Harnessing calcineurin as a novel anti-infective agent against invasive fungal infections.
Abstract
The number of immunocompromised patients with invasive fungal infections continues to increase and new antifungal therapies are not keeping pace with the growing incidence of these infections and their associated mortality. Calcineurin inhibition is currently used to exert effective immunosuppression following organ transplantation and in treating various other conditions. However, the calcineurin pathway is also intricately involved in the growth and pathogenesis of the three major fungal pathogens of humans, Cryptococcus neoformans, Candida albicans and Aspergillus fumigatus, and the exploitation of fungal calcineurin pathways holds great promise for the future development of novel antifungal agents. This Review summarizes our current understanding of calcineurin biology in these fungal species, and its exciting potential role in treating invasive fungal infections.
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The utility of calcineurin inhibitors in antifungal therapy has been complicated by their immunosuppressive effects.
“Perhaps in a related manner, the utility of calcineurin inhibitors in antifungal therapy has been complicated by their immunosuppressive effects [57].”
From Hsp90 Governs Echinocandin Resistance in the Pathogenic Yeast Candida albicans via Calcineurin (2009) · cites this paper as [57]
Cites
The epidemiology of sepsis in the United States from 1979 through 2000
Martin, G. S., Mannino, D. M., Eaton, S., & Moss, M. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa022139 · Cited by 5,841 · see citing works
Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes
Liu, J., Farmer, J. D., Lane, W. S., Friedman, J., Weissman, I., & Schreiber, S. L. (1991) · Cell · doi:10.1016/0092-8674(91)90124-h · Cited by 4,116 · see citing works
Nonfilamentous C. albicans Mutants Are Avirulent
Lo, H.-J., Köhler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., & Fink, G. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80358-x · Cited by 1,809 · see citing works
Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation
Clipstone, N. A., & Crabtree, G. R. (1992) · Nature · doi:10.1038/357695a0 · Cited by 1,635 · see citing works
Epidemiology and Outcome of Mould Infections in Hematopoietic Stem Cell Transplant Recipients
Marr, K. A., Carter, R. A., Crippa, F., Wald, A., & Corey, L. (2002) · Clinical Infectious Diseases · doi:10.1086/339202 · Cited by 1,446 · see citing works
Storb, R. F., Deeg, H. J., Whitehead, J., Appelbaum, F. R., Beatty, P. G., Bensinger, W., Buckner, C. D., Clift, R. A., Doney, K., Farewell, V. T., et al. (1986) · New England Journal of Medicine · doi:10.1056/nejm198603203141201 · Cited by 1,411 · see citing works
Nosocomial Bloodstream Infections in United States Hospitals: A Three‐Year Analysis
Edmond, M. B., Wallace, S. E., McClish, D. K., Pfaller, M. A., Jones, R. N., & Wenzel, R. P. (1999) · Clinical Infectious Diseases · doi:10.1086/520192 · Cited by 1,387 · see citing works
Virulence factors of Candida albicans
Calderone, R. A., & Fonzi, W. A. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02094-7 · Cited by 1,331 · see citing works
Talbot, G. H., Bradley, J. S., Edwards, J. E., Gilbert, D. N., Scheld, M., & Bartlett, J. G. (2006) · Clinical Infectious Diseases · doi:10.1086/499819 · Cited by 1,106 · see citing works
Roe, S. M., Prodromou, C., O'Brien, R., Ladbury, J. E., Piper, P. W., & Pearl, L. H. (1999) · Journal of Medicinal Chemistry · doi:10.1021/jm980403y · Cited by 1,004 · see citing works
X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex
Griffith, J. P., Kim, J. L., Kim, E. E., Sintchak, M. D., Thomson, J. A., Fitzgibbon, M. J., Fleming, M. A., Caron, P. R., Hsiao, K., & Navia, M. A. (1995) · Cell · doi:10.1016/0092-8674(95)90439-5 · Cited by 834 · see citing works
Trends in the postmortem epidemiology of invasive fungal infections at a University Hospital
Groll, A. H., Shah, P. M., MENTZEL, C., Schneider, M., Just‐Nübling, G., & Huebner, K. (1996) · Journal of Infection · doi:10.1016/s0163-4453(96)92700-0 · Cited by 779 · see citing works
Crystal structures of human calcineurin and the human FKBP12–FK506–calcineurin complex
Kissinger, C. R., Parge, H. E., Knighton, D. R., Lewis, C. T., Pelletier, L. A., Tempczyk, A., Kalish, V. J., Tucker, K. D., Showalter, R. E., Moomaw, E. W., et al. (1995) · Nature · doi:10.1038/378641a0 · Cited by 762 · see citing works
Kidd, S. E., Hagen, F., Tscharke, R. L., Huynh, M., Bartlett, K. H., Fyfe, M. W., MacDougall, L., Boekhout, T., Kwon-Chung, K. J., & Meyer, W. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402981101 · Cited by 758 · see citing works
Calcineurin: a calcium- and calmodulin-binding protein of the nervous system.
