Dissection of Ire1 Functions Reveals Stress Response Mechanisms Uniquely Evolved in Candida glabrata

Miyazaki, Taiga; Nakayama, Hironobu; Nagayoshi, Yohsuke; Kakeya, Hiroshi; Kohno, Shigeru

doi:10.1371/journal.ppat.1003160

Cited by 78Endoplasmic Reticulum Stress and DiseaseFungal and yeast genetics researchIon Channels and Receptors

Dissection of Ire1 Functions Reveals Stress Response Mechanisms Uniquely Evolved in Candida glabrata

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Miyazaki, Taiga, Nakayama, Hironobu, Nagayoshi, Yohsuke, Kakeya, Hiroshi, Kohno, Shigeru·2013·PLoS Pathogens

DOI 10.1371/journal.ppat.1003160PMC PMC3561209

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Abstract

Proper protein folding in the endoplasmic reticulum (ER) is vital in all eukaryotes. When misfolded proteins accumulate in the ER lumen, the transmembrane kinase/endoribonuclease Ire1 initiates splicing of HAC1 mRNA to generate the bZIP transcription factor Hac1, which subsequently activates its target genes to increase the protein-folding capacity of the ER. This cellular machinery, called the unfolded protein response (UPR), is believed to be an evolutionarily conserved mechanism in eukaryotes. In this study, we comprehensively characterized mutant phenotypes of IRE1 and other related genes in the human fungal pathogen Candida glabrata. Unexpectedly, Ire1 was required for the ER stress response independently of Hac1 in this fungus. C. glabrata Ire1 did not cleave mRNAs encoding Hac1 and other bZIP transcription factors identified in the C. glabrata genome. Microarray analysis revealed that the transcriptional response to ER stress is not mediated by Ire1, but instead is dependent largely on calcineurin signaling and partially on the Slt2 MAPK pathway. The loss of Ire1 alone did not confer increased antifungal susceptibility in C. glabrata contrary to UPR-defective mutants in other fungi. Taken together, our results suggest that the canonical Ire1-Hac1 UPR is not conserved in C. glabrata. It is known in metazoans that active Ire1 nonspecifically cleaves and degrades a subset of ER-localized mRNAs to reduce the ER load. Intriguingly, this cellular response could occur in an Ire1 nuclease-dependent fashion in C. glabrata. We also uncovered the attenuated virulence of the C. glabrata Δire1 mutant in a mouse model of disseminated candidiasis. This study has unveiled the unique evolution of ER stress response mechanisms in C. glabrata.

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Lack of CgIre1 led to diminished virulence in both immunosuppressed and immunocompetent mice.
“Furthermore, lack of CgIre1 led to diminished virulence in both immunosuppressed and immunocompetent mice [97].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [97]
For survival of ER stress, the essentiality of the key ER stress sensor CgIre1 endoribonuclease was attributed to its role in activation of the non-canonical unfolded protein response pathway.
“For survival of the ER stress, essentiality of the key ER stress sensor, CgIre1 endoribonuclease, was attributed to its role in activation of the non-canonical unfolded protein response pathway [97].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [97]
Duplications and large scale genomic variations, although they can lead to significant issues such as genomic instability, play a major role in yeast evolution.
“As such, ALE studies highlight that duplications and large scale genomic variations, although they can lead to significant issues such as genomic instability [152], play a major role in e.g. yeast evolution; this is also indicated by data on wine yeasts, galactose utilization, comparative genomics and drug resistance [115,153-156].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [154]

