Inactivation of Transcription Factor Gene ACE2 in the Fungal Pathogen Candida glabrata Results in Hypervirulence
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During an infection, the coordinated orchestration of many factors by the invading organism is required for disease to be initiated and to progress. The elucidation of the processes involved is critical to the development of a clear understanding of host-pathogen interactions. For Candida species, the inactivation of many fungal attributes has been shown to result in attenuation. Here we demonstrate that the Candida glabrata homolog of the Saccharomyces cerevisiae transcription factor gene ACE2 encodes a function that mediates virulence in a novel way. Inactivation of C. glabrata ACE2 does not result in attenuation but, conversely, in a strain that is hypervirulent in a murine model of invasive candidiasis. C. glabrata ace2 null mutants cause systemic infections characterized by fungal escape from the vasculature, tissue penetration, proliferation in vivo, and considerable overstimulation of the proinflammatory arm of the innate immune response. Compared to the case with wild-type fungi, mortality occurs much earlier in mice infected with C. glabrata ace2 cells, and furthermore, 200-fold lower doses are required to induce uniformly fatal infections. These data demonstrate that C. glabrata ACE2 encodes a function that plays a critical role in mediating the host-Candida interaction. It is the first virulence-moderating gene to be described for a Candida species.
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Deletion of ACE2 in Candida albicans and Saccharomyces cerevisiae resulted in attenuation of virulence.
“The deletion of ACE2 in C. albicans and Saccharomyces cerevisiae resulted in the attenuation of virulence”
From Cell aggregation mediated by <i>ACE2</i> deletion in <i>Candida auris</i> modulates fungal colonization and host immune responses in the skin (2024) · cites this paper as [39]
Deletion of ACE2 in Candida glabrata provoked virulence.
“but in Candida glabrata provoked virulence (38, 39)”
From Cell aggregation mediated by <i>ACE2</i> deletion in <i>Candida auris</i> modulates fungal colonization and host immune responses in the skin (2024) · cites this paper as [39]
Disruption of the transcription factor CgAce2 leads to cell aggregation due to defects in cell separation, and hypervirulence.
“Furthermore, disruption of the transcription factor CgAce2 is known to lead to cell aggregation, due to defects in cell separation, and hypervirulence [72,73].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [72]
Cites
Chen, Y., Wang, L., Kang, Q., Zhang, X., Yu, G., Wan, X., Wang, J., & Zhu, K. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000477308 · Cited by 10,730 · see citing works
Janeway, C. A., & Medzhitov, R. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.083001.084359 · Cited by 8,394 · see citing works
Transcriptional Regulatory Networks in <i>Saccharomyces cerevisiae</i>
Lee, T. I., Rinaldi, N. J., Robert, F., Odom, D. T., Bar-Joseph, Z., Gerber, G. K., Hannett, N. M., Harbison, C. T., Thompson, C. M., Simon, I., et al. (2002) · Science · doi:10.1126/science.1075090 · Cited by 2,956 · see citing works
The immunopathogenesis of sepsis
Cohen, J. (2002) · Nature · doi:10.1038/nature01326 · Cited by 2,742 · see citing works
Immunosuppressive effects of apoptotic cells
Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., & Girkontaite, I. (1997) · Nature · doi:10.1038/37022 · Cited by 1,787 · see citing works
Simultaneous Identification of Bacterial Virulence Genes by Negative Selection
Hensel, M., Shea, J. E., Gleeson, C., Jones, M. D., Dalton, E. C., & Holden, D. W. (1995) · Science · doi:10.1126/science.7618105 · Cited by 1,200 · see citing works