Klee, C. B., Crouch, T. H., & Krinks, M. H. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6270 · Cited by 738 · see citing works
Hsp90 Potentiates the Rapid Evolution of New Traits: Drug Resistance in Diverse Fungi
Cowen, L. E., & Lindquist, S. (2005) · Science · doi:10.1126/science.1118370 · Cited by 698 · see citing works
Trends in Mortality Due to Invasive Mycotic Diseases in the United States, 1980–1997
McNeil, M. M., Nash, S. L., Hajjeh, R. A., Phelan, M. A., Conn, L. A., Plikaytis, B. D., & Warnock, D. W. (2001) · Clinical Infectious Diseases · doi:10.1086/322606 · Cited by 657 · see citing works
PUTATIVE VIRULENCE FACTORS OF CANDIDA ALBICANS
Cutler, J. E. (1991) · Annual Review of Microbiology · doi:10.1146/annurev.mi.45.100191.001155 · Cited by 632 · see citing works
Candida albicans: A molecular revolution built on lessons from budding yeast
Berman, J., & Sudbery, P. E. (2002) · Nature Reviews Genetics · doi:10.1038/nrg948 · Cited by 578 · see citing works
Activity-Dependent Regulation of MEF2 Transcription Factors Suppresses Excitatory Synapse Number
Flavell, S. W., Cowan, C. W., Kim, T.-K., Greer, P. L., Lin, Y., Paradis, S., Griffith, E. C., Hu, L. S., Chen, C., & Greenberg, M. E. (2006) · Science · doi:10.1126/science.1122511 · Cited by 573 · see citing works
Dawson, T. M., Steiner, J. P., Dawson, V. L., DINERMAN, J. L., Uhl, G. R., & Snyder, S. H. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.21.9808 · Cited by 538 · see citing works
Calcineurin is required for virulence of Cryptococcus neoformans
Odom, A., Muir, S., Lim, E., Toffaletti, D. L., Perfect, J., & Heitman, J. (1997) · The EMBO Journal · doi:10.1093/emboj/16.10.2576 · Cited by 516 · see citing works
NFAT and Osterix cooperatively regulate bone formation
Koga, T., Matsui, Y., Asagiri, M., Kodama, T., Crombrugghe, B. D., Nakashima, K., & Takayanagi, H. (2005) · Nature Medicine · doi:10.1038/nm1270 · Cited by 490 · see citing works
Malleret, G., Haditsch, U., Genoux, D., Jones, M. W., Bliss, T. V. P., Vanhoose, A. M., Weitlauf, C., Kandel, E. R., Winder, D. G., & Mansuy, I. M. (2001) · Cell · doi:10.1016/s0092-8674(01)00264-1 · Cited by 470 · see citing works
Prevention of Cardiac Hypertrophy in Mice by Calcineurin Inhibition
Sussman, M. A., Lim, H. W., Gude, N. A., Taigen, T. L., Olson, E. N., Robbins, J. M., Colbert, M. C., Gualberto, A., Wieczorek, D. F., & Molkentin, J. D. (1998) · Science · doi:10.1126/science.281.5383.1690 · Cited by 461 · see citing works
Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway
Semsarian, C., Wu, M., Ju, Y., Marciniec, T., Yeoh, T., Allen, D. G., Harvey, R. P., & Graham, R. M. (1999) · Nature · doi:10.1038/23054 · Cited by 451 · see citing works
Calcineurin/NFAT signalling regulates pancreatic β-cell growth and function
Heit, J. J., Apelqvist, Å., Gu, X., Winslow, M. M., Neilson, J. R., Crabtree, G. R., & Kim, S. K. (2006) · Nature · doi:10.1038/nature05097 · Cited by 445 · see citing works
Stathopoulos, A. M., & Cyert, M. S. (1997) · Genes & Development · doi:10.1101/gad.11.24.3432 · Cited by 442 · see citing works
Signals Transduced by Ca2+/Calcineurin and NFATc3/c4 Pattern the Developing Vasculature
Graef, I. A., Chen, F., Chen, L., Kuo, A., & Crabtree, G. R. (2001) · Cell · doi:10.1016/s0092-8674(01)00396-8 · Cited by 417 · see citing works
Yoshimoto, H., Saltsman, K., Gasch, A. P., Li, H. X., Ogawa, N., Botstein, D., Brown, P. O., & Cyert, M. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202718200 · Cited by 404 · see citing works
da Silva Ferreira, M. E., Kress, M. R. V. Z., Savoldi, M., Goldman, M. H. S., Härtl, A., Heinekamp, T., Brakhage, A. A., & Goldman, G. H. (2006) · Eukaryotic Cell · doi:10.1128/ec.5.1.207-211.2006 · Cited by 403 · see citing works
Candida albicans proteinases and host/pathogen interactions
Naglik, J., Albrecht, A., Bader, O., & Hube, B. (2004) · Cellular Microbiology · doi:10.1111/j.1462-5822.2004.00439.x · Cited by 399 · see citing works
Friedman, J. S., & Weissman, I. L. (1991) · Cell · doi:10.1016/0092-8674(91)90123-g · Cited by 396 · see citing works
Chayakulkeeree, M., & Perfect, J. R. (2006) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2006.07.001 · Cited by 396 · see citing works
Graef, I. A., Wang, F., Charron, F., Chen, L., Neilson, J., Tessier-Lavigne, M., & Crabtree, G. R. (2003) · Cell · doi:10.1016/s0092-8674(03)00390-8 · Cited by 379 · see citing works
The direct cost and incidence of systemic fungal infections
Wilson, L. S., Reyes, C. M., Stolpman, M., Speckman, J., Allen, K., & Beney, J. (2002) · Value in Health · doi:10.1046/j.1524-4733.2002.51108.x · Cited by 374 · see citing works
Sanglard, D., Ischer, F., Marchetti, O., Entenza, J., & Bille, J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03495.x · Cited by 350 · see citing works
Calcineurin is essential for survival during membrane stress in Candida albicans
Cruz, M. C., Goldstein, A. L., Blankenship, J. R., Del Poeta, M., Davis, D., Cardenas, M. E., Perfect, J. R., McCusker, J. H., & Heitman, J. (2002) · The EMBO Journal · doi:10.1093/emboj/21.4.546 · Cited by 342 · cited 1× · see citing works
“albicans calcineurin catalytic (A) subunit (Cna1/Cmp1) or regulatory (B) subunit (Cnb1) abrogates calcineurin activit”
BackgroundCalcineurin 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
A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis
Chang, C.-P., Neilson, J. R., Bayle, J. H., Gestwicki, J. E., Kuo, A., Stankunas, K., Graef, I. A., & Crabtree, G. R. (2004) · Cell · doi:10.1016/j.cell.2004.08.010 · Cited by 331 · see citing works
Trial of cyclosporin in corticosteroid-dependent chronic severe asthma
Alexander, A. G., Kay, A. B., & Barnes, N. C. (1992) · The Lancet · doi:10.1016/0140-6736(92)91646-p · Cited by 330 · see citing works
Inherent calcineurin inhibitor FKBP38 targets Bcl-2 to mitochondria and inhibits apoptosis
Shirane, M., & Nakayama, K. I. (2002) · Nature Cell Biology · doi:10.1038/ncb894 · Cited by 319 · 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
Pfaller, M. A., Jones, R. N., Doern, G. V., Sader, H. S., Hollis, R. J., Messer, S. A., & Group, F. T. S. P. (1998) · Journal of Clinical Microbiology · doi:10.1128/jcm.36.7.1886-1889.1998 · Cited by 281 · see citing works
Huai, Q., Kim, H.-Y., Liu, Y., Zhao, Y., Mondragon, A., Liu, J. O., & Ke, H. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192206699 · Cited by 278 · see citing works
