The oxidative stress response in yeast cells involves changes in the stability of Aft1 regulon mRNAs

Molecular Microbiology

Volumn 81, Issue 1, 2011, Pages 232-248

  Castells Roca, Laia ^a   Mühlenhoff, Ulrich ^b   Lill, Roland ^b   Herrero, Enrique ^a   Bellí, Gemma ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CERULOPLASMIN; FERROUS ION; IRON; MESSENGER RNA; PEROXIDE; PROTEIN AFT1; PROTEIN CTH2; PROTEIN FET3; PROTEIN FTR1; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; FUNGUS GROWTH; INTERNALIZATION; IRON METABOLISM; IRON TRANSPORT; MRNA DECAY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGULON; RNA STABILITY; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; YEAST CELL;

CERULOPLASMIN; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN PEROXIDE; IRON; MEMBRANE TRANSPORT PROTEINS; OXIDANTS; OXIDATIVE STRESS; REGULON; RNA STABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS;

SACCHAROMYCES CEREVISIAE;

EID: 80955179977     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07689.x     Document Type: Article

References (71)

1. Askwith, C., Eide, D., Van Ho, A., Bernard, P.S., Li, L., Davis-Kaplan, S., etal. (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76: 403-410.
2. Azzouz, N., Panasenko, O.O., Deluen, C., Hsieh, J., Theiler, G., and Collart, M.A. (2010) Specific roles for the Ccr4-Not complex subunits in expression of the genome. RNA 15: 377-383.
3. Balk, J., Aguilar Netz, D.J., Tepper, K., Pierik, A.J., and Lill, R. (2005) The essential WD40 protein Cia1is involved in a late step of cytosolic and nuclear iron-sulfur protein assembly. Mol Cell Biol 24: 10833-10841.
4. Bellí, G., Garí, E., Aldea, M., and Herrero, E. (1998a) Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14: 1127-1138.
5. Bellí, G., Garí, E., Piedrafita, L., Aldea, M., and Herrero, E. (1998b) An activator/repressor dual system allows tight tetracycline-regulated gene expression in budding yeast. Nucleic Acids Res 26: 942-947.
6. 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 set of genes. J Biol Chem 279: 12386-12395.
7. Berthelet, S., Usher, J., Shulist, K., Hamza, A., Maltez, N., Johnston, A., etal. (2010) Functional genomics analysis of the Saccharomyces cerevisiae iron responsive transcription factor Aft1 reveals iron-independent functions. Genetics 185: 1111-1128.
8. Blaiseau, P.L., Lesuisse, E., and Camadro, J.M. (2001) Aft2p, a novel iron-regulated transcription activator that modulates, with Aft1p, intracellular iron use and resistance to oxidative stress in yeast. J Biol Chem 276: 34221-34226.
9. Cabiscol, E., Piulats, E., Echave, P., Herrero, E., and Ros, J. (2000) Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J Biol Chem 275: 27393-27398.
10. Cairo, G., and Recalcati, S. (2007) Iron-regulatory proteins: molecular biology and pathophysiological implications. Expert Rev Mol Med 9: 1-13.
11. Cohen, A., Nelson, H., and Nelson, N. (2000) The family of SMF metal ion transporters in yeast cells. J Biol Chem 275: 33388-33394.
12. Cui, Y., Ramnarain, D.B., Chiang, Y.C., Ding, L.H., McMahon, J.S., and Denis, C.L. (2008) Genome expression analysis of the CCR4-NOT complex indicates that it consists of three modules with the NOT module controlling SAGA-sensitive genes. Mol Genet Genomics 279: 323-337.
13. Davis-Kaplan, S.R., Ward, D.M., Shiflett, S.L., and Kaplan, J. (2004) Genomic-wide analysis of iron-dependent growth reveals a novel yeast gene required for vacuolar acidification. J Biol Chem 279: 4322-4329.
14. De Silva, D.M., Askwith, C.C., Eide, D., and Kaplan, J. (1995) The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J Biol Chem 270: 1098-1101.
15. Dubacq, C., Chevalier, A., Courbeyrette, R., Petat, C., Gidrol, X., and Mann, C. (2006) Role of the iron mobilization and oxidative stress regulons in the genomic response of yeast to hydroxyurea. Mol Genet Genomics 275: 114-124.
16. Dudley, A.M., Janse, D.M., Tanay, A., Shamir, R., and Church, G.M. (2005) A global view of pleiotropy and phenotypically derived gene function in yeast. Mol Syst Biol 1: 2005.0001.
