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

Nicholls, Susan; Leach, Michelle D.; Priest, Claire L.; Brown, Alistair J. P.

doi:10.1111/j.1365-2958.2009.06883.x

Cited by 105Heat shock proteins researchFungal and yeast genetics researchBacterial Genetics and Biotechnology

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

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Nicholls, Susan, Leach, Michelle D., Priest, Claire L., Brown, Alistair J. P.·2009·Molecular Microbiology

DOI 10.1111/j.1365-2958.2009.06883.xPMC PMC3675641

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Abstract

Summary: All organisms have evolved mechanisms that protect them against environmental stress. The major fungal pathogen of humans, Candida albicans , has evolved robust stress responses that protect it against human immune defences and promote its pathogenicity. However, C. albicans is unlikely to be exposed to heat shock as it is obligatorily associated with warm‐blooded animals. Therefore, we examined the role of the heat shock transcription factor (Hsf1) in this pathogen. We show that C. albicans expresses an evolutionarily conserved Hsf1 (orf19.4775) that is phosphorylated in response to heat shock, induces transcription via the heat shock element (HSE), contributes to the global transcriptional response to heat shock, and is essential for viability. Why has Hsf1 been conserved in this obligate animal saprophyte? We reasoned that Hsf1 might contribute to medically relevant stress responses. However, this is not the case, as an Hsf1‐specific HSE‐lacZ reporter is not activated by oxidative, osmotic, weak acid or pH stress. Rather, Hsf1 is required for the expression of essential chaperones in the absence of heat shock (e.g. Hsp104, Hsp90, Hsp70). Furthermore, Hsf1 regulates the expression of HSE‐containing genes in response to growth temperature in C. albicans . Therefore, the main role of Hsf1 in this pathogen might be the homeostatic modulation of chaperone levels in response to growth temperature, rather than the activation of acute responses to sudden thermal transitions.

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Hsp90 is naturally abundant in fungal cells and is induced to even greater levels by heat shock and other proteotoxic stresses.
“Hsp90 is naturally abundant in fungal cells and is induced to even greater levels by heat shock and other proteotoxic stresses10,15,32-35.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [10]
Hsp90 levels increase following environmental challenges.
“Furthermore, although Hsp90 levels increase following environmental challenges, Hsp90 activity is tightly controlled via post-translational regulation and an autoregulatory loop involving the heat shock transcription factor, Hsf1.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [10]
Hsf1 is essential for viability in yeasts, and is required for the basal expression of HSP genes.
“Hsf1 is essential for viability in yeasts10,38,39, and is required for the basal expression of HSP genes10,39,40.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [10]
Hsf1 is activated by hyperphosphorylation in response to specific environmental cues, which in some fungi include glucose starvation, superoxide, oxygen tension and changes in membrane lipid composition as well as heat shock.
“Hsf1 is activated by hyperphosphorylation in response to specific environmental cues, which in some fungi include glucose starvation, superoxide, oxygen tension and changes in membrane lipid composition as well as heat shock10,39,45,46.”
From Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs (2012) · cites this paper as [10]

