Comparison of Sterol Import under Aerobic and Anaerobic Conditions in Three Fungal Species, Candida albicans, Candida glabrata, and Saccharomyces cerevisiae
Open accessAbstract
Sterol import has been characterized under various conditions in three distinct fungal species, the model organism Saccharomyces cerevisiae and two human fungal pathogens Candida glabrata and Candida albicans , employing cholesterol, the sterol of higher eukaryotes, as well as its fungal equivalent, ergosterol. Import was confirmed by the detection of esterified cholesterol within the cells. Comparing the three fungal species, we observe sterol import under three different conditions. First, as previously well characterized, we observe sterol import under low oxygen levels in S. cerevisiae and C. glabrata , which is dependent on the transcription factor Upc2 and/or its orthologs or paralogs. Second, we observe sterol import under aerobic conditions exclusively in the two pathogenic fungi C. glabrata and C. albicans . Uptake emerges during post-exponential-growth phases, is independent of the characterized Upc2-pathway and is slower compared to the anaerobic uptake in S. cerevisiae and C. glabrata . Third, we observe under normoxic conditions in C. glabrata that Upc2-dependent sterol import can be induced in the presence of fetal bovine serum together with fluconazole. In summary, C. glabrata imports sterols both in aerobic and anaerobic conditions, and the limited aerobic uptake can be further stimulated by the presence of serum together with fluconazole. S. cerevisiae imports sterols only in anaerobic conditions, demonstrating aerobic sterol exclusion. Finally, C. albicans imports sterols exclusively aerobically in post-exponential-growth phases, independent of Upc2. For the first time, we provide direct evidence of sterol import into the human fungal pathogen C. albicans , which until now was believed to be incapable of active sterol import.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
C. albicans takes up sterols only under aerobic conditions during the post-exponential growth phase, a process independent of UPC2.
“Zavrel et al. found that C. albicans takes up sterols only under aerobic conditions during the post-exponentialgrowth phase, a process independent of UPC2 .”
From The synthesis, regulation, and functions of sterols in<i>Candida albicans</i>: Well-known but still lots to learn (2016) · cites this paper as [21]
Cites
Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E. M., Li, J., Hieter, P., & Boeke, J. D. (1998) · Yeast · doi:10.1002/(sici)1097-0061(19980130)14:2 · Cited by 3,411 · see citing works
Fidel, P. L., Vazquez, J. A., & Sobel, J. D. (1999) · Clinical Microbiology Reviews · doi:10.1128/cmr.12.1.80 · Cited by 953 · see citing works
Rapid Hypothesis Testing with Candida albicans through Gene Disruption with Short Homology Regions
Wilson, R. B., Davis, D. A., & Mitchell, A. P. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.6.1868-1874.1999 · Cited by 763 · see citing works
The SAT1 flipper, an optimized tool for gene disruption in Candida albicans
Reuß, O., Vik, Å., Kolter, R., & Morschhäuser, J. (2004) · Gene · doi:10.1016/j.gene.2004.06.021 · Cited by 744 · see citing works
Yeast Transformation by the LiAc/SS Carrier DNA/PEG Method
Gietz, R. D. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-0799-1_4 · Cited by 655 · see citing works
Andreasen, A. A., & Stier, T. J. B. (1953) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030410103 · Cited by 555 · see citing works
Schneiter, R., Brügger, B., Sandhoff, R., Zellnig, G., Leber, A., Lampl, M., Athenstaedt, K., Hrastnik, C., Eder, S., Daum, G., et al. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.146.4.741 · Cited by 493 · see citing works
Andreasen, A. A., & Stier, T. J. B. (1954) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030430303 · Cited by 392 · see citing works
Yeast Transformation by the LiAc/SS Carrier DNA/PEG Method
Gietz, R. D., & Woods, R. A. (2005) · Humana Press eBooks · doi:10.1385/1-59259-958-3:107 · Cited by 333 · see citing works
Upc2p and Ecm22p, Dual Regulators of Sterol Biosynthesis in <i>Saccharomyces cerevisiae</i>
