Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence

Reedy, Jennifer L.; Filler, Scott G.; Heitman, Joseph

doi:10.1016/j.fgb.2009.09.002

Cited by 76Fungal and yeast genetics researchAntifungal resistance and susceptibilitySignaling Pathways in Disease

Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence

Open access

Reedy, Jennifer L., Filler, Scott G., Heitman, Joseph·2010·Fungal Genetics and Biology

DOI 10.1016/j.fgb.2009.09.002PMC PMC2815136

Open this paper in CoChat — free account

Abstract

The protein phosphatase calcineurin is a key mediator of virulence and antifungal susceptibility of multiple fungal pathogens including Candida albicans, Cryptococcus neoformans, and Aspergillus fumigatus, and has clinical potential as a therapeutic target to increase the efficacy of the current antifungal armamentarium. Despite the importance of this signaling pathway, few components of the calcineurin-signaling pathway are known in C. albicans. Here we identified and analyzed additional components of the C. albicans calcineurin cascade, including the RCN1 (regulator of calcineurin1), MID1, and CCH1 genes, which mediate calcineurin functions in other species. When heterologously expressed in Saccharomyces cerevisiae, C. albicans Rcn1 inhibited calcineurin function. Although rcn1/rcn1, mid1/mid1, and cch1/cch1 mutant strains share some phenotypes with calcineurin mutants, they do not completely recapitulate the phenotypes of a calcineurin mutant strain. These studies extend our understanding of the C. albicans calcineurin signaling cascade and its host-niche specific role in virulence.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.fgb.2009.09.002

