The Yap family and its role in stress response

Yeast

Volumn 27, Issue 5, 2010, Pages 245-258

  Rodrigues Pousada, Claudina ^a   Menezes, Regina A ^a   Pimentel, Catarina ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Arsenic stresses; Cadmium; H2O2; Iron; Osmotic; Yap transcription factors

Indexed keywords

ARSENIC; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR CTH1; TRANSCRIPTION FACTOR CTH2; TRANSCRIPTION FACTOR GCN4; TRANSCRIPTION FACTOR TPX1; TRANSCRIPTION FACTOR YAP; TRANSCRIPTION FACTOR YAP1; TRANSCRIPTION FACTOR YAP2; TRANSCRIPTION FACTOR YAP3; TRANSCRIPTION FACTOR YAP4; TRANSCRIPTION FACTOR YAP5; TRANSCRIPTION FACTOR YAP6; TRANSCRIPTION FACTOR YAP7; TRANSCRIPTION FACTOR YAP8; UNCLASSIFIED DRUG;

BINDING SITE; CADMIUM STRESS; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELLULAR DISTRIBUTION; DETOXIFICATION; DNA BINDING; EUKARYOTE; GENE REGULATORY NETWORK; GENETIC CONSERVATION; IRON METABOLISM; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; STRESS; TRANSCRIPTION REGULATION;

GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 77952283586     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.1752     Document Type: Review

References (83)