Self-citationSecular Trends in the Epidemiology of Nosocomial Fungal Infections in the United States, 1980-1990
Beck‐Sagué, C. M., Jarvis, W. R., & System, N. N. I. S. (1993) · The Journal of Infectious Diseases · doi:10.1093/infdis/167.5.1247 · Cited by 1,140 · see citing works
Calderone, R. (2012) · ASM Press eBooks · Cited by 912 · see citing works
The Epidemiology of Hematogenous Candidiasis Caused by Different Candida Species
Abi‐Said, D., Anaissie, E., Uzun, O., Raad, I., Pinzcowski, H., & Vartivarian, S. (1997) · Clinical Infectious Diseases · doi:10.1086/513663 · Cited by 755 · see citing works
Tumor Necrosis Factor and Interleuktn-1 in the Serum of Children with Severe Infectious Purpura
Girardin, E. P., Grau, G. E., Dayer, J., Roux-Lombard, P., the J5 Study Group*, & Lambert, P.-H. (1988) · New England Journal of Medicine · doi:10.1056/nejm198808183190703 · Cited by 737 · see citing works
Wisplinghoff, H., Seifert, H., Wenzel, R. P., & Edmond, M. B. (2003) · Clinical Infectious Diseases · doi:10.1086/374339 · Cited by 687 · see citing works
Epidemiology of Nosocomial Fungal Infections, with Emphasis on Candida Species
Jarvis, W. R. (1995) · Clinical Infectious Diseases · doi:10.1093/clinids/20.6.1526 · Cited by 636 · see citing works
Viscoli, C., Girmenia, C., Marinus, A., Collette, L., Martino, P., Vandercam, B., Doyen, C., Lebeau, B., Spence, D., Krcmery, V., et al. (1999) · Clinical Infectious Diseases · doi:10.1086/514731 · Cited by 601 · see citing works
The Role of Toll‐like Receptor (TLR) 2 and TLR4 in the Host Defense against Disseminated Candidiasis
Netea, M. G., van der Graaf, C. A. A., Vonk, A. G., Verschueren, I., van der Meer, J. W. M., & Kullberg, B. J. (2002) · The Journal of Infectious Diseases · doi:10.1086/340511 · Cited by 486 · see citing works
Fungal morphogenesis and host invasion
Gow, N. A. R., Brown, A. J. P., & Odds, F. C. (2002) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(02)00338-7 · Cited by 482 · see citing works
Pittet, D., Li, N., Woolson, R. F., & Wenzel, R. P. (1997) · Clinical Infectious Diseases · doi:10.1086/513640 · Cited by 295 · see citing works
Haynes, K. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02237-5 · Cited by 191 · see citing works
Self-citationHatherill, M., Tibby, S. M., Turner, C., Ratnavel, N., & Murdoch, I. A. (2000) · Critical Care Medicine · doi:10.1097/00003246-200007000-00068 · Cited by 179 · see citing works
Janbon, G., Himmelreich, U., Moyrand, F., Improvisi, L., & Dromer, F. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02651.x · Cited by 174 · see citing works
Virulence genes in the pathogenic yeastCandida albicans
Navarro-García, F., Sánchez, M., Nombela, C., & Plá, J. (2001) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2001.tb00577.x · Cited by 170 · see citing works
Overlapping and distinct roles of the duplicated yeast transcription factors Ace2p and Swi5p
Doolin, M., Johnson, A. L., Johnston, L. H., & Butler, G. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02388.x · Cited by 139 · see citing works
Self-citationTrends in Antifungal Use and Epidemiology of Nosocomial Yeast Infections in a University Hospital
Berrouane, Y. F., Herwaldt, L. A., & Pfaller, M. A. (1999) · Journal of Clinical Microbiology · doi:10.1128/jcm.37.3.531-537.1999 · Cited by 136 · see citing works
A Saccharomyces cerevisiae mutant with increased virulence
Wheeler, R. T., Kupiec, M., Magnelli, P. E., Abeijón, C., & Fink, G. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437995100 · Cited by 99 · see citing works
O'CONALLAIN, C., Doolin, M., Taggart, C. C., Thornton, F., & Butler, G. (1999) · Molecular and General Genetics MGG · doi:10.1007/s004380051084 · Cited by 96 · see citing works
Self-citationACE2, an activator of yeast metallothionein expression which is homologous to SWI5.
