Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals

Molecular Microbiology

Volumn 74, Issue 4, 2009, Pages 844-861

  Nicholls, Susan ^a   Leach, Michelle D ^a   Priest, Claire L ^a   Brown, Alistair J P ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1;

ACIDITY; ARTICLE; CANDIDA ALBICANS; CONTROLLED STUDY; FUNGAL GENOME; FUNGAL VIABILITY; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE LOCUS; GENETIC TRANSCRIPTION; HEAT SHOCK; HEAT SHOCK RESPONSE; HOMEOSTASIS; MOLECULAR EVOLUTION; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULON; REPORTER GENE; THERMAL STIMULATION; TRANSCRIPTION INITIATION;

ANIMALS; CANDIDA ALBICANS; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HOT TEMPERATURE; HUMANS; MICROBIAL VIABILITY; MOLECULAR CHAPERONES; PHOSPHORYLATION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

ANIMALIA; CANDIDA ALBICANS;

EID: 70449568487     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06883.x     Document Type: Article

References (95)

1. Alarco, A.M. Raymond, M. (1999) The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J Bacteriol 181 : 700 708.
2. Alonso-Monge, R., Navarro-Garcia, F., Molero, G., Diez-Orejas, R., Gustin, M., Pla, J., et al. (1999) Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J Bacteriol 181 : 3058 3068.
3. Alonso-Monge, R., Navarro-Garcia, F., Roman, E., Negredo, A.I., Eisman, B., Nombela, C. Pla, J. (2003) The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot Cell 2 : 351 361.
4. Barelle, C.J., Manson, C., MacCallum, D., Odds, F.C., Gow, N.A.R. Brown, A.J.P. (2004) GFP as a quantitative reporter of gene regulation in Candida albicans. Yeast 21: 333 340.
5. Barnett, J.A., Payne, R.W. Yarrow, D. (1983) Yeasts: Characteristics and Identification. Cambridge, UK: Cambridge University Press.
6. Borkovich, K.A., Farrelly, F.W., Finkelstein, D.B., Taulien, J., and Lindquist, S. (1989) Hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol 9: 3919 3930.
7. Bromuro, C., la Valle, R., Sandini, S., Urbani, F., Ausiello, C.M., Morelli, L., et al. (1998) A 70-kilodalton recombinant heat shock protein of Candida albicans is highly immunogenic and enhances systemic murine candidiasis. Infect Immun 66: 2154 2162.
8. Brown, A.J.P., Planta, R.J., Restuhadi, F., Bailey, D.A., Butler, P.R., Cadahia, J.L., et al. (2001) Transcript analysis of 1003 novel yeast genes using high-throughput northern hybridisations. EMBO J 20: 3177 3186.
9. Burnie, J.P., Carter, T.L., Hodgetts, S.J. Matthews, R.C. (2006) Fungal heat-shock proteins in human disease. FEMS Microbiol Rev 30: 53 88.
10. Calderone, R.A. (2002) Candida and Candidiasis. Washington, DC: ASM Press.
11. Causton, H.C., Ren, B., Koh, S.S., Harbison, C.T., Kanin, E., Jennings, E.G., et al. (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12: 323 337.
12. Cheetham, J., Smith, D.A., da Silva Dantas, A., Doris, K.S., Patterson, M.J., Bruce, C.R. Quinn, J. (2007) A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungus Candida albicans. Mol Biol Cell 18: 4603 4614.
13. Chen, D., Toone, W.M., Mata, J., Lyne, R., Burns, G., Kivinen, K., et al. (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14: 214 229.
14. Do Carmo-Sousa, L. (1969) Distribution of yeasts in nature. In The Yeasts, Vol. 1. Rose, A.H. Harrison, J.S. (eds). New York: Academic Press, pp. 79 105.
15. Duina, A.A., Kalton, H.M. Gaber, R.F. (1998) Requirement for Hsp90 and a CyP-40-type cyclophilin in negative regulation of the heat shock response. J Biol Chem 273: 18974 18978.
16. Enjalbert, B. Whiteway, M. (2005) Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell 4: 1203 1210.
17. Enjalbert, B., Nantel, A. Whiteway, M. (2003) Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol Biol Cell 14: 1460 1467.
18. Enjalbert, B., Smith, D.A., Cornell, M.J., Alam, I., Nicholls, S., Brown, A.J.P. Quinn, J. (2006) Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol Biol Cell 17: 1018 1032.