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Conserved RNA structures in the non-canonical Hac1/Xbp1 intron
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The Activity of Yeast Hog1 MAPK Is Required during Endoplasmic Reticulum Stress Induced by Tunicamycin Exposure
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Nonapoptotic Death of Saccharomyces cerevisiae Cells That Is Stimulated by Hsp90 and Inhibited by Calcineurin and Cmk2 in Response to Endoplasmic Reticulum Stresses
Dudgeon, D. D., Zhang, N., Ositelu, O. O., Kim, H., & Cunningham, K. W. (2008) · Eukaryotic Cell · doi:10.1128/ec.00291-08 · Cited by 59 · see citing works
Autoregulation of the HAC1 gene is required for sustained activation of the yeast unfolded protein response
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The virulence of the opportunistic fungal pathogenAspergillus fumigatusrequires cooperation between the endoplasmic reticulum-associated degradation pathway (ERAD) and the unfolded protein response (UPR)
Richie, D. L., Feng, X., Hartl, L., Aimanianda, V., Krishnan, K., Powers‐Fletcher, M. V., Watson, D. S., Galande, A. K., White, S. M., Willett, T., et al. (2011) · Virulence · doi:10.4161/viru.2.1.13345 · Cited by 49 · see citing works
Clinical Evaluation of the ASTY Colorimetric Microdilution Panel for Antifungal Susceptibility Testing
Pfaller, M. A., Arıkan, S., Lozano‐Chiu, M., Chen, Y.-S., Coffman, S. L., Messer, S. A., Rennie, R. P., Sand, C., Heffner, T., Rex, J. H., et al. (1998) · Journal of Clinical Microbiology · doi:10.1128/jcm.36.9.2609-2612.1998 · Cited by 42 · see citing works
Functional characterization of the unconventional splicing of Yarrowia lipolytica HAC1 mRNA induced by unfolded protein response
Oh, M. H., Cheon, S. A., Kang, H. A., & Kim, J. (2010) · Yeast · doi:10.1002/yea.1762 · Cited by 31 · see citing works
The glycosylphosphatidylinositol-linked aspartyl protease Yps1 is transcriptionally regulated by the calcineurin-Crz1 and Slt2 MAPK pathways in Candida glabrata: Transcriptional regulation of YPS1 in C. glabrata
Miyazaki, T., Izumikawa, K., Yamauchi, S., Inamine, T., Nagayoshi, Y., Saijo, T., Seki, M., Kakeya, H., Yamamoto, Y., Yanagihara, K., et al. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00734.x · Cited by 23 · see citing works
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Candida glabrata shuttle vectors suitable for translational fusions to lacZ and use of β-galactosidase as a reporter of gene expression
Barkani, A. E., Haynes, K., Mösch, H., Frosch, M., & Mühlschlegel, F. A. (2000) · Gene · doi:10.1016/s0378-1119(00)00065-2 · Cited by 16 · see citing works

