Activation of stress signalling pathways enhances tolerance of fungi to chemical fungicides and antifungal proteins
Open accessAbstract
Fungal disease is an increasing problem in both agriculture and human health. Treatment of human fungal disease involves the use of chemical fungicides, which generally target the integrity of the fungal plasma membrane or cell wall. Chemical fungicides used for the treatment of plant disease, have more diverse mechanisms of action including inhibition of sterol biosynthesis, microtubule assembly and the mitochondrial respiratory chain. However, these treatments have limitations, including toxicity and the emergence of resistance. This has led to increased interest in the use of antimicrobial peptides for the treatment of fungal disease in both plants and humans. Antimicrobial peptides are a diverse group of molecules with differing mechanisms of action, many of which remain poorly understood. Furthermore, it is becoming increasingly apparent that stress response pathways are involved in the tolerance of fungi to both chemical fungicides and antimicrobial peptides. These signalling pathways such as the cell wall integrity and high-osmolarity glycerol pathway are triggered by stimuli, such as cell wall instability, changes in osmolarity and production of reactive oxygen species. Here we review stress signalling induced by treatment of fungi with chemical fungicides and antifungal peptides. Study of these pathways gives insight into how these molecules exert their antifungal effect and also into the mechanisms used by fungi to tolerate sub-lethal treatment by these molecules. Inactivation of stress response pathways represents a potential method of increasing the efficacy of antifungal molecules.
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Stress response pathways are important for the integrity of the fungal cell wall and cell membrane and have been widely studied in antifungal tolerance and resistance.
“Stress response pathways are important for the integrity of fungal cell wall and cell membrane, thus have been widely studied in antifungal tolerance and resistance [66,67].”
From Antifungal persistence: Clinical relevance and mechanisms (2025) · cites this paper as [67]
Cites
Antimicrobial peptides of multicellular organisms
Zasloff, M. (2002) · Nature · doi:10.1038/415389a · Cited by 8,457 · see citing works
Jenssen, H., Hamill, P., & Hancock, R. E. W. (2006) · Clinical Microbiology Reviews · doi:10.1128/cmr.00056-05 · Cited by 2,532 · see citing works
Ghannoum, M. A., & Rice, L. B. (1999) · Clinical Microbiology Reviews · doi:10.1128/cmr.12.4.501 · Cited by 1,788 · see citing works
Cationic peptides: a new source of antibiotics
Hancock, R. E. W., & Lehrer, R. I. (1998) · Trends in biotechnology · doi:10.1016/s0167-7799(97)01156-6 · Cited by 1,348 · see citing works
The structure and synthesis of the fungal cell wall
Bowman, S. M., & Free, S. J. (2006) · BioEssays · doi:10.1002/bies.20441 · Cited by 1,320 · see citing works
Acquired Antibiotic Resistance Genes: An Overview
van Hoek, A. H. A. M., Mevius, D. J., Guerra, B., Mullany, P. P., Roberts, A. P., & Aarts, H. J. M. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00203 · Cited by 1,150 · see citing works
Cell Wall Integrity Signaling in <i>Saccharomyces cerevisiae</i>
Levin, D. E. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.2.262-291.2005 · Cited by 1,136 · see citing works
Denning, D. W. (2003) · The Lancet · doi:10.1016/s0140-6736(03)14472-8 · Cited by 1,131 · see citing works
A two-component system that regulates an osmosensing MAP kinase cascade in yeast
Maeda, T., Wurgler‐Murphy, S. M., & Saito, H. (1994) · Nature · doi:10.1038/369242a0 · Cited by 1,084 · see citing works
MAP Kinase Pathways in the YeastSaccharomyces cerevisiae