Vik, Å., & Rine, J. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.19.6395-6405.2001 · Cited by 277 · see citing works
Wilcox, L. J., Balderes, D. A., Wharton, B., Tinkelenberg, A. H., Rao, G., & Sturley, S. L. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204707200 · Cited by 250 · see citing works
Yeast Transformation by the LiAc/SS Carrier DNA/PEG Method
Gietz, R. D. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1363-3_1 · Cited by 241 · see citing works
MacPherson, S., Akache, B., Weber, S., De Deken, X., Raymond, M., & Turcotte, B. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.5.1745-1752.2005 · Cited by 238 · see citing works
Kwast, K. E., Lai, L., Menda, N. S., James, D. T., Aref, S., & Burke, P. V. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.1.250-265.2002 · Cited by 232 · see citing works
Gollub, E., Liu, K. P., Dayan, J., Adlersberg, M., & Sprinson, D. B. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)40440-6 · Cited by 227 · see citing works
Role of <i>Candida albicans</i> Transcription Factor Upc2p in Drug Resistance and Sterol Metabolism
Silver, P. M., Oliver, B. G., & White, T. C. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.6.1391-1397.2004 · Cited by 216 · see citing works
Self-citationLi, Z., & Hach, A. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050442 · Cited by 206 · see citing works
Contribution of Are1p and Are2p to steryl ester synthesis in the yeast Saccharomyces cerevisiae
Zweytick, D., Leitner, E., Kohlwein, S. D., Yu, C., Rothblatt, J. A., & Daum, G. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01103.x · Cited by 180 · see citing works
Gaisne, M., Bécam, A. ‐., Verdière, J., & Herbert, C. J. (1999) · Current Genetics · doi:10.1007/s002940050490 · Cited by 147 · see citing works
Li, Y., & Prinz, W. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407600200 · Cited by 144 · see citing works
Dumitru, ., Hornby, J. M., & Nickerson, K. W. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.7.2350-2354.2004 · Cited by 143 · see citing works
Davies, B. S. J., Wang, H. S., & Rine, J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7375-7385.2005 · Cited by 138 · see citing works
Abramova, N. E., Cohen, B. D., Sertil, O., Kapoor, R., Davies, K. J. A., & Lowry, C. V. (2001) · Genetics · doi:10.1093/genetics/157.3.1169 · Cited by 128 · see citing works
A Role for Sterol Levels in Oxygen Sensing in <i>Saccharomyces cerevisiae</i>
Davies, B. S. J., & Rine, J. (2006) · Genetics · doi:10.1534/genetics.106.059964 · Cited by 123 · see citing works
Crowley, J. H., Leak, F. W., Shianna, K. V., Tove, S., & Parks, L. W. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.16.4177-4183.1998 · Cited by 123 · see citing works
Dahl, C., Biemann, H. P., & Dahl, J. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.12.4012 · Cited by 122 · see citing works
Mechanisms of sterol uptake and transport in yeast
Jacquier, N., & Schneiter, R. (2010) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2010.11.014 · Cited by 115 · see citing works
Azole Drugs Are Imported By Facilitated Diffusion in Candida albicans and Other Pathogenic Fungi
Mansfield, B. E., Oltean, H. N., Oliver, B. G., Hoot, S. J., Leyde, S. E., Hedstrom, L., & White, T. C. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001126 · Cited by 111 · see citing works
Self-citationRodriguez, R. J., & Parks, L. W. (1983) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(83)90099-1 · Cited by 111 · see citing works
Hoot, S. J., Smith, A. R., Brown, R. P., & White, T. C. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00995-10 · Cited by 107 · see citing works
Self-citationLorenz, R. T., & Parks, L. W. (1990) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.34.9.1660 · Cited by 104 · see citing works
Ueno, K., Uno, J., Nakayama, H., Sasamoto, K., Mikami, Y., & Chibana, H. (2007) · Eukaryotic Cell · doi:10.1128/ec.00414-06 · Cited by 89 · see citing works
ALIMARDANI, P., RÉGNACQ, M., MOREAU-VAUZELLE, C., FERREIRA, T., ROSSIGNOL, T., BLONDIN, B., & BERGÈS, T. (2004) · Biochemical Journal · doi:10.1042/bj20040297 · Cited by 84 · see citing works
