The Hog1 Mitogen-Activated Protein Kinase Is Essential in the Oxidative Stress Response and Chlamydospore Formation in Candidaalbicans
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Candidaalbicans mutants with mutations in mitogen-activated protein (MAP) kinase HOG1 displayed an increased sensitivity to agents producing reactive oxygen species, such as oxidants (menadione, hydrogen peroxide, or potassium superoxide), and UV light. Consistent with this finding,C.albicans Hog1 was activated not only in response to an increase in external osmolarity, as happens with its Saccharomycescerevisiae homologue, but also in response to hydrogen peroxide. The Hog1-mediated response to oxidative stress was different from that of transcription factor Cap1, the homologue of S.cerevisiae Yap1, as shown by the different sensitivities to oxidants and the kinetics of cell death of cap1 Δ,hog1, and hog1cap1 Δ mutants. Deletion of CAP1 did not influence the level of Hog1 phosphorylation, and deletion of HOG1 did not affect Cap1 nuclear localization. Moreover, we show that the HOG1 gene plays a role in chlamydospore formation, another oxygen-related morphogenetic event, as demonstrated by the fact that hog1 cells were unable to generate these thick-walled structures in several media through a mechanism different from that of the EFG1 regulator. This is the first demonstration of the role of the Hog1-mediated MAP kinase pathway in resistance to oxidative stress in pathogenic fungi, and it allows us to propose a molecular model for the oxidative stress response in C.albicans.
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In C. albicans, Hog1 MAPK is a major regulator of fungal stress response, morphogenesis, and virulence.
“In C. albicans, Hog1 MAPK is a major regulator of fungal stress response, morphogenesis, and virulence (32–34, 36, 61).”
From The <i>Candida auris</i> Hog1 MAP kinase is essential for the colonization of murine skin and intradermal persistence (2024) · cites this paper as [32]
Cites
Exploring the metabolic and genetic control of gene expression on a genomic scale.
Derisi, J., Iyer, V., & Brown, P. (1997) · Science · doi:10.1126/science.278.5338.680 · Cited by 4,832 · see citing works
A MAP Kinase Targeted by Endotoxin and Hyperosmolarity in Mammalian Cells
Han, J., Lee, J. D., Bibbs, L., & Ulevitch, R. J. (1994) · Science · doi:10.1126/science.7914033 · Cited by 2,647 · see citing works
Isogenic strain construction and gene mapping in Candida albicans.
Fonzi, W. A., & Irwin, M. Y. (1993) · Genetics · doi:10.1093/genetics/134.3.717 · Cited by 1,695 · see citing works
Odds, F. C. (1979) · Medical Entomology and Zoology · Cited by 1,297 · see citing works
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
An Osmosensing Signal Transduction Pathway in Yeast
Brewster, J. L., de Valoir, T., Dwyer, N. D., Winter, E., & Gustin, M. C. (1993) · Science · doi:10.1126/science.7681220 · Cited by 1,248 · see citing works
Oxidative stress and the molecular biology of antioxidant defenses.
Scandalios, J. G. (1997) · Cited by 1,037 · see citing works
Parallel signal processing among mammalian MAPKs
Cano, E., & Mahadevan, L. C. (1995) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(00)88978-1 · Cited by 1,009 · see citing works
Root, R. K., Metcalf, J. A., Oshino, N., & Chance, B. (1975) · Journal of Clinical Investigation · doi:10.1172/jci108024 · Cited by 646 · see citing works
Stoldt, V. R., Sonneborn, A., Leuker, C. E., & Ernst, J. F. (1997) · The EMBO Journal · doi:10.1093/emboj/16.8.1982 · Cited by 595 · see citing works
H2O2 Release from Human Granulocytes during Phagocytosis
Root, R. K., & Metcalf, J. A. (1977) · Journal of Clinical Investigation · doi:10.1172/jci108886 · Cited by 587 · see citing works
An Osmosensing Signal Transduction Pathway in Mammalian Cells
Galcheva-Gargova, Z., Dérijard, B., Wu, I., & Davis, R. J. (1994) · Science · doi:10.1126/science.8047888 · Cited by 569 · see citing works
Yap1 and Skn7 Control Two Specialized Oxidative Stress Response Regulons in Yeast
Lee, J., Godon, C., Lagniel, G., Spector, D., Garin, J., Labarre, J., & Tolédano, M. B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.23.16040 · Cited by 567 · see citing works
H2O2 sensing through oxidation of the Yap1 transcription factor
Delaunay, A., Isnard, A., & Tolédano, M. B. (2000) · The EMBO Journal · doi:10.1093/emboj/19.19.5157 · Cited by 529 · see citing works
THE ROLE OF THE SIGMA FACTOR σs (KatF) IN BACTERIAL GLOBAL REGULATION
Loewen, P. C., & Hengge‐Aronis, R. (1994) · Annual Review of Microbiology · doi:10.1146/annurev.mi.48.100194.000413 · Cited by 526 · see citing works
Regulation of yAP‐1 nuclear localization in response to oxidative stress
Kuge, S., Jones, N., & Nomoto, A. (1997) · The EMBO Journal · doi:10.1093/emboj/16.7.1710 · Cited by 445 · see citing works