Gustin, M., Albertyn, J., Alexander, M., & Davenport, K. (1998) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.62.4.1264-1300.1998 · Cited by 1,010 · see citing works
Posas, F., Wurgler‐Murphy, S. M., Maeda, T., Witten, E. A., Thai, T. C., & Saito, H. (1996) · Cell · doi:10.1016/s0092-8674(00)80162-2 · Cited by 881 · see citing works
Levin, D. E. (2011) · Genetics · doi:10.1534/genetics.111.128264 · Cited by 827 · see citing works
Activation of Yeast PBS2 MAPKK by MAPKKKs or by Binding of an SH3-Containing Osmosensor
Maeda, T., Takekawa, M., & Saito, H. (1995) · Science · doi:10.1126/science.7624781 · Cited by 640 · see citing works
García‐Olmedo, F., Molina, A., Alamillo, J. M., & Rodríguez‐Palenzuela, P. (1998) · Biopolymers · doi:10.1002/(sici)1097-0282(1998)47:6 · Cited by 521 · see citing works
Response to Hyperosmotic Stress
Saito, H., & Posas, F. (2012) · Genetics · doi:10.1534/genetics.112.140863 · Cited by 502 · see citing works
Kamada, Y., Jung, U. S., Piotrowski, J., & Levin, D. E. (1995) · Genes & Development · doi:10.1101/gad.9.13.1559 · Cited by 488 · see citing works
Hou, Z., Xue, C., Peng, Y., et al. (2002) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.2002.15.11.1119 · Cited by 475 · see citing works
Xu, J., Staiger, C. J., & Hamer, J. E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.21.12713 · Cited by 460 · see citing works
Stimulation of Chitin Synthesis Rescues Candida albicans from Echinocandins
Walker, L. A., Munro, C. A., de Bruijn, I., Lenardon, M. D., McKinnon, A., & Gow, N. A. R. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000040 · Cited by 445 · see citing works
Cunningham, K. W., & Fink, G. R. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.5.2226 · Cited by 431 · see citing works
Jung, U. S., & Levin, D. E. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01667.x · Cited by 424 · see citing works
Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin β homologs NMD5 and XPO1
Ferrigno, P. K., Posas, F., Koepp, D. M., Saito, H., & Silver, P. A. (1998) · The EMBO Journal · doi:10.1093/emboj/17.19.5606 · Cited by 417 · see citing works
MAP Kinases in Fungal Pathogens
Xu, J. (2000) · Fungal Genetics and Biology · doi:10.1006/fgbi.2000.1237 · Cited by 408 · 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
A Yeast Mitogen-Activated Protein Kinase Homolog (Mpk1p) Mediates Signalling by Protein Kinase C
Lee, K. S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., Matsumoto, K., & Levin, D. E. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.5.3067 · Cited by 377 · see citing works
Multifunctional host defense peptides: intracellular‐targeting antimicrobial peptides
Nicolas, P. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07359.x · Cited by 366 · see citing works
Hsp90 Governs Echinocandin Resistance in the Pathogenic Yeast Candida albicans via Calcineurin
Singh, S. D., Robbins, N., Zaas, A. K., Schell, W. A., Perfect, J. R., & Cowen, L. E. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000532 · Cited by 362 · see citing works
Defensins from Insects and Plants Interact with Fungal Glucosylceramides
Thevissen, K., Warnecke, D. C., François, I., Leipelt, M., Heinz, E., Ott, C., Zähringer, U., Thomma, B. P. H. J., Ferket, K. K. A., & Cammue, B. P. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m311165200 · Cited by 355 · see citing works
Amphotericin B: new life for an old drug
Hartsel, S. C., & Bolard, J. (1996) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(96)01012-7 · Cited by 352 · see citing works
Dixon, K. P., Xu, J., Smirnoff, N., et al. (1999) · The Plant Cell · doi:10.1105/tpc.11.10.2045 · Cited by 350 · 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
Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress.