17. Foury, F., and Talibi, D. (2001) Mitochondrial control of iron homeostasis. A genome wide analysis of the gene expression in a yeast frataxin-deficient strain. J Biol Chem 276: 7762-7768.
18. Garneau, N.L., Wilusz, J., and Wilusz, C.J. (2007) The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8: 113-126.
19. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., etal. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
20. Gietz, R.D., and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 3065-3073.
21. Goldstein, A.L., and McCusker, J.H. (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
22. Halliwell, B., and Gutteridge, J.M.C. (2007) Free Radicals in Biology and Medicine, 4th edn. Oxford: Oxford University Press.
23. Hassett, R.F., Romeo, A.M., and Kosman, D.J. (1998) Regulation of high affinity iron uptake in the yeast Saccharomyces cerevisiae. Role of dioxygen and Fe. J Biol Chem 273: 7628-7636.
24. Hausmann, A., Aguilar Netz, D.J., Balk, J., Pierik, A.J., Mühlenhoff, U., and Lill, R. (2005) The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc Natl Acad Sci USA 102: 3266-3271.
25. Hausmann, A., Samans, B., Lill, R., and Mühlenhoff, U. (2008) Cellular and mitochondrial remodeling upon defects in iron-sulfur protein biogenesis. J Biol Chem 283: 8318-8330.
26. Herrero, E., Ros, J., Bellí, G., and Cabiscol, E. (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780: 1217-1235.
27. Heymann, P., Ernst, J.F., and Winkelmann, G. (2000) A gene of the major facilitator superfamily encodes a transporter for enterobactin (Enb1p) in Saccharomyces cerevisiae. Biometals 13: 65-72.
28. 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.
29. Jensen, L.T., and Culotta, V.C. (2002) Regulation of Saccharomyces cerevisiae FET4 by oxygen and iron. J Mol Biol 318: 251-260.
30. Jo, W.J., Kim, J.H., Oh, E., Jaramillo, D., Holman, P., Loguinov, A.V., etal. (2009) Novel insights into iron metabolism by integrating deletome and transcriptome analysis in an iron deficiency model of the yeast Saccharomyces cerevisiae. BMC Genomics 10: 130.
31. Kaplan, C.D., and Kaplan, J. (2009) Iron acquisition and transcriptional regulation. Chem Rev 109: 4536-4552.
32. Kimura, A., Ohashi, K., and Naganuma, A. (2007) Cisplatin upregulates Saccharomyces cerevisiae genes involved in iron homeostasis through activation of the iron insufficiency-responsive transcription factor Aft1. Cell Physiol 210: 378-384.
33. Kosman, D.J. (2003) Molecular mechanisms of iron uptake in fungi. Mol Microbiol 47: 1185-1197.
34. Kumánovics, A., Chen, O.S., Li, L., Bagley, D., Adkins, E.M., Lin, H., etal. (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.
35. Lamb, T.M., Xu, W., Diamond, A., and Mitchell, A.P. (2001) Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 276: 1850-1856.
36. Lee, A., Henras, A.K., and Chanfreau, G. (2005) Multiple RNA surveillance pathways limit aberrant expression of iron uptake mRNAs and prevent iron toxicity in S. cerevisiae. Mol Cell 19: 39-51.
37. Lesuisse, E., Blaiseau, P.L., Dancis, A., and Camadro, J.M. (2001) Siderophore uptake and use by the yeast Saccharomyces cerevisiae. Microbiology 147: 289-298.
38. Lesuisse, E., Knight, S.A., Courel, M., Santos, R., Camadro, J.M., and Dancis, A. (2005) Genome-wide screen for genes with effects on distinct iron uptake activities in Saccharomyces cerevisiae. Genetics 169: 107-122.
39. Li, H., Mapolelo, D.T., Dingra, N.N., Keller, G., Riggs-Gelasco, P.J., Winge, D.R., etal. (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.
40. 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.
41. Lill, R., and Mühlenhoff, U. (2008) Maturation of iron-sulfur proteins in eukariotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77: 669-700.
42. Molina-Navarro, M.M., Castells-Roca, L., Bellí, G., García-Martínez, J., Marín-Navarro, J., Moreno, J., etal. (2008) Comprehensive transcriptional analysis of the oxidative response in yeast. J Biol Chem 283: 17908-17918.
43. Moye-Rowley, W.S. (2003) Regulation of the transcriptional response to oxidative stress in fungi: similarities and differences. Eukaryot Cell 2: 381-389.