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In silico prediction of protein-protein interactions in human macrophages
Souiai, O., Guerfali, F. Z., Miled, S. B., Brun, C., & Benkahla, A. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-157 · Cited by 10,785 · see citing works
Significance analysis of microarrays applied to the ionizing radiation response
Tusher, V. G., Tibshirani, R., & Chu, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091062498 · Cited by 10,568 · see citing works
Genomic Expression Programs in the Response of Yeast Cells to Environmental Changes
Gasch, A. P., Spellman, P. T., Kao, C. M., Carmel-Harel, O., Eisen, M. B., Storz, G., Botstein, D., & Brown, P. O. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.12.4241 · Cited by 4,815 · see citing works
THE HEAT-SHOCK RESPONSE
Lindquist, S. L. (1986) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.55.070186.005443 · Cited by 4,611 · see citing works
HEAT-SHOCK PROTEINS, MOLECULAR CHAPERONES, AND THE STRESS RESPONSE: Evolutionary and Ecological Physiology
Feder, M. E., & Hofmann, G. E. (1999) · Annual Review of Physiology · doi:10.1146/annurev.physiol.61.1.243 · Cited by 4,299 · see citing works
Getting started with yeast
Sherman, F. (1991) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(91)94004-v · Cited by 4,078 · see citing works
Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulatorsPreprint
Morimoto, R. I. (1998) · Genes & Development · doi:10.1101/gad.12.24.3788 · Cited by 1,898 · see citing works
Yeasts : characteristics and identification
Barnett, J. A., Payne, R. W., Yarrow, D., & Barnett, L. (2000) · Cited by 1,870 · see citing works
Isogenic strain construction and gene mapping in Candida albicans.
Fonzi, W. A., & Irwin, M. Y. (1993) · Genetics · doi:10.1093/genetics/134.3.717 · Cited by 1,695 · see citing works
Remodeling of Yeast Genome Expression in Response to Environmental Changes
Causton, H. C., Ren, B., Koh, S. S., Harbison, C. T., Kanin, E. I., Jennings, E. G., Lee, T. I., True, H. L., Lander, E. S., & Young, R. A. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.2.323 · Cited by 1,364 · see citing works
Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations
Gillum, A. M., Tsay, E. Y. H., & Kirsch, D. R. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00328721 · Cited by 1,253 · see citing works
Killing activity of neutrophils is mediated through activation of proteases by K+ flux
Reeves, E. P., Lu, H., Jacobs, H. L., Messina, C. G. M., Bolsover, S., Gabella, G., Potma, E. O., Warley, A., Roes, J., & Segal, A. W. (2002) · Nature · doi:10.1038/416291a · Cited by 1,153 · see citing works
Roles of the heat shock transcription factors in regulation of the heat shock response and beyond
Pirkkala, L., NYKÄNEN, P., & Sistonen, L. (2001) · The FASEB Journal · doi:10.1096/fj00-0294rev · Cited by 996 · see citing works
Candida and candidiasis.
Calderone, R. (2012) · ASM Press eBooks · Cited by 912 · see citing works
Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation
Sorger, P. K., & Pelham, H. R. B. (1988) · Cell · doi:10.1016/s0092-8674(88)91219-6 · Cited by 832 · see citing works
Global transcriptional responses of fission yeast to environmental stress
Chen, D., Toone, W. M., Mata, J., Lyne, R., Burns, G., Kivinen, K., Brazma, A., Jones, N., & Bähler, J. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-08-0499 · Cited by 796 · see citing works
The SAT1 flipper, an optimized tool for gene disruption in Candida albicans
Reuß, O., Vik, Å., Kolter, R., & Morschhäuser, J. (2004) · Gene · doi:10.1016/j.gene.2004.06.021 · Cited by 744 · see citing works
Transcriptional Response of Candida albicans upon Internalization by Macrophages
Lorenz, M. C., Bender, J. A., & Fink, G. R. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.5.1076-1087.2004 · Cited by 712 · see citing works
Yeasts: Characteristics and identification
Spencer, J. F. T. (1984) · Food Microbiology · doi:10.1016/0740-0020(84)90068-6 · Cited by 680 · see citing works
Candida and Candidiasis
Brandt, M. E. (2002) · Emerging infectious diseases · doi:10.3201/eid0808.020059 · Cited by 646 · see citing works
hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures.
Borkovich, K. A., Farrelly, F. W., Finkelstein, D. B., Taulien, J., & Lindquist, S. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.9.3919 · Cited by 641 · see citing works
Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood
Fradin, C., De Groot, P., MacCallum, D., Schaller, M., Klis, F., Odds, F. C., & Hube, B. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04557.x · Cited by 455 · see citing works
Stimulation of Chitin Synthesis Rescues Candida albicans from Echinocandins