Cites

72 of 72 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Genes involved in several pathways, including calcineurin and PKC signaling, primarily affected FoG and not RAD.
“Consistent with the adjuvant drug responses, genes involved in several pathways, including calcineurin 53 and PKC signaling 44 , primarily affected FoG and not RAD (Fig. 4d, Supplementary Fig. 8, detailed information on genes tested in Supplementary Notes 2-4 and Supplementary Tables 2 and 3).”
From Antifungal tolerance is a subpopulation effect distinct from resistance and is associated with persistent candidemia (2018) · cites this paper as [53]
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation
Clipstone, N. A., & Crabtree, G. R. (1992) · Nature · doi:10.1038/357695a0 · Cited by 1,635 · see citing works
Candida and candidosis
Odds, F. C. (1979) · Medical Entomology and Zoology · Cited by 1,297 · see citing works
Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations
Gillum, A. M., Tsay, E. Y. H., & Kirsch, D. R. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00328721 · Cited by 1,253 · see citing works
Ca 2+ -Induced Apoptosis Through Calcineurin Dephosphorylation of BAD
Wang, H., Pathan, N., Ethell, I. M., Krajewski, S., Yamaguchi, Y., Shibasaki, F., McKeon, F., Bobo, T., Franke, T. F., & Reed, J. C. (1999) · Science · doi:10.1126/science.284.5412.339 · Cited by 1,132 · see citing works
A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber typePreprint
Chin, E. R., Olson, E. N., Richardson, J. A., Yang, Q., Humphries, C. G., Shelton, J. M., Wu, H., Zhu, W., Bassel‐Duby, R., & Williams, R. S. (1998) · Genes & Development · doi:10.1101/gad.12.16.2499 · Cited by 1,015 · see citing works
The changing face of candidemia: emergence of non-Candida albicans species and antifungal resistance
Hong Nguyen, M., Peacock, J. E., Morris, A. J., Tanner, D. C., Nguyen, M. L., Snydman, D. R., Wagener, M. M., Rinaldi, M. G., & Yu, V. L. (1996) · The American Journal of Medicine · doi:10.1016/s0002-9343(95)00010-0 · Cited by 758 · see citing works
The SAT1 flipper, an optimized tool for gene disruption in Candida albicans
Reuß, O., Vik, Å., Kolter, R., & Morschhäuser, J. (2004) · Gene · doi:10.1016/j.gene.2004.06.021 · Cited by 744 · see citing works
Calcineurin: a calcium- and calmodulin-binding protein of the nervous system.
Klee, C. B., Crouch, T. H., & Krinks, M. H. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6270 · Cited by 738 · see citing works
Non-albicans Candida spp. causing fungaemia: pathogenicity and antifungal resistance
Krcmery, V., & Barnes, A. J. (2002) · Journal of Hospital Infection · doi:10.1053/jhin.2001.1151 · Cited by 733 · see citing works
Generic Signals and Specific Outcomes
Crabtree, G. R. (1999) · Cell · doi:10.1016/s0092-8674(00)80571-1 · Cited by 730 · see citing works
The Mechanism of Action of Cyclosporin A and FK506
Ho, S. N., Clipstone, N. A., Timmermann, L., Northrop, J. P., Graef, I. A., Fiorentino, D. F., Nourse, J., & Crabtree, G. R. (1996) · Clinical Immunology and Immunopathology · doi:10.1006/clin.1996.0140 · Cited by 676 · see citing works
New and emerging yeast pathogens
Hazen, K. C. (1995) · Clinical Microbiology Reviews · doi:10.1128/cmr.8.4.462 · Cited by 613 · see citing works
DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways
Fuentes, J. –. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.11.1681 · Cited by 465 · see citing works
Calcineurin acts through theCRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast
Stathopoulos, A. M., & Cyert, M. S. (1997) · Genes & Development · doi:10.1101/gad.11.24.3432 · Cited by 442 · see citing works
Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases
Cunningham, K. W., & Fink, G. R. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.3.351 · Cited by 432 · see citing works
Calcineurin Inhibits VCX 1-Dependent H + /Ca 2 + Exchange and Induces Ca 2 + ATPases in Saccharomyces cerevisiae
Cunningham, K. W., & Fink, G. R. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.5.2226 · Cited by 431 · see citing works
Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction.Preprint
Beals, C. R., Clipstone, N. A., Ho, S. N., & Crabtree, G. R. (1997) · Genes & Development · doi:10.1101/gad.11.7.824 · Cited by 402 · see citing works
Restricted and Regulated Overexpression Reveals Calcineurin as a Key Component in the Transition from Short-Term to Long-Term Memory
Mansuy, I. M., Mayford, M. R., Jacob, B., Kandel, E. R., & Bach, M. E. (1998) · Cell · doi:10.1016/s0092-8674(00)80897-1 · Cited by 361 · see citing works
Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence
Sanglard, D., Ischer, F., Marchetti, O., Entenza, J., & Bille, J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03495.x · Cited by 350 · see citing works
Calcineurin is essential for survival during membrane stress in Candida albicans
Cruz, M. C., Goldstein, A. L., Blankenship, J. R., Del Poeta, M., Davis, D., Cardenas, M. E., Perfect, J. R., McCusker, J. H., & Heitman, J. (2002) · The EMBO Journal · doi:10.1093/emboj/21.4.546 · Cited by 342 · cited 3× · see citing works
“The susceptibility of calcineurin mutants is of particular interest in the clinical setting because calcineurin mutant strains, or wild-type strains in the presence of calcineurin inhibitory drugs (FK506 or Cyclosporin A), are killed by the normally fungistatic azole antifungal drugs (Cruz et al., 2002; Onyewu et al.,…”
BackgroundSelf-citation
Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress.
Cyert, M. S. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01552-3 · Cited by 333 · see citing works
Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae
Matheos, D. P., Kingsbury, T. J., Ahsan, U. S., & Cunningham, K. W. (1997) · Genes & Development · doi:10.1101/gad.11.24.3445 · Cited by 332 · see citing works
Harnessing 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 · see citing works
A conserved family of calcineurin regulatorsPreprint
Kingsbury, T. J., & Cunningham, K. W. (2000) · Genes & Development · doi:10.1101/gad.14.13.1595 · Cited by 305 · see citing works
Ergosterol Biosynthesis Inhibitors Become Fungicidal when Combined with Calcineurin Inhibitors against Candida albicans , Candida glabrata , and Candida krusei
Onyewu, C., Blankenship, J. R., Del Poeta, M., & Heitman, J. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.3.956-964.2003 · Cited by 282 · see citing works
Self-citation
International Surveillance of Bloodstream Infections Due to Candida Species: Frequency of Occurrence and Antifungal Susceptibilities of Isolates Collected in 1997 in the United States, Canada, and South America for the SENTRY Program
Pfaller, M. A., Jones, R. N., Doern, G. V., Sader, H. S., Hollis, R. J., Messer, S. A., & Group, F. T. S. P. (1998) · Journal of Clinical Microbiology · doi:10.1128/jcm.36.7.1886-1889.1998 · Cited by 281 · see citing works
Candida albicans RIM101 pH Response Pathway Is Required for Host-Pathogen Interactions
Davis, D. A., Edwards, J. E., Mitchell, A. P., & Ibrahim, A. S. (2000) · Infection and Immunity · doi:10.1128/iai.68.10.5953-5959.2000 · Cited by 276 · see citing works
Protein phosphatase type 2B (calcineurin)‐mediated, FK506‐sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions.
Nakamura, T., Liu, Y., Hirata, D., Namba, H., Harada, S., Hirokawa, T., & Miyakawa, T. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb06090.x · Cited by 270 · see citing works
Essential role of calcineurin in response to endoplasmic reticulum stress
Bonilla, M., Nastase, K. K., & Cunningham, K. W. (2002) · The EMBO Journal · doi:10.1093/emboj/21.10.2343 · Cited by 255 · see citing works
Calcineurin functions in Ca(2+)-activated cell death in mammalian cells.
Shibasaki, F., & McKeon, F. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.3.735 · Cited by 252 · see citing works
CRZ1 , a target of the calcineurin pathway in Candida albicans
Karababa, M., Valentino, E., Pardini, G., Coste, A. T., Bille, J., & Sanglard, D. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.05037.x · Cited by 231 · see citing works
Calcineurin: Structure, function, and inhibition
Hemenway, C. S., & Heitman, J. (1999) · Cell Biochemistry and Biophysics · doi:10.1007/bf02737887 · Cited by 227 · see citing works
Self-citation
Invasive Candida Infections
Edwards, J. E. (1991) · New England Journal of Medicine · doi:10.1056/nejm199104113241511 · Cited by 222 · see citing works
MID1, a novel Saccharomyces cerevisiae gene encoding a plasma membrane protein, is required for Ca2+ influx and mating.
Iida, H., Nakamura, H., Ono, T., Okumura, M. S., & Anraku, Y. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.12.8259 · Cited by 218 · see citing works
Role of the fungal Ras-protein kinase A pathway in governing epithelial cell interactions during oropharyngeal candidiasis: Mechanisms of oropharyngeal candidiasis
Park, H., Myers, C. L., Sheppard, D. C., Phan, Q. T., Sanchez, A. A., E. Edwards, J., & Filler, S. G. (2004) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00476.x · Cited by 207 · see citing works
Self-citation
Calcineurin mediates inhibition by FK506 and cyclosporin of recovery from α-factor arrest in yeast