Cyert, M. S. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(03)01552-3 · Cited by 333 · see citing works
Matheos, D. P., Kingsbury, T. J., Ahsan, U. S., & Cunningham, K. W. (1997) · Genes & Development · doi:10.1101/gad.11.24.3445 · Cited by 332 · see citing works
LaFayette, S. L., Collins, C., Zaas, A. K., Schell, W. A., Betancourt-Quiroz, M., Gunatilaka, A. A. L., Perfect, J. R., & Cowen, L. E. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001069 · Cited by 329 · see citing works
Guo, M., Chen, Y., Du, Y., Dong, Y., Guo, W., Zhai, S., Zhang, H., Dong, S., Zhang, Z., Wang, Y., et al. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1001302 · Cited by 325 · see citing works
Munro, C. A., Selvaggini, S., De Bruijn, I., Walker, L., Lenardon, M. D., Gerssen, B., Milne, S., Brown, A. J. P., & Gow, N. A. R. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05588.x · Cited by 309 · see citing works
Alonso-Monge, R., Navarro-García, F., Román, E., Negredo, A. I., Eisman, B., Nombela, C., & Pla, J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.2.351-361.2003 · Cited by 308 · see citing works
Onyewu, C., Blankenship, J. R., Del Poeta, M., & Heitman, J. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.3.956-964.2003 · Cited by 282 · see citing works
Properties and mechanisms of action of naturally occurring antifungal peptides
van der Weerden, N. L., Bleackley, M. R., & Anderson, M. A. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1260-1 · Cited by 274 · see citing works
Self-citationBahn, 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
Current Perspectives on Echinocandin Class Drugs
Perlin, D. S. (2011) · Future Microbiology · doi:10.2217/fmb.11.19 · 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
Fungal echinocandin resistance
Walker, L. A., Gow, N. A. R., & Munro, C. A. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.09.003 · Cited by 267 · 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
SBF Cell Cycle Regulator as a Target of the Yeast PKC-MAP Kinase Pathway
Madden, K. T., Sheu, Y.-J., Baetz, K., Andrews, B., & Snyder, M. P. (1997) · Science · doi:10.1126/science.275.5307.1781 · Cited by 250 · 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
Zhang, Y., Lamm, R., Pillonel, C., Lam, S., & Xu, J. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.2.532-538.2002 · Cited by 244 · 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
Stathopoulos-Gerontides, A., Guo, J. J., & Cyert, M. S. (1999) · Genes & Development · doi:10.1101/gad.13.7.798 · Cited by 240 · see citing works
Antifungal proteins: targets, mechanisms and prospective applications
Theis, T., & Stahl, U. (2004) · Cellular and Molecular Life Sciences (CMLS) · doi:10.1007/s00018-003-3231-4 · Cited by 222 · 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
Kraus, P. R., Fox, D. S., Cox, G. M., & Heitman, J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03508.x · Cited by 217 · see citing works
Reiser, V., Ruis, H., & Ammerer, G. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.4.1147 · Cited by 215 · see citing works
Jenczmionka, N. J., Maier, F. J., Lösch, A. P., & Schäfer, W. (2003) · Current Genetics · doi:10.1007/s00294-003-0379-2 · Cited by 213 · see citing works
Zhao, C., Jung, U. S., Garrett-Engele, P., Roe, T., Cyert, M. S., & Levin, D. E. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.2.1013 · 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
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
The Plant Defensin, NaD1, Enters the Cytoplasm of Fusarium Oxysporum Hyphae
van der Weerden, N. L., Lay, F. T., & Anderson, M. A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709867200 · Cited by 203 · see citing works
Self-citationAn Extensive Circuitry for Cell Wall Regulation in Candida albicans
Blankenship, J. R., Fanning, S., Hamaker, J. J., & Mitchell, A. P. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000752 · Cited by 201 · see citing works
Dodou, E., & Treisman, R. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.4.1848 · Cited by 196 · see citing works
Warmka, J. K., Hanneman, J., Lee, J., Amin, D., & Ota, I. M. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.1.51-60.2001 · Cited by 195 · see citing works
Reinoso-Martín, C., Schüller, C., Schuetzer-Muehlbauer, M., & Kuchler, K. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.6.1200-1210.2003 · Cited by 193 · see citing works
Intracellular Targets of Antibacterial Peptides
Cudic, M., & Otvos, L., Jr. (2002) · Current Drug Targets · doi:10.2174/1389450024605445 · Cited by 189 · see citing works
Garrett-Engele, P. W., Moilanen, B., & Cyert, M. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.8.4103 · Cited by 187 · 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