A Genomewide Screen Reveals a Role of Mitochondria in Anaerobic Uptake of Sterols in Yeast
Reiner, S., Micolod, D., Zellnig, G., & Schneiter, R. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-06-0515 · Cited by 81 · see citing works
Pleiotropic mutations in Saccharomyces cerevisiae affecting sterol uptake and metabolism
Lewis, T. L., Keesler, G. A., Fenner, G. P., & Parks, L. W. (1988) · Yeast · doi:10.1002/yea.320040203 · Cited by 80 · see citing works
Nakayama, H., Tanabe, K., Bard, M., Hodgson, W., Wu, S., Takemori, D., Aoyama, T., Kumaraswami, N. S., Metzler, L., Takano, Y., et al. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm321 · Cited by 78 · see citing works
Nagi, M., Nakayama, H., Tanabe, K., Bard, M., Aoyama, T., Okano, M., Higashi, S., Ueno, K., Chibana, H., Niimi, M., et al. (2011) · Genes to Cells · doi:10.1111/j.1365-2443.2010.01470.x · Cited by 68 · see citing works
Involvement of heme biosynthesis in control of sterol uptake by Saccharomyces cerevisiae
Lewis, T. A., Taylor, F. R., & Parks, L. W. (1985) · Journal of Bacteriology · doi:10.1128/jb.163.1.199-207.1985 · Cited by 67 · see citing works
Shianna, K. V., Dotson, W. D., Tove, S. R., & Parks, L. W. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.3.830-834.2001 · Cited by 63 · see citing works
Characteristics of sterol uptake in Saccharomyces cerevisiae
Lorenz, R. T., Rodriguez, R. J., Lewis, T. A., & Parks, L. W. (1986) · Journal of Bacteriology · doi:10.1128/jb.167.3.981-985.1986 · Cited by 61 · see citing works
Sterol uptake in Candida glabrata: Rescue of sterol auxotrophic strains
Bard, M., Sturm, A. M., Pierson, C. A., Brown, S., Rogers, K. M., Nabinger, S., Eckstein, J., Barbuch, R., Lees, N. D., Howell, S. A., et al. (2005) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2005.03.001 · Cited by 58 · see citing works
Candida glabrata erg1 Mutant with Increased Sensitivity to Azoles and to Low Oxygen Tension
Tsai, H., Bard, M., Izumikawa, K., Krol, A. A., Sturm, A. M., Culbertson, N. T., Pierson, C. A., & Bennett, J. E. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.7.2483-2489.2004 · Cited by 56 · see citing works
Schneiter, R., & Daum, G. (2005) · Humana Press eBooks · doi:10.1385/1-59259-958-3:075 · Cited by 55 · see citing works
Depletion of the Squalene Synthase ( ERG9 ) Gene Does Not Impair Growth of Candida glabrata in Mice
Nakayama, H., Izuta, M., Nakayama, N., Arisawa, M., & Aoki, Y. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.9.2411-2418.2000 · Cited by 53 · see citing works
ValachoviÄ, M., Hronská, L., & Hapala, I. (2001) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2001.tb10580.x · Cited by 53 · see citing works
Kohút, P., Wüstner, D., Hronská, L., Kuchler, K., Hapala, I., & Valachovič, M. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.11.099 · Cited by 52 · see citing works
Isolation of Hem3 mutants from Candida albicans by sequential gene disruption
Kurtz, M. B., & Marrinan, J. A. (1989) · Molecular and General Genetics MGG · doi:10.1007/bf00330941 · Cited by 42 · see citing works
Regulation of ergosterol biosynthesis and sterol uptake in a sterol-auxotrophic yeast
Lorenz, R. T., & Parks, L. W. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.8.3707-3711.1987 · Cited by 39 · see citing works
In Vitro and In Vivo Effects of 14α-Demethylase ( ERG11 ) Depletion in Candida glabrata
Nakayama, H., Nakayama, N., Arisawa, M., & Aoki, Y. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.11.3037-3045.2001 · Cited by 39 · see citing works
Characterization of a cytochrome P450 deficient mutant of Candidaalbicans
Bard, M., Lees, N. D., Barbuch, R. J., & Sanglard, D. (1987) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(87)91000-x · Cited by 34 · see citing works
Lorenz, R. T., & Parks, L. W. (1991) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.35.8.1532 · Cited by 34 · see citing works
Influence of sterol structure on yeast plasma membrane properties
Bottema, C. D. K., Rodriguez, R. J., & Parks, L. W. (1985) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(85)90247-0 · Cited by 30 · see citing works
Intracellular sterol transport in eukaryotes, a connection to mitochondrial function?
Schneiter, R. (2006) · Biochimie · doi:10.1016/j.biochi.2006.07.022 · Cited by 25 · see citing works
Uptake and trafficking of exogenous sterols in Saccharomyces cerevisiae
Raychaudhuri, S., & Prinz, W. A. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340359 · Cited by 24 · see citing works
Disappearance of Nystatin Resistance in Candida Mediated by Ergosterol
Mas, J., & Piña, E. (1980) · Microbiology · doi:10.1099/00221287-117-1-249 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Azole Antifungal Resistance in Candida albicans and Emerging Non-albicans Candida Species
Whaley, S. G., Berkow, E. L., Rybak, J. M., Nishimoto, A. T., Barker, K. S., & Rogers, P. D. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02173 · Cited by 900 · 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
Regulation of Ergosterol Biosynthesis in Saccharomyces cerevisiae
Jordá, T., & Puig, S. (2020) · Genes · doi:10.3390/genes11070795 · Cited by 489 · see citing works
Candidiasis and Mechanisms of Antifungal Resistance
Bhattacharya, S., Sae-Tia, S., & Fries, B. C. (2020) · Antibiotics · doi:10.3390/antibiotics9060312 · Cited by 474 · see citing works
Yeast lipid metabolism at a glance
Klug, L., & Daum, G. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12141 · Cited by 349 · see citing works
Structural mechanism of ergosterol regulation by fungal sterol transcription factor Upc2
Yang, H., Tong, J., Lee, C. W., Ha, S., Eom, S. H., & Im, Y. J. (2015) · Nature Communications · doi:10.1038/ncomms7129 · Cited by 223 · see citing works
Recent Advances in Ergosterol Biosynthesis and Regulation Mechanisms in Saccharomyces cerevisiae
Hu, Z., He, B., Ma, L., Sun, Y., Niu, Y., & Zeng, B. (2017) · Indian Journal of Microbiology · doi:10.1007/s12088-017-0657-1 · Cited by 225 · see citing works
Bhattacharya, S., Esquivel, B. D., & White, T. C. (2018) · mBio · doi:10.1128/mbio.01291-18 · Cited by 210 · see citing works
Self-citationChanges in structure and function of fungal community in cow manure composting
Wang, K., Yin, X., Mao, H., Chu, C., & Tian, Y. (2018) · Bioresource Technology · doi:10.1016/j.biortech.2018.01.064 · Cited by 179 · see citing works
Fungal Lanosterol 14α-demethylase: A target for next-generation antifungal design
Monk, B. C., Sagatova, A. A., Hosseini, P., Ruma, Y. N., Wilson, R. K., & Keniya, M. V. (2019) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2019.02.008 · Cited by 136 · see citing works
Lv, Q.-Z., Yan, L., & Jiang, Y.-Y. (2016) · Virulence · doi:10.1080/21505594.2016.1188236 · Cited by 133 · see citing works
Outline of the biosynthesis and regulation of ergosterol in yeast
Liu, J., Xia, J., Nie, K., Wang, F., & Deng, L. (2019) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-019-2673-2 · Cited by 103 · see citing works
Resistance to Antifungal Drugs
Ben‐Ami, R., & Kontoyiannis, D. P. (2021) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2021.03.003 · Cited by 101 · see citing works
Azole Resistance in Candida glabrata
Whaley, S. G., & Rogers, P. D. (2016) · Current Infectious Disease Reports · doi:10.1007/s11908-016-0554-5 · Cited by 85 · see citing works
Buechel, E. R., & Pinkett, H. W. (2020) · FEBS Letters · doi:10.1002/1873-3468.13964 · Cited by 70 · see citing works
Building terpene production platforms in yeast
Zhuang, X., & Chappell, J. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25588 · Cited by 71 · see citing works
Maguire, S. L., Wang, C., Holland, L. M., Brunel, F., Neuvéglise, C., Nicaud, J.-M., Zavrel, M., White, T. C., Wolfe, K. H., & Butler, G. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004076 · Cited by 69 · see citing works
Self-citationMedically Important Fungi Respond to Azole Drugs: An Update
Zavřel, M., & White, T. C. (2015) · Future Microbiology · doi:10.2217/fmb.15.47 · Cited by 64 · see citing works
Self-citationErgosterol Biosynthesis and Regulation Impact the Antifungal Resistance and Virulence of Candida spp
Eliaš, D., Tóth Hervay, N., & Gbelská, Y. (2024) · Stresses · doi:10.3390/stresses4040041 · Cited by 63 · see citing works
Suchodolski, J., Muraszko, J., Bernat, P., & Krasowska, A. (2019) · Microorganisms · doi:10.3390/microorganisms7100378 · Cited by 63 · see citing works
Protein‐facilitated transport of hydrophobic molecules across the yeast plasma membrane
Claus, S., Jezierska, S., & Bogaert, I. V. (2019) · FEBS Letters · doi:10.1002/1873-3468.13469 · Cited by 58 · see citing works
Khunweeraphong, N., & Kuchler, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094806 · Cited by 54 · see citing works
Pinheiro, T., Lip, K. Y. F., García‐Ríos, E., Querol, A., Teixeira, J. A., van Gulik, W. M., Guillamón, J. M., & Domingues, L. (2020) · Scientific Reports · doi:10.1038/s41598-020-77846-w · Cited by 50 · see citing works
Ergosterol Turnover in Yeast: An Interplay between Biosynthesis and Transport
Соколов, С. С., Trushina, N. I., Severin, F. F., & Кнорре, Д. А. (2019) · Biochemistry (Moscow) · doi:10.1134/s0006297919040023 · Cited by 47 · see citing works
Sun, Z., Lian, J., Zhu, L., Jiang, Y., Li, G., Xue, H., Wu, M., Yang, L.-R., & Lin, J. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.681666 · Cited by 43 · 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
O’Meara, T. R., Veri, A. O., Polvi, E. J., Li, X., Valaei, S. F., Diezmann, S., & Cowen, L. E. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006142 · Cited by 41 · see citing works
Joshua, I., & Höfken, T. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040772 · Cited by 40 · see citing works
Robbins, N., Spitzer, M., Wang, W., Waglechner, N., Patel, D. J., O’Brien, J. S., Ejim, L., Ejim, O., Tyers, M., & Wright, G. D. (2016) · Cell Chemical Biology · doi:10.1016/j.chembiol.2016.08.015 · Cited by 41 · see citing works
Engineering the thermotolerant industrial yeast Kluyveromyces marxianus for anaerobic growth
Dekker, W. J. C., Ortiz‐Merino, R. A., Kaljouw, A., Battjes, J., Wiering, F. W., Mooiman, C., Cortés, P. D. L. T., & Pronk, J. T. (2021) · Metabolic Engineering · doi:10.1016/j.ymben.2021.07.006 · Cited by 41 · see citing works
Piva, G. G., Casalta, E., Legras, J., Tesnière, C., Sablayrolles, J.-M., Ferreira, D., Ortiz-Julien, A., Galéote, V., & Mouret, J. (2022) · Fermentation · doi:10.3390/fermentation8020090 · Cited by 42 · see citing works
Duan, H., Ji, M., Xie, Y., Shi, J., Liu, L., Zhang, B., & Sun, J. (2021) · Sustainability · doi:10.3390/su132313035 · Cited by 39 · see citing works
Innate Immune and Fungal Model of Alzheimer’s Disease
Parady, B. (2018) · Journal of Alzheimer s Disease Reports · doi:10.3233/adr-180073 · Cited by 39 · see citing works
Li, Q., Tsai, H., Mandal, A., Walker, B., Noble, J., Fukuda, Y., & Bennett, J. E. (2018) · Molecular Medicine Reports · doi:10.3892/mmr.2018.8716 · Cited by 33 · see citing works
Role of lipid transporters in fungal physiology and pathogenicity
Rizzo, J., Stanchev, L. D., Silva, V. K. A., Nimrichter, L., Pomorski, T. G., & Rodrigues, M. L. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.09.001 · Cited by 36 · see citing works