Christman, M. F., Storz, G., & Ames, B. N. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.10.3484 · Cited by 436 · see citing works
Shiozaki, K., & Russell, P. R. (1996) · Genes & Development · doi:10.1101/gad.10.18.2276 · Cited by 427 · see citing works
Regulation of gene expression by oxygen in Saccharomyces cerevisiae
Zitomer, R. S., & Lowry, C. V. (1992) · Microbiological Reviews · doi:10.1128/mr.56.1.1-11.1992 · Cited by 413 · see citing works
O’Rourke, S. M., & Herskowitz, I. (1998) · Genes & Development · doi:10.1101/gad.12.18.2874 · Cited by 396 · see citing works
Wilkinson, M. G., Samuels, M., Takeda, T., Toone, W. M., Shieh, J., Toda, T., Millar, J. B. A., & Jones, N. (1996) · Genes & Development · doi:10.1101/gad.10.18.2289 · Cited by 373 · see citing works
Alonso-Monge, R., Navarro-García, F., Molero, G., Diez-Orejas, R., Gustin, M., Pla, J., Sánchez, M., & Nombela, C. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.10.3058-3068.1999 · Cited by 344 · see citing works
Self-citationMartı́n, H., Rodrı́guez-Pachón, J. M., Ruiz, C., Nombela, C., & Molina, M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.2.1511 · Cited by 343 · see citing works
Self-citationToone, W. M., Kuge, S., Samuels, M., Morgan, B. A., Toda, T., & Jones, N. (1998) · Genes & Development · doi:10.1101/gad.12.10.1453 · Cited by 305 · see citing works
Activation and Regulation of the Spc1 Stress-Activated Protein Kinase in Schizosaccharomyces pombe
Degols, G., Shiozaki, K., & Russell, P. R. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.6.2870 · Cited by 301 · see citing works
Morgan, B. A., Banks, G. R., Toone, W. M., Raitt, D., Kuge, S., & Johnston, L. H. (1997) · The EMBO Journal · doi:10.1093/emboj/16.5.1035 · Cited by 291 · see citing works
Köhler, J. R., & Fink, G. R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.23.13223 · Cited by 283 · see citing works
The molecular defences against reactive oxygen species in yeast
Moradas‐Ferreira, P., Costa, V., Piper, P. W., & Mager, W. H. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.403940.x · Cited by 267 · see citing works
Alarco, A., & Raymond, M. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.3.700-708.1999 · Cited by 244 · see citing works
Redox signaling and gene control in the Escherichia coli soxRS oxidative stress regulon — a review
Demple, B. (1996) · Gene · doi:10.1016/s0378-1119(96)00329-0 · Cited by 239 · see citing works
Harshman, K., Moye-Rowley, S., & Parker, C. S. (1988) · Cell · doi:10.1016/0092-8674(88)90393-5 · Cited by 239 · see citing works
Saccharomyces cerevisiae has distinct adaptive responses to both hydrogen peroxide and menadione
Jamieson, D. J. (1992) · Journal of Bacteriology · doi:10.1128/jb.174.20.6678-6681.1992 · Cited by 235 · see citing works
Macrophages in resistance to candidiasis
Vázquez‐Torres, A., & Balish, E. (1997) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.61.2.170-192.1997 · Cited by 233 · see citing works
Estruch, F., & Carlson, M. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.7.3872-3881.1993 · Cited by 221 · see citing works
Proft, M., Pascual‐Ahuir, A., de Nadal, E., Ariño, J., Serrano, R., & Posas, F. (2001) · The EMBO Journal · doi:10.1093/emboj/20.5.1123 · Cited by 218 · see citing works
Quinn, J., Findlay, V. J., Dawson, K., Millar, J. B. A., Jones, N., Morgan, B. A., & Toone, W. M. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.01-06-0288 · Cited by 209 · see citing works
Alarco, A., Balan, I., Talibi, D., Mainville, N., & Raymond, M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.31.19304 · Cited by 206 · see citing works
Stephen, D. W. S., Rivers, S. L., & Jamieson, D. J. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.tb02407.x · Cited by 206 · see citing works
Schnell, N. F., Krems, B., & Entian, K. (1992) · Current Genetics · doi:10.1007/bf00351681 · Cited by 205 · see citing works
Cloning and Sequencing of a Candida albicans Catalase Gene and Effects of Disruption of This Gene
Wysong, D. R., Christin, L., Sugar, A. M., Robbins, P. W., & Diamond, R. D. (1998) · Infection and Immunity · doi:10.1128/iai.66.5.1953-1961.1998 · Cited by 201 · see citing works
Kobayashi, N., & McEntee, K. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.1.248-256.1993 · Cited by 196 · see citing works
Evolution of Osmotic Stress Signaling Via Map Kinase Cascades
Kültz, D., & Burg, M. B. (1998) · Journal of Experimental Biology · doi:10.1242/jeb.201.22.3015 · Cited by 194 · see citing works
Köhler, G. A., White, T. C., & Agabian, N. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.7.2331-2338.1997 · Cited by 190 · see citing works
Navarro-García, F., Sánchez, M., Plá, J., & Nombela, C. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.4.2197 · Cited by 182 · see citing works
