Roles of Calcineurin and Crz1 in Antifungal Susceptibility and Virulence of Candida glabrata
Open accessAbstract
A Candida glabrata calcineurin mutant exhibited increased susceptibility to both azole antifungal and cell wall-damaging agents and was also attenuated in virulence. Although a mutant lacking the downstream transcription factor Crz1 displayed a cell wall-associated phenotype intermediate to that of the calcineurin mutant and was modestly attenuated in virulence, it did not show increased azole susceptibility. These results suggest that calcineurin regulates both Crz1-dependent and -independent pathways depending on the type of stress.
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Written from the paper’s full text.
TL;DR
Deletion of the calcineurin regulatory subunit CNB1 in *Candida glabrata* increased susceptibility to azoles and cell wall-damaging agents and attenuated virulence in mice, whereas deletion of the downstream transcription factor CRZ1 produced only an intermediate cell wall phenotype and modest virulence attenuation without increased azole susceptibility. The authors conclude that calcineurin acts through both Crz1-dependent and Crz1-independent pathways depending on the stress type.
Key findings
- The Δcnb1 strain showed increased azole susceptibility (fluconazole MIC 4 μg/ml vs. 16 μg/ml for wild type; miconazole 0.125 vs. 0.5; itraconazole 0.5 vs. 2; voriconazole 0.125 vs. 0.25), while the Δcrz1 strain showed equal or lower susceptibility (fluconazole MIC 32 μg/ml). Neither mutant altered amphotericin B susceptibility (MIC 0.5 μg/ml for all strains).
- Fluconazole was fungicidal for the Δcnb1 strain but not for the Δcrz1 strain, suggesting calcineurin mediates azole tolerance via a Crz1-independent pathway.
- Both Δcnb1 and Δcrz1 had decreased micafungin tolerance; Δcnb1 also showed decreased tolerance to Congo red and calcofluor white, whereas Δcrz1 showed only moderately decreased Congo red tolerance and was unaffected by calcofluor white.
- In a murine disseminated candidiasis model, Δcnb1-infected mice had significantly reduced fungal burden in all examined organs versus wild-type and complemented strains; Δcrz1 CFU reductions were statistically significant in kidney but not liver or spleen.
Methods
- Genetic approach: complete deletion of the CNB1 ORF (calcineurin regulatory B subunit) and CRZ1 by one-step PCR-based gene targeting in *C. glabrata*, verified by PCR and Southern blotting, with plasmid-based complemented strains (pCgACT-PNB, pCgACT-PRZ).
- Antifungal susceptibility testing by MIC assays using the ASTY colorimetric microdilution panel (fluconazole, miconazole, itraconazole, voriconazole, amphotericin B), plus viability assays with and without fluconazole and plate assays with micafungin, Congo red, and calcofluor white.
- Virulence assay: groups of 10 female 8-week-old BALB/c mice infected via lateral tail vein, euthanized 7 days after injection for organ CFU determination; Kruskal-Wallis test with Dunn's posttest, P < 0.05 significant.
Limitations
- Not stated in the paper: the authors do not include a dedicated limitations section.
- Evident from the text: virulence was assessed in a single murine model (disseminated candidiasis, 7-day endpoint, no deaths before euthanasia), so organ CFU is the only virulence readout; the Crz1-independent calcineurin pathway is inferred from mutant phenotypes but no specific target is identified.
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Claims the paper makes
0 of 21 cited sources checked · 0 supported · 0 flagged
- Findingown data§ Abstract
The C. glabrata calcineurin mutant (Δcnb1) exhibits increased susceptibility to cell wall-damaging agents.
“A Candida glabrata calcineurin mutant exhibited increased susceptibility to both azole antifungal and cell wall-damaging agents and was also attenuated in virulence.”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The decreased micafungin tolerance in the Δcnb1 and Δcrz1 strains was reversed in the reconstituted strains.
“and this was reversed in the reconstituted strains (Fig. 2).”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The C. glabrata calcineurin mutant (Δcnb1) exhibits increased susceptibility to azole antifungals.
“Although increased azole susceptibility was observed in the Δcnb1 strain”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The C. glabrata Δcrz1 mutant does not show increased azole susceptibility.
“it did not show increased azole susceptibility.”
- Also stated in: § Abstract · plain
“the Δcrz1 strain displayed susceptibility levels similar to, or in some instances lower than, those of wild-type cells.”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data§ Abstract
Decreased micafungin tolerance was observed in the Δcnb1 strain compared to wild-type.
“Decreased micafungin tolerance was observed in the Δcnb1 and Δcrz1 strains compared to that in the wild-type control”
Quote in the paperSubstantial claim
- Findingown data§ Abstract
The Δcrz1 strain was unaffected by calcofluor white exposure.
“and was unaffected by calcofluor white exposure (Fig. 2B).”
Quote in the paperSubstantial claim - Findingown data§ Abstract
Deletion of either CNB1 or CRZ1 did not affect cell growth at 37°C in C. glabrata.
