Functional connections between cell cycle and proteostasis in the regulation of Candida albicans morphogenesis
Open accessAbstract
Morphological plasticity is a key virulence trait for many fungal pathogens. For the opportunistic fungal pathogen Candida albicans, transitions among yeast, pseudohyphal, and hyphal forms are critical for virulence, because the morphotypes play distinct roles in the infection process. C. albicans morphogenesis is induced in response to many host-relevant conditions and is regulated by complex signaling pathways and cellular processes. Perturbation of either cell-cycle progression or protein homeostasis induces C. albicans filamentation, demonstrating that these processes play a key role in morphogenetic control. Regulators such as cyclin-dependent kinases, checkpoint proteins, the proteasome, the heat shock protein Hsp90, and the heat shock transcription factor Hsf1 all influence morphogenesis, often through interconnected effects on the cell cycle and proteostasis. This review highlights the major cell-cycle and proteostasis regulators that modulate morphogenesis and discusses how these two processes intersect to regulate this key virulence trait.
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
Cites
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?
In C. albicans, Hsp90 client proteins include regulators that play important roles in cell-cycle progression and morphogenesis.
“In C. albicans, Hsp90 client proteins also include regulators that play important roles in cell-cycle progression and morphogenesis (Hossain et al. 2021).”
From Genetic analysis of Hsp90 function in <i>Cryptococcus neoformans</i> highlights key roles in stress tolerance and virulence (2022) · cites this paper as Hossain et al. 2021
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Global and Multi-National Prevalence of Fungal Diseases-Estimate Precision
Bongomin, F., Gago, S., Oladele, R., & Denning, D. (2017) · Journal of Fungi · doi:10.3390/jof3040057 · Cited by 2,953 · cited 1× · see citing works
“albicans imposes a major burden on human health, causing ~700,000 deaths per year globally because of invasive candidiasis (Bongomin et al., 2017).”
BackgroundHSP90 at the hub of protein homeostasis: emerging mechanistic insights
Taipale, M., Jarosz, D. F., & Lindquist, S. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2918 · Cited by 1,818 · see citing works
Themes and variations on ubiquitylation
Weissman, A. M. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35056563 · Cited by 1,472 · see citing works
Whitesell, L., Mimnaugh, E. G., De Costa, B., Myers, C. E., & Neckers, L. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8324 · Cited by 1,444 · see citing works
Kullberg, B. J., & Arendrup, M. C. (2015) · New England Journal of Medicine · doi:10.1056/nejmra1315399 · Cited by 1,315 · see citing works
Growth of Candida albicans hyphae
Sudbery, P. E. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2636 · Cited by 1,110 · see citing works
The distinct morphogenic states of Candida albicans
Sudbery, P., Gow, N., & Berman, J. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2004.05.008 · Cited by 876 · see citing works
Noble, S. M., French, S., Kohn, L. A., Chen, V., & Johnson, A. D. (2010) · Nature Genetics · doi:10.1038/ng.605 · Cited by 678 · see citing works
Saville, S. P., Lazzell, A. L., Monteagudo, C., & Lopez-Ribot, J. L. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.5.1053-1060.2003 · Cited by 655 · see citing works
Regulatory circuitry governing fungal development, drug resistance, and disease.
Shapiro, R. S., Robbins, N., & Cowen, L. E. (2011) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00045-10 · Cited by 576 · see citing works
Candida albicans cell-type switching and functional plasticity in the mammalian host
Noble, S. M., Gianetti, B. A., & Witchley, J. N. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.157 · Cited by 518 · see citing works
Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins.
