306
Views
3
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

A New Variant of Mutational and Polymorphic Signatures in the ERG11 Gene of Fluconazole-Resistant Candida albicans

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 3111-3133 | Published online: 17 Jun 2022

References

  • Jerez Puebla LE. Fungal infections in immunosuppressed patients. Immunodeficiency. 2012. doi:10.5772/51512
  • Rodrigues ML, Nosanchuk JD, Reynolds TB. Fungal diseases as neglected pathogens: a wake-up call to public health officials. PLoS Negl Trop Dis. 2020;14(2):1–9. doi:10.1371/journal.pntd.0007964
  • Low CY, Rotstein C. Emerging fungal infections in immunocompromised patients. F1000 Med Rep. 2011;3(1):1–8. doi:10.3410/M3-14
  • Bongomin F, Gago S, Oladele RO, Denning DW. Global and multi-national prevalence of fungal diseases—estimate precision. J Fungi. 2017;3(4):57. doi:10.3390/jof3040057
  • Hurley R, De Louvois J. Candida vaginitis. Postgrad Med J. 1979;55:645–647. doi:10.1136/pgmj.55.647.645
  • Nyirjesy P. Chronic vulvovaginal candidiasis. Am Fam Physician. 2001;63(4):697–702. doi:10.1056/nejmp048152
  • Paladine HL, Desai UA. Vaginitis: diagnosis and treatment. Am Acad Fam Physicians. 2018;97(5):321–329.
  • Sobel JD. Vulvovaginal candidiasis. Lancet. 2007;369(9577):1961–1971. doi:10.1016/S0140-6736(07)60917-9
  • Musa K, Ahmed M, Shahpudin S, et al. Resistance of Candida glabrata to drugs and the host immune system. Clin Microbiol Infect Dis. 2018;3(3):1–4. doi:10.15761/cmid.1000145
  • Bhattacharjee P. Epidemiology and antifungal susceptibility of Candida species in a tertiary care hospital, Kolkata, India. Curr Med Mycol. 2016;2(2):20–27. doi:10.18869/acadpub.cmm.2.2.5
  • Gullo A. Invasive fungal infections. The challenge continues. Drugs. 2009;69(1):65–73. doi:10.2165/11315530-000000000-00000
  • Lockhart SR, Etienne KA, Vallabhaneni S, et al. Simultaneous emergence of multidrug-resistant Candida auris on 3 continents confirmed by whole-genome sequencing and epidemiological analyses. Clin Infect Dis. 2017;64(2):134–140. doi:10.1093/cid/ciw691
  • Alexander BD, Johnson MD, Pfeiffer CD, et al. Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin Infect Dis. 2013;56(12):1724–1732. doi:10.1093/cid/cit136
  • Rodriguez L, Bustamante B, Huaroto L, et al. A multi-centric study of Candida bloodstream infection in Lima-Callao, Peru: species distribution, antifungal resistance and clinical outcomes. PLoS One. 2017;12(4):1–12. doi:10.1371/journal.pone.0175172
  • Maheronnaghsh M, Fatahinia M, Dehghan P, Teimoori A. Identification of Candida species and antifungal susceptibility in cancer patients with oral lesions in Ahvaz, Southern West of Iran. Adv Biomed Res. 2020;9(1):50. doi:10.4103/abr.abr_214_19
  • Perfect JR. Is there an emerging need for new antifungals? Expert Opin Emerg Drugs. 2016;21(2):129–131. doi:10.1517/14728214.2016.1155554
  • Sheehan DJ, Hitchcock CA, Sibley CM. Current and emerging azole antifungal agents. Clin Microbiol Rev. 1999;12(1):40–79. doi:10.1128/cmr.12.1.40
  • The fungus among us: an antifungal review. https://uspharmacist.com/article/the-fungus-among-us-an-antifungal-review. Accessed October 16, 2021.
  • Scheinfeld N. Ketoconazole: a review of a workhorse antifungal molecule with a focus on new foam and gel formulations. Drugs Today. 2008;44(5):369–380. doi:10.1358/DOT.2008.44.5.1216598
  • McKeny PT, Nessel TA, Zito PM. Antifungal Antibiotics. StatPearls; 2021.
