Mitochondria and Fungal Pathogenesis: Drug Tolerance, Virulence, and Potential for Antifungal Therapy

Shingu-Vazquez, Miguel; Traven, Ana

doi:10.1128/ec.05184-11

Cited by 210Antifungal resistance and susceptibilityFungal and yeast genetics researchMitochondrial Function and Pathology

Mitochondria and Fungal Pathogenesis: Drug Tolerance, Virulence, and Potential for Antifungal Therapy

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Shingu-Vazquez, Miguel, Traven, Ana·2011·Eukaryotic Cell

DOI 10.1128/ec.05184-11PMC PMC3209048

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Abstract

Recently, mitochondria have been identified as important contributors to the virulence and drug tolerance of human fungal pathogens. In different scenarios, either hypo- or hypervirulence can result from changes in mitochondrial function. Similarly, specific mitochondrial mutations lead to either sensitivity or resistance to antifungal drugs. Here, we provide a synthesis of this emerging field, proposing that mitochondrial function in membrane lipid homeostasis is the common denominator underlying the observed effects of mitochondria in drug tolerance (both sensitivity and resistance). We discuss how the contrasting effects of mitochondrial dysfunction on fungal drug tolerance and virulence could be explained and the potential for targeting mitochondrial factors for future antifungal drug development.

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Mitochondria have essential roles in pathogenicity and antifungal drug resistance.
“Mitochondria have essential roles in pathogenicity (46) and antifungal drug resistance (3).”
From Inhibition of Classical and Alternative Modes of Respiration in Candida albicans Leads to Cell Wall Remodeling and Increased Macrophage Recognition (2019) · cites this paper as [3]
C. albicans requires mitochondrial function for normal growth, morphogenesis, and virulence.
“C. albicans requires mitochondrial function for normal growth, morphogenesis, and virulence (2–4)”
From Inhibition of Classical and Alternative Modes of Respiration in Candida albicans Leads to Cell Wall Remodeling and Increased Macrophage Recognition (2019) · cites this paper as [3]
The effect of increased ROS and dead cells may have clinical relevance because oxidative stress reduces microbial pathogenicity by enhanced killing by macrophages.
“Overall, this is an effect that may have clinical relevance because it is known that oxidative stress reduces microbial pathogenicity by enhanced killing by macrophages [35], as shown for A. fumigatus [36].”
From Known Antimicrobials Versus Nortriptyline in Candida albicans: Repositioning an Old Drug for New Targets (2020) · cites this paper as [35]