“In contrast to the C. neoformans calcineurin mutant (21), deletion of either CNB1 or CRZ1 did not affect cell growth at 37°C in C. glabrata (data not shown)”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The Δcnb1 strain showed decreased tolerance to Congo red.
“While the Δcnb1 strain showed decreased tolerance to both Congo red and calcofluor white”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The C. glabrata Δcrz1 mutant is modestly attenuated in virulence.
“was modestly attenuated in virulence”
- Also stated in: § Abstract · plain
“Decreased numbers of CFU of the Δcrz1 strain were statistically significant in the kidney but not in the liver and spleen.”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data§ Abstract
The deletion of CRZ1 did not affect the antifungal activity of fluconazole.
“In contrast, the deletion of CRZ1 did not affect the antifungal activity of fluconazole.”
Quote in the paperSubstantial claim - Findingown data§ Abstract
Fluconazole was fungicidal for the Δcnb1 strain.
“the drug was fungicidal for the Δcnb1 strain (Fig. 1).”
Quote in the paperSubstantial claim - Findingown data§ Abstract
Decreased micafungin tolerance was observed in the Δcrz1 strain compared to wild-type.
“Decreased micafungin tolerance was observed in the Δcnb1 and Δcrz1 strains compared to that in the wild-type control”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The C. glabrata calcineurin mutant (Δcnb1) is attenuated in virulence.
“was also attenuated in virulence.”
- Also stated in: § Abstract · plain
“Mice infected with the Δcnb1 strain showed significantly reduced fungal burden in all examined organs compared to those infected with the wild-type control and CNB1-complemented strains (Fig. 3).”
Quote in the paperSubstantial claim - Also stated in: § Abstract · plain
- Findingown data§ Abstract
The Δcrz1 strain exhibited only moderately decreased tolerance to Congo red.
“the Δcrz1 strain exhibited only moderately decreased tolerance to Congo red”
Quote in the paperSubstantial claim - Findingown data§ Abstract
The Δcnb1 strain showed decreased tolerance to calcofluor white.
“While the Δcnb1 strain showed decreased tolerance to both Congo red and calcofluor white”
Quote in the paperSubstantial claim - Findingown data§ Abstract
Mice infected with the Δcnb1 strain showed significantly reduced fungal burden in all examined organs compared to those infected with the wild-type control and CNB1-complemented strains.
“Mice infected with the Δcnb1 strain showed significantly reduced fungal burden in all examined organs compared to those infected with the wild-type control and CNB1-complemented strains (Fig. 3).”
Quote in the paperSubstantial claim - Interpretationreasoning§ Abstract
Calcineurin regulates both Crz1-dependent and -independent pathways depending on the type of stress.
“These results suggest that calcineurin regulates both Crz1-dependent and -independent pathways depending on the type of stress.”
- Also stated in: § Abstract · hedged
“Taken together, these results indicate that calcineurin-mediated Crz1 regulation is dependent upon the type of stress”
Quote in the paperSubstantial claim - Also stated in: § Abstract · hedged
- Premisecitation§ Abstract
The Δcrz1 mutation has little effect on virulence in Candida albicans.
“this mutation has little effect on virulence in both C. albicans (14, 23) and C. glabrata (Fig. 3).”
Quote in the paperNot a substantial claim0 of 2 sources checked - Interpretationown data§ Abstract
A deletion of CRZ1 causes only a partial reduction in virulence.
“while a deletion of CRZ1 causes only a partial reduction.”
Quote in the paperSubstantial claim - Interpretationcitation§ Abstract
The C. glabrata Δcnb1 strain phenotype (increased susceptibility to azoles and cell wall-damaging agents, decreased virulence) is consistent with previous findings for other pathogenic fungi.
“For example, the observed C. glabrata Δcnb1 strain phenotype, which is characterized by an increased susceptibility to azoles and cell wall-damaging agents as well as decreased virulence, is consistent with previous findings for other pathogenic fungi, such as C. albicans (2-4, 27), C. neoformans (11, 18, 21), and A. fumigatus (9, 30).”
Quote in the paperNot a substantial claim0 of 9 sources checked- cites [2] source
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- cites [27] source
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- Premisecitation§ Abstract
Candida glabrata infections are often difficult to treat due in part to intrinsic or rapidly acquired resistance to azole antifungals.
“Infections caused by the opportunistic fungal pathogen Candida glabrata are often difficult to treat due in part to its intrinsic or rapidly acquired resistance to azole antifungals (25).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [25] source
Not checked in the free run.
- Interpretationreasoning§ Abstract
The regulatory mechanisms vary among fungal species.
“and that the regulatory mechanisms vary among fungal species.”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
The calcineurin-Crz1 pathway plays a role in the response to β-1,3-glucan defects in C. glabrata.
“These results suggest that the calcineurin-Crz1 pathway plays a role in the response to β-1,3-glucan defects”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
The loss of calcineurin results in attenuated virulence.