Butler, G., & Thiele, D. J. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.1.476 · Cited by 89 · see citing works
Self-citationEmerging Evidence of Selection of Fluconazole-Tolerant Fungi in Surgical Intensive Care Units
Gleason, T. G. (1997) · Archives of Surgery · doi:10.1001/archsurg.1997.01430350047008 · Cited by 83 · see citing works
Isolation of a Candida glabrata centromere and its use in construction of plasmid vectors
Kitada, K., Yamaguchi, E., & Arisawa, M. (1996) · Gene · doi:10.1016/0378-1119(96)00132-1 · Cited by 70 · see citing works
Calcagno-Pizarelli, A. M., Bignell, E., Warn, P. A., Jones, M. D., Denning, D. W., Mühlschlegel, F. A., Rogers, T. R., & Haynes, K. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03755.x · Cited by 70 · see citing works
Self-citationHypervirulence and pathogen fitness
Foreman-Wykert, A. K., & Miller, J. F. (2003) · Trends in Microbiology · doi:10.1016/s0966-842x(03)00007-6 · Cited by 55 · see citing works
Weig, M., Haynes, K., Rogers, T. R., Kurzai, O., Frosch, M., & Mühlschlegel, F. A. (2001) · Microbiology · doi:10.1099/00221287-147-8-2007 · Cited by 46 · see citing works
Self-citationACE2, an Activator of Yeast Metallothionein Expression Which Is Homologous to SWI5
Butler, G., & Thiele, D. J. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.1.476-485.1991 · Cited by 32 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
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
Ferrari, S., Ischer, F., Calabrese, D., Posteraro, B., Sanguinetti, M., Fadda, G., Rohde, B., Bauser, C., Bader, O., & Sanglard, D. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000268 · Cited by 295 · see citing works
A yeast by any other name: Candida glabrata and its interaction with the host
Kaur, R., Domergue, R., Zupancic, M. L., & Cormack, B. P. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.06.012 · Cited by 271 · see citing works
Candida glabrata , an Emerging Oral Opportunistic Pathogen
Li, L., Redding, S. W., & Dongari‐Bagtzoglou, A. I. (2007) · Journal of Dental Research · doi:10.1177/154405910708600304 · Cited by 238 · see citing works
Schwarzmüller, T., Ma, B., Hiller, E., Istel, F., Tscherner, M., Brunke, S., Ames, L., Firon, A., Green, B., Cabral, V., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004211 · Cited by 191 · see citing works
Self-citationThe <i>Candida albicans CaACE2</i> gene affects morphogenesis, adherence and virulence
Kelly, M. T., MacCallum, D. M., Clancy, S. D., Odds, F. C., Brown, A. J. P., & Butler, G. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04185.x · Cited by 175 · see citing works
Self-citationNovel Agents and Drug Targets to Meet the Challenges of Resistant Fungi
McCarthy, M. W., Kontoyiannis, D. P., Cornely, O. A., Perfect, J. R., & Walsh, T. J. (2017) · The Journal of Infectious Diseases · doi:10.1093/infdis/jix130 · Cited by 169 · see citing works
Roetzer, A., Gabaldón, T., & Schüller, C. (2011) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.02102.x · Cited by 154 · see citing works
Nobile, C. J., Solis, N., Myers, C. L., Fay, A. J., Deneault, J.-S., Nantel, A., Mitchell, A. P., & Filler, S. G. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01198.x · Cited by 150 · see citing works
Ferrari, S., Sanguinetti, M., De Bernardis, F., Torelli, R., Posteraro, B., Vandeputte, P., & Sanglard, D. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01271-10 · Cited by 144 · see citing works
Portrait of Candida Species Biofilm Regulatory Network Genes
Araújo, D., Henriques, M., & Silva, S. M. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.09.004 · Cited by 135 · see citing works
Mulhern, S. M., Logue, M. E., & Butler, G. (2006) · Eukaryotic Cell · doi:10.1128/ec.00155-06 · Cited by 130 · see citing works
Self-citationCandida glabrata: A Lot More Than Meets the Eye
Kumar, K., Askari, F., Sahu, M. S., & Kaur, R. (2019) · Microorganisms · doi:10.3390/microorganisms7020039 · Cited by 128 · see citing works
Roetzer, A., Gregori, C., Jennings, A. M., Quintin, J., Ferrandon, D., Butler, G., Kuchler, K., Ammerer, G., & Schüller, C. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06301.x · Cited by 124 · see citing works