Poor, F., Parent, S. A., Morin, N. R., Dahl, A., Ramadan, N., Chrebet, G. L., Bostian, K. A., & NIELSEN, J. B. K. (1992) · Nature · doi:10.1038/360682a0 · Cited by 192 · see citing works
Calcineurin Is Essential for Candida albicans Survival in Serum and Virulence
Blankenship, J. R., Wormley, F. L., Boyce, M. K., Schell, W. A., Filler, S. G., Perfect, J. R., & Heitman, J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.3.422-430.2003 · Cited by 186 · see citing works
Self-citation
The Saccharomyces cerevisiae CCH1 gene is involved in calcium influx and mating
Fischer, M., Schnell, N., Chattaway, J., Davies, P., Dixon, G., & Sanders, D. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01466-x · Cited by 185 · see citing works
Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans
Görlach, J. M., Fox, D. S., Cutler, N. S., Cox, G. M., Perfect, J. R., & Heitman, J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.14.3618 · Cited by 172 · see citing works
Self-citation
β-Adrenergic Pathway Induces Apoptosis through Calcineurin Activation in Cardiac Myocytes*
Saito, S., Hiroi, Y., Zou, Y.-Z., Aikawa, R., Toko, H., Shibasaki, F., Yazaki, Y., Nagai, R., & Komuro, I. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002844200 · Cited by 169 · see citing works
Renaming the DSCR1 / Adapt78 gene family as RCAN : regulators of calcineurin
Davies, K. J. A., Ermak, G., Rothermel, B. A., Pritchard, M. A., Heitman, J., Ahnn, J., Henrique‐Silva, F., Crawford, D. R., Canaider, S., Strippoli, P., et al. (2007) · The FASEB Journal · doi:10.1096/fj.06-7246com · Cited by 168 · see citing works
Self-citation
Mitogen-activated Protein Kinase Stimulation of Ca2+Signaling Is Required for Survival of Endoplasmic Reticulum Stress in Yeast
Bonilla, M., & Cunningham, K. W. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-02-0113 · Cited by 165 · see citing works
GSK-3 kinases enhance calcineurin signaling by phosphorylation of RCNsPreprint
Hilioti, Z., Gallagher, D. A., Low-Nam, S. T., Ramaswamy, P., Gajer, P., Kingsbury, T. J., Birchwood, C. J., Levchenko, A., & Cunningham, K. W. (2003) · Genes & Development · doi:10.1101/gad.1159204 · Cited by 161 · see citing works
Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands.
Cardenas, M. E., Hemenway, C. S., Muir, R. S., Ye, R., Fiorentino, D. F., & Heitman, J. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06940.x · Cited by 160 · see citing works
Self-citation
Hyphal Orientation of Candida albicans Is Regulated by a Calcium-Dependent Mechanism
Brand, A., Shanks, S., Duncan, V. M. S., Yang, M., Mackenzie, K. S., & Gow, N. A. R. (2007) · Current Biology · doi:10.1016/j.cub.2006.12.043 · Cited by 154 · see citing works
Multiple Domains of MCIP1 Contribute to Inhibition of Calcineurin Activity
Vega, R. B., Yang, J., Rothermel, B. A., Bassel‐Duby, R., & Williams, R. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200123200 · Cited by 146 · see citing works
Ca2+ Transport in Saccharomyces Cerevisiae
Cunningham, K. W., & Fink, G. R. (1994) · Journal of Experimental Biology · doi:10.1242/jeb.196.1.157 · Cited by 145 · see citing works
Candida and candidosis
Howard, A. (1989) · Journal of Hospital Infection · doi:10.1016/0195-6701(89)90106-0 · Cited by 144 · see citing works
Increased incidence of fungemia caused by Candida krusei
Merz, W. G., Karp, J. E., Schron, D., & Saral, R. (1986) · Journal of Clinical Microbiology · doi:10.1128/jcm.24.4.581-584.1986 · Cited by 139 · see citing works
Calcineurin is essential in cyclosporin A- and FK506-sensitive yeast strains.
Breuder, T., Hemenway, C. S., Movva, N. R., Cardenas, M. E., & Heitman, J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.12.5372 · Cited by 135 · see citing works
Self-citation
Calcineurin Is Essential for Virulence in Candida albicans
Bader, T., Bodendorfer, B., Schröppel, K., & Morschhäuser, J. (2003) · Infection and Immunity · doi:10.1128/iai.71.9.5344-5354.2003 · Cited by 121 · see citing works
The Calcineurin Target, Crz1, Functions in Azole Tolerance but Is Not Required for Virulence of Candida albicans
Onyewu, C., Wormley, F. L., Perfect, J. R., & Heitman, J. (2004) · Infection and Immunity · doi:10.1128/iai.72.12.7330-7333.2004 · Cited by 121 · see citing works
Self-citation
Candida -Host Interactions in HIV Disease: Relationships in Oropharyngeal Candidiasis
Fidel, P. L. (2006) · Advances in Dental Research · doi:10.1177/154407370601900116 · Cited by 119 · see citing works
Molecular analysis of the interaction of calcineurin with drug-immunophilin complexes