1. Hahn JS, Hu Z, Thiele DJ, Iyer VR. 2004. Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24: 5249-5256.
2. Gasch AP, Spellman PT, Kao CM, et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
3. Moye-Rowley WS, Harshman KD, Parker CS. 1989. Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. Genes Dev 3: 283-292.
4. Bossier P, Fernandes L, Rocha D, Rodrigues-Pousada C. 1993. Overexpression of YAP2, coding for a new yAP protein, and YAP1 in Saccharomyces cerevisiae alleviates growth inhibition caused by 1, 10-phenanthroline. J Biol Chem 268: 23640-23645.
5. Rodrigues-Pousada CA, Nevitt T, Menezes R, et al. 2004. Yeast activator proteins and stress response: an overview. FEBS Lett. 567: 80-85.
6. Kim J, Tzamarias D, Ellenberger T, et al. 1993. Adaptability at the protein-DNA interface is an important aspect of sequence recognition by bZIP proteins. Proc Natl Acad Sci USA 90: 4513-4517.
7. Oliphant AR, Brandl CJ, Struhl K. 1989. Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol Cell Biol 9: 2944-2949.
8. Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. 1992. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α-helices: crystal structure of the protein-DNA complex. Cell 71: 1223-1237.
9. Glover JN, Harrison SC. 1995. Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun. bound to DNA. Nature 373: 257-261.
10. Konig P, Richmond TJ. 1993. The X-ray structure of the GCN4-bZIP bound to ATF/CREB site DNA shows the complex depends on DNA flexibility. J Mol Biol 233: 139-154.
11. Kuras L, Cherest H, Surdin-Kerjan Y, Thomas D. 1996. A heteromeric complex containing the centromere binding factor 1 and two basic leucine zipper factors, Met4 and Met28, mediates the transcription activation of yeast sulfur metabolism. EMBO J 15: 2519-2529.
12. Nehlin JO, Carlberg M, Ronne H. 1992. Yeast SKO1 gene encodes a bZIP protein that binds to the CRE motif and acts as a repressor of transcription. Nucleic Acids Res 20: 5271-5278.
13. Nojima H, Kimura I, Kimura M. 1994. The evidence of accelerative interaction between cAMP-dependent protein kinase and external calcium for the desensitization of nicotinic acetylcholine receptor channel in mouse skeletal muscle cells. Neurosci Lett 167: 113-116.
14. Wysocki R, Clemens S, Augustyniak D, et al. 2003. Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p. Biochem Biophys Res Commun 304: 293-300.
15. Ilina Y, Sloma E, Maciaszczyk-Dziubinska E, et al. 2008. Characterization of the DNA-binding motif of the arsenicresponsive transcription factor Yap8p. Biochem J 415: 467-475.
16. Vilela C, Ramirez CV, Linz B, et al. 1999. Post-termination ribosome interactions with the 5' UTR modulate yeast mRNA stability. EMBO J 18: 3139-3152.
17. Toda T, Shimanuki M, Yanagida M. 1991. Fission yeast genes that confer resistance to staurosporine encode an AP-1-like transcription factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev 5: 60-73.
18. Billard P, Dumond H, Bolotin-Fukuhara M. 1997. Characterization of an AP-1-like transcription factor that mediates an oxidative stress response in Kluyveromyces lactis. Mol Gen Genet 257: 62-70.
19. Bussereau F, Casaregola S, Lafay JF, Bolotin-Fukuhara M. 2006. The Kluyveromyces lactis repertoire of transcriptional regulators. FEMS Yeast Res 6: 325-335.
20. 2 sensors as archetypical redox signaling modules. Trends Biochem Sci 29: 351-357.
21. Wu AL, Moye-Rowley WS. 1994. GSH1, which encodes γ-glutamylcysteine synthetase, is a target gene for yAP-1 transcriptional regulation. Mol Cell Biol 14: 5832-5839.
22. Kuge S, Jones N, Nomoto A. 1997. Regulation of yAP-1 nuclear localization in response to oxidative stress. EMBO J 16: 1710-1720.
23. Lee J, Godon C, Lagniel G, et al. 1999. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J Biol Chem 274: 16040-16046.
24. Yan C, Lee LH, Davis LI. 1998. Crm1p mediates regulated nuclear export of a yeast AP-1-like transcription factor. EMBO J. 17: 7416-7429.
25. 2 sensing through oxidation of the Yap1 transcription factor. EMBO J 19: 5157-5166.
26. 2 receptor and redox-transducer in gene activation. Cell 111: 471-481.
27. Wood MJ, Andrade EC, Storz G. 2003. The redox domain of the Yap1p transcription factor contains two disulfide bonds. Biochemistry 42: 11982-11991.
28. 2 stress signal. Mol Cell 27: 675-688.
