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CRZ1 , a target of the calcineurin pathway in Candida albicans
Open accessAbstract
Summary: Calcineurin is a major player in calcium‐dependent signal transduction pathways of eukaryotes. Calcineurin acts on transcription factors (e.g. CRZ1 in Saccharomyces cerevisiae ) and governs the expression of genes in a species‐dependent fashion. In Candida albicans , the calcineurin pathway is involved in tolerance to antifungal agents, cation homeostasis and virulence. However, the components of the calcineurin pathway are still poorly investigated in this yeast species. Taking S. cerevisiae as a model to reconstitute this pathway, two CRZ1 ‐like genes, CRZ1 and CRZ2 (for c alcineurin‐ r esponsive z inc finger 1 and 2 genes), were found with C 2 H 2 zinc finger domains. Only CRZ1 was able to restore the calcium hypersusceptibility of a S. cerevisiae crz1 Δ mutant and to mediate calcium‐dependent gene expression in this yeast species. Several experiments showed that CRZ1 was dependent on calcineurin in C. albicans : (i) phenotypic analysis of a crz1 Δ/Δ mutant showed impaired growth as compared with the wild type in the presence of cations (Ca 2+ , Mn 2+ ) as does a mutant lacking calcineurin subunit A ( cna Δ/Δ) and (ii) a green fluorescent protein (GFP)–Crz1p fusion protein showed a calcium‐ and calcineurin‐dependent nuclear localization. To further analyse the relationship between calcineurin and CRZ1 , a comprehensive analysis of calcineurin/Crz1p‐dependent gene expression following addition of Ca 2+ (200 mM) was performed. Among the expression of 264 genes altered by at least twofold, the upregulation of 60 genes was dependent on both calcineurin and CRZ1 . Interestingly, a motif [5′‐G(C/T)GGT‐3′] with similarity to the target sequence of Crz1p (GNGGCG/TCA) from S. cerevisiae was identified as a putative regulatory sequence in the upstream regions of these calcineurin/Crz1p‐dependent genes. However, additional experiments showed that calcineurin may have other targets in addition to CRZ1 . First, CRZ1 was not involved in tolerance to antifungal agents (fluconazole, terbinafine) on the opposite to calcineurin. Second, CRZ1 was only moderately influencing virulence in a mice model of infection which is in sharp contrast to the strong avirulence of cna Δ/Δ mutant in the same animal model. Even though this work establishes CRZ1 as a calcineurin target, further studies are needed to identify other calcineurin‐dependent elements in C. albicans .
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TL;DR
This study identifies *Candida albicans* CRZ1 as a calcineurin-responsive transcription factor and functional homologue of *S. cerevisiae* Crz1p, showing calcium- and calcineurin-dependent nuclear localization and regulation of a large subset of calcium-activated genes. However, CRZ1 does not account for all calcineurin-dependent phenotypes, especially antifungal tolerance and full virulence, indicating additional calcineurin targets.
Key findings
- Among two *CRZ1*-like genes, only *CRZ1* complemented the calcium hypersensitivity of a *S. cerevisiae crz1Δ* mutant and activated CDRE-dependent reporter expression in a calcium- and FK506-sensitive manner; *CRZ2* did not.
- A *C. albicans crz1Δ/Δ* mutant showed impaired growth on Ca²⁺ and Mn²⁺ but not Li⁺, was less susceptible than *cnaΔ/Δ*, and unlike *cnaΔ/Δ* retained tolerance to terbinafine; *CRZ2* deletion produced no tested phenotype.
- GFP-Crz1p localized to the nucleus after calcium exposure and remained cytosolic with FK506; protein A-Crz1p showed calcium- and calcineurin-dependent mobility shifts, consistent with post-translational modification.
- Microarray analysis of 6039 genes found 264 calcium-regulated genes (≥2-fold), of which 69 were calcineurin-dependent and 65 Crz1p-dependent; 60 genes were regulated by both. A putative CDRE-like motif [5′-G(C/T)GGT-3′] was enriched in their promoters, and mutation of the *UTR2* promoter CDRE-like sequence abolished calcium induction.
- In mice, wild-type infection killed all mice within 9 days, *cnaΔ/Δ* mice survived 30 days, and *crz1Δ/Δ* infection led to 30% survival at 30 days; kidney burdens at day 3 were approximately 10⁶ cfu g⁻¹ for wild type/revertant, 10² for *cnaΔ/Δ*, and 10⁴ for *crz1Δ/Δ*.
Methods
- *C. albicans* CRZ1 and CRZ2 were disrupted using the Ura-blaster strategy; complementation and CDRE reporter assays were performed in *S. cerevisiae*.
- Crz1p localization and modification were assayed with GFP- and protein A-tagged fusions under inducible or constitutive promoters, with calcium and FK506 treatments.
- Genome-wide expression profiling used *C. albicans* cDNA microarrays covering 6039 genes after 200 mM CaCl₂ exposure at 20, 40, and 60 min in wild-type, *cnaΔ/Δ*, and *crz1Δ/Δ* strains; data were analyzed with ANOVA, twofold thresholds, and GeneSpring clustering.
- Virulence was tested in a BALB/c mouse intravenous infection model with groups of 10 mice, survival monitoring for 30 days, and tissue burden counts in kidneys and spleen.
Limitations
- The paper states that further studies are needed to identify other calcineurin-dependent elements in *C. albicans*, because CRZ1 did not explain calcineurin-dependent antifungal tolerance or full virulence.
- The paper notes that the identity of the Crz1p post-translational modifications was not determined and that the precise NLS/NES and possible calcineurin docking motif require further analysis.
- The paper acknowledges that virulence results differ from another study (Onyewu et al., 2004) and suggests possible explanations including strain background, URA3 positional effects, and starting inoculum; evident from the text, the microarray analysis used a single calcium concentration and three time points, so other conditions or targets may be missed.
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94 Own result · 34 Own interpretation · 20 Not checked yet · 8 Own method · 5 No basis given
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“which is in sharp contrast to the strong avirulence of cna D / D mutant in the same animal model.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“Among the expression of 264 genes altered by at least twofold, the upregulation of 60 genes was dependent on both calcineurin and CRZ1 .”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“and to mediate calcium-dependent gene expression in this yeast species.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“Only CRZ1 was able to restore the calcium hypersusceptibility of a S. cerevisiae crz1 D mutant”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“a motif [5 ¢ -G(C/T)GGT-3 ¢ ] with similarity to the target sequence of Crz1p (GNGGCG/TCA) from S. cerevisiae was identified as a putative regulatory sequence in the upstream regions of these cal-cineurin/Crz1p-dependent genes.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“CRZ1 was only moderately influencing virulence in a mice model of infection”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“phenotypic analysis of a crz1 D / D mutant showed impaired growth as compared with the wild type in the presence of cations (Ca 2 + , Mn 2 + )”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“two CRZ1 -like genes, CRZ1 and CRZ2 (for calcineurin-responsive zinc finger 1 and 2 genes), were found with C 2 H 2 zinc finger domains.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“The addition of FK506 to S. cerevisiae cells expressing C. albicans CRZ1 gene abolished calcium responsiveness”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Identification of a C. albicans functional homologue to CRZ1 of S. cerevisiae
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“Among the 6039 genes monitored in the microarray experiments, expression of 264 genes (4.4% of total genome) was altered at least twofold in one of the three WT experiments at time points of 20, 40 and 60 min.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Genome-wide analysis of the calcineurin-activated genes in the presence of calcium
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“This domain was identified in the three different ORFs (orf19.7359,orf19.2356and orf19.9892)and therefore indicates that these ORFs are putative transcription factors.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Identification of a C. albicans functional homologue to CRZ1 of S. cerevisiae
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“CRZ1 was not involved in tolerance to antifungal agents (fluconazole, terbinafine) on the opposite to calcineurin.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Abstract
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“In YEPD medium, the crz1∆/∆ mutant and the wild type showed similar colony appearance in contrast to the cna∆/∆ mutant which formed wrinkled colonies (Fig. 2, first row).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
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“Fluconazole susceptibility was slightly increased by the deletion of one or two CRZ1 copies as compared with the wild type but not to the extent of the cna∆/∆ mutant (Fig. 1A, bottom, lanes 1, 2 and 4)”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
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“Crz1p ∆C and Crz1p ∆232-322 were both localized constitutively in the nucleus (Fig. 3A)”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Crz1p is localized in the nucleus in a calcium-and calcineurin-dependent manner
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“the crz1∆/∆ strain was affected in colony morphology as compared with the wild type but not to the same extent as the cna∆/∆ mutant.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
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“Among genes with known or putative functions, five were involved in cell wall organization (UTR2, ECM331, GSL21, IPF19968 and PMT2), three in cellular organization (AKR1, SAC6.5F and IPF13784), five in cellular transport and homeostasis (CCH1, RTA2, YIP3.3, ENA21.3 and VPS1), seven in cell metabolism and six in protein fate (see Table 3).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Genome-wide analysis of the calcineurin-activated genes in the presence of calcium
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“kidneys from mice infected with the wild type or the CRZ1 revertant contained similar colony-forming units (cfu) (approximately 10 6 cfu g -1 ), whereas those from the cna∆/∆ and crz1∆/∆ mutants contained about 10 2 and 10 4 cfu g -1 respectively (Table 1).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Virulence of the C. albicans crz1∆/∆ mutant in the mice model of infection
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“In the presence of 10 µg ml -1 terbinafine, the crz1∆/∆ mutant showed the same growth pattern as the wild type, whereas cna∆/∆ mutant was not able to grow (Fig. 1A, bottom, lanes 1, 2 and 4).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
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“This region contains a motif rich in guanine (5′-GGGCT-3′) conserved in the CDRE of S. cerevisiae (Fig. 8, bottom) and similar to the motif found in the promoters of the 60 calcineurin/Crz1p-dependent genes [5′-G(C/T)GGT-3′] by genome-wide analysis.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Calcineurin-and Crz1p-dependent regulation of UTR2
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“while the cna∆/∆ mutant was rapidly killed in the presence of terbinafine, the crz1∆/∆ mutant was still able to grow in the presence of this substance.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
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“Only CRZ1 but not CRZ2 from C. albicans was restoring in S. cerevisiae a wild-type phenotype in the presence of calcium (Fig. S1 in Supplementary material)”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Identification of a C. albicans functional homologue to CRZ1 of S. cerevisiae
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“the growth of the crz1∆/∆ mutant was severely impaired by Ca 2+ , Mn 2+ but not Li + (Fig. 1A, top, lane 4).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
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“Only nine and five genes were strictly calcineurin-or Crz1pdependent respectively (Table 3).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Genome-wide analysis of the calcineurin-activated genes in the presence of calcium
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“As shown in Fig. 8 (top), lacZ reporter activity was increased approximately by 3.5-fold in a wild-type strain after 2 h exposure to 200 mM of calcium, whereas this induction was decreased to 2.2-fold in a strain lacking CRZ1 and almost absent (1.1-fold) in the cna∆/∆ mutant.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Calcineurin-and Crz1p-dependent regulation of UTR2
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“The highest frequency of each base occurring at each position was shown: 95% of possible bases at the position 1 correspond to a G, 35% at the position 2 can be at equal probability a C or a T, 75% at the position 3 correspond to a G, 93% at the position 4 to a G and 62% at the position 5 to a T.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Calcineurin-and Crz1p-dependent regulation of UTR2
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“the number of genes with at least a twofold expression ratio reached a maximum at 20 min (176 genes), decreased at 40 min (82 genes) and increased at 60 min (162 genes) (Fig. 6A).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Genome-wide analysis of the calcineurin-activated genes in the presence of calcium
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“In cna∆/∆ and crz1∆/∆ mutant strains, the tested genes were not regulated by calcium and therefore confirmed their calcineurin/Crz1p-dependent regulation”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Genome-wide analysis of the calcineurin-activated genes in the presence of calcium
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“The expression profiles of 264 calcium-regulated genes exhibiting a twofold or greater change were clustered with experiments carried out with the crz1∆/∆ or cna∆/∆ C. albicans strains at 20, 40 and 60 min time points (see Table2for experiment details).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Normalization control.
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“List of common genes regulated by calcineurin in the presence of calcium between S. cerevisiae and C. albicans.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Normalization control.
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“Finally, virulence phenotypes between the crz1∆/∆ and cna∆/∆ mutants were not identical: while calcineurin is essential for virulence in a mice model of infection, CRZ1 has only a moderate effect (Fig. 5).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
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“Moreover, the crz1∆/∆ mutant could survive to terbinafine exposure as demonstrated by time-kill curves (Fig. 2B), which is in strong contrast with the lack of terbinafine tolerance of the cna∆/ ∆ mutant as described (Sanglard et al., 2003).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
What the sources say
- Not checked yetcites Sanglard et al., 2003
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“The CCH1 gene is present in the C. albicans genome and shares 55% of similarity with S. cerevisiae.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
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In the paper
“In addition, the crz1∆/∆ was able to grow on serum-containing agar (Fig. 3), a feature contrasting with the lack of survival of the cna∆/∆ in this medium which was established earlier (Blankenship et al., 2003;Sanglard et al., 2003).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
What the sources say
- Not checked yetcites Blankenship et al., 2003
- Not checked yetcites Sanglard et al., 2003
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“The vast majority of calcineurin-dependent genes have a Crz1p-dependent expression, thus suggesting that Crz1p is a major mediator of calcineurin-activated gene expression in yeast (Yoshimoto et al ., 2002).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Yoshimoto et al., 2002
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“Crz1p contains a C 2 H 2 zinc finger motif that binds to a specific element on the promoter of genes called CDRE (calcineurin-dependent response element) shown to be sufficient for Ca 2 + -and calcineurin-dependent gene expression (Stathopoulos and Cyert, 1997).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Stathopoulos and Cyert, 1997
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“cyclosporin A and tracolimus form complexes with cyclophilin A and FKBP12 (FK506-binding protein 12) respectively.These immunosuppressant drugreceptor complexes bind calcineurin and inhibit its enzymatic activity (Liu et al ., 1991).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Liu et al., 1991
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“In response to increased Ca 2 + , activated calcineurin dephosphorylates Crz1p, thus leading to its nuclear localization (Stathopoulos-Gerontides et al ., 1999).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Stathopoulos-Gerontides et al., 1999
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“In C. albicans , recent reports revealed the involvement of calcineurin in antifungal tolerance, cell morphogenesis and virulence.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Bader et al., 2003
- Not checked yetcites Blankenship et al., 2003
- Not checked yetcites Sanglard et al., 2003
plaincorrelational- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“Calcineurin is a Ca 2 +calmodulin-dependent serine/threonine phosphatase consisting of a catalytic A subunit and a regulatory B subunit.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Rusnak and Mertz, 2000
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“Using DNA microarrays, calcineurin activation induces 153 genes involved in cell wall biosynthesis, ion homeostasis, vesicle trafficking, lipid synthesis and protein degradation.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Introduction
What the sources say
- Not checked yetcites Yoshimoto et al., 2002
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Taken together, these observations indicated that both CRZ1 and CNA regulate cation homeostasis.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“These findings demonstrate that, unlike the avirulence of the cna∆/∆ strain, CRZ1 was partially involved in virulence.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Virulence of the C. albicans crz1∆/∆ mutant in the mice model of infection
boostedconditionaln = 5- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Taken together, these observations suggest that CRZ1 has impact on colony morphology, but also indicate only a partial overlap with phenotypes dependent on calcineurin.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Phenotypic analysis of C. albicans CRZ1 and CRZ2 mutant strains
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“the functional assays performed in S. cerevisiae strongly supported that CRZ1 from C. albicans is the functional homologue of CRZ1 but not CRZ2.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Identification of a C. albicans functional homologue to CRZ1 of S. cerevisiae
boosted- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The obtained strains were also verified by Southern blot for the expected genomic integration and CRZ1 copy number (data not shown).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Virulence of the C. albicans crz1∆/∆ mutant in the mice model of infection
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“These results therefore suggest that Crz1p is localized in the nucleus in the presence of calcium and that this localization is dependent on calcineurin activity.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Crz1p is localized in the nucleus in a calcium-and calcineurin-dependent manner
hedgeddirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The phenotypes of strains constructed for virulence assays (cation and drug susceptibility, colony morphology) were identical to those of strains used in the first part of this study.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Virulence of the C. albicans crz1∆/∆ mutant in the mice model of infection
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As Crz1p is not involved in the survival of C. albicans in the presence of antifungals, the C. albicans Cch1p could be a potential calcineurin target that could explain the fungicidal effect of fluconazole in a strain lacking calcineurin activity and therefore a fully functional CCS.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
hedgedconditional- Asserted: fails — The authors may not put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The authors may not put it forward as true. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“In S. cerevisiae it is well known that calcineurin has several substrates in addition to Crz1p not belonging to transcriptional activators (Cyert, 2001;2003).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
What the sources say
- Not checked yetcites Cyert, 2001;2003
boosted- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Animal experiments were carried out at the CHUV animal facility and were approved by the local ethical committee.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Animal experiments
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“In order to determine a significant threshold in expression ratio, a LOWESS normalization was performed only on the TEF3 spots, TEF3 being an housekeeping gene.The significant threshold was considered above the most modulated TEF3 hybridization signals.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Normalization control.
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Dye swap controls were replaced by WTvsCNA and WTvsCRZ experiments as described above in which cDNA from the wild type exposed to calcium was labelled with Cy-3 instead of Cy-5 as it is the case in the WT experiment (Table 2).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Experimental design.
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This comparison suggests a speciesspecific calcineurin-dependent gene activation, which could result from the role of calcineurin in the adaptation of the organism to its environmental niche.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Calcineurin-and Crz1p-dependent gene expression overlap via a putative regulatory element
hedgedconditional- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
In the paper
“In this yeast species, Crz1p is shuffling from the cytoplasm to the nucleus after post-translational modifications dependent on calcineurin.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > CRZ1 as a calcineurin downstream target
What the sources say
- Not checked yetcites Santos and de Larrinoa, 2005
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As in S. cerevisiae, calcineurin can act on other proteins by post-translational modifications in C. albicans.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: fails — The paper may give no reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.
In the paper
“As calcineurin activity in C. albicans is required for multiple functions important for survival in the host and among them the most relevant are virulence and tolerance to antifungal agents (Sanglard et al., 2003)”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Targets of calcineurin in C. albicans
What the sources say
- Not checked yetcites Sanglard et al., 2003
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: passes — The paper’s conclusions depend on it.
- Based: passes — The paper gives a reason why it holds.
It may state two separate claims as one.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“Samples of inoculum suspensions were plated onto YEPD agar to confirm the accuracy of the infection dose.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Animal experiments
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
What the paper did — it cites no source for this, so there is none to check. The quote shows it is in the paper.
In the paper
“The microarray covers nearly 98% of the total number of C. albicans genes and includes 27 control genes in each block, including, for example, negative controls (intergenic regions), crosshybridization controls (S.cerevisiae genes) and dynamic range controls by a serial dilution of TEF3 gene from 1 to 1/32.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Microarray experiments
plain- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“Recent microarray experiments performed in C. albicans under different pH conditions governed by the Rim101pdependent pathway revealed that CRZ2 was downregulated by Rim101p in alkaline pH (Bensen et al., 2004).”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > CRZ1 as a calcineurin downstream target
What the sources say
- Not checked yetcites Bensen et al., 2004
plaindirect- Asserted: passes — The authors put it forward as true.
- Checkable: passes — It can be checked against evidence.
- Load-bearing: fails — The paper’s conclusions may not depend on it.
- Based: passes — The paper gives a reason why it holds.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
The paper relies on this without support.
The components of the calcineurin pathway are still poorly investigated in C. albicans.
“However, the components of the calcineurin pathway are still poorly investigated in this yeast species.”
The authors state this as an assumption.
The NLS is localized between residues 2 and 207 of Crz1p.
“it can be assumed that the NLS is localized between residues 2 and 207.”