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Evidence for the Bifunctional Nature of Mitochondrial Phosphatidylserine Decarboxylase: Role in Pdr3-Dependent Retrograde Regulation of PDR5 Expression
Gulshan, K., Schmidt, J. A., Shahi, P., & Moye-Rowley, S. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00405-08 · Cited by 46 · see citing works
Up-regulation of the Cell Integrity Pathway in Saccharomyces cerevisiae Suppresses Temperature Sensitivity of the pgs1Δ Mutant
Zhong, Q., Li, G., Gvozdenovic‐Jeremic, J., & Greenberg, M. L. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701055200 · Cited by 45 · see citing works
Disruption of mitochondrial function in Candida albicans leads to reduced cellular ergosterol levels and elevated growth in the presence of amphotericin B
Geraghty, P., & Kavanagh, K. (2003) · Archives of Microbiology · doi:10.1007/s00203-003-0530-y · Cited by 45 · see citing works
Uncoupling of oxidative phosphorylation enables Candida albicans to resist killing by phagocytes and persist in tissue
Cheng, S., Clancy, C. J., Zhang, Z., Hao, B., Wang, W., Iczkowski, K. A., Pfaller, M. A., & Nguyen, M. H. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00805.x · Cited by 45 · see citing works
Involvement of Candida albicans pyruvate dehydrogenase complex protein X (Pdx1) in filamentation
Vellucci, V. F., Gygax, S. E., & Hostetter, M. K. (2007) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2006.12.003 · Cited by 40 · see citing works
Phosphatidylethanolamine synthesized by four different pathways is supplied to the plasma membrane of the yeast Saccharomyces cerevisiae
Schuiki, I., Schnabl, M., Czabany, T., Hrastnik, C., & Daum, G. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2009.12.008 · Cited by 39 · see citing works
Protein Export across the Inner Membrane of Mitochondria
Herrmann, J. M., & Bonnefoy, N. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310468200 · Cited by 39 · see citing works
Phosphatidylethanolamine is the donor of the phosphorylethanolamine linked to the 1,4-linked mannose of yeast GPI structures
Imhof, I., Canivenc-Gansel, E., Meyer, U., & Conzelmann, A. (2000) · Glycobiology · doi:10.1093/glycob/10.12.1271 · Cited by 39 · see citing works
Translocation and Assembly of Mitochondrially Coded Saccharomyces cerevisiae Cytochrome c Oxidase Subunit Cox2 by Oxa1 and Yme1 in the Absence of Cox18
Fiumera, H. L., Dunham, M. J., Saracco, S. A., Butler, C. A., Kelly, J. A., & Fox, T. D. (2009) · Genetics · doi:10.1534/genetics.109.101196 · Cited by 39 · see citing works
Biogenesis and cellular dynamics of aminoglycerophospholipids
Birner‐Gruenberger, R., & Daum, G. (2003) · International review of cytology · doi:10.1016/s0074-7696(05)25007-6 · Cited by 37 · see citing works
Functional characterization of the CgPGS1 gene reveals a link between mitochondrial phospholipid homeostasis and drug resistance in Candida glabrata
Batova, M., Borecka-Melkusova, S., Simockova, M., Dzugasova, V., Goffa, E., & Subik, J. (2008) · Current Genetics · doi:10.1007/s00294-008-0187-9 · Cited by 31 · see citing works
Hypersusceptibility to Azole Antifungals in a Clinical Isolate of Candida glabrata with Reduced Aerobic Growth
Vandeputte, P., Tronchin, G., Rocher, F., Renier, G., Bergès, T., Chabasse, D., & Bouchara, J.-P. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01384-08 · Cited by 26 · see citing works
Erythromycin, an inhibitor of mitoribosomal protein biosynthesis, alters the amphotericin B susceptibility of Candida albicans
Geraghty, P., & Kavanagh, K. (2003) · Journal of Pharmacy and Pharmacology · doi:10.1211/002235702469 · Cited by 23 · see citing works
Roles of dihydrolipoamide dehydrogenase Lpd1 in Candida albicans filamentation
Kim, S.-Y., & Kim, J. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2010.06.005 · Cited by 16 · see citing works
Overexpression of TUF1 restores respiratory growth and fluconazole sensitivity to a Cryptococcus neoformans vad1Δ mutant
Panepinto, J. C., Misener, A. L., Oliver, B. G. G., Hu, G., Park, Y. D., Shin, S., White, T. C., & Williamson, P. R. (2010) · Microbiology · doi:10.1099/mic.0.035923-0 · Cited by 14 · see citing works
Impact of mitochondrial function on yeast susceptibility to antifungal compounds
Šarinová, M., Tichá, E., Obernauerova, M., & Gbelská, Y. (2007) · Folia Microbiologica · doi:10.1007/bf02931302 · Cited by 12 · see citing works