Calcineurin Controls Growth, Morphology, and Pathogenicity in <i>Aspergillus fumigatus</i>
Steinbach, W. J., Cramer, R. A., Perfect, B. Z., Asfaw, Y. G., Sauer, T. C., Najvar, L. K., Kirkpatrick, W. R., Patterson, T. F., Benjamin, D. K., Heitman, J., et al. (2006) · Eukaryotic Cell · doi:10.1128/ec.00139-06 · Cited by 264 · see citing works
Self-citationSingh, N., Alexander, B. D., Lortholary, O., Dromer, F., Gupta, K. L., John, G. T., Busto, R. D., Klintmalm, G. B. G., Somani, J., Lyon, G. M., et al. (2007) · The Journal of Infectious Diseases · doi:10.1086/511438 · Cited by 263 · see citing works
Felk, A., Kretschmar, M., Albrecht, A., Schaller, M., Beinhauer, S., Nichterlein, T., Sanglard, D., Körting, H. C., Schäfer, W., & Hube, B. (2002) · Infection and Immunity · doi:10.1128/iai.70.7.3689-3700.2002 · Cited by 258 · see citing works
Dimorphism and virulence in Candida albicans
Mitchell, A. P. (1998) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(98)80116-1 · Cited by 256 · see citing works
Potent Synergism of the Combination of Fluconazole and Cyclosporine in <i>Candida albicans</i>
Marchetti, O., Moreillon, P., Glauser, M. P., Bille, J., & Sanglard, D. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.9.2373-2381.2000 · Cited by 252 · see citing works
Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin
Jin, L., & Harrison, S. C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.212504399 · Cited by 244 · see citing works
Singh, N., Avery, R. K., Muñóz, P., Pruett, T. L., Alexander, B. D., Jacobs, R. A., Tollemar, J. G., Dominguez, E. A., Chen, Y., Paterson, D. L., et al. (2003) · Clinical Infectious Diseases · doi:10.1086/345441 · Cited by 240 · 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
<i>CRZ1</i> , a target of the calcineurin pathway in <i>Candida albicans</i>
Karababa, M., Valentino, E., Pardini, G., Coste, A. T., Bille, J., & Sanglard, D. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.05037.x · Cited by 231 · see citing works
A Randomized Trial of Inhaled Cyclosporine in Lung-Transplant Recipients
Iacono, A. T., Johnson, B. A., Grgurich, W. F., Youssef, J. G., Corcoran, T. E., Smith-Seiler, D., Dauber, J. H., Smaldone, G. C., Zeevi, A., Yousem, S. A., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa043204 · Cited by 227 · see citing works
Calcineurin: Structure, function, and inhibition
Hemenway, C. S., & Heitman, J. (1999) · Cell Biochemistry and Biophysics · doi:10.1007/bf02737887 · Cited by 227 · see citing works
Advances in combating fungal diseases: vaccines on the threshold
Cutler, J. E., Deepe, G. S., & Klein, B. S. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1537 · Cited by 223 · 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
Self-citationDrew, R. H., Ashley, E. D., Benjamin, D. K., Davis, R. D., Palmer, S. M., & Perfect, J. R. (2004) · Transplantation · doi:10.1097/01.tp.0000101516.08327.a9 · Cited by 198 · see citing works
Husain, S., Tollemar, J. G., Dominguez, E. A., Baumgarten, K. L., Humar, A., Paterson, D. L., Wagener, M. M., Kusne, S., & Singh, N. (2003) · Transplantation · doi:10.1097/01.tp.0000065178.93741.72 · Cited by 194 · see citing works
Calcineurin mediates alpha-adrenergic stimulation of Na+,K(+)-ATPase activity in renal tubule cells.
Aperia, A., Ibarra, F. R., Svensson, L. B., Klee, C., & Greengard, P. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.16.7394 · Cited by 193 · see citing works
Calcineurin Is Essential for <i>Candida albicans</i> Survival in Serum and Virulence
Blankenship, J. R., Wormley, F. L., Boyce, M. K., Schell, W. A., Filler, S. G., Perfect, J. R., & Heitman, J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.3.422-430.2003 · Cited by 186 · see citing works
Self-citationPenetration and damage of endothelial cells by Candida albicans
Filler, S. G., Swerdloff, J. N., Hobbs, C., & Luckett, P. M. (1995) · Infection and Immunity · doi:10.1128/iai.63.3.976-983.1995 · Cited by 184 · see citing works
Berenguer, J., Allende, M. C., Lee, J. W., Garrett, K., Lyman, C., Ali, N. M., Bacher, J., Pizzo, P. A., & Walsh, T. J. (1995) · American journal of respiratory and critical care medicine · doi:10.1164/ajrccm.152.3.7663787 · Cited by 183 · see citing works
Fox, D. S., Cruz, M. C., Sia, R. A. L., Ke, H., Cox, G. M., Cardenas, M. E., & Heitman, J. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02295.x · Cited by 175 · see citing works
Görlach, J. M., Fox, D. S., Cutler, N. S., Cox, G. M., Perfect, J. R., & Heitman, J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.14.3618 · Cited by 172 · see citing works
Truncation and Activation of Calcineurin A by Calpain I in Alzheimer Disease Brain
Liu, F., Grundke, I., Iqbal, K., Oda, Y., Tomizawa, K., & Gong, C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m507475200 · 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
Genetic Architecture of Hsp90-Dependent Drug Resistance
Cowen, L. E., Carpenter, A. E., Matangkasombut, O., Fink, G. R., & Lindquist, S. (2006) · Eukaryotic Cell · doi:10.1128/ec.00274-06 · Cited by 159 · see citing works
John, A. R. O., Poeta, M. D., Perfect, J. R., & Heitman, J. (1997) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.41.1.156 · Cited by 153 · see citing works
Sundstrom, P. (1999) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(99)80062-9 · Cited by 151 · see citing works
Cruz, M. C., Fox, D. S., & Heitman, J. (2001) · The EMBO Journal · doi:10.1093/emboj/20.5.1020 · Cited by 150 · see citing works
Anti-CandidaDrugs — The Biochemical Basis for Their Activity
BOSSCHE, H. V., Willemsens, G., & Marichal, P. (1987) · CRC Critical Reviews in Microbiology · doi:10.3109/10408418709104448 · Cited by 145 · see citing works
Good fungi gone bad: The corruption of calcineurin
Fox, D. S., & Heitman, J. (2002) · BioEssays · doi:10.1002/bies.10157 · Cited by 137 · see citing works
Self-citationIn Vitro Interactions between Antifungals and Immunosuppressants against Aspergillus fumigatus
Steinbach, W. J., Schell, W. A., Blankenship, J. R., Onyewu, C., Heitman, J., & Perfect, J. R. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.5.1664-1669.2004 · Cited by 135 · see citing works
Self-citationSundstrom, P., Balish, E., & Allen, C. M. (2002) · The Journal of Infectious Diseases · doi:10.1086/338836 · Cited by 134 · see citing works
Characterization and expression of the unique calmodulin gene of Aspergillus nidulans.