Self-citationChaturvedi, V, Wong, B., & Newman, S. L. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.10.3836 · Cited by 180 · cited 1× · see citing works
“Other responses of pathogenic fungi to natural oxidative stress are the blocking of the macrophage oxidative burst in Histoplasma capsulatum (29); the production of polyols, such as mannitol, to scavenge reactive oxygen intermediates in Cryptococcus neoformans (7); and the activation of a TEY-MAP kinase-mediated pathw…”
BackgroundJosé, C. S., Monge, R. A., Pérez‐Díaz, R. M., Plá, J., & Nombela, C. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.19.5850-5852.1996 · Cited by 180 · see citing works
Self-citationRep, M., Proft, M., Remize, F., Tamás, M. J., Serrano, R., Thevelein, J. M., & Hohmann, S. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02384.x · Cited by 179 · see citing works
Degols, G., & Russell, P. R. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.6.3356 · Cited by 174 · see citing works
Krems, B., Charizanis, C., & Entian, K. (1996) · Current Genetics · doi:10.1007/bf02208613 · Cited by 153 · see citing works
Zhang, X., De Micheli, M., Coleman, S. T., Sanglard, D., & Moye‐Rowley, W. S. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01877.x · Cited by 146 · see citing works
Yap1p Activates Gene Transcription in an Oxidant-Specific Fashion
Coleman, S. T., Epping, E. A., Steggerda, S. M., & Moye-Rowley, S. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.12.8302 · Cited by 144 · see citing works
Peroxynitrite contributes to the candidacidal activity of nitric oxide-producing macrophages
Vázquez‐Torres, A., Jones‐Carson, J., & Balish, E. (1996) · Infection and Immunity · doi:10.1128/iai.64.8.3127-3133.1996 · Cited by 137 · see citing works
Multiple modes of activation of the stress‐responsive MAP kinase pathway in fission yeast
Samejima, I., Mackie, S., & Fantes, P. A. (1997) · The EMBO Journal · doi:10.1093/emboj/16.20.6162 · Cited by 134 · see citing works
Gounalaki, N., & Thireos, G. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06720.x · Cited by 131 · see citing works
Cloning, analysis and one-step disruption of the ARG5,6 gene of Candida albicans
Negredo, A., Monteoliva, L., Gil, C., Plá, J., & Nombela, C. (1997) · Microbiology · doi:10.1099/00221287-143-2-297 · Cited by 129 · see citing works
Self-citationChlamydospore Formation in Candida albicans Requires the Efg1p Morphogenetic Regulator
Sonneborn, A., Bockmühl, D. P., & Ernst, J. F. (1999) · Infection and Immunity · doi:10.1128/iai.67.10.5514-5517.1999 · Cited by 126 · see citing works
Analysis of the adaptive oxidative stress response ofCandida albicans
Jamieson, D. J., Stephen, D. W. S., & ̈re, E. C. T. (1996) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1996.tb08139.x · Cited by 125 · see citing works
Singh, K. K. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00432-9 · Cited by 119 · see citing works
Recent Developments in Molecular Genetics of Candida Albicans
Backer, M. D. D., Magee, P. T., & Plá, J. (2000) · Annual Review of Microbiology · doi:10.1146/annurev.micro.54.1.463 · Cited by 109 · see citing works
Moradas‐Ferreira, P., & Costa, V. (2000) · Redox Report · doi:10.1179/135100000101535816 · Cited by 105 · see citing works
Bossier, P., Fernandes, L., Rocha, D. D., & Rodrigues‐Pousada, C. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)49510-0 · Cited by 82 · see citing works
The roles of glutathione and antioxidant enzymes in menadione-induced oxidative stress
Chiou, T.-J., & Tzeng, W.-F. (2000) · Toxicology · doi:10.1016/s0300-483x(00)00321-8 · Cited by 79 · see citing works
Oxidative Damage to DNA and Its RepairPreprint
Wallace, S. S. (1997) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969502.34.49 · Cited by 61 · see citing works
Flow cytometric analysis of Saccharomyces cerevisiae autolytic mutants and protoplasts
de la Fuente, J. M., Nombela, C., Sánchez, M., & Alvarez, A. M. (1992) · Yeast · doi:10.1002/yea.320080104 · Cited by 51 · see citing works
Self-citationPlá, J., Pérez‐Díaz, R. M., Navarro, F., Sánchez, M., & Nombela, C. (1995) · Gene · doi:10.1016/0378-1119(95)00492-o · Cited by 50 · see citing works
Self-citationNakagawa, C. W., Yamada, K., & MUTOH, N. (2000) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a022599 · Cited by 46 · see citing works
Fungal infection rates are increasing
Fox, J. L. (1993) · ASM news · Cited by 43 · see citing works
Fox, D. S., & Smulian, A. G. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01606.x · Cited by 34 · see citing works
The Oxygen Paradox: Biochemistry of Active OxygenPreprint
Hauptmann, N., & Cadenas, E. (1997) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969502.34.1 · Cited by 22 · see citing works
Signal transduction pathways and cell-wall construction in Candida albicans.