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Emerging rules for effective antimicrobial coatings
Salwiczek, M., Qu, Y., Gardiner, J., Strugnell, R. A., Lithgow, T. J., McLean, K. M., & Thissen, H. W. (2013) · Trends in biotechnology · doi:10.1016/j.tibtech.2013.09.008 · Cited by 312 · see citing works
System-level impact of mitochondria on fungal virulence: to metabolism and beyond
Calderone, R., Li, D., & Traven, A. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov027 · Cited by 101 · see citing works
Self-citation
Mitochondria Influence CDR1 Efflux Pump Activity, Hog1-Mediated Oxidative Stress Pathway, Iron Homeostasis, and Ergosterol Levels in Candida albicans
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
Aspergillus fumigatus mitochondrial electron transport chain mediates oxidative stress homeostasis, hypoxia responses and fungal pathogenesis
Grahl, N., Dinamarco, T. M., Willger, S. D., Goldman, G. H., & Cramer, R. A. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08034.x · Cited by 99 · 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
Rosmarinic acid–Modes of antimicrobial and antibiofilm activities of a common plant polyphenol
Ivanov, M., Kostić, M., Stojković, D., & Soković, M. (2022) · South African Journal of Botany · doi:10.1016/j.sajb.2021.11.050 · Cited by 98 · see citing works
Azole Susceptibility and Transcriptome Profiling in Candida albicans Mitochondrial Electron Transport Chain Complex I Mutants
Sun, N., Fonzi, W., Chen, H., She, X., Zhang, L., Zhang, L., & Calderone, R. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01520-12 · Cited by 94 · see citing works
Mitochondrial dysfunctions trigger the calcium signaling-dependent fungal multidrug resistance
Li, Y., Zhang, Y., Zhang, C., Wang, H., Wei, X., Chen, P., & Lü, L. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911560116 · Cited by 87 · see citing works
MoDnm1 Dynamin Mediating Peroxisomal and Mitochondrial Fission in Complex with MoFis1 and MoMdv1 Is Important for Development of Functional Appressorium in Magnaporthe oryzae
Zhong, K., Xiao, L., Xinyi, L., Kong, X., Zhang, H., Zheng, X., Wang, P., & Zhang, Z. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005823 · Cited by 83 · see citing works
Mitochondrial dynamics in the pathogenic mold <scp>A</scp> spergillus fumigatus : therapeutic and evolutionary implications
Neubauer, M., Zhu, Z., Penka, M., Helmschrott, C., Wagener, N., & Wagener, J. (2015) · Molecular Microbiology · doi:10.1111/mmi.13167 · Cited by 76 · see citing works
Real-Time Imaging of the Azole Class of Antifungal Drugs in Live Candida Cells
Benhamou, R. I., Bibi, M., Steinbuch, K. B., Engel, H., Levin, M., Roichman, Y., Berman, J., & Fridman, M. (2017) · ACS Chemical Biology · doi:10.1021/acschembio.7b00339 · Cited by 71 · see citing works
Terpenoids with antifungal activity trigger mitochondrial dysfunction in Saccharomyces cerevisiae
Haque, E., Irfan, S., Kamil, M., Sheikh, S., Hasan, A., Ahmad, A., Lakshmi, V., Nazir, A., & Mir, S. S. (2016) · Microbiology · doi:10.1134/s0026261716040093 · Cited by 77 · see citing works
Exploiting mitochondria as targets for the development of new antifungals
Li, D., & Calderone, R. (2017) · Virulence · doi:10.1080/21505594.2016.1188235 · Cited by 67 · see citing works
Comparative Lipidomics in Clinical Isolates of Candida albicans Reveal Crosstalk between Mitochondria, Cell Wall Integrity and Azole Resistance
Singh, A., Yadav, V., & Prasad, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039812 · Cited by 73 · see citing works
Aspergillus terreus: Novel lessons learned on amphotericin B resistance
Posch, W., Blatzer, M., Wilflingseder, D., & Lass‐Flörl, C. (2018) · Medical Mycology · doi:10.1093/mmy/myx119 · Cited by 74 · see citing works
Exploring and exploiting the connection between mitochondria and the virulence of human pathogenic fungi
Verma, S., Shakya, V. P. S., & Idnurm, A. (2018) · Virulence · doi:10.1080/21505594.2017.1414133 · Cited by 67 · see citing works
Fluconazole-Resistant Candida auris Is Susceptible to Salivary Histatin 5 Killing and to Intrinsic Host Defenses