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Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827 · see citing works
Engineering of the unfolded protein response pathway in Pichia pastoris: enhancing production of secreted recombinant proteins
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Candida glabrata: A Lot More Than Meets the Eye
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Calcineurin as a multifunctional regulator: Unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis
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Intracellular survival ofCandida glabratain macrophages: immune evasion and persistence
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Stress Signaling Pathways for the Pathogenicity of Cryptococcus
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The importance of connections between the cell wall integrity pathway and the unfolded protein response in filamentous fungi
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Cleavage of BLOC1S1 mRNA by IRE1 Is Sequence Specific, Temporally Separate from XBP1 Splicing, and Dispensable for Cell Viability under Acute Endoplasmic Reticulum Stress
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The Aspergillus fumigatus pkcAG579R Mutant Is Defective in the Activation of the Cell Wall Integrity Pathway but Is Dispensable for Virulence in a Neutropenic Mouse Infection Model
Rocha, M. C., de Godoy, K. F., de Castro, P. A., Hori, J. I., Bom, V. L. P., Brown, N. A., da Cunha, A. F., Goldman, G. H., & Malavazi, I. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135195 · Cited by 58 · see citing works
Unfolded protein response in filamentous fungi—implications in biotechnology
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Deletion of ADA2 Increases Antifungal Drug Susceptibility and Virulence in Candida glabrata
Yu, S.-J., Chang, Y.-L., & Chen, Y.-L. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01924-17 · Cited by 43 · see citing works
Endoplasmic reticulum stress and fungal pathogenesis
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The Unfolded Protein Response Pathway in the Yeast Kluyveromyces lactis. A Comparative View among Yeast Species
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The protein kinase Ire1 impacts pathogenicity of <scp> Candida albicans </scp> by regulating homeostatic adaptation to endoplasmic reticulum stress
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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
The fungal UPR: A regulatory hub for virulence traits in the mold pathogen Aspergillus fumigatus
Krishnan, K., & Askew, D. S. (2014) · Virulence · doi:10.4161/viru.26571 · Cited by 35 · see citing works
The protein kinase Ire1 has a Hac1-independent essential role in iron uptake and virulence of Candida albicans
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The unfolded protein response (UPR) pathway inCryptococcus
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The Role of Secretory Pathways in Candida albicans Pathogenesis
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Portrait of Matrix Gene Expression in Candida glabrata Biofilms with Stress Induced by Different Drugs
Rodrigues, C. F., & Henriques, M. (2018) · Genes · doi:10.3390/genes9040205 · Cited by 29 · see citing works
To Sense or Die: Mechanisms of Temperature Sensing in Fungal Pathogens
Leach, M. D., & Cowen, L. E. (2014) · Current Fungal Infection Reports · doi:10.1007/s12281-014-0182-1 · Cited by 28 · see citing works
ER stress response mechanisms in the pathogenic yeastCandida glabrataand their roles in virulence
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Self-citation
Polysome profiling reveals broad translatome remodeling during endoplasmic reticulum (ER) stress in the pathogenic fungus Aspergillus fumigatus
Krishnan, K., Ren, Z., Losada, L. C., Nierman, W. C., Lu, L. J., & Askew, D. S. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-159 · Cited by 26 · see citing works
Functional Coupling between the Unfolded Protein Response and Endoplasmic Reticulum/Golgi Ca 2+ -ATPases Promotes Stress Tolerance, Cell Wall Biosynthesis, and Virulence of Aspergillus fumigatus
Weichert, M., Guirao-Abad, J. P., Aimanianda, V., Krishnan, K., Grisham, C., Snyder, P., Sheehan, A., Abbu, R., Liu, H., Filler, S. G., et al. (2020) · mBio · doi:10.1128/mbio.01060-20 · Cited by 24 · see citing works