Lew, D. J., & Reed, S. I. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.120.6.1305 · Cited by 498 · see citing works
A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin
Willems, A. R., Schwab, M. G., & Tyers, M. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.09.027 · Cited by 461 · see citing works
Schulte, T. W., Blagosklonny, M. V., Ingui, C., & Neckers, L. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.41.24585 · Cited by 457 · see citing works
NRG1 represses yeast–hypha morphogenesis and hypha‐specific gene expression in Candida albicans
Murad, A. M. A., Leng, P., Straffon, M., Wishart, J., Macaskill, S., MacCallum, D., Schnell, N., Talibi, D., Marechal, D., Tekaia, F., et al. (2001) · The EMBO Journal · doi:10.1093/emboj/20.17.4742 · Cited by 452 · see citing works
The Ubiquitin–Proteasome System of Saccharomyces cerevisiae
Finley, D. J., Ulrich, H. D., Sommer, T., & Kaiser, P. (2012) · Genetics · doi:10.1534/genetics.112.140467 · Cited by 427 · see citing works
NRG1, a repressor of filamentous growth in C.albicans, is down‐regulated during filament induction
Braun, B. R., Kadosh, D., & Johnson, A. D. (2001) · The EMBO Journal · doi:10.1093/emboj/20.17.4753 · Cited by 345 · see citing works
Zheng, X., Wang, Y.-M., & Wang, Y. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600195 · Cited by 328 · see citing works
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 · see citing works
Self-citationAntifungal Drugs: The Current Armamentarium and Development of New Agents
Robbins, N., Wright, G. D., & Cowen, L. E. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0002-2016 · Cited by 271 · see citing works
Global analysis of fungal morphology exposes mechanisms of host cell escape
O’Meara, T. R., Veri, A. O., Ketela, T., Jiang, B., Roemer, T., & Cowen, L. E. (2015) · Nature Communications · doi:10.1038/ncomms7741 · Cited by 243 · see citing works
Banerjee, M., Thompson, D. S., Lazzell, A., Carlisle, P. L., Pierce, C., Monteagudo, C., López-Ribot, J. L., & Kadosh, D. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-11-1110 · Cited by 243 · see citing works
Morphogenesis and cell cycle progression in Candida albicans
Berman, J. (2006) · Current Opinion in Microbiology · doi:10.1016/j.mib.2006.10.007 · Cited by 237 · see citing works
Carlisle, P. L., Banerjee, M., Lazzell, A., Monteagudo, C., López-Ribot, J. L., & Kadosh, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804061106 · Cited by 215 · see citing works
Swe1Wee1-Dependent Tyrosine Phosphorylation of Hsp90 Regulates Distinct Facets of Chaperone Function
Mollapour, M., Tsutsumi, S., Donnelly, A. C., Beebe, K., Tokita, M. J., Lee, M.-J., Lee, S., Morra, G., Bourboulia, D., Scroggins, B. T., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.005 · Cited by 196 · see citing works
Septin Function in Candida albicans Morphogenesis
Warenda, A. J., & Konopka, J. B. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-01-0013 · Cited by 188 · see citing works
Targeting<i>Candida albicans</i>filamentation for antifungal drug development
Vila, T., Romo, J. A., Pierce, C. G., McHardy, S. F., Saville, S. P., & Lopez-Ribot, J. L. (2017) · Virulence · doi:10.1080/21505594.2016.1197444 · Cited by 174 · see citing works
Cdk1 coordinates cell-surface growth with the cell cycle
McCusker, D., Denison, C., Anderson, S., Egelhofer, T. A., Yates, J. R., Gygi, S. P., & Kellogg, D. R. (2007) · Nature Cell Biology · doi:10.1038/ncb1568 · Cited by 146 · see citing works
Leach, M. D., Budge, S., Walker, L. A., Munro, C. A., Cowen, L. E., & Brown, A. J. P. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003069 · Cited by 133 · see citing works
Shi, Q.-M., Wang, Y.-M., Zheng, X., Lee, R. T. H., & Wang, Y. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-05-0442 · Cited by 124 · see citing works
Structural basis for species-selective targeting of Hsp90 in a pathogenic fungus
Whitesell, L., Robbins, N., Huang, D. S., McLellan, C. A., Shekhar-Guturja, T., LeBlanc, E. V., Nation, C. S., Hui, R., Hutchinson, A., Collins, C., et al. (2019) · Nature Communications · doi:10.1038/s41467-018-08248-w · Cited by 124 · see citing works