Navarro-García, F., Eisman, B., Román, E., Nombela, C., & Pla, J. (2001) · Medical Mycology · doi:10.1080/mmy.39.1.87.100 · Cited by 21 · see citing works
Self-citationDeactivation of macrophage oxidative burstin vitro by different strains ofHistoplasma capsulatum
Ikeda, T., & Little, J. R. (1995) · Mycopathologia · doi:10.1007/bf01103978 · Cited by 11 · see citing works
1996: A vintage year for yeast and Yeast
Goffeau, A. (1996) · Yeast · doi:10.1002/(sici)1097-0061(199612)12:16 · Cited by 2 · see citing works
Self-citationBiochemistry, cell biology and molecular biology of lipids ofSaccharomyces cerevisiae
Daum, G., Lees, N. D., Bard, M., & Dickson, R. (1998) · Yeast · doi:10.1002/(sici)1097-0061(199812)14:16
Flagged first, then by citations
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Sorted by citations
Biswas, S., Dijck, P. V., & Datta, A. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00009-06 · Cited by 516 · see citing works
Sensing the environment: lessons from fungi
Bahn, Y., Xue, C., Idnurm, A., Rutherford, J. C., Heitman, J., & Cardenas, M. E. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1578 · Cited by 416 · see citing works
Morphogenesis in Candida albicans
Whiteway, M. S., & Bachewich, C. (2007) · Annual Review of Microbiology · doi:10.1146/annurev.micro.61.080706.093341 · Cited by 390 · see citing works
Enjalbert, B., Smith, D. A., Cornell, M. J., Alam, I., Nicholls, S., Brown, A. J. P., & Quinn, J. (2006) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0501 · Cited by 381 · see citing works
Mitogen-Activated Protein Kinase Pathways and Fungal Pathogenesis
Zhao, X., Mehrabi, R., & Xu, J. (2007) · Eukaryotic Cell · doi:10.1128/ec.00216-07 · Cited by 367 · see citing works
Ene, I. V., Adya, A. K., Wehmeier, S., Brand, A. C., MacCallum, D. M., Gow, N. A. R., & Brown, A. J. P. (2012) · Cellular Microbiology · doi:10.1111/j.1462-5822.2012.01813.x · Cited by 313 · see citing works
Stress adaptation in a pathogenic fungus
Brown, A. J. P., Budge, S., Kaloriti, D., Tillmann, A., Jacobsen, M. D., Yin, Z., Ene, I. V., Bohovych, I., Sandai, D., Kastora, S., et al. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.088930 · Cited by 299 · see citing works
Oxidative Stress Responses in the Human Fungal Pathogen, Candida albicans
Dantas, A., Day, A., Ikeh, M., Kos, I., Achan, B., & Quinn, J. (2015) · Biomolecules · doi:10.3390/biom5010142 · Cited by 281 · see citing works
Bahn, Y., Kojima, K., Cox, G. M., & Heitman, J. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-11-0987 · Cited by 274 · see citing works
Yeast signaling pathways in the oxidative stress response
Ikner, A., & Shiozaki, K. (2004) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2004.09.006 · Cited by 267 · see citing works
Fuchs, B. B., & Mylonakis, E. (2009) · Eukaryotic Cell · doi:10.1128/ec.00193-09 · Cited by 266 · see citing works
Smith, D. A., Nicholls, S., Morgan, B. A., Brown, A. J. P., & Quinn, J. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-03-0181 · Cited by 263 · see citing works
The MAP kinase signal transduction network in Candida albicans
Alonso‐Monge, R., Román, E., Nombela, C., & Plá, J. (2006) · Microbiology · doi:10.1099/mic.0.28616-0 · Cited by 263 · see citing works
Self-citationGenomic Plasticity of the Human Fungal Pathogen Candida albicans
Selmecki, A., Forche, A., & Berman, J. (2010) · Eukaryotic Cell · doi:10.1128/ec.00060-10 · Cited by 247 · see citing works
Fungicide activity through activation of a fungal signalling pathway
Kojima, K., Takano, Y., Yoshimi, A., Tanaka, C., Kikuchi, T., & Okuno, T. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04244.x · Cited by 243 · see citing works
Antifungal Plant Defensins: Mechanisms of Action and Production
Vriens, K., Cammue, B. P. A., & Thevissen, K. (2014) · Molecules · doi:10.3390/molecules190812280 · Cited by 229 · see citing works
Missall, T. A., Lodge, J. K., & McEwen, J. E. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.4.835-846.2004 · Cited by 223 · see citing works
Segmüller, N., Ellendorff, U., Tudzynski, B., & Tudzynski, P. (2006) · Eukaryotic Cell · doi:10.1128/ec.00153-06 · Cited by 220 · see citing works
Comparative genomics of the environmental stress response in ascomycete fungi
Gasch, A. P. (2007) · Yeast · doi:10.1002/yea.1512 · Cited by 210 · see citing works