Evolutionarily Conserved and Divergent Roles of Unfolded Protein Response (UPR) in the Pathogenic Cryptococcus Species Complex
Jung, K., ‍Lee, K.-T., Averette, A. F., Hoy, M. J., Everitt, J. I., Heitman, J., & Bahn, Y. (2018) · Scientific Reports · doi:10.1038/s41598-018-26405-5 · Cited by 24 · see citing works
Unfolded Protein Response and Scaffold Independent Pheromone MAP Kinase Signaling Control Verticillium dahliae Growth, Development, and Plant Pathogenesis
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RNA sequencing identifies novel regulated IRE1-dependent decay targets that affect multiple myeloma survival and proliferation
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Roles of vacuolar H+-ATPase in the oxidative stress response ofCandida glabrata
Nishikawa, H., Miyazaki, T., Nakayama, H., Minematsu, A., Yamauchi, S., Yamashita, K., Takazono, T., Shimamura, S., Nakamura, S., Izumikawa, K., et al. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow054 · Cited by 22 · see citing works
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Calcineurin-dependent contributions to fitness in the opportunistic pathogen Candida glabrata
Pavesic, M. W., Gale, A. N., Nickels, T. J., Harrington, A. A., Bussey, M., & Cunningham, K. W. (2024) · mSphere · doi:10.1128/msphere.00554-23 · Cited by 22 · see citing works
Identification of an Exceptionally Long Intron in the HAC1 Gene of Candida parapsilosis
Iracane, E., Donovan, P. D., Ola, M., Butler, G., & Holland, L. (2018) · mSphere · doi:10.1128/msphere.00532-18 · Cited by 21 · see citing works
Impact of the UPR on the virulence of the plant fungal pathogenA. brassicicola
Guillemette, T., Calmes, B., & Simoneau, P. (2013) · Virulence · doi:10.4161/viru.26772 · Cited by 21 · see citing works
Endoplasmic reticulum stress differentially inhibits endoplasmic reticulum and inner nuclear membrane protein quality control degradation pathways
Buchanan, B. W., Mehrtash, A. B., Broshar, C., Runnebohm, A. M., Snow, B. J., Scanameo, L. N., Hochstrasser, M., & Rubenstein, E. M. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.010295 · Cited by 21 · see citing works
Puf4 Regulates both Splicing and Decay of HXL1 mRNA Encoding the Unfolded Protein Response Transcription Factor in Cryptococcus neoformans
Glazier, V. E., Kaur, J. N., Brown, N. T., Rivera, A., & Panepinto, J. C. (2015) · Eukaryotic Cell · doi:10.1128/ec.00273-14 · Cited by 21 · see citing works
Functional genomic analysis of Candida albicans protein kinases reveals modulators of morphogenesis in diverse environments
Lee, Y., Hossain, S., MacAlpine, J., Robbins, N., & Cowen, L. E. (2023) · iScience · doi:10.1016/j.isci.2023.106145 · Cited by 18 · see citing works
Identification of Genomewide Alternative Splicing Events in Sequential, Isogenic Clinical Isolates of Candida albicans Reveals a Novel Mechanism of Drug Resistance and Tolerance to Cellular Stresses
Muzafar, S., Sharma, R. D., Shah, A. H., Gaur, N. A., Dasgupta, U., Chauhan, N., & Prasad, R. (2020) · mSphere · doi:10.1128/msphere.00608-20 · Cited by 19 · see citing works
Vacuolar proton-translocating ATPase is required for antifungal resistance and virulence of Candida glabrata
Minematsu, A., Miyazaki, T., Shimamura, S., Nishikawa, H., Nakayama, H., Takazono, T., Saijo, T., Yamamoto, K., Imamura, Y., Yanagihara, K., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210883 · Cited by 19 · see citing works
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The ER stress response and host temperature adaptation in the human fungal pathogenCryptococcus neoformans
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Hansenula polymorpha Hac1p Is Critical to Protein N -Glycosylation Activity Modulation, as Revealed by Functional and Transcriptomic Analyses
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Unexpected effects of azole transporter inhibitors on antifungal susceptibility in Candida glabrata and other pathogenic Candida species
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IreA Controls Endoplasmic Reticulum Stress-Induced Autophagy and Survival through Homeostasis Recovery
Domínguez‐Martín, E., Ongay‐Larios, L., Kawasaki, L., Vincent, O., Coello, G., Coria, R., & Escalante, R. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00054-18 · Cited by 16 · see citing works
Unfolding the Endoplasmic Reticulum of a Social Amoeba: Dictyostelium discoideum as a New Model for the Study of Endoplasmic Reticulum Stress