Rasmussen, C. D., Means, R. L., Lu, K. P., May, G. S., & Means, A. R. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)77415-2 · Cited by 131 · see citing works
Cruz, M. C., Poeta, M. D., Wang, P., Wenger, R. M., Zenke, G., Quesniaux, V. F. J., Movva, N. R., Perfect, J. R., Cardenas, M. E., & Heitman, J. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.1.143-149.2000 · Cited by 129 · see citing works
Kojima, K., Bahn, Y., & Heitman, J. (2006) · Microbiology · doi:10.1099/mic.0.28571-0 · Cited by 125 · see citing works
Functional characterization of the Aspergillus fumigatus calcineurin
Ferreira, M. E. D. S., Heinekamp, T., Härtl, A., Brakhage, A. A., Semighini, C. P., Harris, S. D., Savoldi, M., de Gouvêa, P. F., Goldman, M. H. D. S., & Goldman, G. H. (2007) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2006.08.004 · Cited by 121 · see citing works
Pardini, G., De Groot, P. W. J., Coste, A. T., Karababa, M., Klis, F. M., de Koster, C. G., & Sanglard, D. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606361200 · Cited by 121 · see citing works
Calcineurin Is Essential for Virulence in <i>Candida albicans</i>
Bader, T., Bodendorfer, B., Schröppel, K., & Morschhäuser, J. (2003) · Infection and Immunity · doi:10.1128/iai.71.9.5344-5354.2003 · Cited by 121 · see citing works
Onyewu, C., Wormley, F. L., Perfect, J. R., & Heitman, J. (2004) · Infection and Immunity · doi:10.1128/iai.72.12.7330-7333.2004 · Cited by 121 · see citing works
Wang, P., Cardenas, M. E., Cox, G. M., Perfect, J. R., & Heitman, J. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve109 · Cited by 117 · see citing works
Kontoyiannis, D. P. (2003) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkg090 · Cited by 116 · see citing works
Rasmussen, C. D., Garen, C. R., Brining, S. K., Kincaid, R. L., Means, R. L., & Means, A. R. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06544.x · Cited by 115 · see citing works
Boustany, L. M., & Cyert, M. S. (2002) · Genes & Development · doi:10.1101/gad.967602 · Cited by 115 · see citing works
Marchetti, O., Entenza, J. M., Sanglard, D., Bille, J., Glauser, M. P., & Moreillon, P. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.11.2932-2938.2000 · Cited by 113 · see citing works
Calcineurin Is Required forCandida albicansTo Survive Calcium Stress in Serum
Blankenship, J. R., & Heitman, J. (2005) · Infection and Immunity · doi:10.1128/iai.73.9.5767-5774.2005 · Cited by 111 · see citing works
Desdouits, F., Siciliano, J. C., Greengard, P., & Girault, J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2682 · Cited by 102 · see citing works
Lugardon, K., Chasserot‐Golaz, S., Kieffer, A., Maget‐Dana, R., Nullans, G., Kieffer, B., Aunis, D., & Metz‐Boutigue, M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104670200 · Cited by 98 · see citing works
Bader, T., Schröppel, K., Bentink, S., Agabian, N., Köhler, G., & Morschhäuser, J. (2006) · Infection and Immunity · doi:10.1128/iai.00142-06 · Cited by 81 · see citing works
Santos, M., & de Larrinoa, I. F. (2005) · Current Genetics · doi:10.1007/s00294-005-0003-8 · Cited by 78 · see citing works
Calcineurin and vacuolar-type H + -ATPase modulate macrophage effector functions
Conboy, I. M., Manoli, D. S., Mhaiskar, V., & Jones, P. P. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6324 · Cited by 76 · see citing works
Kraus, P. R., Nichols, C. B., & Heitman, J. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.6.1079-1087.2005 · Cited by 72 · see citing works
Cyclosporin A inhibits the growth of Cryptococcus neoformans in a murine model
Mody, C. H., Toews, G. B., & Lipscomb, M. F. (1988) · Infection and Immunity · doi:10.1128/iai.56.1.7-12.1988 · Cited by 69 · see citing works
Metaxin is required for tumor necrosis factor‐induced cell death
Wang, X., Ono, K., Kim, S. O., Kravchenko, V. V., Lin, S., & Han, J. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve135 · Cited by 68 · see citing works
Heath, V. L., Shaw, S. L., Roy, S., & Cyert, M. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.3.695-704.2004 · Cited by 68 · see citing works
Remitz, A., Harper, J. I., Rustin, M. H. A., Goldschmidt, W. F. M., Palatsi, R., Valk, P. V. D., Sharpe, G., Smith, C. H., DOBOZY, A., & Turjanmaa, K. (2007) · Acta Dermato Venereologica · doi:10.2340/00015555-0167 · Cited by 68 · see citing works
Steinbach, W. J., Singh, N., Miller, J. L., Benjamin, D. K., Schell, W. A., Heitman, J., & Perfect, J. R. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.12.4922-4925.2004 · Cited by 66 · see citing works
Self-citationCalcineurin-dependent nuclear import of the transcription factor Crz1p requires Nmd5p
Polizotto, R. S., & Cyert, M. S. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200104078 · Cited by 63 · see citing works
FK-506-binding protein: three-dimensional structure of the complex with the antagonist L-685,818
Becker, J. W., Rotonda, J., McKeever, B. M., Chan, H., Marcy, A. I., Wiederrecht, G., Hermes, J. D., & Springer, J. P. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)82129-9 · Cited by 62 · see citing works
Aerosol cyclosporin therapy in lung transplant recipients with bronchiolitis obliterans
Iacono, A. T., Corcoran, T. E., Griffith, B. P., Grgurich, W. F., Smith, D. A., Zeevi, A., Smaldone, G. C., McCurry, K. R., Johnson, B. A., & Dauber, J. H. (2004) · European Respiratory Journal · doi:10.1183/09031936.04.00058504 · Cited by 61 · see citing works
Rotonda, J., Burbaum, J. J., Chan, H., Marcy, A. I., & Becker, J. W. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52995-1 · Cited by 61 · see citing works
Mendizabal, I., Pascual-Ahuir, A., Serrano, R., & de Larrinoa, I. (2001) · Molecular Genetics and Genomics · doi:10.1007/s004380100474 · Cited by 57 · see citing works
Marchetti, O., Moreillon, P., Entenza, J. M., Vouillamoz, J., Glauser, M. P., Billé, J., & Sanglard, D. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.5.1565-1570.2003 · Cited by 57 · see citing works
THE ANTIMICROBIAL ACTIVITIES OF CYCLOSPORINE, FK506, AND RAPAMYCIN
High, K. P. (1994) · Transplantation · doi:10.1097/00007890-199457120-00001 · Cited by 57 · see citing works
THE ANTIMICROBIAL ACTIVITIES OF CYCLOSPORINE, FK506, AND RAPAMYCIN
High, K. P. (1994) · Transplantation · doi:10.1097/00007890-199406270-00001 · Cited by 56 · see citing works
Effects of cyclosporine in experimental cryptococcal meningitis
Perfect, J. R., & Durack, D. T. (1985) · Infection and Immunity · doi:10.1128/iai.50.1.22-26.1985 · Cited by 54 · see citing works
Cooperative regulation of cell proliferation by calcium and calmodulin in Aspergillus nidulans
Lu, K. P., Rasmussen, C. D., May, G. S., & Means, A. R. (1992) · Molecular Endocrinology · doi:10.1210/mend.6.3.1584213 · Cited by 54 · see citing works