Self-citationMaubon, D., Park, S., Tanguy, M., Huerre, M., Schmitt, C., Prévost, M., Perlin, D. S., Latgé, J., & Beauvais, A. (2006) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2006.01.006 · Cited by 123 · see citing works
Intracellular survival ofCandida glabratain macrophages: immune evasion and persistence
Kasper, L., Seider, K., & Hube, B. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov042 · Cited by 115 · see citing works
Hull, C. M., Parker, J. E., Bader, O., Weig, M., Gross, U., Warrilow, A. G. S., Kelly, D. E., & Kelly, S. L. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.06253-11 · Cited by 113 · see citing works
Dünkler, A., Walther, A., Specht, C. A., & Wendland, J. (2005) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2005.08.001 · Cited by 98 · see citing works
Oud, B., Medina, V. G., Nijkamp, J. F., de Ridder, D., Pronk, J. T., van Maris, A. J. A., & Daran, J.-M. G. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305949110 · Cited by 93 · see citing works
Romano, J., Nimrod, G., Ben‐Tal, N., Shadkchan, Y., Baruch, K., Sharon, H., & Osherov, N. (2006) · Microbiology · doi:10.1099/mic.0.28936-0 · Cited by 88 · see citing works
Hosting Infection: Experimental Models to AssayCandidaVirulence
MacCallum, D. M. (2011) · International Journal of Microbiology · doi:10.1155/2012/363764 · Cited by 80 · see citing works
Rapid evolution of an adaptive multicellular morphology of Candida auris during systemic infection
Bing, J., Guan, Z., Zheng, T., Ennis, C. L., Nobile, C. J., Chen, C., Chu, H., & Huang, G. (2024) · Nature Communications · doi:10.1038/s41467-024-46786-8 · Cited by 74 · see citing works
Interaction of pathogenic fungi with host cells: Molecular and cellular approaches.
Mendes-Giannini, M., Soares, C., da Silva, J. L. M., & Andreotti, P. F. (2005) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2005.05.014 · Cited by 71 · see citing works
Lowman, D. W., West, L. J., Bearden, D. W., Wempe, M. F., Power, T. D., Ensley, H. E., Haynes, K., Williams, D. L., & Kruppa, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027614 · Cited by 74 · see citing works
Self-citationMutation of the Regulator of G Protein Signaling Crg1 Increases Virulence in Cryptococcus neoformans
Wang, P., Cutler, J. E., King, J., & Palmer, D. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.4.1028-1035.2004 · Cited by 70 · see citing works
The RAM network in pathogenic fungi
Saputo, S., Chabrier-Rosello, Y., Luca, F. C., Kumar, A., & Krysan, D. J. (2012) · Eukaryotic Cell · doi:10.1128/ec.00044-12 · Cited by 65 · see citing works
Brunke, S., Seider, K., Fischer, D., Jacobsen, I. D., Kasper, L., Jablonowski, N., Wartenberg, A., Bader, O., Angoulvant, A., Schaller, M., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004478 · Cited by 62 · see citing works
Differential virulence of Candida glabrata glycosylation mutants
West, L., Lowman, D. W., Mora-Montes, H. M., Grubb, S., Murdoch, C., Thornhill, M. H., Gow, N. A. R., Williams, D., & Haynes, K. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.478743 · Cited by 62 · see citing works
Self-citationPathogenesis and Antifungal Drug Resistance of the Human Fungal Pathogen Candida glabrata
Tscherner, M., Schwarzmüller, T., & Kuchler, K. (2011) · Pharmaceuticals · doi:10.3390/ph4010169 · Cited by 60 · see citing works
Gregori, C., Schüller, C., Roetzer, A., Schwarzmüller, T., Ammerer, G., & Kuchler, K. (2007) · Eukaryotic Cell · doi:10.1128/ec.00106-07 · Cited by 57 · see citing works
Ejzykowicz, D. E., da Cunha, M. M. L., Rozental, S., Solis, N. V., Gravelat, F. N., Sheppard, D. C., & Filler, S. G. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06631.x · Cited by 47 · see citing works
Deletion of <i>ADA2</i> Increases Antifungal Drug Susceptibility and Virulence in Candida glabrata
Yu, S.-J., Chang, Y.-L., & Chen, Y.-L. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01924-17 · Cited by 43 · see citing works
MacCallum, D. M., Findon, H., Kenny, C. C., Butler, G., Haynes, K., & Odds, F. C. (2006) · Infection and Immunity · doi:10.1128/iai.00817-06 · Cited by 45 · see citing works
Self-citationCandida glabrata : a deadly companion?
