Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors

Roetzer, Andreas; Gregori, Christa; Jennings, Ann Marie; Quintin, Jessica; Ferrandon, Dominique; Butler, Geraldine; Kuchler, Karl; Ammerer, Gustav; Schüller, Christoph

doi:10.1111/j.1365-2958.2008.06301.x

Cited by 124Fungal and yeast genetics researchBacterial Genetics and BiotechnologyAntifungal resistance and susceptibility

Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors

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Roetzer, Andreas, Gregori, Christa, Jennings, Ann Marie, Quintin, Jessica, Ferrandon, Dominique, Butler, Geraldine, Kuchler, Karl, Ammerer, Gustav +1 more·2008·Molecular Microbiology

DOI 10.1111/j.1365-2958.2008.06301.xPMC PMC2610386

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Abstract

We determined the genome-wide environmental stress response (ESR) expression profile of Candida glabrata, a human pathogen related to Saccharomyces cerevisiae. Despite different habitats, C. glabrata, S. cerevisiae, Schizosaccharomyces pombe and Candida albicans have a qualitatively similar ESR. We investigate the function of the C. glabrata syntenic orthologues to the ESR transcription factor Msn2. The C. glabrata orthologues CgMsn2 and CgMsn4 contain a motif previously referred to as HD1 (homology domain 1) also present in Msn2 orthologues from fungi closely related to S. cerevisiae. We show that regions including this motif confer stress-regulated intracellular localization when expressed in S. cerevisiae. Site-directed mutagenesis confirms that nuclear export of CgMsn2 in C. glabrata requires an intact HD1. Transcript profiles of CgMsn2/4 mutants and CgMsn2 overexpression strains show that they regulate a part of the CgESR. CgMsn2 complements a S. cerevisiae msn2 null mutant and in stressed C. glabrata cells, rapidly translocates from the cytosol to the nucleus. CgMsn2 is required for full resistance against severe osmotic stress and rapid and full induction of trehalose synthesis genes (TPS1, TPS2). Constitutive activation of CgMsn2 is detrimental for C. glabrata. These results establish an Msn2-regulated general stress response in C. glabrata.

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C. glabrata grows optimally at 37 °C and can grow at 42 °C under heat-stressed conditions.
“Candida glabrata grows optimally at 37 °C and, therefore, thrives best in the human host and can grow at 42 °C under heat-stressed conditions [18,57].”
From Candida glabrata: pathogenicity and resistance mechanisms for adaptation and survival (2021) · cites this paper as [57]
The environmental stress response in C. glabrata is governed by two transcriptional regulators CgMsn2 and CgMsn4.
“The environmental stress response in C. glabrata is governed by two transcriptional regulators CgMsn2 and CgMsn4 [38], while the oxidative stress response is regulated by the sole catalase CgCta1 [80], two superoxide dismutases CgSod1 and CgSod2 [81], and glutathione biosynthetic enzymes CgGsh1 and CgGsh2 [82,83].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [38]