Rotonda, J., Burbaum, J. J., Chan, H., et al. (1993) · PubMed · doi:10.2210/pdb1yat/pdb · Cited by 53 · see citing works
High, K. P., & Washburn, R. G. (1997) · The Journal of Infectious Diseases · doi:10.1093/infdis/175.1.222 · Cited by 51 · see citing works
Singh, N., & Heitman, J. (2004) · Transplantation · doi:10.1097/01.tp.0000117252.75651.d6 · Cited by 50 · see citing works
Reversible blockade of experience-dependent plasticity by calcineurin in mouse visual cortex
Yang, Y., Fischer, Q. S., Zhang, Y., Baumgärtel, K., Mansuy, I. M., & Daw, N. W. (2005) · Nature Neuroscience · doi:10.1038/nn1464 · Cited by 47 · see citing works
Fox, D. S., & Heitman, J. (2005) · Eukaryotic Cell · doi:10.1128/ec.4.9.1526-1538.2005 · Cited by 47 · see citing works
Fox, D. S., Cox, G. M., & Heitman, J. (2003) · Eukaryotic Cell · doi:10.1128/ec.2.5.1025-1035.2003 · Cited by 47 · see citing works
Temekonidis, T. I., Georgiadis, A. N., Alamanos, Y., Bougias, D. V., Voulgari, P. V., & Drosos, A. A. (2002) · Annals of the Rheumatic Diseases · doi:10.1136/ard.61.9.822 · Cited by 46 · see citing works
Juvvadi, P. R., Kuroki, Y., Arioka, M., Nakajima, H., & Kitamoto, K. (2003) · Archives of Microbiology · doi:10.1007/s00203-003-0546-3 · Cited by 44 · see citing works
Satonaka, H., Suzuki, E., Nishimatsu, H., Oba, S., Takeda, R., Goto, A., Omata, M., Fujita, T., Nagai, R., & Hirata, Y. (2004) · Circulation Research · doi:10.1161/01.res.0000118250.67032.5e · Cited by 43 · see citing works
Heitman, J. (2005) · Science · doi:10.1126/science.1119321 · Cited by 42 · see citing works
Treatment of Murine Cryptococcosis with Cyclosporin-A in Normal and Athymic Mice
Mody, C. H., Toews, G. B., & Lipscomb, M. F. (1989) · American Review of Respiratory Disease · doi:10.1164/ajrccm/139.1.8 · Cited by 42 · see citing works
Effects of Methylprednisolone and Cyclosporine A on Fungal Growth In Vitro
Bell, N. P., Karp, C. L., Alfonso, E. C., Schiffman, J., & Miller, D. (1999) · Cornea · doi:10.1097/00003226-199905000-00012 · Cited by 41 · see citing works
Jayashree, T., Rao, J. P., & Subramanyam, C. (2000) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2000.tb08960.x · Cited by 37 · see citing works
Onyewu, C., Afshari, N. A., & Heitman, J. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00393-06 · Cited by 36 · see citing works
Walsh, M. P., Busaan, J. L., Fraser, E. D., Fu, S. Y., Pato, M. D., & Michalak, M. (1995) · Biochemistry · doi:10.1021/bi00016a030 · Cited by 33 · see citing works
Blankenship, J. R., Singh, N., Alexander, B. D., & Heitman, J. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.1.464-467.2005 · Cited by 25 · see citing works
Derkx, P. M. F., & Madrid, S. M. (2001) · Molecular Genetics and Genomics · doi:10.1007/s004380100586 · Cited by 20 · see citing works
Dephosphorylation of Calponin by Type 2B Protein Phosphatase
Fraser, E. D., & Walsh, M. P. (1995) · Biochemistry · doi:10.1021/bi00028a026 · Cited by 18 · see citing works
Reedy, J. L., Husain, S., Ison, M. G., Pruett, T. L., Singh, N., & Heitman, J. (2006) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.50.4.1573-1577.2006 · Cited by 18 · see citing works
Juvvadi, P. R., Arioka, M., Nakajima, H., & Kitamoto, K. (2001) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2001.tb10881.x · Cited by 14 · see citing works
Beg, A. A., & Scheiffele, P. (2006) · Science · doi:10.1126/science.1124541 · Cited by 9 · see citing works
Alternative treatments for focal and segmental glomerular sclerosis.
Ponticelli, C. E., & Passerini, P. (2001) · PubMed · Cited by 8 · see citing works
Plummer, N. A. (1979) · PubMed · Cited by 1 · see citing works
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The Fungal Cell Wall: Structure, Biosynthesis, and Function
Gow, N. A. R., Latge, J.-P., & Munro, C. A. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0035-2016 · Cited by 1,423 · see citing works
Antifungal Drug Resistance: Molecular Mechanisms in <i>Candida albicans</i> and Beyond
Lee, Y., Puumala, E., Robbins, N., & Cowen, L. E. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c00199 · Cited by 801 · see citing works
Segal, B. H. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0808853 · Cited by 659 · see citing works
Mechanisms of Antifungal Drug Resistance
Cowen, L. E., Sanglard, D., Howard, S. J., Rogers, P. D., & Perlin, D. S. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019752 · Cited by 647 · see citing works
Efflux-Mediated Antifungal Drug Resistance
Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Baret, P. V., Keniya, M. V., Tanabe, K., Niimi, M., Goffeau, A., & Monk, B. C. (2009) · Clinical Microbiology Reviews · doi:10.1128/cmr.00051-08 · Cited by 608 · see citing works
Ramage, G., Rajendran, R., Sherry, L., & Williams, C. (2012) · International Journal of Microbiology · doi:10.1155/2012/528521 · Cited by 583 · see citing works
Regulatory circuitry governing fungal development, drug resistance, and disease.
Shapiro, R. S., Robbins, N., & Cowen, L. E. (2011) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00045-10 · Cited by 576 · see citing works
Cryptococcus neoformans and Cryptococcus gattii, the etiologic agents of cryptococcosis
Kwon-Chung, K. J., Fraser, J. A., Doering, T. L., Wang, Z. A., Janbon, G., Idnurm, A., & Bahn, Y.-S. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019760 · Cited by 531 · see citing works
Chitin synthesis and fungal pathogenesis
Lenardon, M. D., Munro, C. A., & Gow, N. A. (2010) · Current Opinion in Microbiology · doi:10.1016/j.mib.2010.05.002 · Cited by 502 · see citing works
Architecture of the dynamic fungal cell wall
Gow, N. A. R., & Lenardon, M. D. (2023) · Nature Reviews Microbiology · doi:10.1038/s41579-022-00796-9 · Cited by 447 · see citing works
Cowen, L. E., Singh, S. D., Köhler, J. R., Collins, C., Zaas, A. K., Schell, W. A., Aziz, H., Mylonakis, E., Perfect, J. R., Whitesell, L., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813394106 · Cited by 413 · see citing works
Self-citationHsp90 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
“Perhaps in a related manner, the utility of calcineurin inhibitors in antifungal therapy has been complicated by their immunosuppressive effects [57].”
BackgroundLaFayette, 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
Self-citationHsp90 Orchestrates Temperature-Dependent Candida albicans Morphogenesis via Ras1-PKA Signaling
Shapiro, R. S., Uppuluri, P., Zaas, A. K., Collins, C., Senn, H., Perfect, J. R., Heitman, J., & Cowen, L. E. (2009) · Current Biology · doi:10.1016/j.cub.2009.03.017 · Cited by 311 · see citing works
Self-citationThe evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype.