“The results from this assay indicate that the loss of calcineurin results in attenuated virulence”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
The C. glabrata Δcrz1 mutant displays a cell wall-associated phenotype intermediate to that of the calcineurin mutant.
“Although a mutant lacking the downstream transcription factor Crz1 displayed a cell wall-associated phenotype intermediate to that of the calcineurin mutant and was modestly attenuated in virulence, it did not show increased azole susceptibility.”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
Calcineurin also regulates a Crz1-independent pathway(s) in response to impaired chitin construction in C. glabrata.
“and that calcineurin also regulates a Crz1-independent pathway(s) in response to impaired chitin construction in C. glabrata.”
Quote in the paperSubstantial claim - Interpretationown data§ Abstract
Calcineurin is involved in azole tolerance via a Crz1-independent pathway in C. glabrata.
“These results suggest that calcineurin is involved in azole tolerance via a Crz1-independent pathway in C. glabrata.”
Quote in the paperSubstantial claim
- May combine two claims. 4
- Classified as probably not a substantial claim. 4
May combine two claims.
Findingown data§ AbstractDecreased numbers of CFU of the Δcrz1 strain were statistically significant in the kidney but not in the liver and spleen.
“Decreased numbers of CFU of the Δcrz1 strain were statistically significant in the kidney but not in the liver and spleen.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data§ AbstractThe C. glabrata Δcrz1 strain exhibited increased susceptibility to micafungin and Congo red but not to calcofluor white.
“In addition, the C. glabrata Δcrz1 strain exhibited increased susceptibility to micafungin and Congo red but not to calcofluor white.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ AbstractThe virulence of a Δcrz1 mutant is highly attenuated in Aspergillus fumigatus.
“Although the virulence of a Δcrz1 mutant is highly attenuated in A. fumigatus (7, 29)”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ AbstractAzole antifungals and calcineurin inhibitors have mild synergistic effects against C. glabrata wild-type strains.
“although it has been reported that azole antifungals and calcineurin inhibitors have mild synergistic effects against C. glabrata wild-type strains (8, 15, 22).”
Quote in the paperNot a substantial claim0 of 3 sources checkedClassified as probably not a substantial claim. May combine two claims.
Premisecitation§ AbstractCalcineurin is a heterodimer consisting of a catalytic A subunit and a Ca2+-binding regulatory B subunit, and the association between the two subunits is necessary for phosphatase activity.
“Calcineurin is a heterodimer consisting of a catalytic A subunit and a Ca2+-binding regulatory B subunit, and the association between the two subunits is necessary for phosphatase activity (19).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [19] source
Not checked in the free run.
Classified as probably not a substantial claim. May combine two claims.
Premisecitation§ AbstractCrz1 is a downstream effector of calcineurin and is involved in azole tolerance in Candida albicans.
“The transcription factor Crz1 is a downstream effector of calcineurin and is involved in azole tolerance in C. albicans (14, 23, 28);”
Quote in the paperSubstantial claim0 of 3 sources checked
The paper relies on this without support.
The antifungal activity of fluconazole is generally fungistatic.
“Although the antifungal activity of fluconazole is generally fungistatic, the drug was fungicidal for the Δcnb1 strain (Fig. 1).”
The paper relies on this without support.
A Crz1 homolog in C. glabrata has yet to be characterized.
“however, a Crz1 homolog in C. glabrata has yet to be characterized.”
The paper relies on this without support.
Very little is known about the calcineurin pathway in C. glabrata.
“To date, very little is known about the calcineurin pathway in C. glabrata, although it has been reported that azole antifungals and calcineurin inhibitors have mild synergistic effects against C. glabrata wild-type strains (8, 15, 22).”
The paper relies on this without support.
The involvement of calcineurin and Crz1 in virulence has not been reported in C. glabrata.
“To date, the involvement of calcineurin and Crz1 in virulence has not been reported in C. glabrata.”
The paper relies on this without support.
Growth at 37°C is a necessary prerequisite for comparing virulence levels.
“which is a necessary prerequisite for comparing virulence levels.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In C. glabrata, the effects of calcineurin were independent of Crz1.
“In C. glabrata, the effects of calcineurin were independent of Crz1 (27, 28).”
From Echinocandin tolerance and persistence <i>in vitro</i> are regulated by calcineurin signaling in <i>Candida glabrata</i> (2026) · cites this paper as [27]
The azole-susceptibility passage (labeled Abstract; page unavailable) says calcineurin acts through a Crz1-independent pathway for azole tolerance. But the cell-wall phenotype passage (also labeled Abstract) identifies a calcineurin–Crz1 pathway as well. The paper therefore supports independence for some effects, not calcineurin's effects generally. (LLM, conf=0.90)
Experimental — accuracy not yet measuredCalcineurin is a critical mediator of fungal cell wall stress responses and survival under antifungal pressure.
“The latter one, a highly conserved calcium/calmodulin‐dependent signaling cascade [17], is a critical mediator of fungal cell wall stress responses and survival under antifungal pressure [14, 18].”