Bensen, E. S., Filler, S. G., & Berman, J. G. (2002) · Eukaryotic Cell · doi:10.1128/ec.1.5.787-798.2002 · Cited by 122 · see citing works
Cyclin-Dependent Kinases Control Septin Phosphorylation in Candida albicans Hyphal Development
Sinha, I., Wang, Y.-M., Philp, R., Li, C.-R., Yap, W. H., & Wang, Y. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.06.011 · Cited by 120 · see citing works
Phosphorylation of Rga2, a Cdc42 GAP, by CDK/Hgc1 is crucial for Candida albicans hyphal growth
Zheng, X., Lee, R. T. H., Wang, Y.-M., Lin, Q., & Wang, Y. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601814 · Cited by 112 · see citing works
The anaphase-promoting complex/cyclosome (APC/C): cell-cycle-dependent and -independent functions
Manchado, E., Eguren, M., & Malumbres, M. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380065 · Cited by 107 · see citing works
Nicholls, S., MacCallum, D. M., Kaffarnik, F., Selway, L., Peck, S. C., & Brown, A. J. P. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2010.08.010 · Cited by 107 · see citing works
Lü, Y., Su, C., Unoje, O., & Liu, H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318690111 · Cited by 105 · see citing works
Nicholls, S., Leach, M. D., Priest, C. L., & Brown, A. J. P. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06883.x · Cited by 105 · see citing works
A G<sub>1</sub> Cyclin Is Necessary for Maintenance of Filamentous Growth in <i>Candida albicans</i>
Loeb, J. D. J., Sepulveda-Becerra, M., Hazan, I., & Liu, H. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.6.4019 · Cited by 105 · see citing works
Regulation of Candida albicans Hyphal Morphogenesis by Endogenous Signals
Kornitzer, D. (2019) · Journal of Fungi · doi:10.3390/jof5010021 · Cited by 105 · see citing works
Circuit diversification in a biofilm regulatory network
Huang, M. Y., Woolford, C. A., May, G. E., McManus, C. J., & Mitchell, A. P. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007787 · Cited by 102 · see citing works
Bachewich, C., Nantel, A., & Whiteway, M. S. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04727.x · Cited by 101 · see citing works
Wightman, R., Bates, S., Amornrrattanapan, P., & Sudbery, P. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200307176 · Cited by 100 · see citing works
Leach, M. D., Farrer, R. A., Tan, K., Miao, Z., Walker, L. A., Cuomo, C. A., Wheeler, R. T., Brown, A. J. P., Wong, K. H., & Cowen, L. E. (2016) · Nature Communications · doi:10.1038/ncomms11704 · Cited by 100 · see citing works
The Mitotic Cyclins Clb2p and Clb4p Affect Morphogenesis in<i>Candida albicans</i>
Bensen, E. S., Clemente-Blanco, A., Finley, K. R., Correa-Bordes, J., & Berman, J. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-12-1081 · Cited by 94 · cited 4× · see citing works
“Clb2-depleted cells are not viable and arrest with hyperelongated projections, whereas Clb4-depleted cells remain viable and grow constitutively as pseudohyphae (Bensen et al., 2005).”
BackgroundInfluentialThe Hsp90 chaperone network modulates Candida virulence traits
O’Meara, T. R., Robbins, N., & Cowen, L. E. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.05.003 · Cited by 92 · see citing works
Opportunistic yeast pathogens: reservoirs, virulence mechanisms, and therapeutic strategies
Polvi, E. J., Li, X., O’Meara, T. R., Leach, M. D., & Cowen, L. E. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1860-z · Cited by 90 · see citing works
Role for the SCF CDC4 Ubiquitin Ligase in Candida albicans Morphogenesis
Atir-Lande, A., Gildor, T., & Kornitzer, D. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-01-0079 · Cited by 90 · see citing works
Morano, K. A., Santoro, N., Koch, K. A., & Thiele, D. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.1.402 · Cited by 87 · see citing works
Cyclin Cln3p Links G 1 Progression to Hyphal and Pseudohyphal Development in Candida albicans
Bachewich, C., & Whiteway, M. S. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.1.95-102.2005 · Cited by 86 · see citing works
The Hsp90 Co-Chaperone Sgt1 Governs Candida albicans Morphogenesis and Drug Resistance