Walker, L. A., Munro, C. A., de Bruijn, I., Lenardon, M. D., McKinnon, A., & Gow, N. A. R. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000040 · Cited by 445 · see citing works
Genome-Wide Analysis of the Biology of Stress Responses through Heat Shock Transcription Factor
Hahn, J., Hu, Z., Thiele, D. J., & Iyer, V. R. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.12.5249-5256.2004 · Cited by 430 · see citing works
Isolation of the gene encoding the S. cerevisiae heat shock transcription factor
Wiederrecht, G., Seto, D., & Parker, C. S. (1988) · Cell · doi:10.1016/s0092-8674(88)91197-x · Cited by 427 · see citing works
Stress signaling in yeast
Ruis, H., & Schüller, C. (1995) · BioEssays · doi:10.1002/bies.950171109 · Cited by 406 · see citing works
Candida and Candidosis
Rippon, J. W. (1989) · JAMA · doi:10.1001/jama.1989.03430190139055 · Cited by 398 · see citing works
Role of the Hog1 Stress-activated Protein Kinase in the Global Transcriptional Response to Stress in the Fungal PathogenCandida albicans
Enjalbert, B., Smith, D. A., Cornell, M. J., Alam, I., Nicholls, S., Brown, A. J. P., & Quinn, J. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0501 · Cited by 381 · see citing works
Self-citation
Transcription Profiling of Candida albicans Cells Undergoing the Yeast-to-Hyphal Transition
Nantel, A., Dignard, D., Bachewich, C., Harcus, D., Marcil, A., Bouin, A.-P., Sensen, C. W., Hogues, H., van het Hoog, M., Gordon, P., et al. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-05-0272 · Cited by 378 · see citing works
Role of the Mitogen-Activated Protein Kinase Hog1p in Morphogenesis and Virulence of Candida albicans
Alonso-Monge, R., Navarro-García, F., Molero, G., Diez-Orejas, R., Gustin, M., Pla, J., Sánchez, M., & Nombela, C. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.10.3058-3068.1999 · Cited by 344 · see citing works
Purification and characterization of a heat‐shock element binding protein from yeast.
Sorger, P. K., & Pelham, H. R. B. (1987) · The EMBO Journal · doi:10.1002/j.1460-2075.1987.tb02609.x · Cited by 340 · see citing works
Phosphorylation of Serine 303 Is a Prerequisite for the Stress-Inducible SUMO Modification of Heat Shock Factor 1
Hietakangas, V., Ahlskog, J. K., Jakobsson, A. M., Hellesuo, M., Sahlberg, N., Holmberg, C. I., Mikhailov, A., Palvimo, J. J., Pirkkala, L., & Sistonen, L. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.8.2953-2968.2003 · Cited by 309 · see citing works
The Hog1 Mitogen-Activated Protein Kinase Is Essential in the Oxidative Stress Response and Chlamydospore Formation inCandidaalbicans
Alonso-Monge, R., Navarro-García, F., Román, E., Negredo, A. I., Eisman, B., Nombela, C., & Pla, J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.2.351-361.2003 · Cited by 308 · see citing works
CIp10, an efficient and convenient integrating vector for Candida albicans
Murad, A. M. A., Lee, P. R., Broadbent, I. D., Barelle, C. J., & Brown, A. J. P. (2000) · Yeast · doi:10.1002/1097-0061(20000315)16:4 · Cited by 303 · see citing works
Self-citation
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
Hwang, C., Rhie, G., Oh, J., Huh, W., Yim, H., & Kang, S.-O. (2002) · Microbiology · doi:10.1099/00221287-148-11-3705 · Cited by 293 · see citing works
Superoxide Dismutases in Candida albicans : Transcriptional Regulation and Functional Characterization of the Hyphal-induced SOD5 Gene
Martchenko, M., Alarco, A.-M., Harcus, D., & Whiteway, M. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-03-0179 · Cited by 290 · see citing works
On mechanisms that control heat shock transcription factor activity in metazoan cells
Voellmy, R. W. (2004) · Cell Stress and Chaperones · doi:10.1379/csc-14r.1 · Cited by 282 · see citing works
Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert.
Gehring, W. J., & Wehner, R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2994 · Cited by 281 · see citing works
Stress-induced Gene Expression inCandida albicans: Absence of a General Stress Response
Enjalbert, B., Nantel, A., & Whiteway, M. S. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-08-0546 · Cited by 277 · see citing works
A Conserved Stress-activated Protein Kinase Regulates a Core Stress Response in the Human Pathogen Candida albicans
Smith, D. A., Nicholls, S., Morgan, B. A., Brown, A. J. P., & Quinn, J. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-03-0181 · Cited by 263 · see citing works
Self-citation
Evolution of alternative transcriptional circuits with identical logic
Tsong, A. E., Tuch, B. B., Li, H., & Johnson, A. D. (2006) · Nature · doi:10.1038/nature05099 · Cited by 255 · see citing works
hsp82 Is an Essential Protein That Is Required in Higher Concentrations for Growth of Cells at Higher Temperatures