44. Ojeda, L., Keller, G., Mühlenhoff, U., Rutherford, J.C., Lill, R., and Winge, D. (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. Pagani, M.A., Casamayor, A., Serrano, R., Atrian, S., and Ariño, J. (2007) Disruption of iron homeostasis in Saccharomyces cerevisiae by high zinc levels: a genome-wide study. Mol Microbiol 65: 521-537.
46. Parker, R., and Song, H. (2004) The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 11: 121-127.
47. Pérez-Ortín, J.E., Alepuz, P., and Moreno, J. (2007) Genomics and gene transcription kinetics in yeast. Trends Genet 23: 250-257.
48. Philpott, C.C. (2006) Iron uptake in fungi: a system for every source. Biochim Biophys Acta 1763: 636-645.
49. Philpott, C.C., and Protchenko, O. (2008) Response to iron deprivation in Saccharomices cerevisiae. Eukaryot Cell 7: 20-27.
50. Portnoy, M.E., Liu, X.F., and Culotta, V.C. (2000) Saccharomyces cerevisiae expresses three functional distinct homologues of the Nramp family of metal transporters. Mol Cell Biol 20: 7893-7902.
51. Protchenko, O., Ferea, T., Rachford, J., Tiedman, J., Brown, P.O., Botstein, D., and Philpott, C.C. (2001) Three cell wall mannoproteins facilitate the uptake of iron in Saccharomyces cerevisiae. J Biol Chem 276: 49244-49250.
52. Puig, S., Askeland, E., and Thiele, D. (2005) Coordinated remodelling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120: 99-110.
53. Puig, S., Vergara, S.V., and Thiele, D.J. (2008) Cooperation of two mRNA-binding proteins drives metabolic adaptation to iron deficiency. Cell Metab 7: 555-564.
54. Pujol-Carrión, N., Bellí, G., Herrero, E., Nogués, A., and de la Torre-Ruiz, M.A. (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress in Saccharomyces cerevisiae. J Cell Sci 119: 4554-4564.
55. Rodríguez-Manzaneque, M.T., Tamarit, J., Bellí, G., Ros, J., and Herrero, E. (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13: 1109-1121.
56. Rutherford, J.C., Jaron, S., Ray, E., Brown, P.O., and Winge, D.R. (2001) A second iron-regulatory system in yeast independent of Aft1p. Proc Natl Acad Sci USA 98: 14322-14327.
57. 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.
58. Shakoury-Elizeh, M., Tiedeman, J., Rashford, J., Ferea, T., Demeter, J., Garcia, E., etal. (2004) Transcriptional remodeling in response to iron deprivation in Saccharomyces cerevisiae. Mol Biol Cell 15: 1233-1243.
59. Shenton, D., Smirnova, J.B., Selley, J.N., Carroll, K., Hubbard, S.J., Pavitt, G.D., etal. (2006) Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J Biol Chem 281: 29011-29021.
60. Sherman, F. (2002) Getting started with yeast. Methods Enzymol 350: 3-41.
61. Simon, E., Camier, S., and Séraphin, B. (2006) New insights into the control of mRNA decapping. Trends Biochem Sci 31: 241-243.
62. Tamarit, J., Irazusta, V., Moreno-Cermeño, A., and Ros, J. (2006) Colorimetric assay for the quantitation of iron in yeast. Anal Biochem 351: 149-151.
63. 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 oxygen species: oxidative-stress-response genes. Proc Natl Acad Sci USA 101: 6564-6569.
64. Ueta, R., Fujiwara, N., Iwai, K., and Yamaguchi-Iwai, Y. (2007) Mechanism underlying the iron-dependent nuclear export of the iron-responsive transcription factor Aft1p in Saccharomyces cerevisiae. Mol Biol Cell 18: 2980-2990.
65. Wach, A., Brachat, A., Pöhlmann, R., and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 13: 1793-1808.
66. Waters, B.M., and Eide, D.J. (2002) Combinatorial control of yeast FET4 gene expression by iron, zinc, and oxygen. J Biol Chem 277: 33749-33757.
67. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., André, B., etal. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
68. 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.
69. Yun, C.W., Ferea, T., Rashford, J., Ardon, O., Brown, P.O., Botstein, D., etal. (2000a) Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae: evidence for two pathways of iron uptake. J Biol Chem 275: 10709-10715.
70. Yun, C.W., Tiedeman, J.S., Moore, R.E., and Philpott, C.C. (2000b) Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem 275: 16354-16359.
71. Yun, C.W., Bauler, M., Moore, R.E., Klebba, P.E., and Philpott, C.C. (2001) The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cerevisiae. J Biol Chem 276: 10218-10223.