Pathirana, R. U., Friedman, J., Norris, H. L., Salvatori, O., McCall, A. D., Kay, J. G., & Edgerton, M. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01872-17 · Cited by 70 · see citing works
Berberine reverses multidrug resistance in Candida albicans by hijacking the drug efflux pump Mdr1p
Tong, Y., Zhang, J., Sun, N., Wang, X.-M., Wei, Q., Zhang, Y., Huang, R., Pu, Y., Dai, H., Ren, B., et al. (2021) · Science Bulletin · doi:10.1016/j.scib.2020.12.035 · Cited by 70 · see citing works
Global Transcriptome Profile of Cryptococcus neoformans during Exposure to Hydrogen Peroxide Induced Oxidative Stress
Upadhya, R., Campbell, L. T., Donlin, M. J., Aurora, R., & Lodge, J. K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055110 · Cited by 69 · see citing works
The Endoplasmic Reticulum-Mitochondrion Tether ERMES Orchestrates Fungal Immune Evasion, Illuminating Inflammasome Responses to Hyphal Signals
Tucey, T. M., Verma-Gaur, J., Nguyen, J., Hewitt, V. L., Lo, T. L., Shingu-Vazquez, M., Robertson, A. A. B., Hill, J. R., Pettolino, F. A., Beddoe, T., et al. (2016) · mSphere · doi:10.1128/msphere.00074-16 · Cited by 66 · see citing works
Self-citation
Are mitochondria the Achilles’ heel of the Kingdom Fungi?
Chatre, L., & Ricchetti, M. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.05.001 · Cited by 66 · see citing works
Stress-Induced Changes in the Lipid Microenvironment of β-(1,3)- <scp>d</scp> -Glucan Synthase Cause Clinically Important Echinocandin Resistance in Aspergillus fumigatus
Satish, S., Jiménez-Ortigosa, C., Zhao, Y., Lee, M. H., Dolgov, E., Krüger, T., Park, S., Denning, D. W., Kniemeyer, O., Brakhage, A. A., et al. (2019) · mBio · doi:10.1128/mbio.00779-19 · Cited by 64 · see citing works
Inhibition of Classical and Alternative Modes of Respiration in Candida albicans Leads to Cell Wall Remodeling and Increased Macrophage Recognition
Duvenage, L., Walker, L. A., Bojarczuk, A., Johnston, S. A., MacCallum, D. M., Munro, C. A., & Gourlay, C. W. (2019) · mBio · doi:10.1128/mbio.02535-18 · Cited by 61 · see citing works
“Mitochondria have essential roles in pathogenicity (46) and antifungal drug resistance (3).”
Maintenance of Mitochondrial Morphology in Cryptococcus neoformans Is Critical for Stress Resistance and Virulence
Chang, A. L., & Doering, T. L. (2018) · mBio · doi:10.1128/mbio.01375-18 · Cited by 60 · see citing works
A Fungal-Selective Cytochrome bc1 Inhibitor Impairs Virulence and Prevents the Evolution of Drug Resistance
Vincent, B. M., Langlois, J.-B., Srinivas, R., Lancaster, A. K., Scherz-Shouval, R., Whitesell, L., Tidor, B., Buchwald, S. L., & Lindquist, S. (2016) · Cell Chemical Biology · doi:10.1016/j.chembiol.2016.06.016 · Cited by 58 · see citing works
“We anticipate that mitochondria will prove essential to many other fungal virulence processes, as others have begun to reveal (Grahl et al., 2015; Shingu-Vazquez and Traven, 2011; Sun et al., 2013).”
Potential targets for the development of new antifungal drugs
Su, H., Han, L., & Huang, X. (2018) · The Journal of Antibiotics · doi:10.1038/s41429-018-0100-9 · Cited by 60 · see citing works
Mitochondrial Sorting and Assembly Machinery Subunit Sam37 in Candida albicans: Insight into the Roles of Mitochondria in Fitness, Cell Wall Integrity, and Virulence
Qu, Y., Jelicic, B., Pettolino, F., Perry, A., Lo, T. L., Hewitt, V. L., Bantun, F., Beilharz, T. H., Peleg, A. Y., Lithgow, T., et al. (2012) · Eukaryotic Cell · doi:10.1128/ec.05292-11 · Cited by 57 · see citing works
Self-citation
The Candida albicans Histone Acetyltransferase Hat1 Regulates Stress Resistance and Virulence via Distinct Chromatin Assembly Pathways
Tscherner, M., Zwolanek, F., Jenull, S., Sedlazeck, F. J., Petryshyn, A., Frohner, I. E., Mavrianos, J., Chauhan, N., von Haeseler, A., & Kuchler, K. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1005218 · Cited by 57 · see citing works
Fungal-specific subunits of theCandida albicansmitochondrial complex I drive diverse cell functions including cell wall synthesis: Defective colonization in host tissues by mitochondrial mutants
She, X., Khamooshi, K., Gao, Y., Shen, Y., Lv, Y., Calderone, R., Fonzi, W., Liu, W., & Li, D. (2015) · Cellular Microbiology · doi:10.1111/cmi.12438 · Cited by 51 · see citing works