Borkovich, K. A., Farrelly, F. W., FINKELSTEIN, D. B., et al. (1989) · Molecular and Cellular Biology · doi:10.1128/mcb.9.9.3919-3930.1989 · Cited by 255 · see citing works
The bZip Transcription Factor Cap1p Is Involved in Multidrug Resistance and Oxidative Stress Response in Candida albicans
Alarco, A., & Raymond, M. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.3.700-708.1999 · Cited by 244 · see citing works
Growth-rate regulated genes have profound impact on interpretation of transcriptome profiling in Saccharomyces cerevisiae
Regenberg, B., Grotkjær, T., Winther, O., Fausbøll, A., Åkesson, M., Bro, C., Hansen, L. K., Brunak, S., & Nielsen, J. (2006) · Genome biology · doi:10.1186/gb-2006-7-11-r107 · Cited by 238 · see citing works
A recyclableCandida albicans URA3 cassette for PCR product-directed gene disruptions
Wilson, R. B., Davis, D. A., Enloe, B. M., & Mitchell, A. P. (2000) · Yeast · doi:10.1002/(sici)1097-0061(20000115)16:1 · Cited by 228 · see citing works
Constitutive binding of yeast heat shock factor to DNA in vivo.
Jakobsen, B. K., & Pelham, H. R. B. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.11.5040 · Cited by 219 · see citing works
Phylogenetic diversity of stress signalling pathways in fungi
Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I., & Brown, A. J. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-44 · Cited by 206 · see citing works
Self-citation
Gcn4 co‐ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans
Tripathi, G., Wiltshire, C. J., Macaskill, S., Tournu, H., Budge, S., & Brown, A. J. P. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf507 · Cited by 204 · see citing works
Self-citation
A Single-Transformation Gene Function Test in Diploid Candida albicans
Enloe, B. M., Diamond, A. E., & Mitchell, A. P. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.20.5730-5736.2000 · Cited by 204 · see citing works
Cloning and Sequencing of a Candida albicans Catalase Gene and Effects of Disruption of This Gene
Wysong, D. R., Christin, L., Sugar, A. M., Robbins, P. W., & Diamond, R. D. (1998) · Infection and Immunity · doi:10.1128/iai.66.5.1953-1961.1998 · Cited by 201 · see citing works
The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans
José, C. S., Monge, R. A., Pérez‐Díaz, R. M., Plá, J., & Nombela, C. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.19.5850-5852.1996 · Cited by 180 · see citing works
Identification of a Novel Class of Target Genes and a Novel Type of Binding Sequence of Heat Shock Transcription Factor in Saccharomyces cerevisiae
Yamamoto, A., Mizukami, Y., & Sakurai, H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m411256200 · Cited by 177 · see citing works
Isolation of immunodominant antigens from sera of patients with systemic candidiasis and characterization of serological response to Candida albicans
Matthews, R., Burnie, J., & Tabaqchali, S. (1987) · Journal of Clinical Microbiology · doi:10.1128/jcm.25.2.230-237.1987 · Cited by 176 · see citing works
The Sho1 Adaptor Protein Links Oxidative Stress to Morphogenesis and Cell Wall Biosynthesis in the Fungal Pathogen Candida albicans
Román, E., Nombela, C., & Plá, J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.23.10611-10627.2005 · Cited by 173 · see citing works
Transcriptional Rewiring of Fungal Galactose-Metabolism Circuitry
Martchenko, M., Levitin, A., Hogues, H., Nantel, A., & Whiteway, M. S. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.017 · Cited by 172 · see citing works
Activation of the Saccharomyces cerevisiae Heat Shock Transcription Factor Under Glucose Starvation Conditions by Snf1 Protein Kinase
Hahn, J., & Thiele, D. J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311005200 · Cited by 167 · see citing works
Rfg1, a Protein Related to the Saccharomyces cerevisiae Hypoxic Regulator Rox1, Controls Filamentous Growth and Virulence in Candida albicans
Kadosh, D., & Johnson, A. D. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.7.2496-2505.2001 · Cited by 166 · see citing works
Fungal heat-shock proteins in human disease
Burnie, J., Carter, T. L., Hodgetts, S. J., & Matthews, R. (2005) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2005.00001.x · Cited by 158 · see citing works
Tetracycline-Regulatable System To Tightly Control Gene Expression in the Pathogenic Fungus Candida albicans
Nakayama, H., Mio, T., Nagahashi, S., Kokado, M., Arisawa, M., & Aoki, Y. (2000) · Infection and Immunity · doi:10.1128/iai.68.12.6712-6719.2000 · Cited by 157 · see citing works
Oxidative stress induced heat shock factor phosphorylation and HSF-dependent activation of yeast metallothionein gene transcription.Preprint
Liu, X., & Thiele, D. J. (1996) · Genes & Development · doi:10.1101/gad.10.5.592 · Cited by 154 · see citing works