19. Enjalbert, B., Moran, G.P., Vaughan, C., Yeomans, T., MacCallum, D.M., Quinn, J., et al. (2009) Genome-wide gene expression profiling and forward genetic screens show that differential expression of the sodium ion transporter Ena21 contributes to the differential tolerance of Candida albicans and Candida dubliniensis to osmotic stress. Mol Microbiol 72: 216 228.
20. Enloe, B., Diamond, A. Mitchell, A.P. (2000) A single-transformation gene function test in diploid Candida albicans. J Bacteriol 182: 5730 5736.
21. Feder, M.E. Hofmann, G.E. (1999) Heat-shock proteins, molular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61: 243 282.
22. Fonzi, W.A. Irwin, M.Y. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717 728.
23. Fradin, C., De Groot, P., MacCallum, D., Schaller, M., Klis, F., Odds, F.C. Hube, B. (2005) Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 56: 397 415.
24. Gallo, G.J., Prentice, H. Kingston, R.E. (1993) Heat shock factor is required for growth at normal temperatures in the fission yeast Schizosaccharomyces pombe. Mol Cell Biol 13: 749 761.
25. Garbuz, D., Evgenev, M.B., Feder, M.E. Zatsepina, O.G. (2003) Evolution of thermotolerance and the heat-shock response: evidence from inter/intraspecific comparison and interspecific hybridization in the virilis species group of Drosophila. I. Thermal phenotype. J Exp Biol 206: 2399 2408.
26. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., et al. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241 4257.
27. Gehring, W.J. Wehner, R. (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. Proc Natl Acad Sci USA 92: 2994 2998.
28. Gentles, J.C. La Touche, C.J. (1969) Yeasts as human and animal pathogens. In The Yeasts, Vol. 1. Rose, A.H. Harrison, J.S. (eds). New York: Academic Press, pp. 108 182.
29. Giardina, C. Lis, J.T. (1995) Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol Cell Biol 15: 2737 2744.
30. Gillum, A.M., Tsay, E.Y. Kirsch, D.R. (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179 182.
31. Hahn, J.S. Thiele, D.J. (2004) Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase. J Biol Chem 279: 5169 5176.
32. Hahn, J.S., Hu, Z., Thiele, D.J. Iyer, V.R. (2004) Genome-wide analysis of the biology of stress responses through heat shock transcription factor. Mol Cell Biol 24: 5249 5256.
33. Hashikawa, N., Mizukami, Y., Imazu, H. Sakurai, H. (2006) Mutated yeast heat shock transcription factor activates transcription independently of hyperphosphorylation. J Biol Chem 281: 3936 3942.
34. Hauser, N.C., Vingron, M., Scheideler, M., Krems, B., Hellmuth, K., Entian, K.D. Hoheisel, J.D. (1998) Transcriptional profiling on all open reading frames of Saccharomyces cerevisiae. Yeast 14: 1209 1221.
35. Hietakangas, V., Ahlskog, J.K., Jakobsson, A.M., Hellesuo, M., Sahlberg, N.M., Holmberg, C.I., et al. (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of Heat Shock Factor 1. Mol Cell Biol 23: 2953 2968.
36. Hwang, C.S., Rhie, G.E., Oh, J.H., Huh, W.K., Yim, H.S. Kang, S.O. (2002) Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 148: 3705 3713.
37. Jacobsen, M.D., Bougnoux, M.E., d'Enfert, C. Odds, F.C. (2008) Multilocus sequence typing of Candida albicans isolates from animals. Res Microbiol 159: 436 440.
38. Jakobsen, B.K. Pelham, H.R. (1988) Constitutive binding of yeast heat shock factor to DNA in vivo. Mol Cell Biol 8: 5040 5042.
39. Jamieson, D.J., Stephen, D.W. Terriere, E.C. (1996) Analysis of the adaptive oxidative stress response of Candida albicans. FEMS Microbiol Lett 138: 83 88.
40. Kadosh, D. Johnson, A.D. (2001) Rfg1, a protein related to the S. cerevisiae hypoxic regulator Rox1, controls filamentous growth and virulence in C. albicans. Mol Cell Biol 21: 2496 2505.
41. Kaiser, B., Munder, T., Saluz, H.P., Kunkel, W. Eck, R. (1999) Identification of a gene encoding the pyruvate decarboxylase gene regulator CaPdc2p from Candida albicans. Yeast 15: 585 591.
42. Kirk, N. Piper, P.W. (1991) The determinants of heat-shock element-directed lacZ expression in Saccharomyces cerevisiae. Yeast 7: 539 546.
43. Krantz, M., Becit, E. Hohmann, S. (2006) Comparative genomics of the HOG-signalling system in fungi. Curr Genet 49: 137 151.