  • Ahmad A, Khan A, Manzoor N, Khan LA. Evolution of ergosterol biosynthesis inhibitors as fungicidal against Candida. Microb Pathog. 2010;48(1):35–41. doi:10.1016/j.micpath.2009.10.001
  • Autmizguine J, Smith PB, Prather K, et al. Effect of fluconazole prophylaxis on Candida fluconazole susceptibility in premature infants. J Antimicrob Chemother. 2018;73(12):3482–3487. doi:10.1093/jac/dky353
  • Gong Y, Liu W, Huang X, Hao L, Li Y, Sun S. Antifungal activity and potential mechanism of n-butylphthalide alone and in combination with fluconazole against Candida albicans. Front Microbiol. 2019;10. doi:10.3389/fmicb.2019.01461
  • Rybak JM, Muñoz JF, Barker KS, et al. Mutations in TAC1B: a novel genetic determinant of clinical fluconazole resistance in Candida auris. mBio. 2020;11(3):1–16. doi:10.1128/mBio.00365-20
  • Warrilow AGS, Melo N, Martel CM, et al. Expression, purification, and characterization of Aspergillus fumigatus sterol 14-α demethylase (CYP51) isoenzymes A and B. Antimicrob Agents Chemother. 2010;54(10):4225–4234. doi:10.1128/AAC.00316-10
  • Warrilow AGS, Mullins JGL, Hull CM, et al. S279 point mutations in Candida albicans sterol 14-α demethylase (CYP51) reduce in vitro inhibition by fluconazole. Antimicrob Agents Chemother. 2012;56(4):2099–2107. doi:10.1128/AAC.05389-11
  • Flowers SA, Colón B, Whaley SG, Schuler MA, David Rogers P. Contribution of clinically derived mutations in ERG11 to azole resistance in Candida albicans. Antimicrob Agents Chemother. 2015;59(1):450–460. doi:10.1128/AAC.03470-14
  • De Petris A, Crestoni ME, Pirolli A, et al. Binding of azole drugs to heme: a combined MS/MS and computational approach. Polyhedron. 2015;90:245–251. doi:10.1016/j.poly.2015.02.011
  • Balding PR, Porro CS, McLean KJ, et al. How do azoles inhibit cytochrome P450 enzymes? A density functional study. J Phys Chem A. 2008;112(50):12911–12918. doi:10.1021/jp802087w
  • Warrilow AG, Parker JE, Kelly DE, Kelly SL. Azole affinity of sterol 14-demethylase (CYP51) enzymes from Candida albicans and homo sapiens. Antimicrob Agents Chemother. 2013;57(3):1352–1360. doi:10.1128/AAC.02067-12
  • Xiang MJ, Liu JY, Ni PH, et al. Erg11 mutations associated with azole resistance in clinical isolates of Candida albicans. FEMS Yeast Res. 2013;13(4):386–393. doi:10.1111/1567-1364.12042
  • Marichal P, Vanden Bossche H, Odds FC, et al. Molecular biological characterization of an azole-resistant Candida glabrata isolate. Antimicrob Agents Chemother. 1997;41(10):2229–2237. doi:10.1128/aac.41.10.2229
  • Marichal P, Koymans L, Willemsens S, et al. Contribution of mutations in the cytochrome P450 14α-demethylase (Erg11p, Cyp51p) to azole resistance in Candida albicans. Microbiology. 1999;145(10):2701–2713. doi:10.1099/00221287-145-10-2701
  • Kumar A, Nair R, Kumar M, et al. Assessment of antifungal resistance and associated molecular mechanism in Candida albicans isolates from different cohorts of patients in North Indian state of Haryana. Folia Microbiol (Praha). 2020;65(4):747–754. doi:10.1007/s12223-020-00785-6
  • Njunda AL, Nsagha DS, Assob JCN, Kamga HL, Teyim P. In vitro antifungal susceptibility patterns of Candida albicans from HIV and aids patients attending the Nylon Health District hospital in Douala, Cameroon. J Public Health Africa. 2012;3(1):4–7. doi:10.4081/jphia.2012.e2
  • Bhargava A, Dakwala F, Saigal S, Mehra S. Identification of Candida albicans by using different culture medias and its association in potentially malignant and malignant lesions. Contemp Clin Dent. 2011;2(3):188. doi:10.4103/0976-237x.86454
  • Matare T, Nziramasanga P, Gwanzura L, Robertson V. Experimental germ tube induction in Candida albicans: an evaluation of the effect of sodium bicarbonate on morphogenesis and comparison with pooled human serum. Biomed Res Int. 2017;2017:8–13. doi:10.1155/2017/1976273