Phylogenetic diversity of stress signalling pathways in fungi
Nikolaou, E., Agrafioti, I., Stumpf, M., Quinn, J., Stansfield, I., & Brown, A. J. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-44 · Cited by 206 · see citing works
Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus
Chauhan, N., Latgé, J., & Calderone, R. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1426 · Cited by 197 · see citing works
Candida morphogenesis and host–pathogen interactions
Whiteway, M. S., & Oberholzer, U. (2004) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.06.005 · Cited by 196 · see citing works
Glucose Promotes Stress Resistance in the Fungal PathogenCandida albicans
Rodaki, A., Bohovych, I., Enjalbert, B., Young, T., Odds, F. C., Gow, N. A. R., & Brown, A. J. P. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-01-0002 · Cited by 192 · see citing works
Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance
Bilsland, E., Molin, C., Swaminathan, S., Ramne, A., & Sunnerhagen, P. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2004.04238.x · Cited by 191 · see citing works
Master and Commander in Fungal Pathogens: the Two-Component System and the HOG Signaling Pathway
Bahn, Y. (2008) · Eukaryotic Cell · doi:10.1128/ec.00323-08 · Cited by 175 · see citing works
The metabolic basis of Candida albicans morphogenesis and quorum sensing.
Han, T.-L., Cannon, R. D., & Villas-Bôas, S. G. (2011) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2011.04.002 · Cited by 173 · see citing works
Román, E., Nombela, C., & Plá, J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.23.10611-10627.2005 · Cited by 173 · see citing works
Self-citationNitrosative and oxidative stress responses in fungal pathogenicity
Brown, A. J. P., Haynes, K., & Quinn, J. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.06.007 · Cited by 167 · see citing works
Eisman, B., Alonso-Monge, R., Román, E., Arana, D., Nombela, C., & Pla, J. (2006) · Eukaryotic Cell · doi:10.1128/ec.5.2.347-358.2006 · Cited by 163 · see citing works
Self-citationFungal responses to reactive oxygen species
Aguirre, J., Hansberg, W., & Navarro, R. E. (2006) · Medical Mycology · doi:10.1080/13693780600900080 · Cited by 162 · see citing works
Role of reactive oxygen species in fungal cellular differentiations
Scott, B., & Eaton, C. J. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.10.008 · Cited by 161 · see citing works
Chauhan, N., Inglis, D., Roman, E., Pla, J., Li, D., Calera, J. A., & Calderone, R. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.5.1018-1024.2003 · Cited by 159 · see citing works
Selmecki, A., Bergmann, S., & Berman, J. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04492.x · Cited by 157 · see citing works
MAP kinase pathways as regulators of fungal virulence
Román, E., Arana, D. M., Nombela, C., Alonso‐Monge, R., & Plá, J. (2007) · Trends in Microbiology · doi:10.1016/j.tim.2007.02.001 · Cited by 158 · see citing works
Self-citationDuran, R. M., Cary, J. W., & Calvo, A. M. (2010) · Toxins · doi:10.3390/toxins2040367 · Cited by 155 · see citing works
Infection-related gene expression in Candida albicans
Brown, A. J. P., Odds, F. C., & Gow, N. A. R. (2007) · Current Opinion in Microbiology · doi:10.1016/j.mib.2007.04.001 · Cited by 148 · see citing works
Functional analysis of the MAPK pathways in fungi
Martínez‐Soto, D., & Ruíz-Herrera, J. (2017) · Revista Iberoamericana de Micología · doi:10.1016/j.riam.2017.02.006 · Cited by 141 · see citing works
Jain, R., Valiante, V., Remme, N., Docimo, T., Heinekamp, T., Hertweck, C., Gershenzon, J., Haas, H., & Brakhage, A. A. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07778.x · Cited by 140 · see citing works
The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans
Navarro-García, F., Eisman, B., Fiuza, S. M., Nombela, C., & Pla, J. (2005) · Microbiology · doi:10.1099/mic.0.28038-0 · Cited by 134 · see citing works
Self-citationNiche-Specific Activation of the Oxidative Stress Response by the Pathogenic Fungus Candida albicans
Enjalbert, B., MacCallum, D. M., Odds, F. C., & Brown, A. J. P. (2007) · Infection and Immunity · doi:10.1128/iai.01680-06 · Cited by 134 · 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