Clipstone, N. A., Fiorentino, D. F., & Crabtree, G. R. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47212-2 · Cited by 118 · see citing works
Targets of immunophilin‐immunosuppressant complexes are distinct highly conserved regions of calcineurin A.
Cardenas, M. E., Muir, R. S., Breuder, T., & Heitman, J. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07277.x · Cited by 118 · see citing works
Self-citation
Fluconazole plus Cyclosporine: a Fungicidal Combination Effective against Experimental Endocarditis Due to Candida albicans
Marchetti, O., Entenza, J. M., Sanglard, D., Bille, J., Glauser, M. P., & Moreillon, P. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.11.2932-2938.2000 · Cited by 113 · see citing works
Calcineurin Is Required forCandida albicansTo Survive Calcium Stress in Serum
Blankenship, J. R., & Heitman, J. (2005) · Infection and Immunity · doi:10.1128/iai.73.9.5767-5774.2005 · Cited by 111 · see citing works
Self-citation
The role of calcium in apoptosis
Krebs, J. J. R. (1998) · BioMetals · doi:10.1023/a:1009226316146 · Cited by 94 · see citing works
Role of Calcineurin in Stress Resistance, Morphogenesis, and Virulence of a Candida albicans Wild-Type Strain
Bader, T., Schröppel, K., Bentink, S., Agabian, N., Köhler, G., & Morschhäuser, J. (2006) · Infection and Immunity · doi:10.1128/iai.00142-06 · Cited by 81 · see citing works
Functional characterization of the Candida albicans CRZ1 gene encoding a calcineurin-regulated transcription factor
Santos, M., & de Larrinoa, I. F. (2005) · Current Genetics · doi:10.1007/s00294-005-0003-8 · Cited by 78 · see citing works
A New Gene Family Including DSCR1 (Down Syndrome Candidate Region 1) and ZAKI-4: Characterization from Yeast to Human and Identification of DSCR1-like 2, a Novel Human Member (DSCR1L2)
Strippoli, P., Lenzi, L., Petrini, M., Carinci, P., & Zannotti, M. (2000) · Genomics · doi:10.1006/geno.2000.6127 · Cited by 78 · see citing works
The Saccharomyces cerevisiae Ca2+ channel Cch1pMid1p is essential for tolerance to cold stress and iron toxicity
Peiter, E., Fischer, M. J. C., Sidaway‐Lee, K., Roberts, S. K., & Sanders, D. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.09.058 · Cited by 77 · see citing works
Cch1 Mediates Calcium Entry in Cryptococcus neoformans and Is Essential in Low-Calcium Environments
Liu, M., Du, P., Heinrich, G., Cox, G. M., & Gelli, A. (2006) · Eukaryotic Cell · doi:10.1128/ec.00158-06 · Cited by 76 · see citing works
Teaching old drugs new tricks: reincarnating immunosuppressants as antifungal drugs.
Blankenship, J. R., Steinbach, W. J., Perfect, J. R., & Heitman, J. (2003) · PubMed · Cited by 67 · see citing works
Self-citation
Inhibiting the Calcineurin-NFAT (Nuclear Factor of Activated T Cells) Signaling Pathway with a Regulator of Calcineurin-derived Peptide without Affecting General Calcineurin Phosphatase Activity
Mulero, M. C., Aubareda, A., Orzáez, M., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m805889200 · Cited by 65 · see citing works
The SCF Cdc4 ubiquitin ligase regulates calcineurin signaling through degradation of phosphorylated Rcn1, an inhibitor of calcineurin
Kishi, T., Ikeda, A., Nagao, R., & Koyama, N. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704951104 · Cited by 61 · see citing works
The RCN family of calcineurin regulators
Hilioti, Z., & Cunningham, K. W. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01515-8 · Cited by 44 · see citing works
Genetic Disruption of Calcineurin Improves Skeletal Muscle Pathology and Cardiac Disease in a Mouse Model of Limb-Girdle Muscular Dystrophy
Parsons, S. A., Millay, D. P., Sargent, M. A., Naya, F. J., McNally, E. M., Sweeney, H. L., & Molkentin, J. D. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m609368200 · Cited by 37 · see citing works
Calcineurin Promotes Infection of the Cornea by Candida albicans and Can Be Targeted To Enhance Fluconazole Therapy
Onyewu, C., Afshari, N. A., & Heitman, J. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00393-06 · Cited by 36 · see citing works
Self-citation
Calcineurin controls the expression of numerous genes in cerebellar granule cells
Krämer, D., Fresu, L. G., Ashby, D. S., et al. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00057-5 · Cited by 29 · see citing works
Selection and pathogenicity of Candida albicans in HIV infection
Sweet, S. P. (1997) · Oral Diseases · doi:10.1111/j.1601-0825.1997.tb00383.x · Cited by 27 · see citing works
Calcineurin, Synaptic Plasticity, and Memory
Weitlauf, C., & Winder, D. G. (2001) · The Scientific World JOURNAL · doi:10.1100/tsw.2001.259 · Cited by 6 · see citing works