“Our current study supports the idea of others that a loss of mitochondrial function causes reduced virulence or biofilm formation in C. albicans (Table 2) (Marchais et al., 2005; Bambach et al., 2009; Becker et al., 2010; Noble et al., 2010; Shingú-Vázquez and Traven, 2011; Qu et al., 2012).”
BackgroundResultInfluential
A phenotypic small-molecule screen identifies halogenated salicylanilides as inhibitors of fungal morphogenesis, biofilm formation and host cell invasion
Garcia, C. A., Burgain, A., Chaillot, J., Pic, É., Khemiri, I., & Sellam, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-29973-8 · Cited by 50 · see citing works
Mitochondria-Mediated Azole Drug Resistance and Fungal Pathogenicity: Opportunities for Therapeutic Development
Song, J., Zhou, J., Zhang, L., & Li, R. (2020) · Microorganisms · doi:10.3390/microorganisms8101574 · Cited by 50 · see citing works
Inhibiting mitochondrial phosphate transport as an unexploited antifungal strategy
McLellan, C. A., Vincent, B. M., Solis, N. V., Lancaster, A. K., Sullivan, L. B., Hartland, C. L., Youngsaye, W., Filler, S. G., Whitesell, L., & Lindquist, S. (2018) · Nature Chemical Biology · doi:10.1038/nchembio.2534 · Cited by 49 · see citing works
Genotypic diversity and unrecognized antifungal resistance among populations of Candida glabrata from positive blood cultures
Badrane, H., Cheng, S., Dupont, C., Hao, B., Driscoll, E., Morder, K., Liu, G., Newbrough, A., Fleres, G., Kaul, D., et al. (2023) · doi:10.21203/rs.3.rs-2706400/v1 · Cited by 48 · see citing works
Ydj1 governs fungal morphogenesis and stress response, and facilitates mitochondrial protein import via Mas1 and Mas2
Xie, J. L., Bohovych, I., Wong, E. O. Y., Lambert, J., Gingras, A., Khalimonchuk, O., Cowen, L. E., & Leach, M. D. (2017) · Microbial Cell · doi:10.15698/mic2017.10.594 · Cited by 45 · see citing works
The Zinc Finger Protein Mig1 Regulates Mitochondrial Function and Azole Drug Susceptibility in the Pathogenic Fungus Cryptococcus neoformans
Caza, M., Hu, G., Price, M., Perfect, J. R., & Kronstad, J. W. (2016) · mSphere · doi:10.1128/msphere.00080-15 · Cited by 48 · see citing works
Membrane Proteome-Wide Response to the Antifungal Drug Clotrimazole in Candida glabrata: Role of the Transcription Factor CgPdr1 and the Drug:H+ Antiporters CgTpo1_1 and CgTpo1_2
Pais, P., Costa, C., Pires, C. M. B. F., Shimizu, K., Chibana, H., & Teixeira, M. C. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.045344 · Cited by 46 · see citing works
Cellular iron homeostasis mediated by the Mrs4–Ccc1–Smf3 pathway is essential for mitochondrial function, morphogenesis and virulence in Candida albicans
Xu, N., Dong, Y., Cheng, X., Yu, Q., Qian, K., Mao, J., Jia, C., Ding, X., Zhang, B., Chen, Y., et al. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.12.009 · Cited by 47 · see citing works
Antifungal Activity of Spent Coffee Ground Extracts
Calheiros, D., Días, M. I., Calhelha, R. C., Barros, L., Ferreira, I. C. F. R., Fernandes, C., & Gonçalves, T. (2023) · Microorganisms · doi:10.3390/microorganisms11020242 · Cited by 48 · see citing works
Promising Perspectives for Detection, Identification, and Quantification of Plant Pathogenic Fungi and Oomycetes through Targeting Mitochondrial DNA
Kulik, T., Bilska, K., & Żelechowski, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21072645 · Cited by 45 · see citing works
Lipids of Candida albicans and their role in multidrug resistance
Prasad, R., & Singh, A. (2013) · Current Genetics · doi:10.1007/s00294-013-0402-1 · Cited by 45 · see citing works
Mitochondrial Complex I Is a Global Regulator of Secondary Metabolism, Virulence and Azole Sensitivity in Fungi
Bromley, M., Johns, A., Davies, E. A., Fraczek, M. G., Gilsenan, J. M., Kurbatova, N., Keays, M., Kapushesky, M., Gut, M., Gut, I. G., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0158724 · Cited by 45 · see citing works
Sequencing and characterization of the complete mitochondrial genomes of three Pneumocystis species provide new insights into divergence between human and rodent Pneumocystis