Ko, Y.-J., Yu, Y. M., Kim, G.-B., Lee, G.-W., Maeng, P. J., Kim, S., Floyd, A. M., Heitman, J., & Bahn, Y. (2009) · Eukaryotic Cell · doi:10.1128/ec.00120-09 · Cited by 132 · see citing works
Holland, L., Schröder, M., Turner, S. A., Taff, H. T., Andes, D. R., Grózer, Z., Gácser, A., Ames, L., Haynes, K., Higgins, D. G., et al. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004365 · Cited by 132 · see citing works
Mehrabi, R., Zwiers, L. H., Waard, M. A. D., & Kema, G. H. J. (2006) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-19-1262 · Cited by 130 · see citing works
Thioredoxin Regulates Multiple Hydrogen Peroxide-Induced Signaling Pathways in Candida albicans
Dantas, A. D. S., Patterson, M. J., Smith, D. A., MacCallum, D. M., Erwig, L. P., Morgan, B. A., & Quinn, J. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00313-10 · Cited by 126 · see citing works
Hayes, B. M. E., Bleackley, M. R., Wiltshire, J. L., Anderson, M. A., Traven, A., & van der Weerden, N. L. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00365-13 · Cited by 123 · see citing works
Mochon, A. B., & Liu, H. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000190 · Cited by 122 · see citing works
A Single MAPKKK Regulates the Hog1 MAPK Pathway in the Pathogenic Fungus Candida albicans
Cheetham, J., Smith, D. A., Dantas, A. D. S., Doris, K. S., Patterson, M. J., Bruce, C. R., & Quinn, J. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-06-0581 · Cited by 120 · see citing works
Jogawat, A., Vadassery, J., Verma, N., Oelmüller, R., Dua, M., Nevo, E., & Johri, A. K. (2016) · Scientific Reports · doi:10.1038/srep36765 · Cited by 119 · see citing works
Xue, T., Nguyen, C. K., Romans, A., & May, G. S. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.2.557-560.2004 · Cited by 117 · see citing works
Segorbe, D., Pietro, A. D., Pérez‐Nadales, E., & Turrà, D. (2016) · Molecular Plant Pathology · doi:10.1111/mpp.12446 · Cited by 116 · see citing works
Hog1 regulates stress tolerance and virulence in the emerging fungal pathogen Candida auris
Day, A. M., McNiff, M. M., da Silva Dantas, A., Gow, N. A. R., & Quinn, J. (2018) · mSphere · doi:10.1128/msphere.00506-18 · Cited by 116 · see citing works
Arana, D. M., Alonso‐Monge, R., Du, C., Calderone, R., & Plá, J. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00898.x · Cited by 116 · see citing works
Self-citationIdentification of the <i>Candida albicans</i> Cap1p Regulon
Znaidi, S., Barker, K. S., Weber, S., Alarco, A.-M., Liu, T. T., Boucher, G., Rogers, P. D., & Raymond, M. (2009) · Eukaryotic Cell · doi:10.1128/ec.00002-09 · Cited by 115 · see citing works
Román, E., Cottier, F., Ernst, J. F., & Pla, J. (2009) · Eukaryotic Cell · doi:10.1128/ec.00081-09 · Cited by 113 · see citing works
Du, C., Sarfati, J., Latgé, J. P., & Calderone, R. (2005) · Medical Mycology · doi:10.1080/13693780500338886 · Cited by 113 · see citing works
The Biology of Pichia membranifaciens Killer Toxins
Belda, I., Ruiz, J., Alonso, A., Marquina, D., & Santos, A. (2017) · Toxins · doi:10.3390/toxins9040112 · Cited by 111 · see citing works
Zhang, H., Liu, K., Zhang, X., Song, W., Zhao, Q., Dong, Y., Guo, M., Zheng, X., & Zhang, Z. (2010) · Current Genetics · doi:10.1007/s00294-010-0319-x · Cited by 110 · see citing works
SKN7 of Candida albicans : Mutant Construction and Phenotype Analysis
Singh, P., Chauhan, N., Ghosh, A. K., Dixon, F., & Calderone, R. (2004) · Infection and Immunity · doi:10.1128/iai.72.4.2390-2394.2004 · Cited by 110 · see citing works
Brown, A. J. P., Cowen, L. E., Pietro, A. D., & Quinn, J. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0048-2016 · Cited by 105 · see citing works
The Hog1 MAP kinase controls respiratory metabolism in the fungal pathogen Candida albicans
Alonso-Monge, R., Carvaihlo, S., Nombela, C., Rial, E., & Pla, J. (2009) · Microbiology · doi:10.1099/mic.0.023309-0 · Cited by 105 · see citing works
Self-citationNicholls, 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
Stress signalling to fungal stress-activated protein kinase pathways
Smith, D. A., Morgan, B. A., & Quinn, J. (2010) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.01937.x · Cited by 105 · see citing works
Thomas, E., Roman, E., Claypool, S., Manzoor, N., Pla, J., & Panwar, S. L. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00889-13 · Cited by 105 · see citing works