The paper relies on this without support.
Calcium activates the calcineurin signalling pathway in C. albicans.
“As calcium is a classical activator of calcineurin activity, this cation was used as an effector to mimic the activation of the calcineurin signalling pathway in C. albicans.”
The paper relies on this without support.
The C. albicans cdr1∆/∆ cdr2∆/∆ mutant strain (DSY1025) allows optimal oestradiol-inducible transcriptional activation of the different fusion proteins.
“All plasmids were used to transform a C. albicans cdr1∆/∆ and cdr2∆/∆ mutant strain (DSY1025) to allow optimal oestradiol-inducible transcriptional activation of the different fusion proteins.”
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?
The cited source doesn’t support the claim as written.
In the citing paper
“Crz1 is the key mediator of calcineurin-dependent transcriptional responses [37],[41] and is implicated in tolerance to azoles in both S. cerevisiae and C. albicans [20],[42].”
From Hsp90 Governs Echinocandin Resistance in the Pathogenic Yeast Candida albicans via Calcineurin (2009) · cites this paper as [37]
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredThe cited source doesn’t support the claim as written.
In the citing paper
“The transcription factor Crz1 is a downstream effector of calcineurin and is involved in azole tolerance in C. albicans (14, 23, 28);”
From Roles of Calcineurin and Crz1 in Antifungal Susceptibility and Virulence of Candida glabrata (2010) · cites this paper as [14]
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“As expected, exposure of cells containing the UTR2-lacZ reporter to calcium chloride resulted in activation of calcineurin relative to the untreated control (P<0.001, ANOVA, Bonferroni's Multiple Comparison Test Figure 4C).”
From Hsp90 Governs Echinocandin Resistance in the Pathogenic Yeast Candida albicans via Calcineurin (2009) · cites this paper as [37]
The cited source says what the claim attributes to it.
In the citing paper
“Calcineurin also promoted tolerance to terbinafine in C. albicans (58), to tunicamycin and dithiothreitol in S. cerevisiae (59, 60), and to SDZ 90-215 in all these species (61).”
From Echinocandin tolerance and persistence in vitro are regulated by calcineurin signaling in Candida glabrata (2026) · cites this paper as [58]
In the citing paper
“this mutation has little effect on virulence in both C. albicans (14, 23) and C. glabrata (Fig. 3).”
From Roles of Calcineurin and Crz1 in Antifungal Susceptibility and Virulence of Candida glabrata (2010) · cites this paper as [14]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Rated major: it would touch a result — a value a result rests on, reported and recomputed p-values on opposite sides of the significance level, two passages that conflict with no sign which is right, or a cited work retracted before this paper was published.
In the paper
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Virulence of the C. albicans crz1∆/∆ mutant in the mice model of infection
“In contrast, at days 3 and 9 after infection, no cna∆/∆ mutant cell could be recovered both in kidney and in spleen.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Normalization control.
“| cna∆/∆ | 5 | 3.3 ± 0.1 | < 2.0 b | < 2.0 | < 2.0 | < 2.0 | < 2.0 |”
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
“These data therefore confirm that the 24 bp sequence localized between -384 and -363 can possess the regulatory element responsible for calcium induction.”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Calcineurin-and Crz1p-dependent regulation of UTR2
Reported 24 · recomputed 21
Rated minor: it would not touch a result — a value no result rests on, a p-value that stays on the same side of the significance level, or a conflict that is clerical, resolved elsewhere in the paper, or outside its own findings.
