating ATPase activity in yeast results in chronic oxidative stress. J. Biol. Chem. 282, 7125-7136.
21. Jamieson, D. J. (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14, 1511-1527.
22. Brombacher, K., Fischer, B. B., Rüfenacht, K., and Eggen, R. I. (2006) The role of Yap1p and Skn7p-mediated oxidative stress response in the defence of Saccharomyces cerevisiae against singlet oxygen. Yeast 23, 741-750.
23. Thorpe, G. W., Fong, C. S., Alic, N., Higgins, V. J., and Dawes, I. W. (2004) Cells have distinct mechanisms to maintain protection against different reactive oxygen species. Oxidative-stress-response genes. Proc. Natl. Acad. Sci. U.S.A. 101, 6564-6569.
24. Berggren, M. I., Husbeck, B., Samulitis, B., Baker, A. F., Gallegos, A., and Powis, G. (2001) Thioredoxin peroxidase-1 (peroxiredoxin-1) is increased in thioredoxin-1 transfected cells and results in enhanced protection against apoptosis caused by hydrogen peroxide but not by other agents including dexamethasone, etoposide, and doxorubicin. Arch. Biochem. Biophys. 392, 103-109.
25. Wong, C. M., Zhou, Y., Ng, R. W., Kung Hf, H. F., and Jin, D. Y. (2002) Cooperation of yeast peroxiredoxins Tsa1p and Tsa2p in the cellular defense against oxidative and nitrosative stress. J. Biol. Chem. 277, 5385-5394.
26. Munhoz, D. C., and Netto, L. E. (2004) Cytosolic thioredoxin peroxidase I and II are important defenses of yeast against organic hydroperoxide insult. Catalases and peroxiredoxins cooperate in the decomposition of H2O2 by yeast. J. Biol. Chem. 279, 35219-35227.
27. Iraqui, I., Kienda, G., Soeur, J., Faye, G., Baldacci, G., Kolodner, R. D., and Huang, M. E. (2009) Peroxiredoxin Tsa1 is the key peroxidase suppressing genome instability and protecting against cell death in Saccharomyces cerevisiae. PLoS Genet. 5, e1000524.
28. Sideri, T. C., Stojanovski, K., Tuite, M. F., and Grant, C. M. (2010) Ribosome-associated peroxiredoxins suppress oxidative stress-induced de novo formation of the [PSI+] prion in yeast. Proc. Natl. Acad. Sci. U.S.A. 107, 6394-6399.
29. Trotter, E. W., Rand, J. D., Vickerstaff, J., and Grant, C. M. (2008) The yeast Tsa1 peroxiredoxin is a ribosome-associated antioxidant. Biochem. J. 412, 73-80.
30. Li, L., Murdock, G., Bagley, D., Jia, X., Ward, D. M., and Kaplan, J. (2010) Genetic dissection of a mitochondria-vacuole signaling pathway in yeast reveals a link between chronic oxidative stress and vacuolar iron transport. J. Biol. Chem. 285, 10232-10242.
31. Philpott, C. C., and Protchenko, O. (2008) Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot. Cell 7, 20-27.
32. Courel, M., Lallet, S., Camadro, J. M., and Blaiseau, P. L. (2005) Direct activation of genes involved in intracellular iron use by the yeast ironresponsive transcription factor Aft2 without its paralog Aft1. Mol. Cell Biol. 25, 6760-6771.
33. Yamaguchi-Iwai, Y., Ueta, R., Fukunaka, A., and Sasaki, R. (2002) Subcellular localization of Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae. J. Biol. Chem. 277, 18914-18918.
34. 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.
35. Kumánovics, A., Chen, O. S., Li, L., Bagley, D., Adkins, E. M., Lin, H., Dingra, N. N., Outten, C. E., Keller, G., Winge, D., Ward, D. M., and Kaplan, J. (2008) Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J. Biol. Chem. 283, 10276-10286.
36. Li, H., Mapolelo, D. T., Dingra, N. N., Naik, S. G., Lees, N. S., Hoffman, B. M., Riggs-Gelasco, P. J., Huynh, B. H., Johnson, M. K., and Outten, C. E. (2009) The yeast iron regulatory proteins Grx3/4 and Fra2 form heterodimeric complexes containing a [2Fe-2S] cluster with cysteinyl and histidyl ligation. Biochemistry 48, 9569-9581.
37. Valko, M., Morris, H., and Cronin, M. T. (2005) Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161-1208.
38. Tong, A. H., Evangelista, M., Parsons, A. B., Xu, H., Bader, G. D., Pagé, N., Robinson, M., Raghibizadeh, S., Hogue, C. W., Bussey, H., Andrews, B., Tyers, M., and Boone, C. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368.
39. Longtine, M. S., McKenzie, A., 3rd, 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.
40. Kane, P. M., Kuehn, M. C., Howald-Stevenson, I., and Stevens, T. H. (1992) Assembly and targeting of peripheral and integral membrane subunits of the yeast vacuolar H+-ATPase. J. Biol. Chem. 267, 447-454.
41. Pierik, A. J., Netz, D. J., and Lill, R. (2009) Analysis of iron-sulfur protein maturation in eukaryotes. Nat. Protoc. 4, 753-766.
42. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003) Global analysis of protein expression in yeast. Nature 425, 737-741.