Shapiro, R. S., Zaas, A. K., Betancourt-Quiroz, M., Perfect, J. R., & Cowen, L. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044734 · Cited by 86 · see citing works
Self-citationDepletion of a Polo-like Kinase inCandida albicansActivates Cyclase-dependent Hyphal-like Growth
Bachewich, C., Thomas, D. Y., & Whiteway, M. S. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.02-05-0076 · Cited by 83 · see citing works
Shapiro, R. S., Sellam, A., Tebbji, F., Whiteway, M., Nantel, A., & Cowen, L. E. (2012) · Current Biology · doi:10.1016/j.cub.2012.01.062 · Cited by 81 · see citing works
The G 1 Cyclin Cln3 Regulates Morphogenesis in Candida albicans
Chapa‐y‐Lazo, B., Bates, S., & Sudbery, P. E. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.1.90-94.2005 · Cited by 80 · see citing works
Wang, A., Raniga, P. P., Lane, S., Lü, Y., & Liu, H. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01502-08 · Cited by 75 · see citing works
González-Novo, A., Correa-Bordes, J., Labrador, L., Sánchez, M., Vázquez de Aldana, C. R., & Jiménez, J. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-09-0876 · Cited by 75 · see citing works
HSF1 as a Mitotic Regulator: Phosphorylation of HSF1 by Plk1 Is Essential for Mitotic Progression
Lee, Y., Kim, E., Lee, J. S., Jeoung, D., Bae, S., Kwon, S., & Lee, Y. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0129 · Cited by 71 · see citing works
Andaluz, E., Ciudad, T., Gómez‐Raja, J., Calderone, R., & Larriba, G. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.05038.x · Cited by 69 · see citing works
Leach, M. D., Stead, D., Argo, E., MacCallum, D. M., & Brown, A. J. P. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07542.x · Cited by 68 · see citing works
Senn, H., Shapiro, R. S., & Cowen, L. E. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-08-0729 · Cited by 67 · see citing works
The vacuole/lysosome is required for cell-cycle progression
Jin, Y., & Weisman, L. S. (2015) · eLife · doi:10.7554/elife.08160 · Cited by 66 · see citing works
Goes, F. S., & Martin, J. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02105.x · Cited by 64 · see citing works
Bai, C. G., Ramanan, N., Wang, Y. M., & Wang, Y. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02995.x · Cited by 64 · see citing works
The Candida albicans Vacuole Is Required for Differentiation and Efficient Macrophage Killing
Palmer, G. E., Kelly, M. N., & Sturtevant, J. E. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.10.1677-1686.2005 · Cited by 63 · see citing works
Enenkel, C. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.03.023 · Cited by 63 · see citing works
Leach, M. D., Tyc, K. M., Brown, A. J. P., & Klipp, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032467 · Cited by 61 · see citing works
Poltermann, S., Nguyen, M., Günther, J., Wendland, J., Härtl, A., Künkel, W., Zipfel, P. F., & Eck, R. (2005) · Microbiology · doi:10.1099/mic.0.27505-0 · Cited by 54 · see citing works
Tscherner, M., Stappler, E., Hnisz, D., & Kuchler, K. (2012) · Molecular Microbiology · doi:10.1111/mmi.12051 · Cited by 53 · see citing works
Candida albicans VPS1 contributes to protease secretion, filamentation, and biofilm formation
Bernardo, S. M., Khalique, Z., Kot, J., Jones, J. K., & Lee, S. A. (2008) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2008.01.001 · Cited by 53 · see citing works
Zarzov, P., Boucherie, H., & Mann, C. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.16.1879 · Cited by 53 · see citing works
Veri, A. O., Miao, Z., Shapiro, R. S., Tebbji, F., O’Meara, T. R., Kim, S. H., Colazo, J., Tan, K., Vyas, V. K., Whiteway, M., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007270 · Cited by 51 · see citing works
Rad6p represses yeast‐hypha morphogenesis in the human fungal pathogen Candida albicans
Leng, R. P., Sudbery, P. E., & Brown, A. J. P. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01801.x · Cited by 49 · see citing works
Rane, H. S., Bernardo, S. M., Raines, S. M., Binder, J., Parra, K. J., & Lee, S. A. (2013) · Eukaryotic Cell · doi:10.1128/ec.00118-13 · Cited by 49 · see citing works
O’Meara, T. R., O’Meara, M. J., Polvi, E. J., Pourhaghighi, M. R., Liston, S. D., Lin, Z.-Y., Veri, A. O., Emili, A., Gingras, A.-C., & Cowen, L. E. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000358 · Cited by 49 · see citing works
