353
Views
2
CrossRef citations to date
0
Altmetric
Research Articles

Molecular simulations of fluconazole-mediated inhibition of sterol biosynthesis

&
Pages 1659-1669 | Received 26 Dec 2018, Accepted 29 Apr 2019, Published online: 16 May 2019

References

  • Balding, P. R., Porro, C. S., McLean, K. J., Sutcliffe, M. J., Maréchal, J.-D., Munro, A. W., & Visser, S. P. D. (2008). How do azoles inhibit cytochrome P450 enzymes? A density functional study. The Journal of Physical Chemistry A, 112(50), 12911–12918. doi: 10.1021/jp802087w
  • Bellamine, A., Mangla, A. T., Nes, W. D., & Waterman, M. R. (1999). Characterization and catalytic properties of the sterol 14alpha-demethylase from Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences of the United States of America, 96(16), 8937–8942. doi: 10.1073/pnas.96.16.8937
  • Bongomin, F., Gago, S., Oladele, R. O., & Denning, D. W. (2017). Global and multi-national prevalence of fungal diseases-estimate precision. Journal of Fungi (Fungi), 3(4), pii: E57. doi: 10.3390/jof3040057
  • Brown, G. D., Denning, D. W., & Levitz, S. M. (2012). Tackling human fungal infections. Science (New York, N.Y.), 336(6082), 647. doi: 10.1126/science.1222236
  • Castanheira, M., Messer, S. A., Jones, R. N., Farrell, D. J., & Pfaller, M. A. (2014). Activity of echinocandins and triazoles against a contemporary (2012) worldwide collection of yeast and moulds collected from invasive infections. International Journal of Antimicrobial Agents, 44(4), 320–326. doi: 10.1016/j.ijantimicag.2014.06.007
  • Choi, J., & Roush, W. (2016). Structure based design of CYP51 inhibitors. Current Topics in Medicinal Chemistry, 17(1), 30–39. doi: 10.2174/1568026616666160719164933
  • de Magalhães, C. S., Almeida, D. M., Barbosa, H. J. C., & Dardenne, L. E. (2014). A dynamic niching genetic algorithm strategy for docking highly flexible ligands. Information Sciences, 289, 206–224. doi: 10.1016/j.ins.2014.08.002
  • de Magalhães, C. S., Barbosa, H. J. C., & Dardenne, L. E. (2004). Selection-insertion schemes in genetic algorithms for the flexible ligand docking problem. In K. Deb (Ed.), Lecture notes in computer science (Vol. 3102, pp. 368–379). Berlin, Heidelberg: Springer.
  • Doğan, İS., Saraç, S., Sari, S., Kart, D., Eşsiz Gökhan, Ş., Vural, İ., & Dalkara, S. (2017). New azole derivatives showing antimicrobial effects and their mechanism of antifungal activity by molecular modeling studies. European Journal of Medicinal Chemistry, 130, 124–138. doi: 10.1016/j.ejmech.2017.02.035
  • Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. doi: 10.1063/1.470117
  • Gao, P., Cui, Y.-L., & Wu, R.-L. (2018). Molecular dynamic modeling of CYP51B in complex with azole inhibitors. Journal of Biomolecular Structure & Dynamics, 36(6), 1511–1519. doi: 10.1080/07391102.2017.1328315
  • Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., & Onufriev, A. (2005). H: A server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Research, 33(Web Server), W368–W371. doi: 10.1093/nar/gki464
  • Hargrove, T., Wawrzak, Z., & Lepesheva, G. (2017). Crystal structure of sterol 14-alpha demethylase (CYP51) from Candida albicans in complex with the tetrazole-based antifungal drug candidate VT1161 (VT1). https://doi.org/10.2210/pdb5tz1/pdb
  • Hargrove, T. Y., Friggeri, L., Wawrzak, Z., Qi, A., Hoekstra, W. J., Schotzinger, R. J., … Lepesheva, G. I. (2017). Structural analyses of Candida albicans sterol 14α-demethylase complexed with azole drugs address the molecular basis of azole-mediated inhibition of fungal sterol biosynthesis. Journal of Biological Chemistry, 292(16), 6728–6743. doi: 10.1074/jbc.M117.778308
  • Hargrove, T. Y., Wawrzak, Z., Lamb, D. C., Guengerich, F. P., & Lepesheva, G. I. (2015). Structure-functional characterization of cytochrome P450 sterol 14α-demethylase (CYP51B) from Aspergillus fumigatus and molecular basis for the development of antifungal drugs. Journal of Biological Chemistry, 290(39), 23916–23934. doi: 10.1074/jbc.M115.677310
  • Huang, J., & MacKerell, A. D. Jr.(2013). CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data. Journal of Computational Chemistry, 34(25), 2135–2145. doi: 10.1002/jcc.23354
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. 27–28. doi: 10.1016/0263-7855(96)00018-5