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Brown, A. J. P., Budge, S., Kaloriti, D., Tillmann, A., Jacobsen, M. D., Yin, Z., Ene, I. V., Bohovych, I., Sandai, D., Kastora, S., et al. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.088930 · Cited by 299 · see citing works
Candida glabrata: A review of its features and resistance
Rodrigues, C. F., Silva, S., & Henriques, M. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2009-3 · Cited by 268 · see citing works
Metabolism impacts upon Candida immunogenicity and pathogenicity at multiple levels
Brown, A. J. P., Brown, G. D., Netea, M. G., & Gow, N. A. R. (2014) · Trends in Microbiology · doi:10.1016/j.tim.2014.07.001 · Cited by 258 · see citing works
The Facultative Intracellular Pathogen Candida glabrata Subverts Macrophage Cytokine Production and Phagolysosome Maturation
Seider, K., Brunke, S., Schild, L., Jablonowski, N., Wilson, D., Majer, O., Barz, D., Haas, A., Kuchler, K., Schaller, M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003730 · Cited by 220 · see citing works
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Candida glabrata: pathogenicity and resistance mechanisms for adaptation and survival
Hassan, Y., Chew, S. Y., & Than, L. T. L. (2021) · Journal of Fungi · doi:10.3390/jof7080667 · Cited by 170 · see citing works
Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape.
Seider, K., Heyken, A., Lüttich, A., Miramón, P., & Hube, B. (2010) · Current Opinion in Microbiology · doi:10.1016/j.mib.2010.05.001 · Cited by 167 · see citing works
From Saccharomyces cerevisiae to Candida glabrata in a few easy steps: important adaptations for an opportunistic pathogen: Candida glabrata stress response
Roetzer, A., Gabaldón, T., & Schüller, C. (2011) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.02102.x · Cited by 154 · see citing works
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Loss of Mitochondrial Functions Associated with Azole Resistance in Candida glabrata Results in Enhanced Virulence in Mice
Ferrari, S., Sanguinetti, M., De Bernardis, F., Torelli, R., Posteraro, B., Vandeputte, P., & Sanglard, D. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01271-10 · Cited by 144 · see citing works
Autophagy supportsCandida glabratasurvival during phagocytosis
Roetzer, A., Gratz, N., Kovarik, P., & SchÃ¼ller, C. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01391.x · Cited by 142 · see citing works
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Candida glabrata: A Lot More Than Meets the Eye
Kumar, K., Askari, F., Sahu, M. S., & Kaur, R. (2019) · Microorganisms · doi:10.3390/microorganisms7020039 · Cited by 128 · see citing works
Regulation of Candida glabrata oxidative stress resistance is adapted to host environment
Roetzer, A., Klopf, E., Gratz, N., Marcet-Houben, M., Hiller, E., Rupp, S., Gabaldón, T., Kovarik, P., & Schüller, C. (2011) · FEBS Letters · doi:10.1016/j.febslet.2010.12.006 · Cited by 90 · see citing works
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Combinatorial stresses kill pathogenicCandidaspecies
Kaloriti, D., Tillmann, A., Cook, E., Jacobsen, M., You, T., Lenardon, M., Ames, L., Barahona, M., Chandrasekaran, K., Coghill, G., et al. (2012) · Medical Mycology · doi:10.3109/13693786.2012.672770 · Cited by 86 · see citing works
Role of glutathione in the oxidative stress response in the fungal pathogen Candida glabrata
Gutiérrez-Escobedo, G., Orta-Zavalza, E., Castaño, I., & De Las Peñas, A. (2013) · Current Genetics · doi:10.1007/s00294-013-0390-1 · Cited by 47 · see citing works
A novel role for a glycosylphosphatidylinositol‐anchored aspartyl protease, CgYps1, in the regulation of pH homeostasis in Candida glabrata
Bairwa, G., & Kaur, R. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07496.x · Cited by 47 · see citing works
Physiologically relevant alternative carbon sources modulate biofilm formation, Cell Wall architecture, and the stress and antifungal resistance of Candida glabrata
Chew, S. Y., Ho, K. L., Cheah, Y. K., Sandai, D., Brown, A. J. P., & Than, L. T. L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133172 · Cited by 40 · see citing works
Transcriptional profiling of Candida glabrata during phagocytosis by neutrophils and in the infected mouse spleen
Fukuda, Y., Tsai, H.-F., Myers, T. G., & Bennett, J. E. (2013) · Infection and Immunity · doi:10.1128/iai.00851-12 · Cited by 41 · see citing works
GPI (glycosylphosphatidylinositol)-linked aspartyl proteases regulate vacuole homoeostasis in Candida glabrata
Bairwa, G., Rasheed, M., Taigwal, R., Sahoo, R., & Kaur, R. (2014) · Biochemical Journal · doi:10.1042/bj20130757 · Cited by 36 · see citing works
A network of paralogous stress response transcription factors in the human pathogen Candida glabrata
Merhej, J., Thiebaut, A., Blugeon, C., Pouch, J., Ali Chaouche, M. E. A., Camadro, J.-M., Le Crom, S., Lelandais, G., & Devaux, F. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00645 · Cited by 36 · see citing works
Candida glabrata’s Genome Plasticity Confers a Unique Pattern of Expressed Cell Wall Proteins
López-Fuentes, E., Gutiérrez-Escobedo, G., Timmermans, B., Van Dijck, P., De Las Peñas, A., & Castaño, I. (2018) · Journal of Fungi · doi:10.3390/jof4020067 · Cited by 35 · see citing works
Transcription factors Asg1p and Hal9p regulate pH homeostasis in Candida glabrata
Wu, J., Chen, X., Cai, L., Tang, L., & Liu, L. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00843 · Cited by 30 · see citing works
Multifactorial Role of Mitochondria in Echinocandin Tolerance Revealed by Transcriptome Analysis of Drug-Tolerant Cells
Garcia-Rubio, R., Jimenez-Ortigosa, C., DeGregorio, L., Quinteros, C., Shor, E., & Perlin, D. S. (2021) · mBio · doi:10.1128/mbio.01959-21 · Cited by 29 · see citing works
Candida glabrata : new tools and technologies—expanding the toolkit
Ho, H.-L., & Haynes, K. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov066 · Cited by 29 · see citing works
Sorbic acid stress activates the Candida glabrata high osmolarity glycerol MAP kinase pathway
Jandric, Z., Gregori, C., Klopf, E., Radolf, M., & Schüller, C. (2013) · Frontiers in Microbiology · doi:10.3389/fmicb.2013.00350 · Cited by 28 · see citing works
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Scw1p Antagonizes the Septation Initiation Network To Regulate Septum Formation and Cell Separation in the Fission Yeast Schizosaccharomyces pombe
Jin, Q., & McCollum, D. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.3.510-520.2003 · Cited by 22 · see citing works
The use of morphomutants to investigate septum formation and cell separation in Schizosaccharomyces pombe
Sipiczki, M., & Bozsik, A. (2000) · Archives of Microbiology · doi:10.1007/s002030000214 · Cited by 24 · see citing works
Three classes of mammalian transcription activation domain stimulate transcription in Schizosaccharomyces pombe
Remacle, J., Albrecht, G., Brys, R., Braus, G. H., & Huylebroeck, D. (1997) · The EMBO Journal · doi:10.1093/emboj/16.18.5722 · Cited by 51 · see citing works
Splicing‐dependent NMD does not require the EJC in Schizosaccharomyces pombe
Wen, J., & Brogna, S. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.48 · Cited by 72 · see citing works
Mammalian promoter element function in the fission yeastSchizosaccharomyces pombe
Prentice, H. L., & Kingston, R. E. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.13.3383 · Cited by 22 · see citing works