44. Lindquist, S. (1986) The heat shock response. Annu Rev Biochem 55: 1151 1191.
45. Liu, X.D. Thiele, D.J. (1996) Oxidative stress induced heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription. Genes Dev 10: 592 603.
46. Liu, Y., Liang, S. Tartakoff, A.M. (1996) Heat shock disassembles the nucleolus and inhibits nuclear protein import and poly(A)+ RNA export. EMBO J 15: 6750 6757.
47. Lorenz, M.C., Bender, J.A. Fink, G.R. (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3: 1076 1087.
48. Martchenko, M., Alarco, A.M., Harcus, D. Whiteway, M. (2004) Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 15: 456 467.
49. Martchenko, M., Levitin, A., Hogues, H., Nantel, A. Whiteway, M. (2007) Transcriptional rewiring of fungal galactose-metabolism circuitry. Curr Biol 17: 1007 1013.
50. Matthews, R.C., Burnie, J.P. Tabaqchali, S. (1987) Isolation of immunodominant antigens from the sera of patients with systemic candidiasis and characterisation of the serological response to Candida albicans. J Clin Microbiol 25: 230 237.
51. Matthews, R.C., Burnie, J.P., Howat, D., Rowland, T. Walton, F. (1991) Autoantibody to HSP90 can mediate protection against systemic candidosis. Immunology 74: 20 24.
52. Morano, K., Liu, P. Thiele, D. (1998) Protein chaperones and the heat shock response in Saccharomyces cerevisiae. Curr Opin Microbiol 1: 197 203.
53. Morimoto, R.I. (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12: 3788 3796.
54. Murad, A.M.A., Lee, P.R., Broadbent, I.D., Barelle, C.J. Brown, A.J.P. (2000) CIp10, an efficient and convenient integrating vector for Candida albicans. Yeast 16: 325 327.
55. Nakayama, H., Mio, T., Nagahashi, S., Kokado, M., Arisawa, M. Aoki, Y. (2000) Tetracycline-regulatable system to tightly control gene expression in the pathogenic fungus Candida albicans. Infect Immun 68: 6712 6719.
56. Nantel, A., Dignard, D., Bachewich, C., Harcus, D., Marcil, A., Bouin, A.-P., et al. (2002) Transcript profiling of Candida albicans cells undergoing the yeast-to-hyphal transition. Mol Biol Cell 13: 3452 3465.
57. Nicholls, S., Straffon, M., Enjalbert, B., Nantel, A., Macaskill, S., Whiteway, M. Brown, A.J.P. (2004) Msn2/4-like transcription factors play no obvious roles in the stress responses of the fungal pathogen, Candida albicans. Eukaryot Cell 3: 1111 1123.
58. Nikolaou, E., Agriafioti, I., Stumpf, M., Quinn, J., Stansfield, I. Brown, A.J.P. (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9: 44.
59. Odds, F.C. (1984) Ecology and epidemiology of Candida species. Zbl Bakt Hyg 257: 207 212.
60. Odds, F.C. (1988) Candida and Candidosis, 2nd edn. London: Bailliere Tindall.
61. Panaretou, B. Zhai, C. (2008) The heat shock proteins: their roles as multi-component machines for protein folding. Fungal Biol Rev 22: 110 119.
62. Pirkkala, L., Nykanen, P. Sistonen, L. (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15: 1118 1131.
63. Quinn, J. Brown, A.J.P. (2007) Stress responses in Candida albicans. In Candida: Comparative and Functional Genomics. Hube, B. d'Enfert, C. (eds). Norfolk: Caister Academic Press, pp. 217 261.
64. Ramsdale, M., Selway, L., Stead, D., Walker, J., Yin, Z., Nicholls, S.M., et al. (2008) The novel gene MNL1 regulates weak acid induced stress responses of the fungal pathogen Candida albicans. Mol Biol Cell 19: 4393 4403.
65. + flux. Nature 416: 291 297.
66. Regenberg, B., Grotkjaer, T., Winther, O., Fausbøll, A., Åkesson, M., Bro, C., et al. (2006) Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae. Genome Biol 7: R107.
67. Reuss, O., Vik, A., Kolter, R. Morschhäuser, J. (2004) The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341: 119 127.
68. Roman, E., Nombela, C. Pla, J. (2005) The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol Cell Biol 25: 10611 10627.
69. Ruis, H. Schuller, C. (1995) Stress signaling in yeast. Bioessays 17: 959 965.
70. Rupp, S. (2002) LacZ assays in yeast. Methods Enzymol 350: 112 131.
71. San Jose, C., Monge, R.A., Perez-Diaz, R., Pla, J. Nombela, C. (1996) The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans. J Bacteriol 178: 5850 5852.