  • Munin E, Giroldo LM, Alves LP, Costa MS. Study of germ tube formation by Candida albicans after photodynamic antimicrobial chemotherapy (PACT). J Photochem Photobiol B. 2007;88(1):16–20. doi:10.1016/j.jphotobiol.2007.04.011
  • Torosantucci A, Romagnoli G, Chiani P, et al. Candida albicans yeast and germ tube forms interfere differently with human monocyte differentiation into dendritic cells: a novel dimorphism-dependent mechanism to escape the host’s immune response. Infect Immun. 2004;72(2):833–843. doi:10.1128/IAI.72.2.833-843.2004
  • Houang ETS, Chu KC, Koehler AP, Cheng AFB. Use of CHROMagar Candida for genital specimens in the diagnostic laboratory. J Clin Pathol. 1997;50(7):563–565. doi:10.1136/jcp.50.7.563
  • Willinger B, Hillowoth C, Selitsch B, Manafi M. Performance of Candida ID, a new chromogenic medium for presumptive identification of Candida species, in comparison to CHROMagar Candida. J Clin Microbiol. 2001;39(10):3793–3795. doi:10.1128/JCM.39.10.3793-3795.2001
  • Merlino J, Tambosis E, Veal D. Chromogenic tube test for presumptive identification or confirmation of isolates as Candida albicans. J Clin Microbiol. 1998;36(4):1157–1159. doi:10.1128/jcm.36.4.1157-1159.1998
  • Odds FC, Bernaerts R. CHROMagar Candida, a new differential isolation medium for presumptive identification of clinically important Candida species. J Clin Microbiol. 1994;32(8):1923–1929. doi:10.1128/jcm.32.8.1923-1929.1994
  • Lahoylahoy LD, Mendoza BC. Evaluation of CHROMagar Candida in the rapid identification of medically important species of Candida. Int J Biosci. 2017;11(1):380–385. doi:10.12692/ijb/11.1.380-385
  • Sharma P, Sambyal S, Shrivastava D. Evaluation of Candida species from clinical specimens by using chromagar. Int J Adv Res. 2017;5(2):1750–1755. doi:10.21474/ijar01/3337
  • Mathavi S, Sasikala G, Kavitha A, Priyadarsini RI. CHROMagar as a primary isolation medium for rapid identification of Candida and its role in mixed Candida infection in sputum samples. Indian J Microbiol Res. 2016;3(2):141. doi:10.5958/2394-5478.2016.00033.9
  • Faraz A, Ghaffar UB, Tahir Ansari WS. Evaluation of diagnostic efficacy of chromagar Candida for differentiation: Taylor’s libraries. ISRA Med J. 2016;8(4):5.
  • Barry AL, Brown SD. Fluconazole disk diffusion procedure for determining susceptibility of Candida species. J Clin Microbiol. 1996;34(9):2154–2157. doi:10.1128/jcm.34.9.2154-2157.1996
  • Yücesoy M, Şentürker Güldaş N, Yuluǧ N. Disk diffusion method for fluconazole susceptibility testing of Candida albicans strains. J Chemother. 2001;13(2):161–166. doi:10.1179/joc.2001.13.2.161
  • Kiraz N, Dag I, Oz Y, Yamac M, Kiremitci A, Kasifoglu N. Correlation between broth microdilution and disk diffusion methods for antifungal susceptibility testing of caspofungin, voriconazole, amphotericin B, itraconazole and fluconazole against Candida glabrata. J Microbiol Methods. 2010;82(2):136–140. doi:10.1016/j.mimet.2010.05.002
  • Clinical and Laboratory Standards Institute Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. Vol. 28. 3rd. Wayne P, ed. Clinical and Laboratory Standards Institute; CLSI Document M27-A3. 2008.
  • Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts. 4th. Wayne P, ed. Clinical and Laboratory Standards Institute; 2017.
  • Alyousef AA. Antifungal activity and mechanism of action of different parts of Myrtus communis growing in Saudi Arabia against. J Nanomater. 2021;2021. doi:10.1155/2021/3484125
  • Pam VK, Akpan JU, Oduyebo OO, et al. Fluconazole susceptibility and ERG11 gene expression in vaginal Candida species isolated from Lagos Nigeria. Int J Mol Epidemiol Genet. 2012;3(1):84–90.