From Calcineurin‐Dependent Stress Adaptation Enables Caspofungin Heteroresistance Leading to Stable Resistance in <i>Candida Glabrata</i> (2026) · cites this paper as [18]
In C. glabrata, both calcineurin and PKC signaling have been implicated in basal tolerance to echinocandins.
“In C. glabrata, both calcineurin and PKC signaling have been implicated in basal tolerance to echinocandins [48], [49], though the role of Hsp90 remains unknown as does the impact of any of these regulators on bona fide echinocandin resistance.”
From Global Analysis of the Evolution and Mechanism of Echinocandin Resistance in Candida glabrata (2012) · cites this paper as [49]
Calcineurin has been implicated in basal tolerance to echinocandins in C. glabrata.
“While calcineurin has been implicated in basal tolerance to echinocandins in C. glabrata [49], whether calcineurin affects bona fide resistance remains unknown.”
From Global Analysis of the Evolution and Mechanism of Echinocandin Resistance in Candida glabrata (2012) · cites this paper as [49]
Even in the absence of antifungals, calcineurin promotes virulence of C. glabrata in mouse models of invasive candidiasis through a mechanism potentially independent of Crz1.
“Even in the absence of antifungals, calcineurin also promotes virulence of C. glabrata in mouse models of invasive candidiasis through a mechanism that is potentially independent of Crz1 (27, 28).”
From Echinocandin tolerance and persistence <i>in vitro</i> are regulated by calcineurin signaling in <i>Candida glabrata</i> (2026) · cites this paper as [27]
Calcineurin signaling promotes virulence of C. glabrata, C. albicans, and other fungal pathogens in mouse models of systemic candidiasis.
“Calcineurin signaling promotes virulence of C. glabrata (27, 28), C. albicans (42, 50, 51), and other fungal pathogens (45, 52–54) in mouse models of systemic candidiasis.”
From Echinocandin tolerance and persistence <i>in vitro</i> are regulated by calcineurin signaling in <i>Candida glabrata</i> (2026) · cites this paper as [27]
Calcineurin signaling plays a pivotal role in the virulence of C. glabrata.
“Calcineurin signaling is also known to play a pivotal role in the virulence of C. glabrata [93,94].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [93]
Both calcineurin and PKC signaling have been implicated in echinocandin resistance in C. glabrata.
“Both calcineurin and PKC signaling have been implicated in echinocandin resistance in C. glabrata [93,103,106].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [93]
Components of calcineurin signaling are essential for maintenance of cell wall integrity.
“In addition, components of the calcineurin signaling have also been found to be essential for maintenance of the cell wall integrity [93,94].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [93]
Calcium signaling is essential for survival of azole treatment, and its absence has the potential to change fluconazole from fungistatic to fungicidal.
“Another study included calcium signaling as essential for the survival of azole treatment and its absence has the potential to change the character of fluconazole from fungistatic to fungicidal [103].”
From Evolutionary Emergence of Drug Resistance in Candida Opportunistic Pathogens (2018) · cites this paper as [103]
Calcineurin regulates both Crz1-dependent and independent pathways depending on the type of stress.
“thereby suggesting that calcineurin regulates both Crz1-dependent and independent pathways depending on the type of stress [99].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [99]
In the absence of Ca2+ signalling, fluconazole has a fungicidal rather than a fungistatic effect on Candida glabrata.
“in the absence of Ca2+ signalling, fluconazole has a fungicidal rather than a fungistatic effect on C. glabrata [99].”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [99]
Calcium signalling is necessary for the survival of azole stress in Candida glabrata.
“This result suggests that calcium signalling is necessary for the survival of azole stress in C. glabrata”
From Candida glabrata Biofilms: How Far Have We Come? (2017) · cites this paper as [99]
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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
Evolutionary Emergence of Drug Resistance in Candida Opportunistic Pathogens
Ksiezopolska, E., & Gabaldón, T. (2018) · Genes · doi:10.3390/genes9090461 · Cited by 230 · see citing works
Global Analysis of the Evolution and Mechanism of Echinocandin Resistance in Candida glabrata
Singh-Babak, S. D., Babak, T., Diezmann, S., Hill, J. A., Xie, J. L., Chen, Y.-L., Poutanen, S. M., Rennie, R. P., Heitman, J., & Cowen, L. E. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002718 · Cited by 204 · see citing works
Systematic functional profiling of transcription factor networks in Cryptococcus neoformans
Jung, K., Yang, D., Maeng, S., Lee, K.-T., So, Y.-S., Hong, J., Choi, J., Byun, H.-J., Kim, H., Bang, S., et al. (2015) · Nature Communications · doi:10.1038/ncomms7757 · Cited by 200 · see citing works
Fungal Resistance to Echinocandins and the MDR Phenomenon in Candida glabrata
Healey, K. R., & Perlin, D. S. (2018) · Journal of Fungi · doi:10.3390/jof4030105 · Cited by 194 · see citing works
Schwarzmüller, T., Ma, B., Hiller, E., Istel, F., Tscherner, M., Brunke, S., Ames, L., Firon, A., Green, B., Cabral, V., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004211 · Cited by 191 · see citing works
Calcineurin-Crz1 Signaling in Lower Eukaryotes
Thewes, S. (2014) · Eukaryotic Cell · doi:10.1128/ec.00038-14 · Cited by 152 · see citing works
Candida glabrata Biofilms: How Far Have We Come?