Finley, K. R., Bouchonville, K. J., Quick, A., & Berman, J. G. (2008) · Journal of Cell Science · doi:10.1242/jcs.015172 · Cited by 48 · see citing works
Woolford, C. A., Lagree, K., Xu, W., Aleynikov, T., Adhikari, H., Sánchez, H., Cullen, P. J., Lanni, F., Andes, D. R., & Mitchell, A. P. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006487 · Cited by 46 · see citing works
Loll‐Krippleber, R., d’Enfert, C., Feri, A., Diogo, D., Perin, A., Marcet‐Houben, M., Bougnoux, M., & Legrand, M. (2013) · Molecular Microbiology · doi:10.1111/mmi.12471 · Cited by 42 · see citing works
Li, W. J., Wang, Y. M., Zheng, X. D., Shi, Q. M., Zhang, T. T., Bai, C., Li, D., Wang, Y., & Wang, Y. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05361.x · Cited by 40 · see citing works
Veri, A. O., Robbins, N., & Cowen, L. E. (2018) · FEMS Yeast Research · doi:10.1093/femsyr/foy041 · Cited by 38 · see citing works
Lü, Y., Su, C., Ray, S., Yuan, Y., & Liu, H. (2019) · mBio · doi:10.1128/mbio.02320-18 · Cited by 38 · see citing works
Caballero‐Lima, D., & Sudbery, P. E. (2014) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-11-0688 · Cited by 35 · see citing works
Li, C.-R., Yong, J. Y. A., Wang, Y., & Wang, Y. (2012) · Journal of Cell Science · doi:10.1242/jcs.104497 · Cited by 32 · see citing works
Proteasome Inhibitors in Cancer Therapy
Orlowski, R. Z. (2005) · Humana Press eBooks · doi:10.1385/1-59259-895-1:339 · Cited by 32 · see citing works
Umeyama, T., Kaneko, A., Niimi, M., & Uehara, Y. (2006) · Yeast · doi:10.1002/yea.1373 · Cited by 31 · see citing works
Hossain, S., Veri, A. O., & Cowen, L. E. (2020) · mBio · doi:10.1128/mbio.00290-20 · Cited by 31 · see citing works
Rane, H. S., Bernardo, S. M., Hayek, S. R., Binder, J., Parra, K. J., & Lee, S. A. (2014) · Eukaryotic Cell · doi:10.1128/ec.00135-14 · Cited by 30 · see citing works
To Sense or Die: Mechanisms of Temperature Sensing in Fungal Pathogens
Leach, M. D., & Cowen, L. E. (2014) · Current Fungal Infection Reports · doi:10.1007/s12281-014-0182-1 · Cited by 28 · see citing works
Sun, L., Li, W. J., Wang, H. T., Chen, J., Deng, P. D. W. P., Wang, Y., & Sang, J. L. (2011) · Eukaryotic Cell · doi:10.1128/ec.05042-11 · Cited by 28 · see citing works
Mendelsohn, S., Pinsky, M., Weissman, Z., & Kornitzer, D. (2017) · mSphere · doi:10.1128/msphere.00248-16 · Cited by 28 · see citing works
Roig, P., & Gozalbo, D. (2003) · Fungal Genetics and Biology · doi:10.1016/s1087-1845(03)00004-5 · Cited by 26 · see citing works
Greig, J. A., Sudbery, I. M., Richardson, J. P., Naglik, J. R., Wang, Y., & Sudbery, P. E. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004630 · Cited by 25 · see citing works
Fifteen years of APC/cyclosome: a short and impressive biography
Simpson-Lavy, K. J., Oren, Y. S., Feine, O., Sajman, J., Listovsky, T., & Brandeis, M. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380078 · Cited by 24 · see citing works
Depletion of the Cullin Cdc53p Induces Morphogenetic Changes in Candida albicans
Trunk, K., Gendron, P., Nantel, A., Lemieux, S., Roemer, T., & Raymond, M. (2009) · Eukaryotic Cell · doi:10.1128/ec.00332-08 · Cited by 23 · see citing works
Wang, H., Gao, J., Li, W., Wong, A. H., Hu, K., Chen, K., Wang, Y., & Sang, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037246 · Cited by 22 · see citing works
Wang, Y. (2016) · The Journal of Microbiology · doi:10.1007/s12275-016-5550-9 · Cited by 22 · see citing works
Virulence-specific cell cycle and morphogenesis connections in pathogenic fungi
Pérez‐Martín, J., Bardetti, P., Castanheira, S. M., de la Torre, A., & Tenorio-Gómez, M. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.03.017 · Cited by 22 · see citing works
Chou, H., Glory, A., & Bachewich, C. (2011) · Eukaryotic Cell · doi:10.1128/ec.00263-10 · Cited by 20 · see citing works
Nair, R., Shariq, M., Dhamgaye, S., Mukhopadhyay, C. K., Shaikh, S., & Prasad, R. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.11.021 · Cited by 19 · see citing works
Cloning and characterization of a cDNA coding for Candida albicans polyubiquitin.