Flagged first, then by citations

Research works printed but not linked: 1

Strippoli P Lenzi L Petrini M Carinci P Zannotti M A new gene family including DSCR1 (Down Syndrome Candidate Region 1) and ZAKI-4: Characterization from yeast to human and identification of DSCR1-like 2, a novel human member (DSCR1L2) Genomics 2000b 64 252 263 10756093

Sorted by citations

PKC Signaling Regulates Drug Resistance of the Fungal Pathogen Candida albicans via Circuitry Comprised of Mkc1, Calcineurin, and Hsp90
LaFayette, 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 · see citing works
Antifungal tolerance is a subpopulation effect distinct from resistance and is associated with persistent candidemia
Rosenberg, A., Ene, I. V., Bibi, M., Zakin, S., Segal, E. S., Ziv, N., Dahan, A. M., Colombo, A. L., Bennett, R. J., & Berman, J. (2018) · Nature Communications · doi:10.1038/s41467-018-04926-x · Cited by 270 · see citing works
Mechanism of Candida pathogenesis: Revisiting the vital drivers
Mba, I. E., & Nweze, E. I. (2020) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-020-03912-w · Cited by 143 · see citing works
Convergent Evolution of Calcineurin Pathway Roles in Thermotolerance and Virulence inCandida glabrata
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
Self-citation
Tolerance to Caspofungin in Candida albicans Is Associated with at Least Three Distinctive Mechanisms That Govern Expression of FKS Genes and Cell Wall Remodeling
Yang, F., Zhang, L., Wakabayashi, H., Myers, J., Jiang, Y., Cao, Y., Jimenez-Ortigosa, C., Perlin, D. S., & Rustchenko, E. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00071-17 · Cited by 81 · see citing works
Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus
Juvvadi, P. R., Fortwendel, J. R., Rogg, L. E., Burns, K. A., Randell, S. H., & Steinbach, W. J. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07886.x · Cited by 80 · see citing works
Phosphorylation of Calcineurin at a Novel Serine-Proline Rich Region Orchestrates Hyphal Growth and Virulence in Aspergillus fumigatus
Juvvadi, P. R., Gehrke, C., Fortwendel, J. R., Lamoth, F., Soderblom, E. J., Cook, E. C., Hast, M. A., Asfaw, Y. G., Moseley, M. A., Creamer, T. P., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003564 · Cited by 57 · 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
Kch1 Family Proteins Mediate Essential Responses to Endoplasmic Reticulum Stresses in the Yeasts Saccharomyces cerevisiae and Candida albicans
Stefan, C. P., & Cunningham, K. W. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.508705 · Cited by 15 · see citing works
Endosomal Trafficking Defects Can Induce Calcium-Dependent Azole Tolerance in Candida albicans
Luna-Tapia, A., Tournu, H., Peters, T. L., & Palmer, G. E. (2016) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01034-16 · Cited by 12 · see citing works