Serratore, N. D., Baker, K. M., Macadlo, L. A., Gress, A. R., Powers, B. L., Atallah, N., Westerhouse, K. M., Hall, M. C., Weake, V. M., & Briggs, S. D. (2018) · Genetics · doi:10.1534/genetics.117.300554 · Cited by 33 · see citing works
Baker, K. M., Hoda, S., Saha, D., Gregor, J. B., Georgescu, L., Serratore, N. D., Zhang, Y., Cheng, L., Lanman, N. A., & Briggs, S. D. (2022) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02250-21 · Cited by 30 · see citing works
Nagy, G., Kiss, S. A., Varghese, R., Bauer, K., Szebenyi, C., Kocsubé́, S., Homa, M., Bodai, L., Zsindely, N., Nagy, G., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.660347 · Cited by 27 · see citing works
Sunyer-Figueres, M., Vázquez, J., Mas, A., Torija, M.-J., & Beltran, G. (2020) · Antioxidants · doi:10.3390/antiox9100947 · Cited by 24 · see citing works
Recent developments and emerging trends in dietary vitamin D sources and biological conversion
Wei, X., Pandohee, J., & Xu, B. (2023) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2023.2220793 · Cited by 24 · see citing works
Xu, Y., Quan, H., Wang, Y., Zhong, H., Sun, J., Xu, J., Jia, N., & Jiang, Y. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00491 · Cited by 23 · see citing works
Çakır, T. (2015) · Scientific Reports · doi:10.1038/srep14563 · Cited by 22 · see citing works
Dietary restriction and lifespan: adaptive reallocation or somatic sacrifice?
Piper, M. D. W., Zanco, B., Sgrò, C. M., Adler, M. I., Mirth, C. K., & Russell Bonduriansky, A. (2022) · FEBS Journal · doi:10.1111/febs.16463 · Cited by 21 · see citing works
den Ridder, M., van den Brandeler, W., Altiner, M., Daran-Lapujade, P. A. S., & Pabst, M. (2023) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2023.100552 · Cited by 20 · see citing works
The Ins and Outs of Azole Antifungal Drug Resistance: Molecular Mechanisms of Transport
Zavřel, M., Esquivel, B. D., & White, T. C. (2017) · Springer eBooks · doi:10.1007/978-1-4939-0694-9_29 · Cited by 20 · see citing works
Self-citationAhumada-Rudolph, R., Cajas-Madriaga, D., Rudolph, A. J., Reinoso, R., Torres, C., Silva, M., & Becerra, J. (2014) · Revista de biología marina y oceanografía · doi:10.4067/s0718-19572014000200009 · Cited by 20 · see citing works
Design strategies of oxidosqualene cyclase inhibitors: Targeting the sterol biosynthetic pathway
Rabelo, V. W., Romeiro, N. C., & Abreu, P. A. (2017) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2017.05.002 · Cited by 19 · see citing works
Serum albumin promotes ATP-binding cassette transporter-dependent sterol uptake in yeast
Marek, M., Silvestro, D., Fredslund, M. D., Andersen, T. G., & Pomorski, T. G. (2014) · FEMS Yeast Research · doi:10.1111/1567-1364.12219 · Cited by 18 · see citing works
Deng, L., Zou, L., Wu, J., Liu, H., Luo, T., Zhou, X., Li, W., & Ren, B. (2019) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2019.02.010 · Cited by 15 · see citing works
Yau, K. P. S., Weerasinghe, H., Olivier, F. A. B., Lo, T. L., Powell, D., Koch, B., Beilharz, T. H., & Traven, A. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011338 · Cited by 15 · see citing works
Bhattacharya, S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819990-9.00070-6 · Cited by 16 · see citing works
Chemical genomic guided engineering of gamma-valerolactone tolerant yeast
Bottoms, S., Dickinson, Q., McGee, M. A., Hinchman, L., Higbee, A. J., Hebert, A. S., Serate, J., Xie, D., Zhang, Y., Coon, J. J., et al. (2018) · Microbial Cell Factories · doi:10.1186/s12934-017-0848-9 · Cited by 14 · see citing works