29. Veal EA, Ross SJ, Malakasi P, et al. 2003. Ybp1 is required for the hydrogen peroxide-induced oxidation of the Yap1 transcription factor. J Biol Chem 278: 30896-30904.
30. 2 levels in fission yeast Schizosaccharomyces pombe. Mol Biol Cell 13: 805-816.
31. Toone WM, Kuge S, Samuels M, et al. 1998. Regulation of the fission yeast transcription factor Pap1 by oxidative stress: requirement for the nuclear export factor Crm1 (Exportin) and the stress-activated MAP kinase Sty1/Spc1. Genes Dev 12: 1453-1463.
32. 2-sensing by the antioxidant Pap1 pathway. Proc Natl Acad Sci USA 102: 8875-8880.
33. Kuge S, Arita M, Murayama A, et al. 2001. Regulation of the yeast Yap1p nuclear export signal is mediated by redox signalinduced reversible disulfide bond formation. Mol Cell Biol 21: 6139-6150.
34. 2 and thiol-reactive chemicals signaling. Free Radic Biol Med 35: 889-900.
35. Wu A, Wemmie JA, Edgington NP, et al. 1993. Yeast bZip proteins mediate pleiotropic drug and metal resistance. J Biol Chem 268: 18850-18858.
36. Azevedo D, Nascimento L, Labarre J, et al. 2007. The S. cerevisiae Yap1 and Yap2 transcription factors share a common cadmium-sensing domain. FEBS Lett 581: 187-195.
37. McHale MW, Kroening KD, Bernlohr DA. 1996. Identification of a class of Saccharomyces cerevisiae mutants defective in fatty acid repression of gene transcription and analysis of the frm2 gene. Yeast 12: 319-331.
38. Ball CA, Dolinski K, Dwight SS, et al. 2000. Integrating functional genomic information into the Saccharomyces genome database. Nucleic Acids Res 28: 77-80.
39. Reiser V, Ruis H, Ammerer G. 1999. Kinase activitydependent nuclear export opposes stress-induced nuclear accumulation and retention of Hog1 mitogen-activated protein kinase in the budding yeast Saccharomyces cerevisiae. Mol Biol Cell 10: 1147-1161.
40. Cohen BA, Pilpel Y, Mitra RD, Church GM. 2002. Discrimination between paralogs using microarray analysis: application to the Yap1p and Yap2p transcriptional networks. Mol Biol Cell 13: 1608-1614.
41. Mendizabal I, Rios G, Mulet JM, et al. 1998. Yeast putative transcription factors involved in salt tolerance. FEBS Lett 425: 323-328.
42. Delling U, Raymond M, Schurr E. 1998. Identification of Saccharomyces cerevisiae genes conferring resistance to quinoline ring-containing antimalarial drugs. Antimicrob Agents Chemother 42: 1034-1041.
43. Furuchi T, Ishikawa H, Miura N, et al. 2001. Two nuclear proteins, Cin5 and Ydr259c, confer resistance to cisplatin in Saccharomyces cerevisiae. Mol Pharmacol 59: 470-474.
44. Sollner S, Schober M, Wagner A, et al. 2009. Quinone reductase acts as a redox switch of the 20S yeast proteasome. EMBO Rep 10: 65-70.
45. Pereira J, Pimentel C, Amaral C, et al. 2009. Yap4 PKA-and GSK3-dependent phosphorylation affects its stability but not its nuclear localization. Yeast 26: 641-653.
46. Nevitt T, Pereira J, Rodrigues-Pousada C. 2004. YAP4 gene expression is induced in response to several forms of stress in Saccharomyces cerevisiae. Yeast 21: 1365-1374.
47. Posas F, Chambers JR, Heyman JA, et al. 2000. The transcriptional response of yeast to saline stress. J Biol Chem 275: 17249-17255.
48. Rep M, Krantz M, Thevelein JM, Hohmann S. 2000. The transcriptional response of Saccharomyces cerevisiae to osmotic shock. Hot1p and Msn2p/Msn4p are required for the induction of subsets of high osmolarity glycerol pathwaydependent genes. J Biol Chem 275: 8290-8300.
49. Nevitt T, Pereira J, Azevedo D, et al. 2004. Expression of YAP 4 in Saccharomyces cerevisiae under osmotic stress. Biochem J 379: 367-374.
50. Ni L, Bruce C, Hart C, et al. 2009. Dynamic and complex transcription factor binding during an inducible response in yeast. Genes Dev 23: 1351-1363.
51. Dunn LL, Rahmanto YS, Richardson DR. 2007. Iron uptake and metabolism in the new millennium. Trends Cell Biol 17: 93-100.
52. Hentze MW, Muckenthaler MU, Andrews NC. 2004. Balancing acts: molecular control of mammalian iron metabolism. Cell 117: 285-297.
53. Rouault TA. 2006. The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat Chem Biol 2: 406-414.
54. Yun CW, Bauler M, Moore RE, et al. 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.
55. Neilands JB. 1995. Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270: 26723-26726.
56. Askwith CC, de Silva D, Kaplan J. 1996. Molecular biology of iron acquisition in Saccharomyces cerevisiae. Mol Microbiol 20: 27-34.
57. Heymann P, Ernst JF, Winkelmann G. 1999. Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1) in Saccharomyces cerevisiae as a member of the major facilitator superfamily. Biometals 12: 301-306.
58. Yun CW, Tiedeman JS, Moore RE, Philpott CC. 2000. Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem 275: 16354-16359.
59. Blaiseau PL, Lesuisse E, Camadro JM. 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.
60. Rutherford JC, Bird AJ. 2004. Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 3: 1-13.
61. Yamaguchi-Iwai Y, Dancis A, Klausner RD. 1995. AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J 14: 1231-1239.
62. Lesuisse E, Raguzzi F, Crichton RR. 1987. Iron uptake by the yeast Saccharomyces cerevisiae: involvement of a reduction step. J Gen Microbiol 133: 3229-3236.
63. Li L, Bagley D, Ward DM, Kaplan J. 2008. Yap5 is an ironresponsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol Cell Biol 28: 1326-1337.
64. Rosen BP. 2002. Transport and detoxification systems for transition metals, heavy metals and metalloids in eukaryotic and prokaryotic microbes. Comp Biochem Physiol A Mol Integr Physiol 133: 689-693.
65. Hu J, Liu YF, Wu CF, et al. 2009. Long-term efficacy and safety of all-trans retinoic acid/arsenic trioxide-based therapy in newly diagnosed acute promyelocytic leukemia. Proc Natl Acad Sci USA 106: 3342-3347.
66. Borst P, Ouellette M. 1995. New mechanisms of drug resistance in parasitic protozoa. Annu Rev Microbiol 49: 427-460.
67. Menezes RA, Amaral C, Delaunay A, et al. 2004. Yap8p activation in Saccharomyces cerevisiae under arsenic conditions. FEBS Lett. 566: 141-146.
68. Wysocki R, Fortier PK, Maciaszczyk E, et al. 2004. Transcriptional activation of metalloid tolerance genes in Saccharomyces cerevisiae requires the AP-1-like proteins Yap1p and Yap8p. Mol Biol Cell 15: 2049-2060.
69. Menezes RA, Amaral C, Batista-Nascimento L, et al. 2008. Contribution of Yap1 towards Saccharomyces cerevisiae adaptation to arsenic-mediated oxidative stress. Biochem J 414: 301-311.
70. Haugen AC, Kelley R, Collins JB, et al. 2004. Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol 5: R95.
71. Di Y, Tamas MJ. 2007. Regulation of the arsenic-responsive transcription factor Yap8p involves the ubiquitin-proteasome pathway. J Cell Sci 120: 256-264.
72. Thorsen M, Lagniel G, Kristiansson E, et al. 2007. Quantitative transcriptome, proteome, and sulfur metabolite profiling of the Saccharomyces cerevisiae response to arsenite. Physiol Genom 30: 35-43.
73. Sotelo J, Rodriguez-Gabriel MA. 2006. Mitogen-activated protein kinase Hog1 is essential for the response to arsenite in Saccharomyces cerevisiae. Eukaryot Cell 5: 1826-1830.
74. Thorsen M, Di Y, Tangemo C, et al. 2006. The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol Biol Cell 17: 4400-4410.
75. Yang X, Talibi D, Weber S, et al. 2001. Functional isolation of the Candida albicans FCR3 gene encoding a bZip transcription factor homologous to Saccharomyces cerevisiae Yap3p. Yeast 18: 1217-1225.
76. Huh WK, Falvo JV, Gerke LC, et al. 2003. Global analysis of protein localization in budding yeast. Nature 425: 686-691.
77. Tan K, Feizi H, Luo C, et al. 2008. A systems approach to delineate functions of paralogous transcription factors: role of the Yap family in the DNA damage response. Proc Natl Acad Sci USA 105: 2934-2939.
78. Lee TI, Rinaldi NJ, Robert F, et al. 2002. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298: 799-804.
79. Amoros M, Estruch F. 2001. Hsf1p and Msn2/4p cooperate in the expression of Saccharomyces cerevisiae genes HSP26 and HSP104 in a gene-and stress type-dependent manner. Mol Microbiol 39: 1523-1532.
80. Grably MR, Stanhill A, Tell O, Engelberg D. 2002. HSF and Msn2/4p can exclusively or cooperatively activate the yeast HSP104 gene. Mol Microbiol 44: 21-35.
81. Hahn JS, Neef DW, Thiele DJ. 2006. A stress regulatory network for co-ordinated activation of proteasome expression mediated by yeast heat shock transcription factor. Mol Microbiol 60: 240-251.
82. Workman CT, Mak HC, McCuine S, et al. 2006. A systems approach to mapping DNA damage response pathways. Science 312: 1054-1059.
83. Banerjee N, Zhang MQ. 2003. Identifying cooperativity among transcription factors controlling the cell cycle in yeast. Nucleic Acids Res 31: 7024-7031.