Sepúlveda, P., Cervera, A. M., Lopez-Ribot, J. L., Chaffin, W. L., Martinez, J. P., & Gozalbo, D. (1996) · PubMed · Cited by 18 · see citing works
Keniry, M. E., Kemp, H. A., Rivers, D. M., & Sprague, G. F. (2004) · Genetics · doi:10.1534/genetics.166.3.1177 · Cited by 18 · see citing works
Wang, H., Huang, Z., Yong, J. Y. A., Zou, H., Zeng, G., Gao, J., Wang, Y., Wong, A. H., & Wang, Y. (2016) · Molecular Microbiology · doi:10.1111/mmi.13386 · Cited by 18 · see citing works
G1 and S phase arrest in Candida albicans induces filamentous growth via distinct mechanisms
Chen, C., Zeng, G., & Wang, Y. (2018) · Molecular Microbiology · doi:10.1111/mmi.14097 · Cited by 16 · see citing works
Cloning and characterization of a cDNA coding forCandida albicanspolyubiquitin
Sepúlveda, P., Cervera, A. M., Lopez-Ribot, J. L., Chaffin, W. L., Martinez, J. P., & Gozalbo, D. (1996) · Medical Mycology · doi:10.1080/02681219680000541 · Cited by 15 · see citing works
Neddylation and CAND1 Independently Stimulate SCF Ubiquitin Ligase Activity in Candida albicans
Sela, N., Atir-Lande, A., & Kornitzer, D. (2011) · Eukaryotic Cell · doi:10.1128/ec.05250-11 · Cited by 14 · see citing works
Tpd3‐Pph21 phosphatase plays a direct role in Sep7 dephosphorylation in Candida albicans
Liu, Q., Han, Q., Wang, N., Yao, G., Zeng, G., Wang, Y., Huang, Z., Sang, J., & Wang, Y. (2016) · Molecular Microbiology · doi:10.1111/mmi.13376 · Cited by 14 · see citing works
Han, Q., Pan, C., Wang, Y., Wang, N., Wang, Y., & Sang, J. (2019) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2019.103240 · Cited by 14 · see citing works
Role of Candida albicans Tem1 in mitotic exit and cytokinesis
Milne, S. W., Cheetham, J., Lloyd, D., Shaw, S., Moore, K., Paszkiewicz, K. H., Aves, S. J., & Bates, S. (2014) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2014.06.007 · Cited by 13 · see citing works
Candida albicans Cdc15 is essential for mitotic exit and cytokinesis
Bates, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-27157-y · Cited by 13 · see citing works
Kamthan, M., Nalla, V. K., Ruhela, D., Kamthan, A., Maiti, P., & Datta, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101517 · Cited by 12 · see citing works
Feng, J., Duan, Y., Wei, S., Qin, Y., Zhuang, Z., Zhu, D., Sun, X., & Jiang, L. (2016) · FEMS Yeast Research · doi:10.1093/femsyr/fow009 · Cited by 11 · see citing works
The Proteasome in Cell-Cycle Regulation
Adams, J. (2004) · Humana Press eBooks · doi:10.1007/978-1-59259-794-9_6 · Cited by 5 · see citing works
Hsp90 Is Essential for Chl1-Mediated Chromosome Segregation and Sister Chromatid Cohesion
Khurana, N., Bakshi, S., Tabassum, W., Bhattacharyya, M. K., & Bhattacharyya, S. (2018) · mSphere · doi:10.1128/msphere.00225-18 · Cited by 5 · see citing works
Flagged first, then by citations
1 of the 113 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Xu, Z., Hu, Q., Xie, M., Liu, J., Su, A., Xu, H., & Yang, W. (2023) · Food Science and Human Wellness · doi:10.1016/j.fshw.2023.02.041 · Cited by 40 · see citing works
Reinforcement amid genetic diversity in the Candida albicans biofilm regulatory network
Cravener, M. V., Do, E., May, G. E., Żarnowski, R., Andes, D. R., McManus, C. J., & Mitchell, A. P. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011109 · Cited by 34 · see citing works