Sterol uptake analysis in Saccharomyces and non-Saccharomyces wine yeast species
Tesnière, C., Pradal, M., & Legras, J. (2021) · FEMS Yeast Research · doi:10.1093/femsyr/foab020 · Cited by 14 · see citing works
Antifungal resistance and clinical significance in small animals
Kaya, Y., Dokuzeylül, B., Bakırel, U., & Or, M. E. (2022) · German Journal of Veterinary Research · doi:10.51585/gjvr.2022.2.0034 · Cited by 13 · see citing works
Ruan, R., Chen, Y., Li, H., & Wang, M. (2019) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2019.103239 · Cited by 13 · see citing works
Bautista-Crescencio, C., Casimiro-Ramos, A., Fragoso-Vázquez, M. J., Correa‐Basurto, J., Olano, C., Hernández, G., & Villa‐Tanaca, L. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.01271-23 · Cited by 26 · see citing works
Limosilactobacillus fermentum Limits Candida glabrata Growth by Ergosterol Depletion
Zangl, I., Beyer, R., Gattesco, A., Labuda, R., Pap, I.-J., Strauss, J., & Schüller, C. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.03326-22 · Cited by 10 · see citing works
Xi, Y., Zhang, J., Fan, B., Sun, M., Cao, W., Liu, X., Gai, Y., Shen, C., Wang, H., & Wang, M. (2024) · Journal of Fungi · doi:10.3390/jof10050360 · Cited by 10 · see citing works
Jaiswal, N., & Kumar, A. (2024) · Molecular Biotechnology · doi:10.1007/s12033-023-01017-1 · Cited by 9 · see citing works
The mannoprotein TIR3 (CAGL0C03872g) is required for sterol uptake in Candida glabrata
Inukai, T., Nagi, M., Morita, A., Tanabe, K., Aoyama, T., Miyazaki, Y., Bard, M., & Nakayama, H. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2014.11.002 · Cited by 8 · see citing works
Chattopadhyay, A., Singh, R., Mitra, M., Das, A. K., & Maiti, M. K. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2020.158725 · Cited by 9 · see citing works
Li, X., Li, M., Liu, X., Jiang, Y., Zhao, D., Gao, J., Wang, Z., Jiang, Y., & Chen, C. (2022) · Journal of Fungi · doi:10.3390/jof8080779 · Cited by 8 · see citing works
Kodedová, M., Valachovič, M., & Sychrová, H. (2024) · Microbes and Infection · doi:10.1016/j.micinf.2024.105409 · Cited by 7 · see citing works
Farfour, É., Brun, C. L., Mizrahi, A., Bargain, P., Durieux, M.-F., Boquel, F., Corvec, S., Jeddi, F., Muggeo, A., Huguenin, A., et al. (2022) · Medical Mycology · doi:10.1093/mmy/myac021 · Cited by 7 · see citing works
Merdan, O., Şişman, A. S., Aksoy, S. A., Kızıl, S., Tüzemen, N. Ü., Yılmaz, E., & Ener, B. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00776-22 · Cited by 6 · see citing works
Evolution of regulatory networks inCandida glabrata: learning to live with the human host
Roy, S., & Thompson, D. A. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov087 · Cited by 7 · see citing works
The Ins and Outs of Azole Antifungal Drug Resistance: Molecular Mechanisms of Transport
Zavřel, M., Esquivel, B. D., & White, T. C. (2014) · Springer eBooks · doi:10.1007/978-1-4939-0667-3_29-1 · Cited by 5 · see citing works
Self-citationWang, Y., Zhang, R., Yao, M., Xiao, W., Wang, Y., & Yuan, Y. (2025) · Synthetic and Systems Biotechnology · doi:10.1016/j.synbio.2025.04.008 · Cited by 4 · see citing works
Saha, D., Gregor, J. B., Hoda, S., Eastman, K. E., Gutierrez-Schultz, V. A., Navarrete, M., Wisecaver, J. H., & Briggs, S. D. (2024) · mSphere · doi:10.1128/msphere.00524-24 · Cited by 4 · see citing works
Mechanism and Engineering Strategies of Sterol Homeostasis in Yeast
Li, M., Yu, H., & Ye, L. (2025) · ACS Synthetic Biology · doi:10.1021/acssynbio.5c00508 · Cited by 4 · see citing works