Autoantibody to heat-shock protein 90 can mediate protection against systemic candidosis.
Matthews, R., Burnie, J., Howat, D. W., Rowland, T., & Walton, F. (1991) · PubMed Central · Cited by 148 · see citing works
Release from Quorum-Sensing Molecules Triggers Hyphal Formation during Candida albicans Resumption of Growth
Enjalbert, B., & Whiteway, M. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.7.1203-1210.2005 · Cited by 145 · see citing works
Requirement for Hsp90 and a CyP-40-type Cyclophilin in Negative Regulation of the Heat Shock Response
Duina, A. A., Kalton, H. M., & Gaber, R. F. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.30.18974 · Cited by 143 · see citing works
Msn2- and Msn4-Like Transcription Factors Play No Obvious Roles in the Stress Responses of the Fungal Pathogen Candida albicans
Nicholls, S., Straffon, M. J., Enjalbert, B., Nantel, A., Macaskill, S., Whiteway, M. S., & Brown, A. J. P. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.5.1111-1123.2004 · Cited by 140 · see citing works
Self-citation
Transcriptional profiling on all open reading frames ofSaccharomyces cerevisiae
Hauser, N. C., Vingron, M., Scheideler, M., Krems, B., Hellmuth, K., Entian, K.-D., & Hoheisel, J. D. (1998) · Yeast · doi:10.1002/(sici)1097-0061(19980930)14:13 · Cited by 131 · see citing works
Analysis of the adaptive oxidative stress response ofCandida albicans
Jamieson, D. J., Stephen, D. W. S., & ̈re, E. C. T. (1996) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1996.tb08139.x · Cited by 125 · see citing works
GFP as a quantitative reporter of gene regulation in Candida albicans
Barelle, C. J., Manson, C. L., MacCallum, D. M., Odds, F. C., Gow, N. A. R., & Brown, A. J. P. (2004) · Yeast · doi:10.1002/yea.1099 · Cited by 122 · see citing works
Self-citation
A Single MAPKKK Regulates the Hog1 MAPK Pathway in the Pathogenic Fungus Candida albicans
Cheetham, J., Smith, D. A., Dantas, A. D. S., Doris, K. S., Patterson, M. J., Bruce, C. R., & Quinn, J. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-06-0581 · Cited by 120 · see citing works
Impact of the unfolded protein response upon genome-wide expression patterns, and the role of Hac1 in the polarized growth, of Candida albicans
Wimalasena, T. T., Enjalbert, B., Guillemette, T., Plumridge, A., Budge, S., Yin, Z., Brown, A. J. P., & Archer, D. B. (2008) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2008.06.001 · Cited by 118 · see citing works
Self-citation
Heat Shock Element Architecture Is an Important Determinant in the Temperature and Transactivation Domain Requirements for Heat Shock Transcription Factor
Santoro, N., Johansson, N., & Thiele, D. J. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.11.6340 · Cited by 118 · see citing works
Heat-shock proteins Hsp104 and Hsp70 reactivate mRNA splicing after heat inactivation
Vogel, J. L., Parsell, D. A., & Lindquist, S. L. (1995) · Current Biology · doi:10.1016/s0960-9822(95)00061-3 · Cited by 113 · see citing works
Dynamic Protein-DNA Architecture of a Yeast Heat Shock Promoter
Giardina, C. A., & Lis, J. T. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.5.2737 · Cited by 110 · see citing works
Candida: Comparative and Functional Genomics
D'Enfert, C., & Hube, B. (2007) · Estudis Romànics (Institut d'Estudis Catalans) · Cited by 102 · see citing works
Heat Shock Factor Is Required for Growth at Normal Temperatures in the Fission Yeast Schizosaccharomyces pombe
Gallo, G. J., Prentice, H. L., & Kingston, R. E. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.2.749 · Cited by 101 · see citing works
Development of Streptococcus thermophilus lacZ as a reporter gene for Candida albicans
Uhl, M., & Johnson, A. D. (2001) · Microbiology · doi:10.1099/00221287-147-5-1189 · Cited by 90 · see citing works
Structure and regulation of the HSP90 gene from the pathogenic fungus Candida albicans
Swoboda, R. K., Bertram, G., Budge, S., Gooday, G. W., Gow, N. A., & Brown, A. J. (1995) · Infection and Immunity · doi:10.1128/iai.63.11.4506-4514.1995 · Cited by 89 · see citing works
Self-citation
Proteomic response to amino acid starvation in Candida albicans and Saccharomyces cerevisiae
Yin, Z., Stead, D., Selway, L., Walker, J., Riba‐Garcia, I., Mclnerney, T., Gaskell, S. J., Oliver, S. G., Cash, P., & Brown, A. J. P. (2004) · PROTEOMICS · doi:10.1002/pmic.200300760 · Cited by 86 · see citing works
Self-citation
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
Garbuz, D. G., Evgen’ev, M. B., Feder, M. E., et al. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00429 · Cited by 79 · see citing works
MNL1Regulates Weak Acid–induced Stress Responses of the Fungal PathogenCandida albicans