Cowen, L. E. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1835 · Cited by 311 · see citing works
Rispail, N., Soanes, D. M., Ant, C., Czajkowski, R., Grünler, A., Huguet, R., Pérez‐Nadales, E., Poli, A., Sartorel, E., Valiante, V., et al. (2009) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.01.002 · Cited by 312 · see citing works
Molecular mechanisms governing antifungal drug resistance
Lee, Y., Robbins, N., & Cowen, L. E. (2023) · npj Antimicrobials and Resistance · doi:10.1038/s44259-023-00007-2 · Cited by 304 · see citing works
Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance.
Cowen, L. E., & Steinbach, W. J. (2008) · Eukaryotic Cell · doi:10.1128/ec.00041-08 · Cited by 285 · see citing works
Aspergillus fumigatus and Related SpeciesPreprint
Sugui, J. A., Kwon-Chung, K. J., Juvvadi, P. R., Latgé, J., & Steinbach, W. J. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019786 · Cited by 286 · see citing works
Self-citationEchinocandins – structure, mechanism of action and use in antifungal therapy
Szymański, M., Chmielewska, S., Czyżewska, U., Malinowska, M., & Tylicki, A. (2022) · Journal of Enzyme Inhibition and Medicinal Chemistry · doi:10.1080/14756366.2022.2050224 · Cited by 281 · see citing works
Antifungal Drugs: The Current Armamentarium and Development of New Agents
Robbins, N., Wright, G. D., & Cowen, L. E. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0002-2016 · Cited by 271 · see citing works
Scedosporium and Lomentospora: an updated overview of underrated opportunists
Ramirez-Garcia, A., Pellon, A., Rementeria, A., Buldain, I., Barreto-Bergter, E., Rollin-Pinheiro, R., de Meirelles, J. V., Xisto, M. I. D. S., Ranque, S., Havlicek, V., et al. (2018) · Medical Mycology · doi:10.1093/mmy/myx113 · Cited by 264 · 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
Uppuluri, P., Nett, J., Heitman, J., & Andes, D. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01397-07 · Cited by 228 · see citing works
Self-citationCombinatorial strategies for combating invasive fungal infections
Spitzer, M., Robbins, N., & Wright, G. D. (2016) · Virulence · doi:10.1080/21505594.2016.1196300 · Cited by 218 · see citing works
Costa-de-Oliveira, S., & Rodrigues, A. G. (2020) · Microorganisms · doi:10.3390/microorganisms8020154 · Cited by 229 · see citing works
Candida albicans drug resistance—Another way to cope with stress
Cannon, R. D., Lamping, E., Holmes, A. R., Niimi, K., Tanabe, K., Niimi, M., & Monk, B. C. (2007) · Microbiology · doi:10.1099/mic.0.2007/010405-0 · Cited by 208 · see citing works
Global Analysis of the Evolution and Mechanism of Echinocandin Resistance in Candida glabrata
Singh-Babak, S. D., Babak, T., Diezmann, S., Hill, J. A., Xie, J. L., Chen, Y.-L., Poutanen, S. M., Rennie, R. P., Heitman, J., & Cowen, L. E. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002718 · Cited by 204 · see citing works
Park, H.-S., Lee, S. C., Cardenas, M. E., & Heitman, J. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.08.004 · Cited by 168 · see citing works
Mucormycosis: its contemporary face and management strategies
Sun, H., & Singh, N. (2011) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(10)70316-9 · Cited by 174 · see citing works
Juvvadi, P. R., Lee, S. C., Heitman, J., & Steinbach, W. J. (2016) · Virulence · doi:10.1080/21505594.2016.1201250 · Cited by 172 · see citing works
Self-citationCramer, R. A., Perfect, B. Z., Pinchai, N., Park, S., Perlin, D. S., Asfaw, Y. G., Heitman, J., Perfect, J. R., & Steinbach, W. J. (2008) · Eukaryotic Cell · doi:10.1128/ec.00086-08 · Cited by 172 · see citing works
Self-citationSynergistic combinations of antifungals and anti-virulence agents to fight against Candida albicans
Cui, J., Ren, B., Tong, Y., Dai, H., & Zhang, L. (2015) · Virulence · doi:10.1080/21505594.2015.1039885 · Cited by 173 · see citing works
FKBP Ligands—Where We Are and Where to Go?
Kolos, J. M., Voll, A. M., Bauder, M., & Hausch, F. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01425 · Cited by 158 · see citing works
Novel 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
Functional characterization of the <i>Aspergillus fumigatus</i> CRZ1 homologue, CrzA
Soriani, F. M., Malavazi, I., Da Silva Ferreira, M. E., Savoldi, M., Von Zeska Kress, M. R., De Souza Goldman, M. H., Loss, O., Bignell, E., & Goldman, G. H. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06122.x · Cited by 168 · see citing works
Antifungal drug resistance of oral fungi
Niimi, M., Firth, N. A., & Cannon, R. D. (2010) · Odontology · doi:10.1007/s10266-009-0118-3 · Cited by 169 · see citing works
Candida albicans and Candida glabrata : global priority pathogens
Katsipoulaki, M., Stappers, M. H. T., Malavia, D., Brunke, S., Hube, B., & Gow, N. A. R. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00021-23 · Cited by 174 · see citing works
Commensal Gut Bacteria Convert the Immunosuppressant Tacrolimus to Less Potent Metabolites
Guo, Y., Crnkovic, C. M., Won, K., Yang, X., Lee, J. R., Orjala, J., Lee, H., & Jeong, H. (2018) · Drug Metabolism and Disposition · doi:10.1124/dmd.118.084772 · Cited by 161 · see citing works
Holmes, A. R., Lin, Y.-H., Niimi, K., Lamping, E., Keniya, M. V., Niimi, M., Tanabe, K., Monk, B. C., & Cannon, R. D. (2008) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00463-08 · Cited by 160 · see citing works
Schumacher, J., Fernandez-de-Larrinoa, Í., & Tudzynski, B. (2008) · Eukaryotic Cell · doi:10.1128/ec.00426-07 · Cited by 155 · see citing works
Signalling pathways in the pathogenesis of Cryptococcus
Kozubowski, L., Lee, S. C., & Heitman, J. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01273.x · Cited by 150 · see citing works
Liu, S., Hou, Y., Chen, X., Gao, Y., Li, H., & Sun, S. (2014) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2013.12.009 · Cited by 148 · see citing works
Tackling Fungal Resistance by Biofilm Inhibitors
Wu, S., Wang, Y., Liu, N., Dong, G., & Sheng, C. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.6b01203 · Cited by 134 · see citing works
Ben‐Ami, R., Lewis, R. E., & Kontoyiannis, D. P. (2010) · British Journal of Haematology · doi:10.1111/j.1365-2141.2010.08283.x · Cited by 132 · see citing works