Uses and challenges of novel compounds for plant disease control
Gullino, M. L., Leroux, P., & Smith, C. M. (2000) · Crop Protection · doi:10.1016/s0261-2194(99)00095-2 · Cited by 181 · see citing works
José, 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
Jacoby, T., Flanagan, H., Faykin, A., Seto, A. G., Mattison, C. P., & Ota, I. M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.28.17749 · Cited by 171 · see citing works
Del Poeta, M., Cruz, M. C., Cardenas, M. E., Perfect, J. R., & Heitman, J. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.3.739-746.2000 · Cited by 169 · see citing works
Bonilla, M., & Cunningham, K. W. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-02-0113 · Cited by 165 · see citing works
Cross-talk and decision making in MAP kinase pathways
McClean, M. N., Mody, A., Broach, J. R., & Ramanathan, S. (2007) · Nature Genetics · doi:10.1038/ng1957 · Cited by 159 · see citing works
Valiante, V., Heinekamp, T., Jain, R., Härtl, A., & Brakhage, A. A. (2007) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2007.09.006 · Cited by 153 · see citing works
Acquired resistance to echinocandins in Candida albicans: case report and review
Baixench, M.-T., Aoun, N. B. T., Desnos‐Ollivier, M., Garcia‐Hermoso, D., Bretagne, S., Ramires, S., Piketty, C., & Dannaoui, É. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm095 · Cited by 149 · see citing works
Temme, N., & Tudzynski, P. (2009) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-22-8-0987 · Cited by 149 · see citing works
Gaughran, J. P., LAI, M. H., Kirsch, D. R., & Silverman, S. J. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.18.5857-5860.1994 · Cited by 148 · 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
Yoshimi, A., Kojima, K., Takano, Y., et al. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.11.1820-1828.2005 · Cited by 141 · see citing works
Navarro-García, F., Alonso‐Monge, R., Rico, H., Plá, J., Sentandreu, R., & Nombela, C. (1998) · Microbiology · doi:10.1099/00221287-144-2-411 · Cited by 138 · see citing works
Montañés, F. M., Pascual‐Ahuir, A., & Proft, M. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07502.x · Cited by 137 · see citing works
Ramamoorthy, V., Zhao, X., Snyder, A. K., Xu, J., & Shah, D. M. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00887.x · Cited by 136 · see citing works
Schubert, S., Barker, K. S., Znaidi, S., Schneider, S., Dierolf, F., Dunkel, N., Aïd, M., Boucher, G., Rogers, P. D., Raymond, M., et al. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01343-10 · Cited by 135 · 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
Muller, E. M., Locke, E., & Cunningham, K. W. (2001) · Genetics · doi:10.1093/genetics/159.4.1527 · 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
Choi, J., Kim, Y., Kim, S., Park, J., & Lee, Y. (2008) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2008.11.010 · Cited by 131 · see citing works
Wiederhold, N. P., Kontoyiannis, D. P., Prince, R. A., & Lewis, R. E. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.12.5146-5148.2005 · Cited by 131 · see citing works
Chemical control of plant diseases
Hirooka, T., & Ishii, H. (2013) · Journal of General Plant Pathology · doi:10.1007/s10327-013-0470-6 · Cited by 130 · see citing works
Thevissen, K., Tavares, P. D. M., Xu, D., Blankenship, J. R., Vandenbosch, D., Idkowiak‐Baldys, J., Govaert, G., Bink, A., Rozental, S., de Groot, P. W. J., et al. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08017.x · Cited by 130 · see citing works
A Yeast Mitogen-Activated Protein Kinase Homolog (Mpk1p) Mediates Signalling by Protein Kinase C
Lee, K. S., Irie, K., Gotoh, Y., et al. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.5.3067-3075.1993 · Cited by 127 · see citing works
Effect of Phenylpyrroles on Glycerol Accumulation and Protein Kinase Activity ofNeurospora crassa
Pillonel, C., & Meyer, T. (1997) · Pesticide Science · doi:10.1002/(sici)1096-9063(199703)49:3 · Cited by 127 · see citing works
Baetz, K., Moffat, J., Haynes, J., Chang, M., & Andrews, B. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.19.6515-6528.2001 · Cited by 125 · see citing works
Marcireau, C., Guilloton, M., & Karst, F. (1990) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.34.6.989 · Cited by 125 · see citing works
Kojima, K., Bahn, Y., & Heitman, J. (2006) · Microbiology · doi:10.1099/mic.0.28571-0 · Cited by 125 · see citing works
RUI, O., & Hahn, M. (2007) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2007.00383.x · Cited by 124 · see citing works
Role of HSP90 in salt stress tolerance via stabilization and regulation of calcineurin.