Ramsdale, M., Selway, L., Stead, D., Walker, J., Yin, Z., Nicholls, S. M., Crowe, J. D., Sheils, E., & Brown, A. J. P. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-09-0946 · Cited by 79 · see citing works
Self-citation
Comparative genomics of the HOG-signalling system in fungi
Krantz, M., Becit, E., & Hohmann, S. (2006) · Current Genetics · doi:10.1007/s00294-005-0038-x · Cited by 78 · see citing works
A 70-Kilodalton Recombinant Heat Shock Protein ofCandida albicansIs Highly Immunogenic and Enhances Systemic Murine Candidiasis
Bromuro, C., La Valle, R., Sandini, S., Urbani, F., Ausiello, C. M., Morelli, L., Féd’ostiani, C., Romani, L., & Cassone, A. (1998) · Infection and Immunity · doi:10.1128/iai.66.5.2154-2162.1998 · Cited by 73 · see citing works
Heat shock disassembles the nucleolus and inhibits nuclear protein import and poly(A)+ RNA export.
Liu, Y., Liang, S., & Tartakoff, A. M. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb01064.x · Cited by 66 · see citing works
Protein chaperones and the heat shock response in Saccharomyces cerevisiae
Morano, K. A., Liu, P. C. C., & Thiele, D. J. (1998) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(98)80011-8 · Cited by 65 · see citing works
Disruption of the KEX1 gene inPichia pastoris allows expression of full-length murine and human endostatin
Boehm, T., Pirie-Shepherd, S. R., Trinh, L. B., Shiloach, J., & Folkman, J. (1999) · Yeast · doi:10.1002/(sici)1097-0061(199905)15:7 · Cited by 64 · see citing works
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Sewell, A. K., Yokoya, F., Yu, W., Miyagawa, T., Murayama, T., & Winge, D. R. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.42.25079 · Cited by 61 · see citing works
A physical comparison of chromosome III in six strains of Saccharomyces cerevisiae
Wicksteed, B. L., Collins, I. J., Dershowitz, A., et al. (1994) · Yeast · doi:10.1002/yea.320100105 · Cited by 54 · see citing works
LacZ assays in yeast
Rupp, S. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)50959-9 · Cited by 51 · see citing works
Transcript analysis of 1003 novel yeast genes using high‐throughput northern hybridizations
Brown, A. J. P., Planta, R. J., Restuhadi, F., Bailey, D. A., Butler, P. R., Cadahia, J. L., Cerdán, M. E., Jonge, M. D., Gardner, D. C. J., Gent, M. E., et al. (2001) · The EMBO Journal · doi:10.1093/emboj/20.12.3177 · Cited by 47 · see citing works
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Mutated Yeast Heat Shock Transcription Factor Activates Transcription Independently of Hyperphosphorylation
Hashikawa, N., Mizukami, Y., Imazu, H., & Sakurai, H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510827200 · Cited by 42 · see citing works
Multilocus sequence typing of Candida albicans isolates from animals
Jacobsen, M. D., Bougnoux, M., d’Enfert, C., et al. (2008) · Research in Microbiology · doi:10.1016/j.resmic.2008.05.003 · Cited by 35 · see citing works
Ecology and Epidemiology of Candida Species
Odds, F. C. (1984) · Zentralblatt für Bakteriologie Mikrobiologie und Hygiene 1 Abt Originale A Medizinische Mikrobiologie Infektionskrankheiten und Parasitologie · doi:10.1016/s0174-3031(84)80073-6 · Cited by 32 · see citing works
The [ PSI + ] Prion of Saccharomyces cerevisiae Can Be Propagated by an Hsp104 Orthologue from Candida albicans
Zenthon, J., Ness, F., Cox, B. S., et al. (2006) · Eukaryotic Cell · doi:10.1128/ec.5.2.217-225.2006 · Cited by 31 · see citing works
The determinants of heat‐shock element‐directed lacZ expression in Saccharomyces cerevisiae
Kirk, N., & Piper, P. W. (1991) · Yeast · doi:10.1002/yea.320070602 · Cited by 30 · see citing works
Heat Shock Factor Is Required for Growth at Normal Temperatures in the Fission Yeast Schizosaccharomyces pombe
Gallo, G. J., Prentice, H. L., & Kingston, R. E. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.2.749-761.1993 · Cited by 19 · see citing works
Heat-inducible ATP-binding proteins of Candida albicans are recognized by sera of infected patients
Swoboda, R., Miyasaki, S. H., Greenspan, D., et al. (1993) · Journal of General Microbiology · doi:10.1099/00221287-139-12-2995 · Cited by 16 · see citing works
Gene expression of 70 kDa heat shock protein of Candida albicans: transcriptional activation and response to heat shock
Sandini, S., Melchionna, R., Bromuro, C., & Valle, R. L. (2002) · Medical Mycology · doi:10.1080/mmy.40.5.471.478 · Cited by 9 · see citing works
Stress responses in Candida albicans.
Quinn, J., Brown, A. J. P., d’Enfert, C., & Hube, B. (2007) · Cited by 5 · see citing works
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Do Carmo-Sousa L Rose AH Harrison JS Distribution of yeasts in nature The Yeasts 1969 1 New York Academic Press 79 105
Gentles JC La Touche CJ Rose AH Harrison JS Yeasts as human and animal pathogens The Yeasts 1969 1 New York Academic Press 108 182