In the paper
“Two fragments of 500 bp corresponding to the 5′-and 3′-flanking regions of UTR2 (sequence from nt -1550 to -1050 and +1014 to +1564, respectively, with respect to the first ATG)”
§ CRZ1 , a target of the calcineurin pathway in Candida albicans > Construction of UTR2-lacZ fusions
Reported 500 · recomputed 550
Citations
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Fonzi, W. A., & Irwin, M. Y. (1993) · Genetics · doi:10.1093/genetics/134.3.717 · Cited by 1,695
Calcineurin: Form and Function
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Resistance of Candida species to fluconazole
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Self-citationResistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences
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Calcineurin is required for virulence of Cryptococcus neoformans
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Research works printed but not linked: 1
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Cited by
Sorted by citations
The Fungal Cell Wall: Structure, Biosynthesis, and Function
Gow, N. A. R., Latge, J.-P., & Munro, C. A. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0035-2016 · Cited by 1,423
Efflux-Mediated Antifungal Drug Resistance
Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Baret, P. V., Keniya, M. V., Tanabe, K., Niimi, M., Goffeau, A., & Monk, B. C. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00051-08 · Cited by 608
Hsp90 Governs Echinocandin Resistance in the Pathogenic Yeast Candida albicans via Calcineurin
Singh, S. D., Robbins, N., Zaas, A. K., Schell, W. A., Perfect, J. R., & Cowen, L. E. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000532 · Cited by 362
“We used a strain harboring a construct with the UTR2 promoter, which contains a CDRE element and is regulated by calcineurin [37], fused to lacZ and integrated at the UTR2 locus [40].”
BackgroundMethodLaFayette, S. L., Collins, C., Zaas, A. K., Schell, W. A., Betancourt-Quiroz, M., Gunatilaka, A. A. L., Perfect, J. R., & Cowen, L. E. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001069 · Cited by 329
Fitness Trade-offs Restrict the Evolution of Resistance to Amphotericin B
Vincent, B. M., Lancaster, A. K., Scherz-Shouval, R., Whitesell, L., & Lindquist, S. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001692 · Cited by 322
“These include targets of the known HSP90 client calcineurin [30,33], as well as genes involved in the response to iron starvation or oxidative stress, two stresses tightly linked to membrane sterol homeostasis.”
BackgroundHarnessing calcineurin as a novel anti-infective agent against invasive fungal infections.
Steinbach, W. J., Reedy, J. L., Cramer, R. A., Perfect, J. R., & Heitman, J. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1680 · Cited by 313
Hsp90 Orchestrates Temperature-Dependent Candida albicans Morphogenesis via Ras1-PKA Signaling
Shapiro, R. S., Uppuluri, P., Zaas, A. K., Collins, C., Senn, H., Perfect, J. R., Heitman, J., & Cowen, L. E. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.017 · Cited by 311
The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype.
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Metadata
- Authors
- Karababa, M., Valentino, E., Pardini, G., Coste, A. T., Bille, J., & Sanglard, D.
- Affiliations
- Centre Hospitalier Universitaire Vaudois (CH)
- Corresponding author
- Sanglard, Dominique
- Venue
- Molecular Microbiology
- Publisher
- Wiley
- Published
- 2006-01-20
- Volume
- 59
- Issue
- 5
- Pages
- 1429-1451
- ISSN
- 0950-382X (ISSN-L)
- 1365-2958
- OpenAlex
- W1557800963
- Semantic Scholar
- a3d8b4bef12bfb3e470306f4cf4502a61002bff7
- Cited by
- 231
- References
- 60
- Citations by year
- 2026: 13 · 2025: 6 · 2024: 3 · 2023: 11 · 2022: 15 · 2021: 14 · 2020: 11 · 2019: 6 · 2018: 10 · 2017: 11 · 2016: 11 · 2015: 7 · 2014: 16 · 2013: 9 · 2012: 15
- FWCI
- 6.35
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- Crz1, calcineurin, Candida albicans, calcium signaling, transcriptional regulation, C2H2 zinc finger, antifungal drug tolerance, cation homeostasis, virulence, nuclear localization, gene expression, Saccharomyces cerevisiae model, fluconazole resistance
- MeSH terms
- Animals, Antifungal Agents, Calcium, Candida albicans, Candidiasis, Cell Nucleus, Female, Fungal Proteins, Glycoside Hydrolases, Mice, Inbred BALB C, Mutation, Regulatory Sequences, Nucleic Acid, Virulence, Signal Transduction, Gene Expression Regulation, Fungal, Zinc Fingers, Genome, Fungal, Calcineurin, Saccharomyces cerevisiae Proteins, Intracellular Signaling Peptides and Proteins, Mice
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