Bolotin‐Fukuhara, M., & Fairhead, C. (2014) · Yeast · doi:10.1002/yea.3019 · Cited by 42 · see citing works
Li, L., Kashleva, H., & Dongari‐Bagtzoglou, A. I. (2007) · Microbial Pathogenesis · doi:10.1016/j.micpath.2006.12.003 · Cited by 40 · see citing works
Aspergillus fumigatusvirulence through the lens of transcription factors: Table 1.
Bultman, K. M., Kowalski, C. H., & Cramer, R. A. (2016) · Medical Mycology · doi:10.1093/mmy/myw120 · Cited by 35 · see citing works
Pais, P., Costa, C., Cavalheiro, M., Romão, D., & Teixeira, M. C. (2016) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2016.00131 · Cited by 32 · see citing works
Malavia-Jones, D., Farrer, R. A., Stappers, M. H. T., Edmondson, M. B., Borman, A. M., Johnson, E. M., Lipke, P. N., & Gow, N. A. R. (2023) · The Cell Surface · doi:10.1016/j.tcsw.2023.100110 · Cited by 29 · see citing works
Impact of the transcriptional regulator, Ace2, on the Candida glabrata secretome
Stead, D., Walker, J., Holcombe, L. J., Gibbs, S. R. S., Yin, Z., Selway, L., Butler, G., Brown, A. J. P., & Haynes, K. (2009) · PROTEOMICS · doi:10.1002/pmic.200800706 · Cited by 29 · see citing works
Self-citationBateman, S. L., & Seed, P. C. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.07977.x · Cited by 28 · see citing works
Alex, D., Gay‐Andrieu, F., May, J. P., Thampi, L. M., Dou, D., Mooney, A., Groutas, W. C., & Calderone, R. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00477-12 · Cited by 28 · see citing works
Westwater, C., Schofield, D. A., Nicholas, P. J., Paulling, E. E., & Balish, E. (2007) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2007.00287.x · Cited by 28 · see citing works
Xiong, D., Wang, Y., Deng, C., Hu, R., & Tian, C. (2015) · Gene · doi:10.1016/j.gene.2015.02.063 · Cited by 25 · see citing works
The trans-kingdom identification of negative regulators of pathogen hypervirulence
Brown, N. A., Urban, M., & Hammond-Kosack, K. E. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv042 · Cited by 25 · see citing works
Amn1 governs post-mitotic cell separation in Saccharomyces cerevisiae
Fang, O., Hu, X., Wang, L., Jiang, N., Yang, J., Li, B., & Luo, Z. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007691 · Cited by 23 · see citing works
Global Secretome Characterization of the Pathogenic Yeast Candida glabrata
Rasheed, M., Kumar, N., & Kaur, R. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00299 · Cited by 23 · see citing works
Stead, D., Findon, H., Yin, Z., Walker, J., Selway, L., Cash, P., Dujon, B., Hennequin, C., Brown, A. J. P., & Haynes, K. (2005) · PROTEOMICS · doi:10.1002/pmic.200401064 · Cited by 22 · see citing works
Self-citationRecent Advances in Understanding the Human Fungal Pathogen Hypoxia Response in Disease Progression
Puerner, C. T. S., Vellanki, S., Strauch, J. L., & Cramer, R. A. (2023) · Annual Review of Microbiology · doi:10.1146/annurev-micro-032521-021745 · Cited by 20 · see citing works
Human albumin enhances the pathogenic potential of Candida glabrata on vaginal epithelial cells
Pekmezovic, M. G., Kaune, A.-K., Austermeier, S., Hitzler, S. U. J., Mogavero, S., Hovhannisyan, H., Gabaldón, T., Gresnigt, M. S., & Hube, B. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1010037 · Cited by 19 · see citing works