Rodrigues, C., Rodrigues, M., Silva, S., & Henriques, M. (2017) · Journal of Fungi · doi:10.3390/jof3010011 · Cited by 129 · see citing works
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
Juvvadi, P. R., Lamoth, F., & Steinbach, W. J. (2014) · Fungal Biology Reviews · doi:10.1016/j.fbr.2014.02.004 · Cited by 116 · see citing works
Intracellular survival ofCandida glabratain macrophages: immune evasion and persistence
Kasper, L., Seider, K., & Hube, B. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov042 · Cited by 115 · see citing works
Curcumin Targets Cell Wall Integrity via Calcineurin-Mediated Signaling in Candida albicans
Kumar, A., Dhamgaye, S., Maurya, I. K., Singh, A., Sharma, M., & Prasad, R. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01385-13 · Cited by 111 · see citing works
Calcineurin controls drug tolerance, hyphal growth, and virulence in Candida dubliniensis
Chen, Y.-L., Brand, A., Morrison, E. L., Silao, F. G. S., Bigol, U. G., Malbas, F. F., Nett, J. E., Andes, D. R., Solis, N. V., Filler, S. G., et al. (2011) · Eukaryotic Cell · doi:10.1128/ec.00310-10 · Cited by 107 · see citing works
Chow, E. W. L., Clancey, S. A., Billmyre, R. B., Averette, A. F., Granek, J. A., Mieczkowski, P. A., Cardenas, M. E., & Heitman, J. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006667 · Cited by 100 · see citing works
Chen, Y.-L., Konieczka, J. H., Springer, D. J., Bowen, S. E., Zhang, J., Silao, F. G. S., Bungay, A. A. C., Bigol, U. G., Nicolas, M. G., Abraham, S. N., et al. (2012) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.112.002279 · Cited by 97 · see citing works
Genetic Drivers of Multidrug Resistance in Candida glabrata
Healey, K. R., Jimenez Ortigosa, C., Shor, E., & Perlin, D. S. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01995 · Cited by 93 · see citing works
Drug resistance mechanisms and their regulation in non- albicans Candida species
Kołaczkowska, A., & Kołaczkowski, M. (2016) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkv445 · Cited by 88 · see citing works
Hosting Infection: Experimental Models to AssayCandidaVirulence
MacCallum, D. M. (2011) · International Journal of Microbiology · doi:10.1155/2012/363764 · Cited by 80 · see citing works
Dissection of Ire1 Functions Reveals Stress Response Mechanisms Uniquely Evolved in Candida glabrata
Miyazaki, T., Nakayama, H., Nagayoshi, Y., Kakeya, H., & Kohno, S. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003160 · Cited by 78 · see citing works
Self-citationZhang, T., Xu, Q., Sun, X., & Li, H. (2013) · Microbiological Research · doi:10.1016/j.micres.2012.11.006 · Cited by 75 · see citing works
Multilocus resistance evolution to azole fungicides in fungal plant pathogen populations
Mohd‐Assaad, N., McDonald, B. A., & Croll, D. (2016) · Molecular Ecology · doi:10.1111/mec.13916 · Cited by 73 · see citing works
The effect of antifungal resistance development on the virulence of Candida species
Bohner, F., Papp, C., & Gácser, A. (2022) · FEMS Yeast Research · doi:10.1093/femsyr/foac019 · Cited by 62 · see citing works
Chen, L., Tong, Q., Zhang, C., & Ding, K. (2018) · Current Genetics · doi:10.1007/s00294-018-0853-5 · Cited by 58 · see citing works
Gale, A. N., Sakhawala, R. M., Levitan, A., Sharan, R., Berman, J., Timp, W., & Cunningham, K. W. (2020) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.120.401595 · Cited by 56 · see citing works
Fungal resistance to echinocandins and the MDR phenomenon in Candida glabrata
Healey, K., & Perlin, D. S. (2018) · doi:10.20944/preprints201808.0306.v1 · Cited by 194 · see citing works
Song, J., Zhou, J., Zhang, L., & Li, R. (2020) · Microorganisms · doi:10.3390/microorganisms8101574 · Cited by 50 · see citing works
Endoplasmic reticulum stress and fungal pathogenesis
Krishnan, K., & Askew, D. S. (2014) · Fungal Biology Reviews · doi:10.1016/j.fbr.2014.07.001 · Cited by 46 · see citing works
Cao, Y., Du, M., Luo, S., & Xia, Y. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-014-5876-3 · Cited by 43 · see citing works
Progress and prospects for targeting Hsp90 to treat fungal infections
Veri, A. O., & Cowen, L. E. (2014) · Parasitology · doi:10.1017/s0031182013002072 · Cited by 43 · see citing works
Candida glabrata : a deadly companion?