Imai, J., & Yahara, I. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.24.9262-9270.2000 · Cited by 123 · 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
Self-citationSorgo, A. G., Heilmann, C. J., Dekker, H. L., Bekker, M., Brul, S., de Koster, C. G., de Koning, L. J., & Klis, F. M. (2011) · Eukaryotic Cell · doi:10.1128/ec.05011-11 · Cited by 120 · 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
The gene encoding squalene epoxidase from Saccharomyces cerevisiae: cloning and characterization
Jandrositz, A., Turnowsky, F., & Högenauer, G. (1991) · Gene · doi:10.1016/0378-1119(91)90310-8 · Cited by 119 · see citing works
Sussman, A., Huss, K., Chio, L.-C., Heidler, S. A., Shaw, M., Ma, D., Zhu, G., Campbell, R. M., Park, T., Kulanthaivel, P., et al. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.4.932-943.2004 · Cited by 113 · see citing works
The Antifungal Plant Defensin HsAFP1 from Heuchera Sanguinea Induces Apoptosis in Candida Albicans
Aerts, A., Bammens, L., Govaert, G., Carmona‐Gutiérrez, D., Madeo, F., Cammue, B. P. A., & Thevissen, K. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00047 · Cited by 113 · 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
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
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
The Antifungal Protein AFP from Aspergillus giganteus Inhibits Chitin Synthesis in Sensitive Fungi
Hagen, S., Marx, F., Ram, A. F. J., & Meyer, V. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02497-06 · Cited by 102 · see citing works
Lev, S., Hadar, R., Amedeo, P., Baker, S., Yoder, O. C., & Horwitz, B. A. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.2.443-454.2005 · Cited by 94 · see citing works
Motoyama, T., Ochiai, N., Morita, M., Iida, Y., Usami, R., & Kudo, T. (2008) · Current Genetics · doi:10.1007/s00294-008-0211-0 · Cited by 91 · 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
Munro, C. A. (2013) · Advances in applied microbiology · doi:10.1016/b978-0-12-407678-5.00004-0 · Cited by 87 · see citing works
Effects of Iprodione and Fludioxonil on Glycerol Synthesis and Hyphal Development inCandida albicans
Ochiai, N., Fujimura, M., Oshima, M., Motoyama, T., Ichiishi, A., Yamada‐Okabe, H., & Yamaguchi, I. (2002) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.66.2209 · Cited by 85 · see citing works
Hagiwara, D., Asano, Y., Marui, J., et al. (2009) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.07.003 · Cited by 77 · see citing works
GSK‐3 kinase Mck1 and calcineurin coordinately mediate Hsl1 down‐regulation by Ca2+ in budding yeast
Mizunuma, M., Hirata, D., Miyaoka, R., & Miyakawa, T. (2001) · The EMBO Journal · doi:10.1093/emboj/20.5.1074 · Cited by 75 · see citing works
Miyazaki, T., Inamine, T., Yamauchi, S., Nagayoshi, Y., Saijo, T., Izumikawa, K., Seki, M., Kakeya, H., Yamamoto, Y., Yanagihara, K., et al. (2010) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2010.00611.x · Cited by 70 · see citing works
Torres‐Quiroz, F., García-Marqués, S., Coria, R., Rández‐Gil, F., & Prieto, J. A. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.063578 · Cited by 66 · see citing works
Merchan, S., Bernal, D., Serrano, R., et al. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.1.100-107.2004 · 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
Pn-AMP1, a Plant Defense Protein, Induces Actin Depolarization in Yeasts
Koo, J. C., Lee, B., Young, M. E., et al. (2004) · Plant and Cell Physiology · doi:10.1093/pcp/pch189 · Cited by 62 · see citing works
Chemical.Control.of.Plant.Diseases
Trigiano, R. N. (2007) · CRC Press eBooks · doi:10.1201/b15333-46 · Cited by 61 · see citing works