43. Urbanowski, J. L., and Piper, R. C. (1999) The iron transporter Fth1p forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane. J. Biol. Chem. 274, 38061-38070.
44. 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.
45. 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.
46. Pujol-Carrion, N., Belli, G., Herrero, E., Nogues, A., and de la Torre-Ruiz, M. A. (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J. Cell Sci. 119, 4554-4564.
47. Li, H., Mapolelo, D. T., Dingra, N. N., Keller, G., Riggs-Gelasco, P. J., Winge, D. R., Johnson, M. K., and Outten, C. E. (2011) Histidine 103 in Fra2 is an iron-sulfur cluster ligand in the [2Fe-2S] Fra2-Grx3 complex and is required for in vivo iron signaling in yeast. J. Biol. Chem. 286, 867-876.
48. Irazusta, V., Moreno-Cermeño, A., Cabiscol, E., Ros, J., and Tamarit, J. (2008) Major targets of iron-induced protein oxidative damage in frataxin-deficient yeasts are magnesium-binding proteins. Free Radic. Biol. Med. 44, 1712-1723.
49. Wong, C. M., Ching, Y. P., Zhou, Y., Kung, H. F., and Jin, D. Y. (2003) Transcriptional regulation of yeast peroxiredoxin gene TSA2 through Hap1p, Rox1p, and Hap2/3/5p. Free Radic. Biol. Med. 34, 585-597.
50. Herrero, E., Ros, J., Bellí, G., and Cabiscol, E. (2008) Redox control and oxidative stress in yeast cells. Biochim. Biophys. Acta 1780, 1217-1235.
51. Follmann, M., Ochrombel, I., Krämer, R., Trötschel, C., Poetsch, A., Rückert, C., Hüser, A., Persicke, M., Seiferling, D., Kalinowski, J., and Marin, K. (2009) Functional genomics of pH homeostasis in Corynebacterium glutamicum revealed novel links between pH response, oxidative stress, iron homeostasis and methionine synthesis. BMC Genomics 10, 621.
52. Cockrell, A. L., Holmes-Hampton, G. P., McCormick, S. P., Chakrabarti, M., and Lindahl, P. A. (2011) Mossbauer and EPR study of iron in vacuoles from fermenting Saccharomyces cerevisiae. Biochemistry 50, 10275-10283.
53. Davis-Kaplan, S. R., Ward, D. M., Shiflett, S. L., and Kaplan, J. (2004) Genome-wide analysis of iron-dependent growth reveals a novel yeast gene required for vacuolar acidification. J. Biol. Chem. 279, 4322-4329.
54. Rand, J. D., and Grant, C. M. (2006) The thioredoxin system protects ribosomes against stress-induced aggregation. Mol. Biol. Cell 17, 387-401.
55. Jang, H. H., Lee, K. O., Chi, Y. H., Jung, B. G., Park, S. K., Park, J. H., Lee, J. R., Lee, S. S., Moon, J. C., Yun, J. W., Choi, Y. O., Kim, W. Y., Kang, J. S., Cheong, G. W., Yun, D. J., Rhee, S. G., Cho, M. J., and Lee, S. Y. (2004) Two enzymes in one. Two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 117, 625-635.
56. Serrano, R., Bernal, D., Simón, E., and Ariño, J. (2004) Copper and iron are the limiting factors for growth of the yeast Saccharomyces cerevisiae in an alkaline environment. J. Biol. Chem. 279, 19698-19704.
57. Davis-Kaplan, S. R., Askwith, C. C., Bengtzen, A. C., Radisky, D., and Kaplan, J. (1998) Chloride is an allosteric effector of copper assembly for the yeast multicopper oxidase Fet3p. An unexpected role for intracellular chloride channels. Proc. Natl. Acad. Sci. U.S.A. 95, 13641-13645.
58. Spizzo, T., Byersdorfer, C., Duesterhoeft, S., and Eide, D. (1997) The yeast FET5 gene encodes a FET3-related multicopper oxidase implicated in iron transport. Mol. Gen. Genet. 256, 547-556.
59. Hirsch, J., Marin, E., Floriani, M., Chiarenza, S., Richaud, P., Nussaume, L., and Thibaud, M. C. (2006) Phosphate deficiency promotes modification of iron distribution in Arabidopsis plants. Biochimie 88, 1767-1771.
60. Yang, K. S., Kang, S. W., Woo, H. A., Hwang, S. C., Chae, H. Z., Kim, K., and Rhee, S. G. (2002) Inactivation of human peroxiredoxin I during catalysis as the result of the oxidation of the catalytic site cysteine to cysteine-sulfinic acid. J. Biol. Chem. 277, 38029-38036.
61. Fomenko, D. E., Koc, A., Agisheva, N., Jacobsen, M., Kaya, A., Malinouski, M., Rutherford, J. C., Siu, K. L., Jin, D. Y., Winge, D. R., and Gladyshev, V. N. (2011) Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proc. Natl. Acad. Sci. U.S.A. 108, 2729-2734.
62. Delaunay, A., Pflieger, D., Barrault, M. B., Vinh, J., and Toledano, M. B. (2002) A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell 111, 471-481.
63. Iwai, K., Naganuma, A., and Kuge, S. (2010) Peroxiredoxin Ahp1 acts as a receptor for alkylhydroperoxides to induce disulfide bond formation in the Cad1 transcription factor. J. Biol. Chem. 285, 10597-10604.
64. 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.
65. 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.