Hsp90 orchestrates stress response signaling governing fungal drug resistance
Cowen, L. E. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000471 · Cited by 130 · see citing works
Proton transport and pH control in fungi
Kane, P. M. (2016) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-319-25304-6_3 · Cited by 131 · see citing works
Dinamarco, T. M., Freitas, F. Z., Almeida, R. S., Brown, N. A., dos Reis, T. F., Ramalho, L. N. Z., Savoldi, M., Goldman, M. H. S., Bertolini, M. C., & Goldman, G. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037591 · Cited by 127 · see citing works
Petřík, M., Franssen, G. M., Haas, H., Laverman, P., Hörtnagl, C., Schrettl, M., Helbok, A., Lass‐Flörl, C., & Decristoforo, C. (2012) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-012-2110-3 · Cited by 123 · see citing works
Juvvadi, P. R., Fox, D., Bobay, B. G., Hoy, M. J., Gobeil, S. M. C., Venters, R. A., Chang, Z., Lin, J. J., Averette, A. F., Cole, D. C., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12199-1 · Cited by 116 · see citing works
Self-citationJuvvadi, P. R., Lamoth, F., & Steinbach, W. J. (2014) · Fungal Biology Reviews · doi:10.1016/j.fbr.2014.02.004 · Cited by 116 · see citing works
Self-citationA small protein that fights fungi: AFP as a new promising antifungal agent of biotechnological value
Meyer, V. (2007) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-007-1291-3 · Cited by 116 · see citing works
Lu, H., Lin, J., Xu, C., Sun, M., Zuo, K., Zhang, X., Li, M., Huang, H., Li, Z., Wu, W. H., et al. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.334 · Cited by 111 · see citing works
Goldman, A., Roy, J., Bodenmiller, B., Wanka, S., Landry, C. R., Aebersold, R., & Cyert, M. S. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.012 · Cited by 109 · see citing works
Zhang, H., Zhao, Q., Liu, K., Zhang, Z., Wang, Y., & Zheng, X. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01524.x · Cited by 109 · see citing works
Advancements and challenges in antifungal therapeutic development
Puumala, E., Fallah, S., Robbins, N., & Cowen, L. E. (2024) · Clinical Microbiology Reviews · doi:10.1128/cmr.00142-23 · Cited by 118 · see citing works
Calcineurin controls drug tolerance, hyphal growth, and virulence in Candida dubliniensis
Chen, Y.-L., Brand, A., Morrison, E. L., Silao, F. G. S., Bigol, U. G., Malbas, F. F., Nett, J. E., Andes, D. R., Solis, N. V., Filler, S. G., et al. (2011) · Eukaryotic Cell · doi:10.1128/ec.00310-10 · Cited by 107 · see citing works
Recent Approaches to Antifungal Therapy for Invasive Mycoses
Mathew, B. P., & Nath, M. (2009) · ChemMedChem · doi:10.1002/cmdc.200800353 · Cited by 105 · see citing works
Microbial pathogens in the fungal kingdom
Heitman, J. (2011) · Fungal Biology Reviews · doi:10.1016/j.fbr.2011.01.003 · Cited by 104 · see citing works
Gong, Y., Li, T., Yu, C., & Sun, S. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00520 · Cited by 101 · see citing works
Dual action antifungal small molecule modulates multidrug efflux and TOR signaling
Shekhar-Guturja, T., Gunaherath, G. M. K. B., Wijeratne, E. M. K., Lambert, J.-P., Averette, A. F., Lee, S. C., Kim, T., Bahn, Y.-S., Tripodi, F., Ammar, R., et al. (2016) · Nature Chemical Biology · doi:10.1038/nchembio.2165 · Cited by 101 · see citing works
Self-citationIannitti, R., Carvalho, A., Cunha, C., Luca, A. D., Giovannini, G., Casagrande, A., Zelante, T., Vacca, C., Fallarino, F., Puccetti, P., et al. (2013) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201207-1346oc · Cited by 104 · see citing works
Elucidating Drug Resistance in Human Fungal Pathogens
Xie, J. L., Polvi, E. J., Shekhar‐Guturja, T., & Cowen, L. E. (2014) · Future Microbiology · doi:10.2217/fmb.14.18 · Cited by 98 · see citing works
Antifungal Drug Discovery: The Process and Outcomes
Calderone, R., Sun, N., Gay‐Andrieu, F., Groutas, W. C., Weerawarna, P. M., Prasad, S., Alex, D., & Li, D. (2014) · Future Microbiology · doi:10.2217/fmb.14.32 · Cited by 98 · see citing works
Calcineurin Targets Involved in Stress Survival and Fungal Virulence
Hee-Soo, P., Chow, E. W. L., Fu, C., Soderblom, E. J., Moseley, M. A., Heitman, J., & Cardenas, M. E. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005873 · Cited by 94 · see citing works
Genetic and Genomic Architecture of the Evolution of Resistance to Antifungal Drug Combinations
Hill, J. A., Ammar, R., Torti, D., Nislow, C., & Cowen, L. E. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003390 · Cited by 93 · see citing works
Cryptococcal therapies and drug targets: the old, the new and the promising
Coelho, C., & Casadevall, A. (2016) · Cellular Microbiology · doi:10.1111/cmi.12590 · Cited by 94 · see citing works
Roles of Calcineurin and Crz1 in Antifungal Susceptibility and Virulence of <i>Candida glabrata</i>
Miyazaki, T., Yamauchi, S., Inamine, T., Nagayoshi, Y., Saijo, T., Izumikawa, K., Seki, M., Kakeya, H., Yamamoto, Y., Yanagihara, K., et al. (2010) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01364-09 · Cited by 88 · see citing works
Stress Signaling Pathways for the Pathogenicity of Cryptococcus
Bahn, Y.-S., & Jung, K.-W. (2013) · Eukaryotic Cell · doi:10.1128/ec.00218-13 · Cited by 84 · see citing works
The Fungal Cell Wall: Structure, Biosynthesis, and Function
Gow, N. A. R., Latgé, J., & Munro, C. A. (2017) · ASM Press eBooks · doi:10.1128/9781555819583.ch12 · Cited by 89 · see citing works
Pavlovian Conditioning of Immunological and Neuroendocrine Functions
Hadamitzky, M., Lückemann, L., Pacheco‐López, G., & Schedlowski, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00033.2018 · Cited by 87 · see citing works
Wang, Y., Ju, Z., Cao, B., Gao, X., Zhu, Y., Qiu, P., Xu, H., Pan, P., Bao, H., Wang, L., et al. (2015) · ACS Nano · doi:10.1021/acsnano.5b01074 · Cited by 83 · see citing works
Juvvadi, P. R., Fortwendel, J. R., Rogg, L. E., Burns, K. A., Randell, S. H., & Steinbach, W. J. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07886.x · Cited by 80 · see citing works
Self-citationThe contribution of Aspergillus fumigatus stress responses to virulence and antifungal resistance
Brown, N. A., & Goldman, G. H. (2016) · The Journal of Microbiology · doi:10.1007/s12275-016-5510-4 · Cited by 77 · see citing works