Bolotin‐Fukuhara, M., & Fairhead, C. (2014) · Yeast · doi:10.1002/yea.3019 · Cited by 42 · see citing works
Hernández-Elvira, M., Torres‐Quiroz, F., Escamilla‐Ayala, A., Domínguez‐Martín, E., Escalante, R., Kawasaki, L., Ongay‐Larios, L., & Coria, R. (2018) · Cells · doi:10.3390/cells7080106 · Cited by 42 · see citing works
Chen, S. C.-A., Lewis, R. E., & Kontoyiannis, D. P. (2011) · Virulence · doi:10.4161/viru.2.4.16764 · Cited by 41 · see citing works
Tisi, R., Rigamonti, M. M., Groppi, S., & Belotti, F. (2016) · AIMS molecular science · doi:10.3934/molsci.2016.4.505 · Cited by 40 · see citing works
Yang, Y. Y., Xie, P., Li, Y., Bi, Y., & Prusky, D. (2022) · Journal of Fungi · doi:10.3390/jof8101082 · Cited by 39 · see citing works
On the Roles of Calcineurin in Fungal Growth and Pathogenesis
Chen, Y., Kozubowski, L., Cardenas, M. E., & Heitman, J. (2010) · Current Fungal Infection Reports · doi:10.1007/s12281-010-0027-5 · Cited by 39 · see citing works
Crz1p Regulates pH Homeostasis in Candida glabrata by Altering Membrane Lipid Composition
Yan, D., Lin, X., Qi, Y., Liu, H., Chen, X., Liu, L., & Chen, J. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.02186-16 · Cited by 37 · see citing works
Bairwa, G., Rasheed, M., Taigwal, R., Sahoo, R., & Kaur, R. (2014) · Biochemical Journal · doi:10.1042/bj20130757 · Cited by 36 · see citing works
Chen, X., Liu, Y., Keyhani, N. O., Xia, Y., & Cao, Y. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8290-9 · Cited by 32 · see citing works
Structure-guided approaches to targeting stress responses in human fungal pathogens
LeBlanc, E. V., Polvi, E. J., Veri, A. O., Privé, G. G., & Cowen, L. E. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.013731 · Cited by 31 · see citing works
Calcineurin: The Achilles’ heel of fungal pathogens
Yadav, V., & Heitman, J. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011445 · Cited by 29 · see citing works
Hosogaya, N., Miyazaki, T., Nagi, M., Tanabe, K., Minematsu, A., Nagayoshi, Y., Yamauchi, S., Nakamura, S., Imamura, Y., Izumikawa, K., et al. (2013) · FEMS Yeast Research · doi:10.1111/1567-1364.12043 · Cited by 28 · see citing works
Self-citationER stress response mechanisms in the pathogenic yeastCandida glabrataand their roles in virulence
Miyazaki, T., & Kohno, S. (2013) · Virulence · doi:10.4161/viru.27373 · Cited by 27 · see citing works
Self-citationAutophagy-Inducing Factor Atg1 Is Required for Virulence in the Pathogenic Fungus Candida glabrata
Shimamura, S., Miyazaki, T., Tashiro, M., Takazono, T., Saijo, T., Yamamoto, K., Imamura, Y., Izumikawa, K., Yanagihara, K., Kohno, S., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00027 · Cited by 25 · see citing works
Self-citationHistone Acetylation Regulator Gcn5 Mediates Drug Resistance and Virulence of Candida glabrata
Yu, S., Paderu, P., Lee, A., Eirekat, S., Healey, K., Chen, L., Perlin, D. S., & Zhao, Y. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00963-22 · Cited by 23 · see citing works
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
Self-citationCalcineurin-dependent contributions to fitness in the opportunistic pathogen <i>Candida glabrata</i>
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
Rosenwald, A., Arora, G. S., Ferrandino, R. M., Gerace, E. L., Mohammednetej, M., Nosair, W., Rattila, S., Subic, A. Z., & Rolfes, R. J. (2016) · G3 Genes Genomes Genetics · doi:10.1534/g3.116.032490 · Cited by 22 · see citing works
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
Self-citationClinical and Microbiological Characteristics of Candida guilliermondii and Candida fermentati
Hirayama, T., Miyazaki, T., Yamagishi, Y., Mikamo, H., Ueda, T., Nakajima, K., Takesue, Y., Higashi, Y., Yamamoto, Y., Kimura, M., et al. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02528-17 · Cited by 22 · see citing works
Self-citationYang, Y., Xie, P., Yuan, J., Liu, Y., Zhang, M., Li, Y., Bi, Y., & Prusky, D. (2022) · Postharvest Biology and Technology · doi:10.1016/j.postharvbio.2022.112064 · Cited by 21 · see citing works
Cen, Y., Timmermans, B., Souffriau, B., Thevelein, J. M., & Dijck, P. V. (2017) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2017.08.004 · Cited by 21 · see citing works
Wang, H., Gai, Y., Zhao, Y. F., Wang, M., & Ma, Z. (2022) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2022.105311 · Cited by 19 · see citing works
Candida auris biofilm: a review on model to mechanism conservation