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A Human IRE1 Inhibitor Blocks the Unfolded Protein Response in the Pathogenic Fungus Aspergillus fumigatus and Suggests Noncanonical Functions within the Pathway
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Investigation of protein secretion and secretion stress in Ashbya gossypii
Aguiar, T. Q., Ribeiro, O., Arvas, M., Wiebe, M. G., Penttilä, M. E., & Domingues, L. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1137 · Cited by 14 · see citing works
KRE5 Suppression Induces Cell Wall Stress and Alternative ER Stress Response Required for Maintaining Cell Wall Integrity in Candida glabrata
Tanaka, Y., Sasaki, M., Ito, F., Aoyama, T., Okamoto, M., Takahashi‐Nakaguchi, A., Chibana, H., & Shibata, N. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161371 · Cited by 14 · see citing works
Cooperation between ER stress and calcineurin signaling contributes to the maintenance of cell wall integrity in Candida glabrata
Tanaka, Y., Sasaki, M., Ito, F., Aoyama, T., Sato-Okamoto, M., Takahashi-Nakaguchi, A., Chibana, H., & Shibata, N. (2018) · Fungal Biology · doi:10.1016/j.funbio.2017.09.007 · Cited by 13 · see citing works
TAC1b mutation in Candida auris decreases manogepix susceptibility owing to increased CDR1 expression
Hirayama, T., Miyazaki, T., Tanaka, R., Kitahori, N., Yoshida, M., Takeda, K., Ide, S., Iwanaga, N., Tashiro, M., Takazono, T., et al. (2024) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01508-24 · Cited by 12 · see citing works
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Contribution of the Slt2-regulated transcription factors to echinocandin tolerance in Candida glabrata
Nagayoshi, Y., Miyazaki, T., Minematsu, A., Yamauchi, S., Takazono, T., Nakamura, S., Imamura, Y., Izumikawa, K., Kakeya, H., Yanagihara, K., et al. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12204 · Cited by 12 · see citing works
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Antifungal drug resistance in Candida glabrata : role of cellular signaling and gene regulatory networks
Naskar, S., Prajapati, A., & Kaur, R. (2025) · FEMS Yeast Research · doi:10.1093/femsyr/foaf025 · Cited by 11 · see citing works
Mechanisms of multidrug resistance caused by an Ipi1 mutation in the fungal pathogen Candida glabrata
Miyazaki, T., Shimamura, S., Nagayoshi, Y., Nakayama, H., Morita, A., Tanaka, Y., Matsumoto, Y., Inamine, T., Nishikawa, H., Nakada, N., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-56269-z · Cited by 10 · see citing works
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Physiological ER stress caused by amylase production induces regulated Ire1-dependent mRNA decay in Aspergillus oryzae
Tanaka, M., Zhang, S., Sato, S., Yokota, J., Sugiyama, Y., Kawarasaki, Y., Yamagata, Y., Gomi, K., & Shintani, T. (2023) · Communications Biology · doi:10.1038/s42003-023-05386-w · Cited by 9 · see citing works
Andrographolide Induces ROS-Mediated Cytotoxicity, Lipid Peroxidation, and Compromised Cell Integrity in Saccharomyces cerevisiae
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The response of trypanosomes and other eukaryotes to ER stress and the spliced leader RNA silencing (SLS) pathway inTrypanosoma brucei
Michaeli, S. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1042541 · Cited by 9 · see citing works
Protomer alignment modulates specificity of RNA substrate recognition by Ire1
Li, W., Crotty, K., Ruiz, D. G., Voorhies, M., Rivera, C., Sil, A., Mullins, R. D., Jacobson, M. P., Peschek, J., & Walter, P. (2021) · eLife · doi:10.7554/elife.67425 · Cited by 9 · see citing works
Cell death induction in Aspergillus fumigatus: accentuating drug toxicity through inhibition of the unfolded protein response (UPR)
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Roles of Elm1 in antifungal susceptibility and virulence in Candida glabrata
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Self-citation
Transcriptional and post-transcriptional regulation of genes encoding secretory proteins in Aspergillus oryzae
Tanaka, M. (2024) · Bioscience Biotechnology and Biochemistry · doi:10.1093/bbb/zbae004 · Cited by 7 · see citing works
Development of a versatile copper‐responsive gene expression system in the plant‐pathogenic fungus Fusarium graminearum
Kim, S., Park, J., Kim, D., Choi, S., Moon, H., Shin, J. Y., Kim, J., & Son, H. (2021) · Molecular Plant Pathology · doi:10.1111/mpp.13118 · Cited by 6 · see citing works