Fu, C., Beattie, S. R., Jezewski, A. J., Robbins, N., Whitesell, L., Krysan, D. J., & Cowen, L. E. (2022) · Genetics · doi:10.1093/genetics/iyab164 · Cited by 31 · see citing works
Insights and Perspectives on the Role of Proteostasis and Heat Shock Proteins in Fungal Infections
Neves‐da‐Rocha, J., Santos-Saboya, M. J., Lopes, M. E. R., Rossi, A., & Martinez-Rossi, N. M. (2023) · Microorganisms · doi:10.3390/microorganisms11081878 · Cited by 27 · see citing works
Dumeaux, V., Massahi, S., Bettauer, V., Mottola, A., Dukovny, A., Khurdia, S. S., Costa, A. C. B. P., Omran, R. P., Simpson, S., Xie, J. L., et al. (2023) · eLife · doi:10.7554/elife.81406 · Cited by 25 · see citing works
Lee, Y., Hossain, S., MacAlpine, J., Robbins, N., & Cowen, L. E. (2023) · iScience · doi:10.1016/j.isci.2023.106145 · Cited by 18 · see citing works
Wani, M. Y., Alghamidi, M. S. S., Srivastava, V., Ahmad, A., Aqlan, F. M., & Al‐Bogami, A. S. (2023) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2023.106562 · Cited by 19 · see citing works
Xiao, K., Liu, L., He, R., Rollins, J. A., Li, A., Zhang, G., He, X., Wang, R., Liu, J., Zhang, X., et al. (2023) · New Phytologist · doi:10.1111/nph.19484 · Cited by 19 · see citing works
Min, K., Jannace, T. F., Si, H., Veeramah, K. R., Haley, J. D., & Konopka, J. B. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009861 · Cited by 18 · see citing works
Hgc1 Independence of Biofilm Hyphae in Candida albicans
Sharma, A., Solis, N. V., Huang, M. Y., Lanni, F., Filler, S. G., & Mitchell, A. P. (2023) · mBio · doi:10.1128/mbio.03498-22 · Cited by 18 · see citing works
Hossain, S., Veri, A. O., Liu, Z., Iyer, K. R., O’Meara, T. R., Robbins, N., & Cowen, L. E. (2021) · Genetics · doi:10.1093/genetics/iyab095 · Cited by 17 · see citing works
The impact of phenotypic heterogeneity on fungal pathogenicity and drug resistance
Kozubowski, L., & Berman, J. G. (2025) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaf001 · Cited by 14 · see citing works
Quorum sensing molecules in yeast wastewater treatment and their regulation of yeast cell morphology
Zhang, Q., Xiang, J., Lv, W., Liu, Y., Sun, J., Wan, P., & Li, J. (2022) · Journal of Water Process Engineering · doi:10.1016/j.jwpe.2022.103191 · Cited by 10 · see citing works
Li, R., Yang, X.-X., Dan, W., & Dai, J.-K. (2025) · Bioorganic & Medicinal Chemistry · doi:10.1016/j.bmc.2025.118435 · Cited by 7 · see citing works
Pariano, M., Puccetti, M., Fabi, C., Nunzi, E., Balucchi, S., Perioli, L., Ricci, M., Giovagnoli, S., Garaci, E., & Romani, L. R. (2025) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2025.2569831 · Cited by 6 · see citing works
Guo, J.-C., Yang, L., Dai, L.-T., Ma, Q., Yan, J., Xie, Q., Wu, Y., Dai, H., & Zhao, Y. (2025) · Chinese Journal of Natural Medicines · doi:10.1016/s1875-5364(25)60828-4 · Cited by 5 · see citing works
Vahabi, M., Xu, G., Sarkisjan, D., Hassouni, B. E., Mantini, G., Donati, V. L., Wang, B., Lencioni, G., Honeywell, R. J., Deng, D., et al. (2025) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-025-03470-z · Cited by 5 · see citing works
Fu, C., Xiong, E. H., Kupczok, L., Archambault, L. S., Wang, T. R. W., Holleran, C., Carruthers-Lay, D., Zhuang, T. X., Marcoccia, S., Zhang, H., et al. (2025) · PLoS Biology · doi:10.1371/journal.pbio.3003409 · Cited by 2 · see citing works