Ma, L., Huang, D., Cuomo, C. A., Sykes, S. M., Fantoni, G., Das, B., Sherman, B. T., Yang, J., Huber, C., Xia, Y., et al. (2013) · The FASEB Journal · doi:10.1096/fj.12-224444 · Cited by 44 · see citing works
Transient mitochondria dysfunction confers fungal cross-resistance against phagocytic killing and fluconazole
Siscar-Lewin, S., Gabaldón, T., Aldejohann, A. M., Kurzai, O., Hube, B., & Brunke, S. (2021) · mBio · doi:10.1128/mbio.01128-21 · Cited by 36 · see citing works
Can Saccharomyces cerevisiae keep up as a model system in fungal azole susceptibility research?
Demuyser, L., & Dijck, P. V. (2019) · Drug Resistance Updates · doi:10.1016/j.drup.2019.02.002 · Cited by 41 · see citing works
Candida glabrata : a deadly companion?
Bolotin‐Fukuhara, M., & Fairhead, C. (2014) · Yeast · doi:10.1002/yea.3019 · Cited by 42 · see citing works
MSS2 maintains mitochondrial function and is required for chitosan resistance, invasive growth, biofilm formation and virulence in Candida albicans
Ke, C.-L., Liao, Y.-T., & Lin, C.-H. (2021) · Virulence · doi:10.1080/21505594.2020.1870082 · Cited by 41 · see citing works
Derivatives of the Antimalarial Drug Mefloquine Are Broad-Spectrum Antifungal Molecules with Activity against Drug-Resistant Clinical Isolates
Montoya, M. C., Beattie, S., Alden, K. M., & Krysan, D. J. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02331-19 · Cited by 42 · see citing works
Fungal KATs/KDACs: A New Highway to Better Antifungal Drugs?
Kuchler, K., Jenull, S., Shivarathri, R., & Chauhan, N. (2016) · PLOS Pathogens · doi:10.1371/journal.ppat.1005938 · Cited by 40 · see citing works
Sphingolipids: Regulators of azole drug resistance and fungal pathogenicity
Song, J., Xiao, L., & Li, R. (2020) · Molecular Microbiology · doi:10.1111/mmi.14586 · Cited by 38 · see citing works
Enhanced Efflux Pump Expression in Candida Mutants Results in Decreased Manogepix Susceptibility
Liston, S. D., Whitesell, L. J., Kapoor, M., Shaw, K. J., & Cowen, L. E. (2020) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00261-20 · Cited by 40 · see citing works
Mechanistic insights into Candida biofilm eradication potential of eucalyptol
Gupta, P., Pruthi, V., & Poluri, K. M. (2020) · Journal of Applied Microbiology · doi:10.1111/jam.14940 · Cited by 40 · see citing works
The Rbf1, Hfl1 and Dbp4 of Candida albicans regulate common as well as transcription factor-specific mitochondrial and other cell activities
Khamooshi, K., Sikorski, P., Sun, N., Calderone, R., & Li, D. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-56 · Cited by 37 · see citing works
Identification and Analysis of Cation Channel Homologues in Human Pathogenic Fungi
Prole, D. L., & Taylor, C. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042404 · Cited by 37 · see citing works
Transcriptional Profiling of a Yeast Colony Provides New Insight into the Heterogeneity of Multicellular Fungal Communities
Traven, A., Jänicke, A., Harrison, P. F., Swaminathan, A., Seemann, T., & Beilharz, T. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046243 · Cited by 36 · see citing works
Self-citation
Comparative Genomics of Sibling Fungal Pathogenic Taxa Identifies Adaptive Evolution without Divergence in Pathogenicity Genes or Genomic Structure
Sillo, F., Garbelotto, M. M., Friedman, M., & Gonthier, P. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv209 · Cited by 36 · see citing works
A Putative Mitochondrial Iron Transporter MrsA in Aspergillus fumigatus Plays Important Roles in Azole-, Oxidative Stress Responses and Virulence
Long, N., Xu, X., Qian, H., Zhang, S., & Lü, L. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00716 · Cited by 36 · see citing works
An Assessment of Growth Media Enrichment on Lipid Metabolome and the Concurrent Phenotypic Properties of Candida albicans
Mahto, K. K., Singh, A., Khandelwal, N., Bhardwaj, N., Jaykar, J., & Prasad, R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113664 · Cited by 35 · see citing works
Mitochondrial Respiratory Pathways Inhibition in Rhizopus oryzae Potentiates Activity of Posaconazole and Itraconazole via Apoptosis
Shirazi, F., & Kontoyiannis, D. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063393 · Cited by 35 · see citing works