Arana, D. M., Nombela, C., Alonso‐Monge, R., & Plá, J. (2005) · Microbiology · doi:10.1099/mic.0.27723-0 · Cited by 104 · see citing works
Self-citationGalán-Díez, M., Arana, D. M., Serrano‐Gómez, D., Kremer, L., Casasnovas, J. M., Ortega, M., Cuesta‐Domínguez, Á., Corbí, A. L., Plá, J., & Fernández‐Ruiz, E. (2010) · Infection and Immunity · doi:10.1128/iai.00989-09 · Cited by 98 · see citing works
Prieto, D., Román, E., Correia, I., & Plá, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087128 · Cited by 95 · see citing works
Bambach, A., Fernandes, M. P., Ghosh, A., Kruppa, M., Alex, D., Li, D., Fonzi, W. A., Chauhan, N., Sun, N., Agrellos, O. A., et al. (2009) · Eukaryotic Cell · doi:10.1128/ec.00066-09 · Cited by 95 · see citing works
Reyes, G. H., Romans, A., Nguyen, C. K., & May, G. S. (2006) · Eukaryotic Cell · doi:10.1128/ec.00178-06 · Cited by 95 · see citing works
Staib, P., & Morschhäuser, J. (2006) · Mycoses · doi:10.1111/j.1439-0507.2006.01308.x · Cited by 94 · see citing works
Hayes, B. M. E., Anderson, M. A., Traven, A., van der Weerden, N. L., & Bleackley, M. R. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1573-8 · Cited by 93 · see citing works
ThHog1 controls the hyperosmotic stress response in Trichoderma harzianum
Delgado‐Jarana, J., Sousa, S., González, F., Rey, M., & Llobell, A. (2006) · Microbiology · doi:10.1099/mic.0.28729-0 · Cited by 92 · see citing works
Genetic control of chlamydospore formation in Candida albicans
Nobile, C. J., Bruno, V. M., Richard, M. L., Davis, D. A., & Mitchell, A. P. (2003) · Microbiology · doi:10.1099/mic.0.26640-0 · Cited by 89 · see citing works
Integrative Model of Oxidative Stress Adaptation in the Fungal Pathogen Candida albicans
Komalapriya, C., Kaloriti, D., Tillmann, A., Yin, Z., Herrero-de-Dios, C. M., Jacobsen, M. D., Belmonte, R. C., Cameron, G. A., Haynes, K., Grebogi, C., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137750 · Cited by 88 · see citing works
Vylkova, S., Jang, W. S., Li, W., Nayyar, N., & Edgerton, M. (2007) · Eukaryotic Cell · doi:10.1128/ec.00039-07 · Cited by 88 · see citing works
Kaloriti, D., Jacobsen, M. D., Yin, Z., Patterson, M. J., Tillmann, A., Smith, D. A., Cook, E., You, T., Grimm, M. J., Bohovych, I., et al. (2014) · mBio · doi:10.1128/mbio.01334-14 · Cited by 88 · see citing works
Farnesol signalling in Candida albicans – more than just communication
Polke, M., Leonhardt, I., Kurzai, O., & Jacobsen, I. D. (2017) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2017.1337711 · Cited by 87 · see citing works
Combinatorial stresses kill pathogenic<i>Candida</i>species
Kaloriti, D., Tillmann, A., Cook, E., Jacobsen, M., You, T., Lenardon, M., Ames, L., Barahona, M., Chandrasekaran, K., Coghill, G., et al. (2012) · Medical Mycology · doi:10.3109/13693786.2012.672770 · Cited by 86 · see citing works
Wang, Y., Tian, L., Xiong, D., Klosterman, S. J., Xiao, S., & Tian, C. (2016) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2016.01.011 · Cited by 84 · see citing works
Two-component signal transduction in human fungal pathogens
Kruppa, M., & Calderone, R. (2006) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2006.00024.x · Cited by 84 · see citing works
Yu, Q., Wang, H., Peng, Q., Li, Y., Liu, Z., & Li, M. (2017) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2017.04.026 · Cited by 81 · see citing works
Lee, C., Nantel, A., Jiang, L., Whiteway, M. S., & Shen, S. (2004) · Molecular Microbiology · doi:10.1111/j.1365-2958.2003.03879.x · Cited by 79 · see citing works
The high osmolarity glycerol (HOG) pathway in fungi †
Yaakoub, H., Sanchez, N. S., Ongay-Larios, L., Courdavault, V., Calenda, A., Bouchara, J.-P., Coria, R., & Papon, N. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2021.2011834 · Cited by 77 · see citing works
Chlamydospore Formation during Hyphal Growth in Cryptococcus neoformans
Lin, X., & Heitman, J. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.10.1746-1754.2005 · Cited by 77 · see citing works
Jin, K., Ming, Y., & Xia, Y. X. (2012) · Microbiology · doi:10.1099/mic.0.059469-0 · Cited by 76 · see citing works
The HOG MAPK pathway in Candida albicans: more than an osmosensing pathway