  • Alastruey-Izquierdo A, Cuenca-Estrella M. EUCAST and CLSI: how to assess in vitro susceptibility and clinical resistance. Curr Fungal Infect Rep. 2012;6(3):229–234. doi:10.1007/s12281-012-0100-3
  • Cuesta I, Bielza C, Cuenca-Estrella M, Larrañaga P, Rodríguez-Tudela JL. Evaluation by data mining techniques of fluconazole breakpoints established by the Clinical and Laboratory Standards Institute (CLSI) and comparison with those of the European Committee on Antimicrobial Susceptibility Testing (EUCAST). Antimicrob Agents Chemother. 2010;54(4):1541–1546. doi:10.1128/AAC.01688-09
  • Pfaller MA, Diekema DJ, Sheehan DJ. Interpretive breakpoints for fluconazole and Candida revisited: a blueprint for the future of antifungal susceptibility testing. Clin Microbiol Rev. 2006;19(2):435–447. doi:10.1128/CMR.19.2.435-447.2006
  • Rex JH, Pfaller MA, Galgiani JN, et al. Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and Candida infections. Clin Infect Dis. 1997;24(2):235–249. doi:10.1093/clinids/24.2.235
  • Ortiz B, Pérez-Alemán E, Galo C, Fontecha G. Molecular identification of Candida species from urinary infections in Honduras. Rev Iberoam Micol. 2018;35(2):73–77. doi:10.1016/j.riam.2017.07.003
  • Erazo BM, Ramírez GA, Cerrato LE, et al. Prevalence of Hb S (HHB: c.20A>T) in a Honduran population of African descent. Hemoglobin. 2015;39(2):134–137. doi:10.3109/03630269.2015.1012294
  • Sayers EW, Beck J, Brister JR, et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2020;48(D1):D9–D16. doi:10.1093/nar/gkz899
  • Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res. 2000;28(1):235–242. doi:10.1093/nar/28.1.235
  • Hargrove TY, Friggeri L, Wawrzak Z, et al. Structural analyses of Candida albicans sterol 14α-demethylase complexed with azole drugs address the molecular basis of azole-mediated inhibition of fungal sterol biosynthesis. J Biol Chem. 2017;292(16):6728–6743. doi:10.1074/jbc.M117.778308
  • Sagatova AA, Keniya MV, Wilson RK, Monk BC, Tyndall JDA. Structural insights into binding of the antifungal drug fluconazole to Saccharomyces cerevisiae lanosterol 14α-demethylase. Antimicrob Agents Chemother. 2015;59(8):4982–4989. doi:10.1128/AAC.00925-15
  • Sievers F, Higgins DG. Clustal Omega for making accurate alignments of many protein sequences. Protein Sci. 2018;27(1):135–145. doi:10.1002/pro.3290
  • Faure G, Joseph AP, Craveur P, et al. IPBAvizu: a PyMOL plugin for an efficient 3D protein structure superimposition approach. Source Code Biol Med. 2019;14(1):1–5. doi:10.1186/s13029-019-0075-3
  • Adasme MF, Linnemann KL, Bolz SN, et al. PLIP 2021: expanding the scope of the protein-ligand interaction profiler to DNA and RNA. Nucleic Acids Res. 2021;49(W1):W530–W534. doi:10.1093/nar/gkab294
  • Berendsen HJC, van der Spoel D, van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comput Phys Commun. 1995;91(1–3):43–56. doi:10.1016/0010-4655(95)00042-E
  • Abraham MJ, Murtola T, Schulz R, et al. Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX. 2015;1–2:19–25. doi:10.1016/j.softx.2015.06.001
  • Geneious Prime. Geneious all rights reserved. molecular biology and sequence analysis software. Available from: https://www.geneious.com/prime/. Accessed November 22, 2021.
  • Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870–1874. doi:10.1093/molbev/msw054
  • Zhang J, Li L, Lv Q, Yan L, Wang Y, Jiang Y. The fungal CYP51s: their functions, structures, related drug resistance, and inhibitors. Front Microbiol. 2019;10. doi:10.3389/fmicb.2019.00691
  • Liu M, Zheng N, Li D, et al. Cyp51A-based mechanism of azole resistance in Aspergillus fumigatus: illustration by a new 3D Structural Model of Aspergillus fumigatus CYP51A protein. Med Mycol. 2016;54(4):400–408. doi:10.1093/mmy/myv102
  • Sagatova AA, Keniya MV, Wilson RK, Sabherwal M, Tyndall JDA, Monk BC. Triazole resistance mediated by mutations of a conserved active site tyrosine in fungal lanosterol 14α-demethylase. Sci Rep. 2016;6:1–11. doi:10.1038/srep26213
  • Parker JE, Warrilow AGS, Price CL, Mullins JGL, Kelly DE, Kelly SL. Resistance to antifungals that target CYP51. J Chem Biol. 2014;7(4):143–161. doi:10.1007/s12154-014-0121-1
  • Becher R, Wirsel SGR. Fungal cytochrome P450 sterol 14α-demethylase (CYP51) and azole resistance in plant and human pathogens. Appl Microbiol Biotechnol. 2012;95(4):825–840. doi:10.1007/s00253-012-4195-9
  • Lamb DC, Kelly DE, Schunck WH, et al. The mutation T315A in Candida albicans sterol 14α-demethylase causes reduced enzyme activity and fluconazole resistance through reduced affinity. J Biol Chem. 1997;272(9):5682–5688. doi:10.1074/jbc.272.9.5682
  • Sun B, Huang W, Liu M. Evaluation of the combination mode of azoles antifungal inhibitors with CACYP51 and the influence of Site-directed mutation. J Mol Graph Model. 2017;73:157–165. doi:10.1016/j.jmgm.2017.02.009
  • Rosam K, Monk BC, Lackner M. Sterol 14α-demethylase ligand-binding pocket-mediated acquired and intrinsic azole resistance in fungal pathogens. J Fungi. 2021;7(1):1–22. doi:10.3390/jof7010001
  • Scouras AD, Daggett V. The dynameomics rotamer library: amino acid side chain conformations and dynamics from comprehensive molecular dynamics simulations in water. Protein Sci. 2011;20(2):341–352. doi:10.1002/pro.565
  • Kufareva I, Abagyan R. Methods of protein structure comparison in homology modeling: methods and protocols. In: Methods of Protein Structure Comparison in Homology Modeling: Methods and Protocols, Methods in Molecular Biology. Vol. 857. Humana Press; 2012:231–257. doi:10.1007/978-1-61779-588-6
  • Aier I, Varadwaj PK, Raj U. Structural insights into conformational stability of both wild-type and mutant EZH2 receptor. Sci Rep. 2016;6:1–10. doi:10.1038/srep34984
  • Lobanov MI, Bogatyreva NS, Galzitskaia OV. Radius of gyration is indicator of compactness of protein structure. Mol Biol (Mosk). 2008;42(4):701–706.
  • Lobanov MY, Bogatyreva NS, Galzitskaya OV. Radius of gyration as an indicator of protein structure compactness. Mol Biol. 2008;42(4):623–628. doi:10.1134/S0026893308040195
  • Tsai CJ, Nussinov R. Hydrophobic folding units at protein-protein interfaces: implications to protein folding and to protein-protein association. Protein Sci. 1997;6(7):1426–1437. doi:10.1002/pro.5560060707
  • Gromiha MM. Protein structure prediction. Protein Bioinform. 2010;1986:143–207. doi:10.1016/b978-8-1312-2297-3.50005-9
  • Fullerton GD, Cameron IL. Water compartments in cells. Methods Enzymol. 2007;428:1–28. doi:10.1016/S0076-6879(07)28001-2
  • Hubbard RE, Kamran Haider M. Hydrogen bonds in proteins: role and strength. Encycloped Life Sci. 2010. doi:10.1002/9780470015902.a0003011.pub2
  • Montes K, Ortiz B, Galindo C, Figueroa I, Braham S, Fontecha G. Identification of Candida species from clinical samples in a Honduran tertiary hospital. Pathogens. 2019;8(4):1–11. doi:10.3390/pathogens8040237
  • Khadka S, Sherchand JB, Pokhrel BM, et al. Isolation, speciation and antifungal susceptibility testing of Candida isolates from various clinical specimens at a tertiary care hospital, Nepal. BMC Res Notes. 2017;10(1):1–5. doi:10.1186/s13104-017-2547-3
  • Manikandan C, Amsath A. Characterization and susceptibility pattern of Candida species isolated from urine samples in Pattukkottai, Tamilnadu, India. Int J Pure Appl Zool. 2015;3(1):17–23.