Pleiotropic Effects of the P5-Type ATPase SpfA on Stress Response Networks Contribute to Virulence in the Pathogenic Mold Aspergillus fumigatus
Guirao-Abad, J. P., Weichert, M., Luengo‐Gil, G., Wong, S. S. W., Aimanianda, V., Grisham, C., Malev, N., Reddy, S., Woollett, L. A., & Askew, D. S. (2021) · mBio · doi:10.1128/mbio.02735-21 · Cited by 6 · see citing works
Genetics of the Unfolded Protein Response in Fungi
Harting, R., & Heimel, K. (2020) · Springer eBooks · doi:10.1007/978-3-030-49924-2_3 · Cited by 4 · see citing works
Hypovirus‐Induced Phosphorylation of CpIre1 Modulates Unfolded Protein Response and Virulence in Cryphonectria parasitica
Zhao, L., Wang, F., Chen, F., Su, S., Qiu, J., Chen, B., & Li, R. (2026) · Molecular Plant Pathology · doi:10.1111/mpp.70227 · Cited by 2 · see citing works
Promising Therapies for Fungal Infection Based on the Study to Elucidate Mechanisms to Cope with Stress in Candida Species.
Hirai, K., Inukai, T., & Nakayama, H. (2016) · Medical Mycology Journal · doi:10.3314/mmj.16.007 · Cited by 2 · see citing works
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Hac1-independent functions of Ire1 drive morphogenesis in Candida albicans through distinct transcriptional programs
Stack-Couture, S., Marsiglio-Librais, G. N., Lung, B., Genereaux, J. L., Halder, V., Dumeaux, V., Shapiro, R. S., & Lajoie, P. (2026) · Journal of Cell Science · doi:10.1242/jcs.264610 · Cited by 1 · see citing works
HAC1 contributes to stress adaptation and virulence in the emerging fungal pathogen Candida auris
Oiki, S., Abe, M., Hirasawa, A., Koizumi, A., Otani, A., Shinohara, T., & Miyazaki, Y. (2026) · Medical Mycology · doi:10.1093/mmy/myag067 · Cited by 1 · see citing works
Harnessing the PpHog1 Regulatory Network to Engineer a UPR ‐Adaptive Komagataella phaffii Chassis for High‐Copy Secretory Protein Production
Shi, J., Lv, Z., Lu, C., Fang, B., Zou, Z., & Zhou, M. (2026) · Microbial Biotechnology · doi:10.1111/1751-7915.70410 · Cited by 1 · see citing works
In the Crossroad Between Drug Resistance and Virulence in Fungal Pathogens
Cavalheiro, M., & Teixeira, M. C. (2018) · Springer eBooks · doi:10.1007/978-3-030-00683-9_7 · Cited by 1 · see citing works
Interplay of Verticillium signaling genes favoring beneficial or detrimental outcomes in interactions with plant hosts
Starke, J. (2020) · doi:10.53846/goediss-8101 · Cited by 1 · see citing works
Secretory Homeostasis and Fungal Pathogenesis: Characterization of the Contribution of Calnexin, SrgA, and the IreA Kinase to the Growth and Virulence of Aspergillus fumigatus
Powers-Fletcher, M. M. (2013) · OhioLink ETD Center (Ohio Library and Information Network)
Promising Therapies for Fungal Infection Based on the Study to Elucidate Mechanisms to Cope with Stress in Candida Species [Translated Article]
Hirai, K., Inukai, T., & Nakayama, H. (2017) · Medical Mycology Journal · doi:10.3314/mmj.17.007
Self-citation
Computational inference of the transcriptional regulatory network of Candida glabrata
Xu, N., & Liu, L. (2019) · FEMS Yeast Research · doi:10.1093/femsyr/foz036
Splicing HAC1/XBP1 mRNAs in Cytoplasm: The Non-Conventional mRNA Splicing Reaction in the Unfolded Protein Response
Song, Y., Rivera, C., Mai, J., Sun, A., & Li, W. (2020) · OBM Genetics · doi:10.21926/obm.genet.2002110
New insights into plasma cell differentiation and unfolded protein response in multiple myeloma: role of DEPTOR and IRE1
Quwaider, D. (2020) · doi:10.14201/gredos.145437
Analyse der UPR vermittelten Stressantwort und ihrer Funktion während der biotrophen Entwicklung von Ustilago maydis
Hampel, M. (2016) · doi:10.53846/goediss-6026
The Unfolded Protein Response and its interplay with the MAPK-mediated pheromone response pathway in Ustilago maydis
Schmitz, L. (2019) · doi:10.53846/goediss-7748
Unfolded Protein Response: a Key Coordinator of Endoplasmic Reticulum Stress and Pathogenicity in Human Fungal Pathogens
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Distinct Ire1-driven transcriptional responses control morphogenesis in Candida albicansPreprint
Stack-Couture, S., Marsiglio-Librais, G. N., Lung, B., Genereaux, J. L., Halder, V., Dumeaux, V., Shapiro, R. S., & Lajoie, P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.13.688365
Transcriptional networks of the stress responses in the human pathogen Candida glabrata
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Ikhrami, M. A., & Kimata, Y. (2026) · Cells · doi:10.3390/cells15201883