Khari, A., Biswas, B., Gangwar, G., Thakur, A., & Puria, R. (2023) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2023.2179036 · Cited by 18 · see citing works
Lim, Y., & Lee, Y. (2020) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2020.103473 · Cited by 18 · see citing works
Functional characterization of the regulators of calcineurin in Candida glabrata
Miyazaki, T., Izumikawa, K., Nagayoshi, Y., Saijo, T., Yamauchi, S., Morinaga, Y., Seki, M., Kakeya, H., Yamamoto, Y., Yanagihara, K., et al. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00751.x · Cited by 17 · see citing works
Self-citationHad1 Is Required for Cell Wall Integrity and Fungal Virulence in Cryptococcus neoformans
Jung, W. H., Son, Y.-E., Oh, S., Fu, C., Kim, H., Kwak, J., Cardenas, M. E., Heitman, J., & Park, H.-S. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.300444 · Cited by 17 · see citing works
Cen, Y., Fiori, A., & Dijck, P. V. (2015) · Eukaryotic Cell · doi:10.1128/ec.00281-14 · Cited by 17 · see citing works
CRZ1 transcription factor is involved in cell survival, stress tolerance, and virulence in fungi
Gupta, S., Kumar, A., & Tamuli, R. (2022) · Journal of Biosciences · doi:10.1007/s12038-022-00294-3 · Cited by 16 · see citing works
Bhakt, P., Raney, M., & Kaur, R. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.102485 · Cited by 15 · see citing works
Nagayoshi, Y., Miyazaki, T., Shimamura, S., Nakayama, H., Minematsu, A., Yamauchi, S., Takazono, T., Nakamura, S., Yanagihara, K., Kohno, S., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180990 · Cited by 15 · see citing works
Self-citationMalik, A., Afaq, S., El-Gamal, B., Ellatif, M. E. A., Hassan, W. N., Dera, A. A., Noor, R., & Tarique, M. (2019) · Bioinformation · doi:10.6026/97320630015277 · Cited by 14 · see citing works
Ceballos-Garzón, A., Román, E., Plá, J., Pagniez, F., Amado, D., Alméciga-Díaz, C. J., Pape, P. L., & Parra‐Giraldo, C. M. (2022) · PLoS ONE · doi:10.1371/journal.pone.0265777 · Cited by 14 · see citing works
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
Filler, E. E., Liu, Y., Solis, N. V., Wang, L., Diaz, L. F., Edwards, J. E., Filler, S. G., & Yeaman, M. R. (2020) · Infection and Immunity · doi:10.1128/iai.00146-20 · Cited by 13 · see citing works
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
Self-citationNaskar, S., Prajapati, A., & Kaur, R. (2025) · FEMS Yeast Research · doi:10.1093/femsyr/foaf025 · Cited by 11 · see citing works
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
Self-citationCalcium signaling components in the human pathogenCryptococcus neoformans
Kmetzsch, L., Staats, C. C., Rodrigues, M. L., Schrank, A., & Vainstein, M. H. (2011) · Communicative & Integrative Biology · doi:10.4161/cib.4.2.14271 · Cited by 10 · see citing works
Echinocandin resistance in human pathogenic fungi
Munro, C. A. (2012) · Expert Review of Anti-infective Therapy · doi:10.1586/eri.11.171 · Cited by 9 · see citing works
Roles of Elm1 in antifungal susceptibility and virulence in Candida glabrata
Ito, Y., Miyazaki, T., Tanaka, Y., Suematsu, T., Nakayama, H., Morita, A., Hirayama, T., Tashiro, M., Takazono, T., Saijo, T., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66620-7 · Cited by 8 · see citing works
Self-citationKumari, S., Kumar, M., Esquivel, B. D., Wasi, M., Pandey, A. K., Khandelwal, N., Mondal, A. K., White, T. C., Prasad, R., & Gaur, N. A. (2022) · mBio · doi:10.1128/mbio.03545-21 · Cited by 8 · see citing works
Miranda, I. M., Gonçalves, M. F. M., Pinheiro, D., Hilário, S., Paiva, J. A., Guimarães, J. T., & Costa‐de‐Oliveira, S. (2025) · Journal of Fungi · doi:10.3390/jof11100716 · Cited by 7 · see citing works
Evolution of regulatory networks inCandida glabrata: learning to live with the human host
Roy, S., & Thompson, D. A. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov087 · Cited by 7 · see citing works
Lukumay, N. R., Li, Y., Wang, H., & Wei, W. (2025) · Virulence · doi:10.1080/21505594.2025.2569624 · Cited by 5 · see citing works
Chronic Fungal Infection, Up-to-date
Kakeya, H., IMAMURA, S., Miyazaki, T., Izumikawa, K., Yamamoto, Y., Tashiro, T., & Kohno, S. (2011) · Kansenshogaku zasshi · doi:10.11150/kansenshogakuzasshi.85.333 · Cited by 5 · see citing works
Self-citationHarrington, A. A., Nickels, T. J., & Cunningham, K. W. (2026) · mBio · doi:10.1128/mbio.02546-25 · Cited by 4 · see citing works
“Calcineurin signaling promotes virulence of C. glabrata (27, 28) , C. albicans (42, 50, 51), and other fungal pathogens (45, 52–54) in mouse models of systemic candidiasis.”