72. Sandini, S., Melchionna, R., Bromuro, C. La Valle, R. (2002) Gene expression of 70 kDa heat shock protein of Candida albicans: transcriptional activation and response to heat shock. Med Mycol 40: 471 478.
73. Santoro, N., Johansson, N. Thiele, D.J. (1998) Heat shock element architecture is an important determinant in the temperature and transactivation domain requirements for heat shock transcription factor. Mol Cell Biol 18: 6340 6352.
74. Sewell, A.K., Yokoya, F., Yu, W., Miyagawa, T., Murayama, T. Winge, D.R. (1995) Mutated yeast heat shock transcription factor exhibits elevated basal transcriptional activation and confers metal resistance. J Biol Chem 270: 25079 25086.
75. Sherman, F. (1991) Getting started with yeast. Methods Enzymol 194: 3 21.
76. Smith, D.A., Nicholls, S., Morgan, B.A., Brown, A.J.P. Quinn, J. (2004) A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 15: 4179 4190.
77. Sorger, P.K. Pelham, H.R. (1987) Purification and characterization of a heat-shock element binding protein from yeast. EMBO J 6: 3035 3041.
78. Sorger, P.K. Pelham, H.R.B. (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54: 855 864.
79. Swoboda, R., Miyasaki, S., Greenspan, D. Greenspan, J.S. (1993) Heat-inducible ATP-binding proteins of Candida-albicans are recognized by sera of infected patients. J Gen Microbiol 139: 2995 3003.
80. Swoboda, R.K., Bertram, G., Budge, S., Gooday, G.W., Gow, N.A.R. Brown, A.J.P. (1995) Structure and regulation of the HSP90 gene from the pathogenic fungus Candida albicans. Infect Immun 63: 4506 4514.
81. Tripathi, G., Wiltshire, C., Macaskill, S., Tournu, H., Budge, S. Brown, A.J.P. (2002) CaGcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO J 21: 5448 5456.
82. Tsong, A.E., Tuch, B.B., Li, H. Johnson, A.D. (2006) Evolution of alternative transcriptional circuits with identical logic. Nature 443: 415 420.
83. Tusher, V.G., Tibshirani, R. Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116 5121.
84. Uhl, M.A. Johnson, A.D. (2001) Development of Streptococcus thermophilus lacZ as a reporter gene for Candida albicans. Microbiology 147: 1189 1195.
85. Voellmy, R. (2004) On mechanisms that control heat shock transcription factor activity in metazoan cells. Cell Stress Chaperones 9: 122 133.
86. Vogel, J.L., Parsellt, D.A. Lindquist, S. (1995) Heat-shock proteins Hspl04 and Hsp70 reactivate mRNA splicing after heat inactivation. Curr Biol 5: 306 317.
87. Walker, L.A., Munro, C.A., de Bruijn, I., Lenardon, M.D., McKinnon, A. Gow, N.A.R. (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4: e1000040.
88. Wicksteed, B.L., Collins, I., Dershowitz, A., Stateva, L.I., Green, R.P., Oliver, S.G., et al. (1994) A physical comparison of chromosome III in six strains of Saccharomyces cerevisiae. Yeast 10: 39 57.
89. Wiederrecht, G., Seto, D. Parker, C.S. (1988) Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 54: 841 853.
90. Wilson, R.B., Davis, D., Enloe, B.M. Mitchell, A.P. (2000) A recyclable Candida albicans URA3 cassette for PCR product-directed disruptions. Yeast 16: 65 70.
91. Wimalasena, T.T., Enjalbert, B., Guillemette, T., Plumridge, A., Budge, S., Yin, Z., et al. (2008) Impact of the unfolded protein response upon the genome-wide expression patterns and polarized growth of Candida albicans. Fungal Genet Biol 45: 1235 1247.
92. Wysong, D.R., Christin, L., Sugar, A.M., Robbins, P.W. Diamond, R.D. (1998) Cloning and sequencing of a Candida albicans catalase gene and effects of disruption of this gene. Infect Immun 66: 1953 1961.
93. Yamamoto, A., Mizukami, Y. Sakurai, H. (2005) Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J Biol Chem 280: 11911 11919.
94. Yin, Z., Stead, D., Selway, L., Walker, J., Riba-Garcia, I., Mclnerney, T., et al. (2004) Proteomic response to amino acid starvation in Candida albicans and Saccharomyces cerevisiae. Proteomics 4: 2425 2436.
95. Zenthon, J.F., Ness, F., Cox, B. Tuite, M.F. (2006) The [PSI+] prion of Saccharomyces cerevisiae can be propagated by an Hsp104 orthologue from Candida albicans. Eukaryot Cell 5: 217 225.