Román, E., Correia, I., Prieto, D., Alonso‐Monge, R., & Plá, J. (2019) · International Microbiology · doi:10.1007/s10123-019-00069-1 · Cited by 73 · see citing works
Self-citationRomán, E., Alonso‐Monge, R., Gong, Q., Li, D., Calderone, R., & Plá, J. (2009) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2009.00545.x · Cited by 70 · see citing works
Self-citationLow virulent strains of Candida albicans: Unravelling the antigens for a future vaccine
Fernández‐Arenas, E., Molero, G., Nombela, C., Diez‐Orejas, R., & Gil, C. (2004) · PROTEOMICS · doi:10.1002/pmic.200400929 · Cited by 69 · see citing works
Self-citationStress-Activated Protein Kinases in Human Fungal Pathogens
Day, A. M., & Quinn, J. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00261 · Cited by 68 · see citing works
Jin, Y., Weining, S., & Nevo, E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509653102 · Cited by 68 · see citing works
Moriwaki, A., Kubo, E., Arase, S., & Kihara, J. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00178.x · Cited by 67 · see citing works
Martin, S. W., Douglas, L. M., & Konopka, J. B. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.7.1191-1202.2005 · Cited by 66 · see citing works
Haque, F., Verma, N. K., Alfatah, M., Bijlani, S., & Bhattacharyya, M. S. (2019) · RSC Advances · doi:10.1039/c9ra07599b · Cited by 65 · see citing works
Role of Heat Shock Transcription Factor in Saccharomyces cerevisiae Oxidative Stress Response
Yamamoto, A., Ueda, J., Yamamoto, N., Hashikawa, N., & Sakurai, H. (2007) · Eukaryotic Cell · doi:10.1128/ec.00098-07 · Cited by 64 · see citing works
Lushchak, V. I. (2010) · Biochemistry (Moscow) · doi:10.1134/s0006297910030041 · Cited by 64 · see citing works
Abbey, D., Hickman, M. A., Gresham, D., & Berman, J. G. (2011) · G3 Genes Genomes Genetics · doi:10.1534/g3.111.000885 · Cited by 64 · see citing works
Fungi sensing environmental stress
Alonso‐Monge, R., Román, E., Arana, D. M., Plá, J., & Nombela, C. (2009) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2008.02690.x · Cited by 62 · see citing works
Self-citationYin, Z., Stead, D., Walker, J., Selway, L., Smith, D. A., Brown, A. J. P., & Quinn, J. (2009) · PROTEOMICS · doi:10.1002/pmic.200800958 · Cited by 62 · see citing works
Alonso‐Monge, R., Román, E., Arana, D. M., Prieto, D., Urrialde, V., Nombela, C., & Plá, J. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2010.03.009 · Cited by 62 · see citing works
Self-citationRegulation of Yeast-to-Hyphae Transition in Yarrowia lipolytica
Pomraning, K., Bredeweg, E., Kerkhoven, E. J., Barry, K., Haridas, S., Hundley, H. N., LaButti, K. M., Lipzen, A., Yan, M., Magnuson, J. K., et al. (2018) · mSphere · doi:10.1128/msphere.00541-18 · Cited by 59 · see citing works
- Authors
- Alonso-Monge, R., Navarro-García, F., Román, E., Negredo, A. I., Eisman, B., Nombela, C., & Pla, J.
- Affiliations
- Departamento de Microbiología II, Facultad de Farmacia, Universidad Complutense de Madrid, E-28040 Madrid, Spain
- Universidad Complutense de Madrid (ES)
- Venue
- Eukaryotic Cell
- Publisher
- American Society for Microbiology
- Published
- 2003-04
- Volume
- 2
- Issue
- 2
- Pages
- 351-361
- ISSN
- 1535-9778 (ISSN-L)
- 1535-9786
- PMC
- PMC154845
- OpenAlex
- W2146807721
- Cited by
- 308
- References
- 73
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 10 · 2023: 8 · 2022: 7 · 2021: 9 · 2020: 12 · 2019: 10 · 2018: 15 · 2017: 22 · 2016: 15 · 2015: 11 · 2014: 18 · 2013: 12 · 2012: 11
- FWCI
- 6.56
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Locations
- Eukaryotic Cell (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerio de Ciencia y Tecnología
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Keywords
- Hog1 MAP kinase, Candida albicans, oxidative stress response, chlamydospore formation, hydrogen peroxide, reactive oxygen species, EFG1, fungal pathogenicity, cell death
- MeSH terms
- Candida albicans, Cell Nucleus, Cells, Cultured, Fungal Proteins, Mutation, Osmolar Concentration, Phosphorylation, Spores, Fungal, Ultraviolet Rays, Organelles, Oxidants, Cell Death, Reactive Oxygen Species, Oxidative Stress, Cell Cycle Proteins, Mitogen-Activated Protein Kinases, MAP Kinase Signaling System, Saccharomyces cerevisiae Proteins, Basic-Leucine Zipper Transcription Factors
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