Calcineurin Inhibition or Mutation Enhances Cell Wall Inhibitors against Aspergillus fumigatus
Steinbach, W. J., Cramer, R. A., Perfect, B. Z., Henn, C., Nielsen, K., Heitman, J., & Perfect, J. R. (2007) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01394-06 · Cited by 108 · see citing works
Self-citation
BH3I-1 DERIVATIVES INHIBIT THE FILAMENTOUS GROWTH OF THE CEA10 STRAIN OF ASPERGILLUS FUMIGATUS
Johnson, R., Goffena, J., Butler, D. K., et al. (2015) · Intermountain journal of sciences
Differential host susceptibility to intracerebral infections with Candida albicans and Cryptococcus neoformans
Blasi, E., Barluzzi, R., Mazzolla, R., et al. (1993) · Infection and Immunity · doi:10.1128/iai.61.8.3476-3481.1993 · Cited by 33 · see citing works
Candida albicans, Cryptococcus neoformans or Aspergillus fumigatus Induces an Antifungal Activity in Mouse Serum, which is Different from Transferrin
OKAZAKI, K.-I., Asakura, M., Sugimoto, N., Hinenoya, A., & Yamasaki, S. (2009) · Journal of Veterinary Medical Science · doi:10.1292/jvms.001459 · Cited by 2 · see citing works
The three Aspergillus fumigatus CFEM-domain GPI-anchored proteins (CfmA-C) affect cell-wall stability but do not play a role in fungal virulence
Vaknin, Y., Shadkchan, Y., Levdansky, E., Morozov, M., Romano, J., & Osherov, N. (2013) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2013.12.005 · Cited by 70 · see citing works

Authors: Reedy, J. L., Filler, S. G., & Heitman, J.
Affiliations: Duke University (US)
University of California, Los Angeles (US)
Corresponding author: Heitman, Joseph
ORCID: Reedy, Jennifer L.
Filler, Scott G.
Heitman, Joseph
Venue: Fungal Genetics and Biology
Publisher: Elsevier BV
Published: 2010-02
Volume: 47
Issue: 2
Pages: 107-116
ISSN: 1087-1845 (ISSN-L)
DOI: 10.1016/j.fgb.2009.09.002
PMC: PMC2815136
OpenAlex: W1994548351
Cited by: 76
References: 72
Citations by year: 2026: 3 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 8 · 2020: 7 · 2019: 5 · 2018: 1 · 2017: 1 · 2016: 7 · 2015: 5 · 2014: 10 · 2013: 7 · 2012: 7
FWCI: 2.26
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Fungal Genetics and Biology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIAID R01 (AI42159, AI50438)
NIDCR R01 (DE017088)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Signaling Pathways in Disease
Keywords: Candida albicans, calcineurin signaling, RCN1, MID1, stress response, virulence, antifungal susceptibility, protein phosphatase, heterologous expression in Saccharomyces cerevisiae
MeSH terms: Amino Acid Sequence, Animals, Antifungal Agents, Candida albicans, Candidiasis, Fungal Proteins, Genetic Complementation Test, Mice, Inbred ICR, Molecular Sequence Data, Mutation, Saccharomyces cerevisiae, Sodium Dodecyl Sulfate, Virulence, Signal Transduction, Fluconazole, Gene Expression Regulation, Fungal, Sequence Homology, Amino Acid, Lithium Chloride, Calcineurin, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks