Drug-Resistant Epimutants Exhibit Organ-Specific Stability and Induction during Murine Infections Caused by the Human Fungal Pathogen Mucor circinelloides
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Abstract
The emerging fungal pathogen Mucor circinelloides causes a severe infection, mucormycosis, which leads to considerable morbidity and mortality. Treatment of Mucor infection is challenging because Mucor is inherently resistant to nearly all clinical antifungal agents. An RNAi-dependent and reversible mechanism of antifungal resistance, epimutation, was recently reported for Mucor . Epimutation has not been studied in vivo , and it was unclear whether it would contribute to antifungal resistance observed clinically. We demonstrate that epimutation can both be induced and reverted after in vivo passage through a mouse; rates of both induction and reversion are higher after brain infection than after infection of other organs (liver, spleen, kidneys, or lungs). Elucidating the roles played by epimutation in drug resistance and infection will improve our understanding of Mucor and other fungal pathogens and may have implications for antifungal treatment.
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Epimutation-mediated drug resistance represents a potential clinically-relevant factor affecting drug resistance.
“In a systemic mouse model of Mucor infection, epimutation-mediated drug resistance can be rapidly induced and reverted over the course of the infection, and thus represents a potential clinically-relevant factor affecting drug resistance103.”
From Molecular mechanisms governing antifungal drug resistance (2023) · cites this paper as [103]
In a systemic mouse model of Mucor infection, epimutation-mediated drug resistance can be rapidly induced and reverted over the course of the infection.
“In a systemic mouse model of Mucor infection, epimutation-mediated drug resistance can be rapidly induced and reverted over the course of the infection, and thus represents a potential clinically-relevant factor affecting drug resistance103.”
From Molecular mechanisms governing antifungal drug resistance (2023) · cites this paper as [103]
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Epidemiology and Outcome of Zygomycosis: A Review of 929 Reported Cases
Roden, M. M., Zaoutis, T. E., Buchanan, W. L., Knudsen, T. A., Sarkisova, T. A., Schaufele, R. L., Sein, M. T., Sein, T., Chiou, C. C., Chu, J. H., et al. (2005) · Clinical Infectious Diseases · doi:10.1086/432579 · Cited by 3,048 · see citing works
Kino, T., Hatanaka, H., Hashimoto, M., Nishiyama, M., Goto, T., OKUHARA, M., KOHSAKA, M., AOKI, H., & Imanaka, H. (1987) · The Journal of Antibiotics · doi:10.7164/antibiotics.40.1249 · Cited by 1,244 · see citing works
Jeong, W., Keighley, C., Wolfe, R. S., Lee, W. L., Slavin, M. A., Kong, D. C. M., & Chen, S. C.-A. (2018) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2018.07.011 · Cited by 1,105 · see citing works
Global Epidemiology of Mucormycosis
Prakash, H., & Chakrabarti, A. (2019) · Journal of Fungi · doi:10.3390/jof5010026 · Cited by 955 · see citing works
Sehgal, S. N., BAKER, H., & Vézina, C. (1975) · The Journal of Antibiotics · doi:10.7164/antibiotics.28.727 · Cited by 949 · see citing works
Isavuconazole treatment for mucormycosis: a single-arm open-label trial and case-control analysis
Marty, F. M., Ostrosky‐Zeichner, L., Cornely, O. A., Mullane, K. M., Perfect, J. R., Thompson, G. R., Alangaden, G. J., Brown, J. W., Fredricks, D. N., Heinz, W., et al. (2016) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(16)00071-2 · Cited by 714 · see citing works
Retro-orbital injections in mice
Yardeni, T., Eckhaus, M., Morris, H. D., Huizing, M., & Hoogstraten-Miller, S. L. (2011) · Lab Animal · doi:10.1038/laban0511-155 · Cited by 533 · see citing works
Kontoyiannis, D. P., & Lewis, R. E. (2011) · Blood · doi:10.1182/blood-2011-03-316430 · Cited by 376 · see citing works
Necrotizing Cutaneous Mucormycosis after a Tornado in Joplin, Missouri, in 2011
Neblett Fanfair, R., Benedict, K., Bos, J., Bennett, S. D., Lo, Y.-C., Adebanjo, T., Etienne, K., Deak, E., Derado, G., Shieh, W.-J., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1204781 · Cited by 360 · see citing works
Kelly, S. L., Lamb, D. C., Kelly, D. E., Manning, N. J., Loeffler, J., Hebart, H., Schumacher, U., & Einsele, H. (1997) · FEBS Letters · doi:10.1016/s0014-5793(96)01360-9 · Cited by 351 · see citing works
INDUCTION OF YEASTLIKE DEVELOPMENT IN MUCOR BY CARBON DIOXIDE
Bartnicki-García, S., & Nickerson, W. J. (1962) · Journal of Bacteriology · doi:10.1128/jb.84.4.829-840.1962 · Cited by 246 · see citing works
Singh, N., Aguado, J. M., Bonatti, H., Forrest, G. N., Gupta, K. L., Safdar, N., John, G. T., Pursell, K. J., Muñóz, P., Patel, R., et al. (2009) · The Journal of Infectious Diseases · doi:10.1086/605445 · Cited by 232 · see citing works
Nolte, F. S., Parkinson, T., Falconer, D. J., Dix, S. P., Williams, J. M., Gilmore, C., Geller, R., & Wingard, J. R. (1997) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.41.1.196 · Cited by 219 · see citing works
Disruption of Ergosterol Biosynthesis Confers Resistance to Amphotericin B inCandida lusitaniae
Young, L. Y., Hull, C. M., & Heitman, J. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.9.2717-2724.2003 · Cited by 184 · see citing works
Self-citationAntifungal drug resistance evoked via RNAi-dependent epimutations
Calo, S., Shertz-Wall, C., Lee, S. C., Bastidas, R. J., Nicolás, F. E., Granek, J. A., Mieczkowski, P., Torres-Martínez, S., Ruiz-Vázquez, R. M., Cardenas, M. E., et al. (2014) · Nature · doi:10.1038/nature13575 · Cited by 175 · see citing works
Self-citationLee, S. C., Li, A., Calo, S., & Heitman, J. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003625 · Cited by 172 · see citing works
Self-citationSporangiospore Size Dimorphism Is Linked to Virulence of Mucor circinelloides
Li, C. H., Cervantes, M., Springer, D. J., Boekhout, T., Ruiz‐Vázquez, R. M., Torres‐Martínez, S., Heitman, J., & Lee, S. C. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002086 · Cited by 151 · see citing works
Self-citationResistance to fluconazole and amphotericin in Candida albicans from AIDS patients
Kelly, S. L., Lamb, D. C., Kelly, D. E., Loeffler, J., & Einsele, H. (1996) · The Lancet · doi:10.1016/s0140-6736(05)65949-1 · Cited by 140 · see citing works
Lee, S. C., Billmyre, R. B., Li, A., Carson, S. A., Sykes, S. M., Huh, E. Y., Mieczkowski, P. A., Ko, D. C., Cuomo, C. A., & Heitman, J. (2014) · mBio · doi:10.1128/mbio.01390-14 · Cited by 133 · see citing works
Self-citationTwo classes of small antisense RNAs in fungal RNA silencing triggered by non‐integrative transgenes
Nicolás, F. E., Torres‐Martínez, S., & Ruiz‐Vázquez, R. M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg384 · Cited by 132 · see citing works
Kontoyiannis, D. P., Yang, H., Song, J., Kelkar, S. S., Yang, X., Azie, N., Harrington, R., Fan, A., Lee, E., & Spalding, J. R. (2016) · BMC Infectious Diseases · doi:10.1186/s12879-016-2023-z · Cited by 132 · see citing works
Mucormycosis Outbreak Associated With Hospital Linens
Duffy, J., Harris, J., Gade, L., Sehulster, L. M., Newhouse, E., Moulton-Meissner, H. A., Noble‐Wang, J., Rao, C. Y., Balajee, S. A., & Chiller, T. M. (2014) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0000000000000261 · Cited by 130 · see citing works
Antifungal resistance in mucorales
Dannaoui, É. (2017) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2017.08.010 · Cited by 123 · see citing works
Distinct white collar‐1 genes control specific light responses in Mucor circinelloides
Silva-Franco, F., Torres‐Martínez, S., & Garre, V. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05291.x · Cited by 115 · see citing works
Steel, C., Stephens, A. L., Hahto, S. M., Singletary, S. J., & Ciavarra, R. P. (2007) · Lab Animal · doi:10.1038/laban0108-26 · Cited by 113 · see citing works
Lee, S. C., Li, A., Calo, S., Inoue, M., Tonthat, N. K., Bain, J. M., Louw, J., Shinohara, M. L., Erwig, L. P., Schumacher, M. A., et al. (2015) · Molecular Microbiology · doi:10.1111/mmi.13071 · Cited by 90 · see citing works
Self-citationAcquired multidrug antifungal resistance in Candida lusitaniae during therapy
Asner, S. A., Giulieri, S., Diezi, M., Marchetti, O., & Sanglard, D. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02204-15 · Cited by 82 · see citing works
Bastidas, R. J., Shertz, C. A., Lee, S. C., Heitman, J., & Cardenas, M. E. (2011) · Eukaryotic Cell · doi:10.1128/ec.05284-11 · Cited by 79 · see citing works
Self-citationThe environmental source of emerging Apophysomyces variabilis infection in India
Prakash, H., Ghosh, A. K., Rudramurthy, S. M., Paul, R. A., Gupta, S., Negi, V., & Chakrabarti, A. (2016) · Medical Mycology · doi:10.1093/mmy/myw014 · Cited by 73 · see citing works
RNAi-Based Functional Genomics Identifies New Virulence Determinants in Mucormycosis
Trieu, T. A., Navarro-Mendoza, M. I., Arques, C. P., Sanchis, M., Capilla, J., Navarro-Rodríguez, P., López‐Fernández, L., Torres‐Martínez, S., Garre, V., Ruiz‐Vázquez, R. M., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006150 · Cited by 73 · see citing works
Chang, Z., Billmyre, R. B., Lee, S. C., & Heitman, J. (2019) · PLOS Genetics · doi:10.1371/journal.pgen.1007957 · Cited by 72 · see citing works
Self-citationCalo, S., Nicolás, F. E., Lee, S. C., Vila, A., Cervantes, M., Torres-Martinez, S., Ruiz-Vazquez, R. M., Cardenas, M. E., & Heitman, J. (2017) · PLOS Genetics · doi:10.1371/journal.pgen.1006686 · Cited by 65 · see citing works
Self-citationA Non-canonical RNA Silencing Pathway Promotes mRNA Degradation in Basal Fungi
Trieu, T. A., Calo, S., Nicolás, F. E., Vila, A., Moxon, S., Dalmay, T., Torres‐Martínez, S., Garre, V., & Ruiz‐Vázquez, R. M. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005168 · Cited by 64 · see citing works
Characterization and control of Mucor circinelloides spoilage in yogurt
Snyder, A. B., Churey, J. J., & Worobo, R. W. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.04.008 · Cited by 45 · see citing works
Sundermann, A. J., Clancy, C. J., Pasculle, A. W., Liu, G., Cumbie, R. B., Driscoll, E., Ayres, A. M., Donahue, L., Pergam, S. A., Abbo, L. M., et al. (2018) · Clinical Infectious Diseases · doi:10.1093/cid/ciy669 · Cited by 44 · see citing works
Metabolic control of antifungal drug resistance
Robbins, N., Collins, C., Morhayim, J., & Cowen, L. E. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.07.004 · Cited by 40 · see citing works
Price, J. E., Barth, R. F., Johnson, C. W., & Staubus, A. E. (1984) · Experimental Biology and Medicine · doi:10.3181/00379727-177-41955 · Cited by 34 · see citing works
Animal Models to Study Mucormycosis
Jacobsen, I. D. (2019) · Journal of Fungi · doi:10.3390/jof5020027 · Cited by 34 · see citing works
Luna-Tapia, A., Willems, H. M. E., Parker, J. E., Tournu, H., Barker, K. S., Nishimoto, A. T., Rogers, P. D., Kelly, S. L., Peters, B. M., & Palmer, G. E. (2018) · mBio · doi:10.1128/mbio.00225-18 · Cited by 29 · see citing works
Rivaldi, J. D., de Carvalho, A. K. F., da Conceição, L. R. V., & Castro, H. F. (2017) · Preparative Biochemistry & Biotechnology · doi:10.1080/10826068.2017.1365246 · Cited by 26 · see citing works
Morris, M., & Smith, S. H. (1996) · The Lancet · doi:10.1016/s0140-6736(05)65945-4 · Cited by 25 · see citing works
Garcia, A., Adedoyin, G., Heitman, J., & Lee, S. C. (2017) · G3 Genes Genomes Genetics · doi:10.1534/g3.117.041095 · Cited by 25 · see citing works
Self-citationGastrointestinal microbiota alteration induced by Mucor circinelloides in a murine model
Mueller, K. D., Zhang, H., Serrano, C. R., Billmyre, R. B., Huh, E. Y., Wiemann, P., Keller, N. P., Wang, Y., Heitman, J., & Lee, S. C. (2019) · The Journal of Microbiology · doi:10.1007/s12275-019-8682-x · Cited by 25 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
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
Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota
Shen, X., Steenwyk, J. L., LaBella, A. L., Opulente, D. A., Zhou, X., Kominek, J., Li, Y., Groenewald, M., Hittinger, C. T., & Rokas, A. (2020) · Science Advances · doi:10.1126/sciadv.abd0079 · Cited by 157 · see citing works
Genotypic and Phenotypic Diversity among Human Isolates of Akkermansia muciniphila
Becken, B., Davey, L., Middleton, D. R., Mueller, K. D., Sharma, A., Holmes, Z. C., Dallow, E., Remick, B., Barton, G. M., David, L. A., et al. (2021) · mBio · doi:10.1128/mbio.00478-21 · Cited by 125 · see citing works
Mucorales Species and Macrophages
Nicolás, F. E., Murcia, L., Navarro, E., Navarro-Mendoza, M. I., Arques, C. P., & Garre, V. (2020) · Journal of Fungi · doi:10.3390/jof6020094 · Cited by 80 · see citing works
Genes, Pathways, and Mechanisms Involved in the Virulence of Mucorales
Lax, C., Arques, C. P., Navarro-Mendoza, M. I., Cánovas-Márquez, J. T., Tahiri, G., Pérez-Ruiz, J. A., Osorio-Concepción, M., Murcia, L., Navarro, E., Garre, V., et al. (2020) · Genes · doi:10.3390/genes11030317 · Cited by 76 · see citing works
The Evolutionary Significance of RNAi in the Fungal Kingdom
Lax, C., Tahiri, G., Patiño-Medina, J. A., Cánovas-Márquez, J. T., Pérez-Ruiz, J. A., Osorio-Concepción, M., Navarro, E., & Calo, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249348 · Cited by 76 · see citing works
Breathing and Tilting: Mesoscale Simulations Illuminate Influenza Glycoprotein Vulnerabilities
Casalino, L., Seitz, C., Lederhofer, J., Tsybovsky, Y., Wilson, I. A., Kanekiyo, M., & Amaro, R. (2022) · ACS Central Science · doi:10.1021/acscentsci.2c00981 · Cited by 53 · see citing works
Constraints on the Efficiency of Engineered Electromicrobial Production
Salimijazi, F., Kim, J., Schmitz, A. M., Grenville, R., Bocarsly, A. B., & Barstow, B. (2020) · Joule · doi:10.1016/j.joule.2020.08.010 · Cited by 61 · see citing works
Martelli, F., Hernandes, N. H., Zuo, Z., Wang, J., Wong, C.-O., Karagas, N. E., Roessner, U., Rupasinghe, T., Robin, C., Venkatachalam, K., et al. (2022) · eLife · doi:10.7554/elife.73812 · Cited by 59 · see citing works
Otter, C. J., Fausto, A., Tan, L. H., Khosla, A. S., Cohen, N. A., & Weiss, S. R. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2218083120 · Cited by 56 · see citing works
Priority effects dictate community structure and alter virulence of fungal-bacterial biofilms
Cheong, J. Z. A., Johnson, C. J., Wan, H., Liu, A., Kernien, J. F., Gibson, A. L. F., Nett, J. E., & Kalan, L. (2021) · The ISME Journal · doi:10.1038/s41396-021-00901-5 · Cited by 56 · see citing works
Microbial hitchhiking: how Streptomyces spores are transported by motile soil bacteria
Muok, A. R., Claessen, D., & Briegel, A. (2021) · The ISME Journal · doi:10.1038/s41396-021-00952-8 · Cited by 55 · see citing works
Insights into bacterial cell division from a structure of EnvC bound to the FtsX periplasmic domain
Cook, J., Baverstock, T. C., McAndrew, M. B. L., Stansfeld, P. J., Roper, D. I., & Crow, A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2017134117 · Cited by 55 · see citing works
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Büke, F., Grilli, J., Lagomarsino, M. C., Bokinsky, G., & Tans, S. J. (2022) · Current Biology · doi:10.1016/j.cub.2021.12.033 · Cited by 54 · see citing works
Ramadan, M., Kohail, M., Alharbi, Y. R., Abadel, A. A., Binyahya, A. S., & Mohsen, A. (2023) · Journal of Materials Research and Technology · doi:10.1016/j.jmrt.2023.01.158 · Cited by 49 · see citing works
The archaeal protein SepF is essential for cell division in Haloferax volcanii
Nußbaum, P., Gerstner, M., Dingethal, M., Erb, C., & Albers, S. (2021) · Nature Communications · doi:10.1038/s41467-021-23686-9 · Cited by 43 · see citing works
Kalem, M. C., Subbiah, H., Leipheimer, J., Glazier, V. E., & Panepinto, J. C. (2021) · mBio · doi:10.1128/mbio.03225-20 · Cited by 44 · see citing works
Kumar, N. G., Nieto, V., Kroken, A. R., Jedel, E., Grosser, M. R., Hallsten, M. E., Metruccio, M. M. E., Yahr, T. L., Evans, D. J., & Fleiszig, S. M. J. (2022) · mBio · doi:10.1128/mbio.02742-22 · Cited by 43 · see citing works
A non-canonical RNAi pathway controls virulence and genome stability in Mucorales
Arques, C. P., Navarro-Mendoza, M. I., Murcia, L., Navarro, E., Garre, V., & Nicolás, F. E. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008611 · Cited by 43 · see citing works
Chrissian, C., Camacho, E., Kelly, J. E., Wang, H., Casadevall, A., & Stark, R. E. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.015201 · Cited by 40 · see citing works
Antigen spacing on protein nanoparticles influences antibody responses to vaccination
Ellis, D., Dosey, A. M., Boyoglu-Barnum, S., Park, Y., Gillespie, R. A., Syeda, H., Hutchinson, G. B., Tsybovsky, Y., Murphy, M., Pettie, D., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113552 · Cited by 42 · see citing works
Bejerman, N., Dietzgen, R. G., & Debat, H. (2023) · Viruses · doi:10.3390/v15122402 · Cited by 40 · see citing works
Regulation of protein abundance in genetically diverse mouse populations
Keele, G. R., Zhang, T., Pham, D. T., Vincent, M. J., Bell, T. A., Hock, P., Shaw, G. D., Paulo, J. A., Munger, S. C., de Villena, F. P., et al. (2021) · Cell Genomics · doi:10.1016/j.xgen.2021.100003 · Cited by 38 · see citing works
Steinberg, A. P., Lin, M., & Kussell, E. L. (2022) · eLife · doi:10.7554/elife.78533 · Cited by 38 · see citing works
Mucorales and Mucormycosis: Recent Insights and Future Prospects
Tahiri, G., Lax, C., Cánovas-Márquez, J. T., Carrillo-Marín, P., Sanchis, M., Navarro, E., Garre, V., & Nicolás, F. E. (2023) · Journal of Fungi · doi:10.3390/jof9030335 · Cited by 37 · see citing works
Hendriks, A., van Dalen, R., Ali, S., Gerlach, D., van der Marel, G. A., Fuchsberger, F. F., Aerts, P. C., de Haas, C. J. C., Peschel, A., Rademacher, C., et al. (2021) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.0c00822 · Cited by 34 · see citing works
Evolution of two-component quorum sensing systems
Giannakara, M., & Koumandou, V. L. (2022) · Access Microbiology · doi:10.1099/acmi.0.000303 · Cited by 35 · see citing works
Lax, C., Navarro-Mendoza, M. I., Arques, C. P., Navarro, E., Nicolás, F. E., & Garre, V. (2021) · Cell Reports Methods · doi:10.1016/j.crmeth.2021.100124 · Cited by 34 · see citing works
Liang, J., Li, Y., Dodds, P. N., Figueroa, M., Sperschneider, J., Han, S., Tsui, C. K. M., Zhang, K., Li, L., Ma, Z., et al. (2022) · Molecular Ecology Resources · doi:10.1111/1755-0998.13739 · Cited by 32 · see citing works
Estimating hepatitis B virus cccDNA persistence in chronic infection†
Lythgoe, K., Lumley, S., Pellis, L., McKeating, J. A., & Matthews, P. C. (2020) · Virus Evolution · doi:10.1093/ve/veaa063 · Cited by 31 · see citing works
Genetically controlled mtDNA deletions prevent ROS damage by arresting oxidative phosphorylation
Stenberg, S., Li, J., Gjuvsland, A. B., Persson, K. O., Demitz-Helin, E., Peña, C. G., Yue, J., Gilchrist, C., Ärengård, T., Ghiaci, P., et al. (2022) · eLife · doi:10.7554/elife.76095 · Cited by 31 · see citing works
Brandel, A., Aigal, S., Lagies, S., Schlimpert, M., Meléndez, A. V., Xu, M., Lehmann, A., Hummel, D. R., Fisch, D., Madl, J., et al. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03766-1 · Cited by 30 · see citing works
Horta, M. A. C., Steenwyk, J. L., Mead, M. E., dos Santos, L. H. B., Zhao, S., Gibbons, J. G., Marcet‐Houben, M., Gabaldón, T., Rokas, A., & Goldman, G. H. (2022) · mBio · doi:10.1128/mbio.01519-22 · Cited by 30 · see citing works
Molecular mechanisms that govern infection and antifungal resistance in Mucorales
Lax, C., Nicolás, F. E., Navarro, E., & Garre, V. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00188-22 · Cited by 29 · see citing works
Rangarajan, A. A., Chia, H. E., Azaldegui, C. A., Olszewski, M., Pereira, G. V., Koropatkin, N. M., & Biteen, J. S. (2022) · Microbiology · doi:10.1099/mic.0.001180 · Cited by 28 · see citing works
cotH Genes Are Necessary for Normal Spore Formation and Virulence in Mucor lusitanicus
Szebenyi, C., Gu, Y., Gebremariam, T., Kocsubé́, S., Kiss-Vetráb, S., Jáger, O., Patai, R., Spisák, K., Sinka, R., Binder, U., et al. (2023) · mBio · doi:10.1128/mbio.03386-22 · Cited by 28 · see citing works
Lax, C., Mondo, S. J., Osorio-Concepción, M., Muszewska, A., Corrochano-Luque, M., Gutiérrez, G., Riley, R. W., Lipzen, A., Guo, J., Hundley, H. N., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50365-2 · Cited by 27 · see citing works
Cicchese, J. M., Sambarey, A., Kirschner, D. E., Linderman, J. J., & Chandrasekaran, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-84827-0 · Cited by 26 · see citing works
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Y-Box Binding Protein 1 Interacts with Dengue Virus Nucleocapsid and Mediates Viral Assembly
Toro, M. D., Kennedy, D. R., Chuo, V., Popov, V. L., Pompon, J., & García-Blanco, M. A. (2022) · mBio · doi:10.1128/mbio.00196-22 · Cited by 26 · see citing works
Atypical chemoreceptor arrays accommodate high membrane curvature
Muok, A. R., Ortega, D. R., Kurniyati, K., Yang, W. J., Maschmann, Z. A., Mabrouk, A. S., Li, C., Crane, B. R., & Briegel, A. (2020) · Nature Communications · doi:10.1038/s41467-020-19628-6 · Cited by 25 · see citing works
Molecular pathways to high-level azithromycin resistance in Neisseria gonorrhoeae
Laumen, J., Manoharan-Basil, S. S., Verhoeven, E., Abdellati, S., Baetselier, I. D., Crucitti, T., Xavier, B. B., Chapelle, S., Lammens, C., Dijck, C. V., et al. (2021) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkab084 · Cited by 25 · see citing works
Amyloid Aggregation of Streptococcus mutans Cnm Influences Its Collagen-Binding Activity
di Cologna, N. D. M., Samaddar, S., Valle, C. A., Vargas, J., Avilés-Reyes, A., Morales, J. C. T., Ganguly, T., Pileggi, R., Brady, L. J., Lemos, J. A. C., et al. (2021) · Applied and Environmental Microbiology · doi:10.1128/aem.01149-21 · Cited by 25 · see citing works
Cardiac Microlesions Form During Severe Bacteremic Enterococcus faecalis Infection
Brown, A. O., Singh, K. V., Cruz, M. R., Kaval, K. G., Francisco, L. E., Murray, B. E., & Garsin, D. A. (2020) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiaa371 · Cited by 24 · see citing works
Rescue of Escherichia coli auxotrophy by de novo small proteins
Babina, A. M., Surkov, S., Ye, W., Jerlström-Hultqvist, J., Larsson, M., Holmqvist, E., Jemth, P., Andersson, D. I., & Knopp, M. (2023) · eLife · doi:10.7554/elife.78299 · Cited by 24 · see citing works
Human cytomegalovirus UL138 interaction with USP1 activates STAT1 in infection
Zarrella, K., Longmire, P., Zeltzer, S., Collins-McMillen, D. K., Hancock, M. H., Buehler, J., Reitsma, J. M., Terhune, S. S., Nelson, J. A., & Goodrum, F. D. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011185 · Cited by 23 · see citing works
Chakrabarti, A., & Singh, S. (2020) · Current Fungal Infection Reports · doi:10.1007/s12281-020-00406-2 · Cited by 23 · see citing works
Ióca, L. P., Dai, Y., Kunakom, S., Diaz‐Espinosa, J., Krunić, A., Crnkovic, C. M., Orjala, J., Sanchez, L. M., Ferreira, A. G., Berlinck, R. G. S., et al. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202017320 · Cited by 23 · see citing works
Niggli, S., & Kümmerli, R. (2020) · Applied and Environmental Microbiology · doi:10.1128/aem.00962-20 · Cited by 22 · see citing works
Stambuk, F., Ojeda, C., Matos, G. M., Rosa, R. D., Mercado, L. A., & Schmitt, P. (2021) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2021.10.037 · Cited by 23 · see citing works
Engineering quorum quenching acylases with improved kinetic and biochemical properties
Sompiyachoke, K., & Elias, M. H. (2024) · Protein Science · doi:10.1002/pro.4954 · Cited by 22 · see citing works
Petersen, B., Liu, M. S., Podicheti, R., Yang, A. Y.-P., Simpson, C. A., Hemmerich, C., Rusch, D., & van Kessel, J. C. (2021) · bioRxiv · doi:10.1128/jb.00276-21 · Cited by 19 · see citing works
Recent Advances and Future Directions in the Understanding of Mucormycosis
Garre, V. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.850581 · Cited by 22 · see citing works
Schumacher, K., Gelhausen, R., Kion-Crosby, W., Barquist, L., Backofen, R., & Jung, K. (2023) · mSystems · doi:10.1128/msystems.01037-23 · Cited by 22 · see citing works
Simpson, C. A., Petersen, B. D., Haas, N. W., Geyman, L. J., Lee, A., Podicheti, R., Pepin, R. H., Brown, L. C. W., Rusch, D. B., Manzella, M. P., et al. (2021) · Environmental Microbiology · doi:10.1111/1462-2920.15602 · Cited by 21 · see citing works
HelR is a helicase-like protein that protects RNA polymerase from rifamycin antibiotics
Surette, M. D., Waglechner, N., Koteva, K. K., & Wright, G. D. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.06.019 · Cited by 21 · see citing works
Navarro-Mendoza, M. I., Arques, C. P., Parker, J. E., Xu, Z., Kelly, S. L., & Heitman, J. (2024) · mBio · doi:10.1128/mbio.01661-24 · Cited by 20 · see citing works
Self-citationSiri, M., Mangiarotti, A., Vázquéz-Dávila, M., & Bidan, C. M. (2023) · Macromolecular Bioscience · doi:10.1002/mabi.202300234 · Cited by 20 · see citing works
A Win–Loss Interaction on Fe0 Between Methanogens and Acetogens From a Climate Lake
Palacios, P. A., Francis, W. R., & Rotaru, A. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.638282 · Cited by 20 · see citing works
Scoggin, K., Lynch, R., Gupta, J., Nagarajan, A., Sheffield, M., Elsaadi, A. M., Bowden, C., Aminian, M., Peterson, A., Adams, L. G., et al. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1010075 · Cited by 19 · see citing works
Vass, M., Eriksson, K. I. A., Carlsson‐Granér, U., Wikner, J., & Andersson, A. (2022) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiac120 · Cited by 19 · see citing works
Navarro-Mendoza, M. I., Arques, C. P., & Heitman, J. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2220475120 · Cited by 18 · see citing works
Self-citationRNAi epimutations conferring antifungal drug resistance are inheritable
Arques, C. P., Navarro-Mendoza, M. I., Xu, Z., Walther, G., & Heitman, J. (2025) · Nature Communications · doi:10.1038/s41467-025-62572-6 · Cited by 18 · see citing works
Self-citationExistence of log-phase Escherichia coli persisters and lasting memory of a starvation pulse
Svenningsen, M. S., Svenningsen, S. L., Sørensen, M. A., & Mitarai, N. (2021) · Life Science Alliance · doi:10.26508/lsa.202101076 · Cited by 16 · see citing works
Differential Gene Expression of Mucor lusitanicus under Aerobic and Anaerobic Conditions
Homa, M., Ibragimova, S., Szebenyi, C., Nagy, G., Zsindely, N., Bodai, L., Vágvölgyi, C., Nagy, G., & Papp, T. (2022) · Journal of Fungi · doi:10.3390/jof8040404 · Cited by 17 · see citing works
Systematic mapping of chemoreceptor specificities for Pseudomonas aeruginosa
Xu, W., Cerna‐Vargas, J. P., Tajuelo, A., Lozano‐Montoya, A., Kivoloka, M., Krink, N., Monteagudo‐Cascales, E., Matilla, M. A., Krell, T., & Sourjik, V. (2023) · mBio · doi:10.1128/mbio.02099-23 · Cited by 15 · see citing works
Niggli, S., Wechsler, T., & Kümmerli, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.733991 · Cited by 16 · see citing works
Runtuvuori‐Salmela, A., Kunttu, H. M. T., Laanto, E., Almeida, G. M. D. F., Mäkelä, K., Middelboe, M., & Sundberg, L. (2022) · Environmental Microbiology · doi:10.1111/1462-2920.15901 · Cited by 16 · see citing works
Nuclear ingression of cytoplasmic bodies accompanies a boost in autophagy
Garcia, M., Kumanski, S., Elías-Villalobos, A., Cazevieille, C., Soulet, C., & Moriel‐Carretero, M. (2022) · Life Science Alliance · doi:10.26508/lsa.202101160 · Cited by 16 · see citing works
High-resolution in situ structures of hantavirus glycoprotein tetramers
Guo, L., McFadden, E., Slough, M. M., Stone, E. T., Berrigan, J. L., Mittler, E., Hatzakis, K., Hinkley, T. C., Kain, H. S., Ke, Z., et al. (2026) · Cell · doi:10.1016/j.cell.2026.01.030 · Cited by 19 · see citing works
Paulson, A. R., Lougheed, S. C., Huang, D., & Colautti, R. I. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.01404-23 · Cited by 15 · see citing works
Epigenetic dynamics of centromeres and neocentromeres in Cryptococcus deuterogattii
Schotanus, K., Yadav, V., & Heitman, J. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009743 · Cited by 15 · see citing works
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Lax, C., Cánovas-Márquez, J. T., Tahiri, G., Navarro, E., Garre, V., & Nicolás, F. E. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073454 · Cited by 15 · see citing works
Quek, S., Cerdeira, L., Jeffries, C. L., Tomlinson, S., Walker, T., Hughes, G. L., & Heinz, E. (2022) · Microbial Genomics · doi:10.1099/mgen.0.000805 · Cited by 14 · see citing works
Hällgren, J., Koonce, K. C., Felletti, M., Mortier, J., Turco, E., & Jonas, K. (2023) · PLoS Genetics · doi:10.1371/journal.pgen.1010882 · Cited by 14 · see citing works
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Lehman, K. M., Smith, H. C., & Grabowicz, M. (2022) · mBio · doi:10.1128/mbio.00757-22 · Cited by 13 · see citing works
The RNAi Mechanism Regulates a New Exonuclease Gene Involved in the Virulence of Mucorales
Arques, C. P., Navarro-Mendoza, M. I., Murcia, L., Navarro, E., Garre, V., & Nicolás, F. E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052282 · Cited by 12 · see citing works
Strohdiek, A., Köhler, A. M., Harting, R., Stupperich, H., Gerke, J., Bastakis, E., Neumann, P., Ahmed, Y. L., Ficner, R., & Braus, G. H. (2025) · PLOS Genetics · doi:10.1371/journal.pgen.1011687 · Cited by 12 · see citing works
Kortenbosch, H. H., van Leuven, F., van den Heuvel, C., Schoustra, S. E., Zwaan, B. J., & Snelders, E. (2024) · Applied and Environmental Microbiology · doi:10.1128/aem.00271-24 · Cited by 12 · see citing works
Heterogeneous efflux pump expression underpins phenotypic resistance to antimicrobial peptides
Lee, K. K., Łapińska, U., Tolle, G., Micaletto, M., Zhang, B., Phetsang, W., Verderosa, A. D., Invergo, B. M., Westley, J., Bebes, A., et al. (2025) · eLife · doi:10.7554/elife.99752.4 · Cited by 12 · see citing works
Hamame, A., Davoust, B., Rolain, J., & Diene, S. M. (2022) · Journal of Global Antimicrobial Resistance · doi:10.1016/j.jgar.2022.01.014 · Cited by 12 · see citing works
Arques, C. P., Navarro-Mendoza, M. I., Murcia, L., Lax, C., Sanchis, M., Capilla, J., Navarro, E., Garre, V., & Nicolás, F. E. (2021) · Microorganisms · doi:10.3390/microorganisms9020459 · Cited by 12 · see citing works
The histone code of the fungal genus Aspergillus uncovered by evolutionary and proteomic analyses
Zhang, X., Noberini, R., Bonaldi, T., Collemare, J., & Seidl, M. F. (2022) · Microbial Genomics · doi:10.1099/mgen.0.000856 · Cited by 11 · see citing works
Navigating the fungal battlefield: cysteine-rich antifungal proteins and peptides from Eurotiales
Holzknecht, J., & Marx, F. (2024) · Frontiers in Fungal Biology · doi:10.3389/ffunb.2024.1451455 · Cited by 13 · see citing works
Quorum sensing regulates virulence factors in the coral pathogen Vibrio coralliilyticus
Lydick, V. N., Mass, S., Pepin, R. H., Podicheti, R., Klempic, E., Rusch, D. B., Ushijima, B., Brown, L. C. W., Salomon, D., & van Kessel, J. C. (2025) · Applied and Environmental Microbiology · doi:10.1128/aem.01143-24 · Cited by 11 · see citing works
Solution structure and RNA-binding of a minimal ProQ-homolog fromLegionella pneumophila(Lpp1663)
Immer, C., Hacker, C., & Wöhnert, J. (2020) · RNA · doi:10.1261/rna.077354.120 · Cited by 11 · see citing works
Igwe, A. N., Quasem, B., Liu, N., & Vannette, R. L. (2021) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiab085 · Cited by 11 · see citing works
Grande, F. D., Jamilloux, V., Choisne, N., Calchera, A., Rolshausen, G., Petersen, M., Schulz, M., Nilsson, M. A., & Schmitt, I. (2021) · Biology · doi:10.3390/biology11010024 · Cited by 9 · see citing works
Łazowski, K. (2023) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2023.111816 · Cited by 10 · see citing works
Homeostatic control of an iron repressor in a GI tract resident
Wang, Y., Mao, Y., Chen, X., Huang, X., Jiang, Z., Yang, K., Tian, L., Jiang, T., Zou, Y., Ma, X., et al. (2023) · eLife · doi:10.7554/elife.86075 · Cited by 9 · see citing works
A New Contact Killing Toxin Permeabilizes Cells and Belongs to a Broadly Distributed Protein Family
Crisan, C. V., Chandrashekar, H., Everly, C., Steinbach, G., Hill, S. E., Yunker, P. J., Lieberman, R. R., & Hammer, B. K. (2021) · mSphere · doi:10.1128/msphere.00318-21 · Cited by 9 · see citing works
Influenza A virus hemagglutinin prevents extensive membrane damage upon dehydration
Iriarte-Alonso, M. A., Bittner, A. M., & Chiantia, S. (2022) · BBA Advances · doi:10.1016/j.bbadva.2022.100048 · Cited by 9 · see citing works
Beattie, S. R., Jezewski, A. J., Ristow, L. C., Wellington, M. A., & Krysan, D. J. (2022) · mSphere · doi:10.1128/msphere.00163-22 · Cited by 9 · see citing works
Yadav, V., Mohan, R., Sun, S., & Heitman, J. (2024) · Genetics · doi:10.1093/genetics/iyae010 · Cited by 8 · see citing works
Self-citationPaulson, A. R., O’Callaghan, M., Zhang, X., Rainey, P. B., & Hurst, M. R. H. (2020) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkaa024 · Cited by 8 · see citing works
Jäger, F., Lamy, A., Sun, W.-S. W., Guerini, N., & Berntsson, R. P. ‐. (2022) · Structure · doi:10.1016/j.str.2022.03.013 · Cited by 8 · see citing works
Schmitz, D. A., Allen, R. C., & Kümmerli, R. (2023) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2023.1119 · Cited by 7 · see citing works
Andreu, V. P., Augustijn, H. E., van den Berg, K., van der Hooft, J. J. J., Fischbach, M. A., & Medema, M. H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.14.422671 · Cited by 8 · see citing works
Gélinas, M., Museau, L., Milot, A., & Beauregard, P. B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.11.422287 · Cited by 8 · see citing works
Dosey, A. M., Ellis, D., Boyoglu-Barnum, S., Syeda, H., Saunders, M., Watson, M., Kraft, J. C., Pham, M. N., Guttman, M., Lee, K. K., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.23.541996 · Cited by 8 · see citing works
- Authors
- Chang, Z., & Heitman, J.
- Affiliations
- Duke University (US)
- Corresponding author
- Heitman, Joseph
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2019-12-24
- Volume
- 10
- Issue
- 6
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC6831780
- OpenAlex
- W2985567791
- Cited by
- 202
- References
- 43
- Citations by year
- 2026: 21 · 2025: 16 · 2024: 22 · 2023: 30 · 2022: 42 · 2021: 39 · 2020: 30 · 2019: 2
- FWCI
- 21.85
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- HHS | National Institutes of Health (AI39115-21, AI50113-15, AI104533-05, AI112595-04)
- 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
- Mucor circinelloides, mucormycosis, epimutations, antifungal resistance, brain infection, fungal pathogens
- MeSH terms
- Animals, Antifungal Agents, Disease Models, Animal, Humans, Male, Mice, Inbred BALB C, Mucor, Mucormycosis, Tacrolimus, Sirolimus, Drug Resistance, Fungal, RNA Interference, Epigenesis, Genetic, Mice
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