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Authors: Nicholls, S., Leach, M. D., Priest, C. L., & Brown, A. J. P.
Affiliations: University of Aberdeen (GB)
Corresponding author: Brown, Alistair J. P.
ORCID: Leach, Michelle D.
Brown, Alistair J. P.
Venue: Molecular Microbiology
Publisher: Wiley
Published: 2009-11
Volume: 74
Issue: 4
Pages: 844-861
ISSN: 0950-382X (ISSN-L)
1365-2958
DOI: 10.1111/j.1365-2958.2009.06883.x
PMC: PMC3675641
OpenAlex: W2126700110
Cited by: 105
References: 99
Citations by year: 2026: 3 · 2025: 4 · 2024: 6 · 2023: 6 · 2022: 4 · 2021: 6 · 2020: 10 · 2019: 2 · 2018: 10 · 2017: 9 · 2016: 6 · 2015: 6 · 2014: 7 · 2013: 5 · 2012: 13
FWCI: 2.82
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Molecular Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
Funders: Wellcome Trust (214004, 080088)
European Commission (214004)
Biotechnology and Biological Sciences Research Council (BB/D009308/1, BB/F00513X/1)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: HSF1, heat shock transcription factor, Candida albicans, heat shock response, heat shock element, molecular chaperones, Hsp104, HSP90, HSP70, growth temperature, stress response, fungal pathogens, essential genes, transcriptional regulation
MeSH terms: Heat Shock Transcription Factors, Animals, Candida albicans, DNA-Binding Proteins, Fungal Proteins, Hot Temperature, Humans, Phosphorylation, Stress, Physiological, Transcription Factors, Gene Expression Regulation, Fungal, Molecular Chaperones, Microbial Viability

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

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