McClelland, E. E., Ramagopal, U. A., Rivera, J., Cox, J. E., Nakouzi, A. S., Prabu, M. M., Almo, S. C., & Casadevall, A. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005849 · Cited by 19 · see citing works
Ranjith, K., Chakravarthy, S. K., Adicherla, H., Sharma, S., & Shivaji, S. (2018) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.17-22933 · Cited by 17 · see citing works
The virulence of Aspergillus fumigatus
Osherov, N. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6397-8_8 · Cited by 15 · see citing works
Dekker, N., de Haan, A., & Hochstenbach, F. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.04.061 · Cited by 13 · see citing works
Balakumar, A., Cox, A., & Thangamani, S. (2024) · mSphere · doi:10.1128/msphere.00734-24 · Cited by 12 · see citing works
Revealing Candida glabrata biofilm matrix proteome: global characterization and pH response
Gonçalves, B., Azevedo, N. F., Osório, H., Henriques, M., & Silva, S. M. (2021) · Biochemical Journal · doi:10.1042/bcj20200844 · Cited by 11 · see citing works
Kottom, T. J., & LIMPER, A. H. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.471243 · Cited by 9 · see citing works
Roles of Elm1 in antifungal susceptibility and virulence in Candida glabrata
Ito, Y., Miyazaki, T., Tanaka, Y., Suematsu, T., Nakayama, H., Morita, A., Hirayama, T., Tashiro, M., Takazono, T., Saijo, T., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-66620-7 · Cited by 8 · see citing works
Evolution of regulatory networks inCandida glabrata: learning to live with the human host
Roy, S., & Thompson, D. A. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov087 · Cited by 7 · see citing works
Ding, Z., HuiJiao, L., Liu, L., Lu, T., Xu, Y., Peng, J., Ren, Y., Peng, J., Xu, T., & Zhang, X. (2024) · Fungal Biology · doi:10.1016/j.funbio.2024.06.002 · Cited by 5 · see citing works
Clumping Morphology Influences Virulence Uncoupled from Echinocandin Resistance in Candida glabrata
Hu, C., Fong, G. R., Wurster, S., Kontoyiannis, D. P., & Beyda, N. D. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01837-21 · Cited by 5 · see citing works
Experimental evolution of multicellularity via cuboidal cell packing in fission yeast
Pineau, R. M., Kahn, P. C., Lac, D. T., Belpaire, T. E. R., Denning, M. G., Wong, W., Ratcliff, W. C., & Bozdag, G. O. (2024) · Evolution Letters · doi:10.1093/evlett/qrae024 · Cited by 4 · see citing works
Lertwattanasakul, N., Pattanakittivorakul, S., Nitiyon, S., Matsutani, M., Oguchi, A., Hirata, K., Kosaka, T., Limtong, S., & Yamada, M. C. (2023) · Fuels · doi:10.3390/fuels4040029 · Cited by 4 · see citing works
Host-Fungal Interactions: Pathogenicity versus Immunity
Tavanti, A., Naglik, J. R., & Osherov, N. (2012) · International Journal of Microbiology · doi:10.1155/2012/562480 · Cited by 3 · see citing works
Biofilm Formation in Candida Species
Elibe, M. I., & Innocent, N. E. (2024) · Springer eBooks · doi:10.1007/978-981-97-4909-6_9 · Cited by 2 · see citing works
Evolution of PathogenicCandidaSpecies
Odds, F. C. (2014) · ASM Press eBooks · doi:10.1128/9781555815639.ch47 · Cited by 2 · see citing works