InfluentialWen, Z., Liu, J., Li, Y., Liu, S., & Nian, H. (2022) · Current Microbiology · doi:10.1007/s00284-022-02831-7 · Cited by 3 · see citing works
Su, Y., Li, Y., Xiao, M., Guo, D., Perlin, D. S., Shor, E., Xu, Y., & Li, Y. (2026) · Advanced Science · doi:10.1002/advs.76369 · Cited by 2 · see citing works
Yang, Y. Y., Xie, P., Nan, Y., Xu, X., Yuan, J., Li, Y., Bi, Y., & Prusky, D. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252211950 · Cited by 2 · see citing works
Ellagic Acid Combined with Tacrolimus Showed Synergistic Cell Growth Inhibition in Fission Yeast
Hagihara, K., Hosonaka, K., HOSHINO, S., Iwata, K., OGAWA, N., Satoh, R., Takasaki, T., Maeda, T., & Sugiura, R. (2022) · Biocontrol Science · doi:10.4265/bio.27.31 · Cited by 2 · see citing works
Uncovering actionable trade-offs of antifungal resistance in a yeast pathogen
Nunez‐Rodriguez, J. C., Schikora-Tamarit, M. À., & Gabaldón, T. (2026) · Molecular Systems Biology · doi:10.1038/s44320-025-00185-3 · 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
albicansated Signaling in Candida Curcumin Targets Cell Wall Integrity via
Singh, A., Sharma, M., Kumar, A., Dhamgaye, S., & Kumar, I. M. K. (2014)
The Roles of Hsp90 and Calcineurin in Antifungal Drug Resistance
Singh, S. (2012) · TSpace (University of Toronto)
Multidrug Resistance Transcriptional Regulatory Networks in Candida
Rogers, P. D., & Barker, K. S. (2014) · ASM Press eBooks · doi:10.1128/9781555817176.ch25
(2010) · Yeast · doi:10.1002/yea.1720
Dissemination of Candida auris Biofilms: A Medical Abrosia
Gangwar, G., Singh, B., & Puria, R. (2024) · Springer eBooks · doi:10.1007/978-981-97-4909-6_10
Cen, Y., Zhang, L.-L., Zhang, Z., Zhang, Y.-J., Lu, T.-X., Zhou, W.-Y., Xiang, C., Xue, Y., & Zheng, Y. (2025) · Biochemical Journal · doi:10.1042/bcj20253193
- Authors
- Miyazaki, T., Yamauchi, S., Inamine, T., Nagayoshi, Y., Saijo, T., Izumikawa, K., Seki, M., Kakeya, H., Yamamoto, Y., Yanagihara, K., Miyazaki, Y., & Kohno, S.
- Affiliations
- Nagasaki University (JP)
- National Institute of Infectious Diseases (JP)
- ORCID
- Venue
- Antimicrobial Agents and Chemotherapy
- Publisher
- American Society for Microbiology
- Published
- 2010-04
- Volume
- 54
- Issue
- 4
- Pages
- 1639-1643
- ISSN
- 0066-4804 (ISSN-L)
- 1098-6596
- PMC
- PMC2849377
- OpenAlex
- W2106090528
- Cited by
- 88
- References
- 31
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 4 · 2023: 2 · 2022: 11 · 2021: 1 · 2020: 7 · 2019: 3 · 2018: 6 · 2017: 7 · 2016: 7 · 2015: 4 · 2014: 9 · 2013: 6 · 2012: 5
- FWCI
- 4.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Antimicrobial Agents and Chemotherapy (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Nagasaki University's Academic Output SITE (Nagasaki University) (submittedVersion, cc-by-nc-nd)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (21390305)
- Japan Society for the Promotion of Science (19790324)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- calcineurin, Crz1, Candida glabrata, antifungal susceptibility, virulence, azole antifungals, cell wall stress, transcription factor regulation
- MeSH terms
- Animals, Antifungal Agents, Base Sequence, Candidiasis, DNA, Fungal, Female, Fungal Proteins, Genes, Fungal, Humans, Mice, Inbred BALB C, Microbial Sensitivity Tests, Mutation, Opportunistic Infections, Transcription Factors, Virulence, DNA Primers, Calcineurin, Drug Resistance, Fungal, Candida glabrata, Mice, In Vitro Techniques
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