  • Reddy Edula A. Antifungal susceptibility of clinically significant Candida species by disk diffusion method. IP Int J Med Microbiol Trop Dis. 2021;7(2):77–80. doi:10.18231/j.ijmmtd.2021.017
  • Swoboda-Kopec E, Kawecki D, Wroblewska M, Krawczyk M, Luczak M. Epidemiology and susceptibility to antifungal agents of fungi isolated from clinical specimens from patients hospitalized in the Department of General and Liver Surgery of the Medical University of Warsaw. Transplant Proc. 2003;35(6):2298–2303. doi:10.1016/S0041-1345(03)00757-7
  • Mokaddas EM, Al-Sweih NA, Khan ZU. Species distribution and antifungal susceptibility of Candida bloodstream isolates in Kuwait: a 10-year study. J Med Microbiol. 2007;56(PART2):255–259. doi:10.1099/jmm.0.46817-0
  • Pfaller MA, Andes DR, Diekema DJ, et al. Epidemiology and outcomes of invasive candidiasis due to non-albicans species of Candida in 2496 patients: data from the Prospective Antifungal Therapy (PATH) registry 2004–2008. PLoS One. 2014;9(7). doi:10.1371/journal.pone.0101510
  • Gutiérrez J, Morales P, González MA, Quindós G. Candida dubliniensis, a new fungal pathogen. J Basic Microbiol. 2002;42(3):207–227. doi:10.32388/ef9mql
  • Khan Z, Ahmad S, Joseph L, Chandy R. Candida dubliniensis: an appraisal of its clinical significance as a bloodstream pathogen. PLoS One. 2012;7(3):e32952. doi:10.1371/journal.pone.0032952
  • Pfaller MA, Messer SA, Gee S, et al. In vitro susceptibilities of Candida dubliniensis isolates tested against the new triazole and echinocandin antifungal agents. J Clin Microbiol. 1999;37(3):870–872. doi:10.1128/jcm.37.3.870-872.1999
  • Whaley SG, Berkow EL, Rybak JM, Nishimoto AT, Barker KS, Rogers PD. Azole antifungal resistance in Candida albicans and emerging non-albicans Candida species. Front Microbiol. 2017;7:1–12. doi:10.3389/fmicb.2016.02173
  • Mølgaard-Nielsen D, Pasternak B, Hviid A. Use of oral fluconazole during pregnancy and the risk of birth defects. N Engl J Med. 2013;369(9):830–839. doi:10.1056/nejmoa1301066
  • Martin MV. Review The use of fluconazole and itraconazole in the treatment of. J Antimicrob Chemother. 1999;44:429–437. doi:10.1093/jac/44.4.429
  • Pasko MT, Piscitelli SC, Van Slooten AD. Formulary forum. Ann Pharmacother. 1989;24(9):860–867.
  • Sobel JD, Wiesenfeld HC, Martens M, et al. Maintenance fluconazole therapy for recurrent vulvovaginal candidiasis. N Engl J Med. 2004;351(9):876–883. doi:10.1056/nejmoa033114
  • Maertens JA. History of the development of azole derivatives. Clin Microbiol Infect. 2004;10(SUPPL. 1):1–10. doi:10.1111/j.1470-9465.2004.00841.x
  • Nielsen LE, Forrester JB, Girotto JE, Dassner AM, Humphries R. One size fits all? Application of susceptible-dose-dependent breakpoints to pediatric patients and laboratory reporting. J Clin Microbiol. 2020;58(1):1–8. doi:10.1128/JCM.01446-19
  • Sanguinetti M, Posteraro B, Fiori B, Ranno S, Torelli R, Fadda G. Mechanisms of azole resistance in clinical isolates of Candida glabrata collected during a hospital survey of antifungal resistance. Antimicrob Agents Chemother. 2005;49(2):668–679. doi:10.1128/AAC.49.2.668-679.2005
  • Teo JQM, Lee SJY, Tan AL, et al. Molecular mechanisms of azole resistance in Candida bloodstream isolates. BMC Infect Dis. 2019;19(1):1–4. doi:10.1186/s12879-019-3672-5
  • Yao D, Chen J, Chen W, Li Z, Hu X. Mechanisms of azole resistance in clinical isolates of Candida glabrata from two hospitals in China. Infect Drug Resist. 2019;12:771–781. doi:10.2147/IDR.S202058
  • Pfaller MA, Boyken LB, Hollis RJ, et al. Validation of 24-hour fluconazole MIC readings versus the CLSI 48-hour broth microdilution reference method: results from a global Candida antifungal surveillance program. J Clin Microbiol. 2008;46(11):3585–3590. doi:10.1128/JCM.01391-08
  • Espinel-Ingroff A, Canton E, Peman J, Rinaldi MG, Fothergill AW. Comparison of 24-hour and 48-hour voriconazole MICs as determined by the Clinical and Laboratory Standards Institute Broth Microdilution Method (M27-A3 document) in three laboratories: results obtained with 2162 clinical isolates of Candida spp. and other. J Clin Microbiol. 2009;47(9):2766–2771. doi:10.1128/JCM.00654-09
  • Wang JM, Bennett RJ, Andersona MZ. The genome of the human pathogen Candida albicans is shaped by mutation and cryptic sexual recombination. MBio. 2018;9(5):1–16.