Lilić, D., & Haynes, K. (2007) · Springer eBooks · doi:10.1007/1-4020-5492-0_16 · Cited by 2 · see citing works
Self-citationCandida glabrata and the host: a neglected affair
Ghosh, M., Raney, M., & Kaur, R. (2026) · Journal of Medical Microbiology · doi:10.1099/jmm.0.002161 · Cited by 1 · see citing works
Using Bioluminescence to Image Candida glabrata Urinary Tract Infections in Mice
Schrevens, S., Torelli, R., Sanguinetti, M., & Sanglard, D. (2023) · Methods in molecular biology · doi:10.1007/978-1-0716-3155-3_17 · Cited by 1 · see citing works
Novel strategies for engineering redox metabolism in Saccharomyces cerevisiae
Medina, V. G. (2013) · Research Repository (Delft University of Technology) · doi:10.4233/uuid:a3795084-4b85-40e9-9ba1-b545408954a2 · Cited by 1 · see citing works
Regulators of Candida glabrata Pathogenicity
Haynes, K. (2006) · Springer eBooks · doi:10.1007/3-540-30809-1_11
Self-citationChapter 7 Ace2 and fungal virulence
Findon, H., & Haynes, K. (2008) · The British Mycological Society symposium series · doi:10.1016/s0275-0287(08)80049-5
Self-citationGenome dynamics and virulence in the human pathogen Candida glabrata
Ahmad, K. M. (2014) · Lund University Publications (Lund University)
Mitotic Exit: Thresholds and Targets
Procko, A. L. (2025) · Digital Commons - RU (Rockefeller University) · doi:10.48496/pr4n-dh66
The Roles of Hsp90 and Calcineurin in Antifungal Drug Resistance
Singh, S. (2012) · TSpace (University of Toronto)
(2004) · Yeast · doi:10.1002/yea.1095
- Authors
- Kamran, M., Calcagno, A.-M., Findon, H., Bignell, E., Jones, M. D., Warn, P., Hopkins, P., Denning, D. W., Butler, G., Rogers, T., Mühlschlegel, F. A., & Haynes, K.
- Affiliations
- Imperial College London (GB)
- Department of Infectious Diseases, Imperial College London, London
- University of Manchester (GB)
- University College Dublin (IE)
- Research School of Biosciences, University of Kent Canterbury, United Kingdom
- Corresponding author
- Haynes, Ken
- ORCID
- Venue
- Eukaryotic Cell
- Publisher
- American Society for Microbiology
- Published
- 2004-04
- Volume
- 3
- Issue
- 2
- Pages
- 546-552
- ISSN
- 1535-9778 (ISSN-L)
- 1535-9786
- PMC
- PMC387657
- OpenAlex
- W2126597545
- Cited by
- 75
- References
- 31
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 1 · 2021: 2 · 2020: 1 · 2019: 2 · 2018: 3 · 2017: 1 · 2016: 4 · 2015: 4 · 2014: 5 · 2013: 4 · 2012: 6
- FWCI
- 4.05
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Locations
- Eukaryotic Cell (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Kent Academic Repository (University of Kent) (submittedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- Wellcome Trust
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Candida glabrata, hypervirulence, fungal virulence, invasive candidiasis, host-pathogen interaction, innate immune response, inflammatory cytokines, systemic fungal infection, tissue penetration, virulence genes
- MeSH terms
- Alleles, Animals, Candidiasis, Chitinases, DNA-Binding Proteins, Fungal Proteins, Interferon-gamma, Liver, Lung, Phenotype, Transcription Factors, Tumor Necrosis Factor-alpha, Virulence, Interleukin-6, Gene Silencing, Saccharomyces cerevisiae Proteins, Candida glabrata, Mice
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