Leu1 plays a role in iron metabolism and is required for virulence in Cryptococcus neoformans
Do, E., Hu, G., Caza, M., Oliveira, D. L., Kronstad, J. W., & Jung, W. H. (2014) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2014.12.006 · Cited by 34 · see citing works
Connecting iron regulation and mitochondrial function in Cryptococcus neoformans
Horianopoulos, L. C., & Kronstad, J. W. (2019) · Current Opinion in Microbiology · doi:10.1016/j.mib.2019.04.002 · Cited by 32 · see citing works
Integration of Posttranscriptional Gene Networks into Metabolic Adaptation and Biofilm Maturation in Candida albicans
Verma‐Gaur, J., Qu, Y., Harrison, P. F., Lo, T. L., Quenault, T., Dagley, M. J., Belousoff, M. J., Powell, D., Beilharz, T. H., & Traven, A. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005590 · Cited by 33 · see citing works
Self-citation
Metabolomic profiling for the identification of potential biomarkers involved in a laboratory azole resistance in Candida albicans
Li, L., Liao, Z., Yang, Y., Lv, L., Cao, Y., & Zhu, Z. (2018) · PLoS ONE · doi:10.1371/journal.pone.0192328 · Cited by 31 · see citing works
Amphotericin B Resistance in Aspergillus terreus Is Overpowered by Coapplication of Pro-oxidants
Blatzer, M., Jukic, E., Posch, W., Schöpf, B., Binder, U., Steger, M., Blum, G., Hackl, H., Gnaiger, E., Lass‐Flörl, C., et al. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6220 · Cited by 31 · see citing works
Lipidomics and in Vitro Azole Resistance in Candida albicans
Singh, A., Mahto, K. K., & Prasad, R. (2013) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2012.0075 · Cited by 31 · see citing works
Multidrug-Resistant Transporter Mdr1p-Mediated Uptake of a Novel Antifungal Compound
Sun, N., Li, D., Fonzi, W. A., Li, X. V., Zhang, L., & Calderone, R. (2013) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01504-13 · Cited by 30 · see citing works
The ERMES (Endoplasmic Reticulum and Mitochondria Encounter Structures) mediated functions in fungi
Kundu, D., & Pasrija, R. (2020) · Mitochondrion · doi:10.1016/j.mito.2020.02.010 · Cited by 30 · see citing works
The Novel J-Domain Protein Mrj1 Is Required for Mitochondrial Respiration and Virulence in Cryptococcus neoformans
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MINIREVIEWS Mitochondria and Fungal Pathogenesis: Drug Tolerance, Virulence, and Potential for Antifungal Therapy
Shingú-Vázquez, M., & Traven, A. (2011)
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Authors: Shingu-Vazquez, M., & Traven, A.
Affiliations: Department of Biochemistry and Molecular Biology, Monash University, Clayton 3800, Victoria, Australia
Monash University (AU)
Corresponding author: Traven, Ana
ORCID: Traven, Ana
Venue: Eukaryotic Cell
Publisher: American Society for Microbiology
Published: 2011-11
Volume: 10
Issue: 11
Pages: 1376-1383
ISSN: 1535-9778 (ISSN-L)
1535-9786
DOI: 10.1128/ec.05184-11
PMC: PMC3209048
OpenAlex: W2155416658
Cited by: 209
References: 91
Citations by year: 2026: 15 · 2025: 21 · 2024: 13 · 2023: 18 · 2022: 10 · 2021: 12 · 2020: 17 · 2019: 19 · 2018: 14 · 2017: 11 · 2016: 14 · 2015: 14 · 2014: 9 · 2013: 16 · 2012: 6
FWCI: 1.23
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Eukaryotic Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Monash University Research Portal (Monash University) (submittedVersion, other-oa)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Keywords: mitochondria, fungal pathogenesis, drug tolerance, antifungal resistance, fungal virulence, mitochondrial dysfunction, membrane lipid homeostasis, mitochondrial mutations, antifungal drug development, hypervirulence
MeSH terms: Antifungal Agents, Azoles, Candida albicans, Cryptococcus neoformans, Fungi, Humans, Membrane Lipids, Microbial Sensitivity Tests, Mitochondria, Mycoses, Polyenes, Saccharomyces cerevisiae, Drug Resistance, Fungal, Candida glabrata, Mitochondrial Membranes, Drug Discovery

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Mitochondria and Fungal Pathogenesis: Drug Tolerance, Virulence, and Potential for Antifungal Therapy

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