ER stress response mechanisms in the pathogenic yeast Candida glabrata and their roles in virulence
Miyazaki, T., & Kohno, S. (2014) · Institutional Repositories DataBase (IRDB)
Self-citation
The protein kinase Ire1 impacts pathogenicity of <scp> Candida albicans </scp> by regulating homeostatic adaptation to endoplasmic reticulum stress
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HacA-Independent Functions of the ER Stress Sensor IreA Synergize with the Canonical UPR to Influence Virulence Traits in Aspergillus fumigatus
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HacAIndependent Functions of the ER Stress Sensor IreA Synergize with the Canonical UPR to Influence Virulence Traits in Aspergillus fumigatus. PLoS Pathog 7: e1002330
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Authors: Miyazaki, T., Nakayama, H., Nagayoshi, Y., Kakeya, H., & Kohno, S.
Affiliations: Nagasaki University (JP)
Suzuka University of Medical Science (JP)
Corresponding author: Miyazaki, Taiga
ORCID: Miyazaki, Taiga
Nakayama, Hironobu
Nagayoshi, Yohsuke
Kakeya, Hiroshi
Venue: PLoS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2013-01-31
Volume: 9
Issue: 1
Pages: e1003160
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.1003160
PMC: PMC3561209
OpenAlex: W2054729583
Cited by: 78
References: 90
Citations by year: 2026: 5 · 2025: 4 · 2024: 3 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 10 · 2019: 5 · 2018: 9 · 2017: 3 · 2016: 5 · 2015: 6 · 2014: 8 · 2013: 8
FWCI: 5.22
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Pathogens (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by-nc-nd)
Nagasaki University's Academic Output SITE (Nagasaki University) (submittedVersion, cc-by-nc-nd)
Funders: Ministry of Education, Culture, Sports, Science and Technology (21390305, 24791027)
Japan Society for the Promotion of Science (24791027, 21390305)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Endoplasmic Reticulum Stress and Disease
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Keywords: IRE1, HAC1, unfolded protein response, ER stress response, Candida glabrata, calcineurin signaling, endoplasmic reticulum protein folding, antifungal susceptibility, virulence, systemic candidiasis
MeSH terms: Amino Acid Sequence, Animals, Candidiasis, Disease Models, Animal, Endoribonucleases, Humans, Immunocompetence, Molecular Sequence Data, RNA, Messenger, Rodent Diseases, Species Specificity, Gene Expression Regulation, Enzymologic, Survival Rate, Calcineurin, Sequence Analysis, Protein, MAP Kinase Signaling System, Candida glabrata, Microarray Analysis, Basic-Leucine Zipper Transcription Factors, Mice, Unfolded Protein Response, Endoplasmic Reticulum Stress

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Dissection of Ire1 Functions Reveals Stress Response Mechanisms Uniquely Evolved in Candida glabrata

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