Essid, R., Hammami, M., Gharbi, D., Karkouch, I., Hamouda, T. B., Elkahoui, S., Limam, F., & Tabbene, O. (2017) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-017-8442-y · Cited by 78 · see citing works
Reedy, J. L., Filler, S. G., & Heitman, J. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.09.002 · Cited by 76 · see citing works
Kim, A., & Cunningham, K. W. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-08-0581 · Cited by 67 · see citing works
Kim, S., Hu, J., Oh, Y., Park, J., Choi, J., Lee, Y., Dean, R. A., & Mitchell, T. K. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000909 · Cited by 72 · see citing works
Developmental regulators in Aspergillus fumigatus
Park, H.-S., & Yu, J. (2016) · The Journal of Microbiology · doi:10.1007/s12275-016-5619-5 · Cited by 71 · see citing works
Matsumoto, Y., Miyazaki, S., Fukunaga, D. H., Shimizu, K., Kawamoto, S., & Sekimizu, K. (2011) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2011.05186.x · Cited by 70 · see citing works
Chen, Y., Lehman, V. N., Averette, A. F., Perfect, J. R., & Heitman, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057672 · Cited by 69 · see citing works
Calcineurin Controls Hyphal Growth, Virulence, and Drug Tolerance of Candida tropicalis
Chen, Y., Yu, S.-J., Huang, H., Chang, Y.-L., Lehman, V. N., Silao, F. G. S., Bigol, U. G., Bungay, A. A. C., Averette, A. F., & Heitman, J. (2014) · Eukaryotic Cell · doi:10.1128/ec.00302-13 · Cited by 68 · see citing works
Xiong, D., Wang, Y., Tang, C., Fang, Y., Zou, J., & Tian, C. (2015) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2015.07.011 · Cited by 66 · see citing works
Defects in Phosphate Acquisition and Storage Influence Virulence of Cryptococcus neoformans
Kretschmer, M., Reiner, E., Hu, G., Tam, N. M., Oliveira, D. L., Caza, M., Yeon, J. H., Kim, J., Kastrup, C. J., Jung, W. H., et al. (2014) · Infection and Immunity · doi:10.1128/iai.01607-14 · Cited by 65 · see citing works
Wang, S., Cao, J., Liu, X., Hu, H., Shi, J. R., Zhang, S., Keller, N. P., & Lü, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046564 · Cited by 64 · see citing works
Screening Repurposing Libraries for Identification of Drugs with Novel Antifungal Activity
Wall, G., & Lopez-Ribot, J. L. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00924-20 · Cited by 63 · see citing works
Epp, E., Vanier, G., Harcus, D., Lee, A. Y., Jansen, G., Hallett, M., Sheppard, D. C., Thomas, D. Y., Munro, C. A., Mullick, A., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000753 · Cited by 61 · see citing works
Zhang, J., Silao, F. G. S., Bigol, U. G., Bungay, A. A. C., Nicolas, M. G., Heitman, J., & Chen, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044192 · Cited by 61 · see citing works
The Involvement of the Mid1/Cch1/Yvc1 Calcium Channels in Aspergillus fumigatus Virulence
de Castro, P. A., Chiaratto, J., Winkelströter, L. K., Bom, V. L. P., Ramalho, L. N. Z., Goldman, M. H. S., Brown, N. A., & Goldman, G. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103957 · Cited by 60 · see citing works
Dudgeon, D. D., Zhang, N., Ositelu, O. O., Kim, H., & Cunningham, K. W. (2008) · Eukaryotic Cell · doi:10.1128/ec.00291-08 · Cited by 59 · see citing works
Kozubowski, L., Aboobakar, E. F., Cardenas, M. E., & Heitman, J. (2011) · Eukaryotic Cell · doi:10.1128/ec.05087-11 · Cited by 60 · see citing works
Shekhar‐Guturja, T., Tebung, W. A., Mount, H. O., Liu, N.-N., Köhler, J. R., Whiteway, M. S., & Cowen, L. E. (2016) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01959-16 · Cited by 59 · see citing works
Kim, H., Kim, A., & Cunningham, K. W. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.363390 · Cited by 60 · see citing works
Colutellin A, an immunosuppressive peptide from Colletotrichum dematium
Ren, Y., Strobel, G. A., Graff, J. C., Jutila, M. A., Park, S., Gosh, S., Teplow, D. B., Condron, M. M., Pang, E. S., Hess, W. M., et al. (2008) · Microbiology · doi:10.1099/mic.0.2008/017954-0 · Cited by 59 · see citing works
Calcineurin signaling: lessons from Candida species
Yu, S.-J., Chang, Y.-L., & Chen, Y. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov016 · Cited by 58 · see citing works
Chen, L., Tong, Q., Zhang, C., & Ding, K. (2018) · Current Genetics · doi:10.1007/s00294-018-0853-5 · 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
Self-citationde Castro, P. A., Chen, C., Almeida, R. S., Freitas, F. Z., Bertolini, M. C., Morais, E. R., Brown, N. A., Ramalho, L. N. Z., Hagiwara, D., Mitchell, T. K., et al. (2014) · Molecular Microbiology · doi:10.1111/mmi.12785 · Cited by 56 · see citing works
Identification of possible targets of the Aspergillus fumigatus CRZ1 homologue, CrzA
Soriani, F. M., Malavazi, I., Savoldi, M., Espeso, E. A., Dinamarco, T. M., Bernardes, L. Â. D. S., Ferreira, M. E. S., Goldman, M. H. S., & Goldman, G. H. (2010) · BMC Microbiology · doi:10.1186/1471-2180-10-12 · Cited by 56 · see citing works
Lin, C.-J., & Chen, Y.-L. (2018) · Journal of Fungi · doi:10.3390/jof4020068 · Cited by 55 · see citing works
- Authors
- Steinbach, W. J., Reedy, J. L., Cramer, R. A., Perfect, J. R., & Heitman, J.
- Affiliations
- Duke University (US)
- Duke Medical Center (US)
- Corresponding author
- Steinbach, William J.
- Venue
- Nature Reviews Microbiology
- Published
- 2007-06
- Volume
- 5
- Issue
- 6
- Pages
- 418-430
- ISSN
- 1740-1526 (ISSN-L)
- 1740-1534
- OpenAlex
- W2081581252
- Cited by
- 313
- References
- 132
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 9 · 2023: 9 · 2022: 13 · 2021: 10 · 2020: 23 · 2019: 15 · 2018: 13 · 2017: 23 · 2016: 23 · 2015: 20 · 2014: 26 · 2013: 17 · 2012: 20
- FWCI
- 2.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Microbiology (publishedVersion)
- PubMed (publishedVersion)
- 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
- calcineurin, calcineurin inhibition, antifungal agents, invasive fungal infections, Cryptococcus neoformans, Candida albicans, Aspergillus fumigatus, immunocompromised patients, fungal pathogenesis, calcineurin pathway
- MeSH terms
- Antifungal Agents, Fungi, Humans, Mycoses, Signal Transduction, Calcineurin, Calcineurin Inhibitors
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