Mechanistic model for nuclear migration in hyphae during mitosis
Som, S., & Paul, R. (2023) · Physical review. E · doi:10.1103/physreve.108.014401 · Cited by 2 · see citing works
Zhao, X. L., Wu, Q., Weng, C., Xu, S., Wang, Y., Yuan, W., Xiong, X., Chen, W., & Wei, X. (2025) · Mycopathologia · doi:10.1007/s11046-025-00990-2 · Cited by 3 · see citing works
Song, Y., Lin, Z., Liu, A., & Ma, J. (2025) · World Journal of Gastroenterology · doi:10.3748/wjg.v31.i7.101104 · Cited by 1 · see citing works
Dantuslia, S. K., Doshi, A., Prajapati, B., & Prabha, C. R. (2025) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-025-01772-9 · Cited by 1 · see citing works
Lv, X., Tu, J.-Y., Liu, Q., Wu, Z.-Q., Chen, L., Zhou, T., Yu, X., & Xu, Y. (2025) · Insects · doi:10.3390/insects16090895 · Cited by 1 · see citing works
Cytrynbaum, E. G., & McClean, M. N. (2025) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2025.115740 · Cited by 1 · see citing works
Möslinger, A., Weiner, A., Schäuble, S., Ramı́rez-Zavala, B., Jablonowski, N., Cseresnyés, Z., Schille, T. B., Figge, M. T., Panagiotou, G., Morschhäuser, J., et al. (2026) · mBio · doi:10.1128/mbio.01764-26 · Cited by 1 · see citing works
Elshazly, R. G., Sobieh, S. S., Zaki, S. S., & Tawab, S. (2022) · Journal of Scientific Research in Science /Journal of Scientific Research in Science · doi:10.21608/jsrs.2022.275792 · Cited by 1 · see citing works
Essential anticandidal targets
Kumar, A., & Jha, A. (2023) · Elsevier eBooks · doi:10.1016/b978-0-443-18744-5.00009-5 · Cited by 1 · see citing works
Performing Livelier Biosecurity in Human–Candida Artistic Encounters
Timurgalieva, O. (2022) · Performance Research · doi:10.1080/13528165.2022.2092282
Dantuslia, S. K., Prajapati, B., & Prabha, C. R. (2026) · Cell Biochemistry and Biophysics · doi:10.1007/s12013-026-02041-z
Feng, R., Wang, S., Wu, J., Wang, T., Cao, Y., Feng, A., & Sun, S. (2026) · Future Microbiology · doi:10.1080/17460913.2026.2721915
- Authors
- Hossain, S., Lash, E., Veri, A. O., & Cowen, L. E.
- Affiliations
- University of Toronto (CA)
- Corresponding author
- Cowen, Leah E.
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2021-02
- Volume
- 34
- Issue
- 8
- Pages
- 108781
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC7971348
- OpenAlex
- W3132483202
- Cited by
- 31
- References
- 113
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 1 · 2023: 10 · 2022: 3 · 2021: 3
- FWCI
- 0.45
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (R01AI127375, R01)
- CIHR III (FDN-154288)
- Canada Research Chairs
- Canadian Institutes of Health Research
- Canadian Institute for Advanced Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Candida albicans, morphogenesis, cell cycle, proteostasis, filamentation, yeast-to-hypha transition, pseudohyphal growth, virulence, cyclin-dependent kinases, checkpoint proteins, proteasome, HSP90, HSF1, heat shock response, morphological plasticity
- MeSH terms
- Proteostasis, Animals, Candida albicans, Cell Cycle, Fungal Proteins, Morphogenesis, Virulence, Signal Transduction, Gene Expression Regulation, Fungal, Cyclic AMP-Dependent Protein Kinases, Cell Cycle Proteins, HSP90 Heat-Shock Proteins
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