  • Sitterlé E, Maufrais C, Sertour N, Palayret M, d’Enfert C, Bougnoux ME. Within-host genomic diversity of Candida albicans in healthy carriers. Sci Rep. 2019;9(1):1–12. doi:10.1038/s41598-019-38768-4
  • Pryszcz LP, Németh T, Gácser A, Gabaldón T. Unexpected genomic variability in clinical and environmental strains of the pathogenic yeast Candida parapsilosis. Genome Biol Evol. 2013;5(12):2382–2392. doi:10.1093/gbe/evt185
  • Roman EA, Faraj SE, Gallo M, Salvay AG, Ferreiro DU, Santos J. Protein stability and dynamics modulation: the case of human frataxin. PLoS One. 2012;7(9):e45743. doi:10.1371/journal.pone.0045743
  • Bahar I, Lezon TR, Yang LW, Eyal E. Global dynamics of proteins: bridging between structure and function. Annu Rev Biophys. 2010;39(1):23–42. doi:10.1146/annurev.biophys.093008.131258
  • Laskowski RA, Gerick F, Thornton JM. The structural basis of allosteric regulation in proteins. FEBS Lett. 2009;583(11):1692–1698. doi:10.1016/j.febslet.2009.03.019
  • Mane A, Vidhate P, Kusro C, et al. Molecular mechanisms associated with Fluconazole resistance in clinical Candida albicans isolates from India. Mycoses. 2016;59(2):93–100. doi:10.1111/myc.12439
  • Morschhäuser J. The development of fluconazole resistance in Candida albicans – an example of microevolution of a fungal pathogen. J Microbiol. 2016;54(3):192–201. doi:10.1007/s12275-016-5628-4
  • Prakash SMU, Nazeer Y, Jayanthi S, Kabir MA. Computational insights into fluconazole resistance by the suspected mutations in lanosterol 14α-demethylase (Erg11p) of Candida albicans. Mol Biol Res Commun. 2020;9(4):155–167. doi:10.22099/mbrc.2020.36298.1476
  • Morio F, Loge C, Besse B, Hennequin C, Le Pape P. Screening for amino acid substitutions in the Candida albicans Erg11 protein of azole-susceptible and azole-resistant clinical isolates: new substitutions and a review of the literature. Diagn Microbiol Infect Dis. 2010;66(4):373–384. doi:10.1016/j.diagmicrobio.2009.11.006
  • Lepesheva GI, Waterman MR. Sterol 14alpha-demethylase cytochrome P450 (CYP51), a P450 in all Biological Kingdoms. Biochim Biophys Acta. 2008;1770(3):467–477. doi:10.1016/j.bbagen.2006.07.018
  • Lepesheva GI, Waterman MR. Structural basis for conservation in the CYP51 family. Biochimica et Biophysica Acta. 2011;1814(1):88–93. doi:10.1016/j.bbapap.2010.06.006
  • Lepesheva GI, Waterman MR. CYP51 - the omnipotent P450. Mol Cell Endocrinol. 2004;215(1–2):165–170. doi:10.1016/j.mce.2003.11.016
  • Lepesheva GI, Virus C, Waterman MR. Conservation in the CYP51 family. Role of the B′ helix/BC loop and helices F and G in enzymatic function. Biochemistry. 2003;42(30):9091–9101. doi:10.1021/bi034663f