Survival Strategies of Yeast and Filamentous Fungi against the Antifungal Protein AFP
Ouedraogo, J., Hagen, S., Spielvogel, A., Engelhardt, S., & Meyer, V. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.203588 · Cited by 58 · see citing works
Juvvadi, P. R., Gehrke, C., Fortwendel, J. R., Lamoth, F., Soderblom, E. J., Cook, E. C., Hast, M. A., Asfaw, Y. G., Moseley, M. A., Creamer, T. P., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003564 · Cited by 57 · see citing works
Herrero de Dios, C., Roman, E., Alonso Monge, R., & Pla, J. (2010) · Current Protein & Peptide Science · doi:10.2174/138920310794557655 · Cited by 55 · see citing works
Yaakov, G., Bell, M. I., Hohmann, S., & Engelberg, D. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.14.4826-4840.2003 · Cited by 55 · see citing works
Argimón, S., Fanning, S., Blankenship, J. R., & Mitchell, A. P. (2010) · Eukaryotic Cell · doi:10.1128/ec.00133-10 · Cited by 46 · see citing works
Signaling the glycoshield: Maintenance of the Candida albicans cell wall
Ernst, J. F., & Plá, J. (2011) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2011.04.003 · Cited by 38 · see citing works
Exposure to caspofungin activates Cap and Hog pathways inCandida albicans
Kelly, J., Rowan, R., McCann, M., & Kavanagh, K. A. (2009) · Medical Mycology · doi:10.3109/13693780802552606 · Cited by 36 · see citing works
Fungicides - Beneficial and Harmful Aspects
(2011) · InTech eBooks · doi:10.5772/2308 · Cited by 32 · see citing works
Emese, D., Hornok, L., & Attila, L. (2011) · InTech eBooks · doi:10.5772/27320 · Cited by 5 · see citing works
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Draft genome of a commonly misdiagnosed multidrug resistant pathogen Candida auris
Chatterjee, S., Alampalli, S. V., Nageshan, R. K., Chettiar, S. T., Joshi, S., & Tatu, U. S. (2015) · BMC Genomics · doi:10.1186/s12864-015-1863-z · Cited by 247 · see citing works
Sharma, C., Kumar, N., Pandey, R., Meis, J. F., & Chowdhary, A. (2016) · New Microbes and New Infections · doi:10.1016/j.nmni.2016.07.003 · Cited by 202 · see citing works
Antifungal persistence: Clinical relevance and mechanisms
Wang, R., Lv, J., Chen, L., Zhao, Y., & Du, H. (2025) · PLoS pathogens · doi:10.1371/journal.ppat.1013456 · Cited by 12 · see citing works
- Authors
- Hayes, B. M. E., Anderson, M. A., Traven, A., van der Weerden, N. L., & Bleackley, M. R.
- Affiliations
- La Trobe University (AU)
- Monash University (AU)
- Corresponding author
- Bleackley, Mark R.
- Venue
- Cellular and Molecular Life Sciences
- Published
- 2014-02-14
- Volume
- 71
- Issue
- 14
- Pages
- 2651-2666
- ISSN
- 1420-682X (ISSN-L)
- 1420-9071
- PMC
- PMC11113482
- OpenAlex
- W1965291654
- Cited by
- 93
- References
- 128
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 2 · 2023: 5 · 2022: 5 · 2021: 7 · 2020: 12 · 2019: 5 · 2018: 9 · 2017: 5 · 2016: 9 · 2015: 9 · 2014: 5
- FWCI
- 0.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cellular and Molecular Life Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Fungal Plant Pathogen Control
- Keywords
- chemical fungicides, antifungal peptides, antimicrobial peptides, stress tolerance, cell wall integrity pathway, high-osmolarity glycerol pathway, reactive oxygen species, fungicide resistance, fungal diseases, sterol biosynthesis inhibition, microtubule assembly inhibition, mitochondrial respiratory chain inhibition
- MeSH terms
- Antifungal Agents, Cell Wall, Drug Tolerance, Fungi, Fungicides, Industrial, Osmotic Pressure, Stress, Physiological, Signal Transduction, Oxidative Stress
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.
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