Authors: Roetzer, A., Gregori, C., Jennings, A. M., Quintin, J., Ferrandon, D., Butler, G., Kuchler, K., Ammerer, G., & Schüller, C.
Affiliations: University of Vienna (AT)
Max Perutz Labs (AT)
University College Dublin (IE)
Centre National de la Recherche Scientifique (FR)
Corresponding author: Schüller, Christoph
ORCID: Quintin, Jessica
Ferrandon, Dominique
Butler, Geraldine
Kuchler, Karl
Ammerer, Gustav
Schüller, Christoph
Venue: Molecular Microbiology
Publisher: Wiley
Published: 2008-07-10
Volume: 69
Issue: 3
Pages: 603-620
ISSN: 0950-382X (ISSN-L)
1365-2958
DOI: 10.1111/j.1365-2958.2008.06301.x
PMC: PMC2610386
OpenAlex: W2157490841
Cited by: 124
References: 76
Citations by year: 2026: 3 · 2025: 6 · 2024: 7 · 2023: 5 · 2022: 6 · 2021: 9 · 2020: 7 · 2019: 11 · 2018: 5 · 2017: 8 · 2016: 3 · 2015: 9 · 2014: 9 · 2013: 11 · 2012: 4
FWCI: 2.88
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Molecular Microbiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Phaidra (Universität Wien) (submittedVersion, cc-by-nc-nd)
HAL (submittedVersion)
Funders: Wellcome Trust (072420)
Vienna Science and Technology Fund
Austrian Science Fund
Centre National de la Recherche Scientifique
Topics: 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
Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Keywords: Candida glabrata, environmental stress response, Msn2, Msn4, transcription factors, nuclear export, osmotic stress, trehalose biosynthesis, TPS1, TPS2, gene expression profiling, orthologs, fungal stress response
MeSH terms: Amino Acid Sequence, Animals, Candidiasis, DNA-Binding Proteins, Drosophila melanogaster, Fungal Proteins, Humans, Molecular Sequence Data, Osmotic Pressure, Transcription Factors, Transcription, Genetic, Virulence, Yeasts, Gene Expression Regulation, Fungal, Regulon, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Saccharomyces cerevisiae Proteins, Candida glabrata

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Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors

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