Singh, G. (2022) · Current Drug Discovery Technologies · doi:10.2174/1570163819666220615142933 · Cited by 4 · see citing works
Petrisková, L., Kodedová, M., Balážová, M., Sychrová, H., & Valachovič, M. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2024.159523 · Cited by 3 · see citing works
Hirai, K., Inukai, T., & Nakayama, H. (2016) · Medical Mycology Journal · doi:10.3314/mmj.16.007 · Cited by 2 · see citing works
Indrastiti, R. K., Rahmayanti, F., & Kurnia, D. (2025) · AIP conference proceedings · doi:10.1063/5.0273164 · Cited by 1 · see citing works
Cytrynbaum, E. G., & McClean, M. N. (2025) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2025.115740 · Cited by 1 · see citing works
Ahmed, N., & Chen, Z. (2026) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2026.107237 · Cited by 1 · see citing works
Host-Induced Stress Response in Human Pathogenic Fungi
Viana, R., Pais, P., Cavalheiro, M., Galocha, M., & Teixeira, M. C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819990-9.00035-4 · Cited by 1 · see citing works
Hirai, K., Inukai, T., & Nakayama, H. (2017) · Medical Mycology Journal · doi:10.3314/mmj.17.007
Quon, E. (2018) · Summit (Simon Fraser University)
Duan, H., Ji, M., Ai, C., Xie, S., Sun, J., Shi, J., Li, X., & Zhang, B. (2021) · Research Square · doi:10.21203/rs.3.rs-234233/v1
Combinatorial approach to combat drug resistance in human pathogenic fungi
Mir, M. A., Qadri, H., Aisha, S., & Shah, A. H. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-96127-1.00011-5
Saha, D., Gregor, J. B., Hoda, S., Eastman, K. E., Navarrete, M., Wisecaver, J. H., & Briggs, S. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.06.20.599910
Bioactive Drugs from Mushrooms and Fungi
Swaroop, A. (2025) · Royal Society of Chemistry eBooks · doi:10.1039/9781837676989-00101
Etude des besoins en stérols des souches de levures œnologiques (Saccharomyces Cerevisiae)
Piva, G. G. (2022) · theses.fr (ABES) · doi:10.70675/8a3d39d9z1c93z47b6z900fz2213d379468e
- Authors
- Zavrel, M., Hoot, S. J., & White, T. C.
- Affiliations
- University of Missouri-Kansas City, School of Biological Sciences, Cell Biology and Biophysics, Kansas City, Missouri, USA
- Center for Infectious Disease Research (US)
- University of Missouri–Kansas City (US)
- ORCID
- White, Theodore C.
- Venue
- Eukaryotic Cell
- Publisher
- American Society for Microbiology
- Published
- 2013-05
- Volume
- 12
- Issue
- 5
- Pages
- 725-738
- ISSN
- 1535-9778 (ISSN-L)
- 1535-9786
- PMC
- PMC3647772
- OpenAlex
- W2110966198
- Cited by
- 86
- References
- 55
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 8 · 2023: 5 · 2022: 10 · 2021: 10 · 2020: 8 · 2019: 8 · 2018: 6 · 2017: 8 · 2016: 5 · 2015: 5 · 2014: 7
- FWCI
- 2.54
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Locations
- Eukaryotic Cell (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Missouri-Kansas City
- National Institutes of Health
- National Institute of Dental and Craniofacial Research (R01DE011367, R01DE017078, R01 DE-11367, R01 DE 14161, R01DE014161)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- cholesterol absorption, ergosterol, Candida albicans, Candida glabrata, Saccharomyces cerevisiae, fluconazole, fetal bovine serum, esterified cholesterol
- MeSH terms
- Aerobiosis, Anaerobiosis, Antifungal Agents, Candida albicans, Cholesterol, Culture Media, Ergosterol, Esterification, Microbial Sensitivity Tests, Saccharomyces cerevisiae, Fluconazole, Candida glabrata, Gene Knockout Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review