  • Jacob K., S., Ganguly, S., Kumar, P., Poddar, R., & Kumar, A. (2017). Homology model, molecular dynamics simulation and novel pyrazole analogs design of Candida albicans CYP450 lanosterol 14 α-demethylase, a target enzyme for antifungal therapy. Journal of Biomolecular Structure & Dynamics, 35(7), 1446–1463. doi: 10.1080/07391102.2016.1185380
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. doi: 10.1063/1.445869
  • Kalé, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., … Schulten, K. (1999). NAMD2: Greater scalability for parallel molecular dynamics. Journal of Computational Physics, 151(1), 283–312. doi: 10.1006/jcph.1999.6201
  • Keighobadi, M., Emami, S., Lagzian, M., Fakhar, M., Rafiei, A., & Valadan, R. (2018). Molecular modeling and structural stability of wild-type and mutant CYP51 from Leishmania major: In vitro and in silico analysis of a laboratory strain. Molecules, 23(3), pii:E696. doi: 10.3390/molecules23030696
  • Kenaan, C., Zhang, H., Shea, E. V., & Hollenberg, P. F. (2011). Uncovering the role of hydrophobic residues in cytochrome P450-cytochrome P450 reductase interactions. Biochemistry, 50(19), 3957–3967. doi: 10.1021/bi1020748
  • Kontoyianni, M., & Lacy, B. (2018). Toward computational understanding of molecular recognition in the human metabolizing cytochrome P450s. Current Medicinal Chemistry, 25(28), 3353–3373. doi: 10.2174/0929867325666180226104126
  • Lepesheva, G. I., & Waterman, M. R. (2007). Sterol 14alpha-demethylase cytochrome P450 (CYP51), a P450 in all biological kingdoms. Biochimica et Biophysica Acta, 1770(3), 467–477. doi: 10.1016/j.bbagen.2006.07.018
  • Lepesheva, G. I., & Waterman, M. R. (2011). Structural basis for conservation in the CYP51 family. Biochimica et Biophysica Acta, 1814(1), 88–93. doi: 10.1016/j.bbapap.2010.06.006
  • Lupetti, A., Danesi, R., Campa, M., Del Tacca, M., & Kelly, S. (2002). Molecular basis of resistance to azole antifungals. Trends in Molecular Medicine, 8(2), 76–81.
  • MacKerell, A. D., Bashford, D., Bellott, M., Dunbrack, R. L., Evanseck, J. D., Field, M. J., … Karplus, M. (1998). All-atom empirical potential for molecular modeling and dynamics studies of proteins. The Journal of Physical Chemistry B, 102(18), 3586–3616. doi: 10.1021/jp973084f
  • Marichal, P., Gorrens, J., Laurijssens, L., Vermuyten, K., Van Hove, C., Le Jeune, L., … Vanden Bossche, H. (1999). Accumulation of 3-ketosteroids induced by itraconazole in azole-resistant clinical Candida albicans isolates. Antimicrobial Agents and Chemotherapy, 43(11), 2663–2670. doi: 10.1128/AAC.43.11.2663
  • Martínez, L. (2015). Automatic identification of mobile and rigid substructures in molecular dynamics simulations and fractional structural fluctuation analysis. PLoS One, 10(3), e0119264. doi: 10.1371/journal.pone.0119264
  • Martínez, L. (2017). MDAnalysis (Version 17.224). Retrieved from http://leandro.iqm.unicamp.br/mdanalysis
  • Mayne, C. G., Saam, J., Schulten, K., Tajkhorshid, E., & Gumbart, J. C. (2013). Rapid parameterization of small molecules using the Force Field Toolkit. Journal of Computational Chemistry, 34(32), 2757–2770. doi: 10.1002/jcc.23422
  • McLean, K. J., Clift, D., Lewis, D. G., Sabri, M., Balding, P. R., Sutcliffe, M. J., … Munro, A. W. (2006). The preponderance of P450s in the Mycobacterium tuberculosis genome. Trends in Microbiology, 14(5), 220–228. doi: 10.1016/j.tim.2006.03.002
  • Park, H.-G., Lee, I.-S., Chun, Y.-J., Yun, C.-H., Johnston, J. B., Montellano, P. R. O., de, & … Im, D. (2011). Heterologous expression and characterization of the sterol 14α-demethylase CYP51F1 from Candida albicans. Archives of Biochemistry and Biophysics, 509(1), 9–15. doi: 10.1016/j.abb.2011.02.002
  • Pfaller, M. A., Andes, D. R., Diekema, D. J., Horn, D. L., Reboli, A. C., Rotstein, C., … Azie, N. E. (2014). Epidemiology and outcomes of invasive candidiasis due to non-albicans species of Candida in 2,496 patients: Data from the Prospective Antifungal Therapy (PATH) registry 2004-2008. PLoS One, 9(7), e101510. doi: 10.1371/journal.pone.0101510
  • Podust, L. M., Poulos, T. L., & Waterman, M. R. (2001). Crystal structure of cytochrome P450 14alpha -sterol demethylase (CYP51) from Mycobacterium tuberculosis in complex with azole inhibitors. Proceedings of the National Academy of Sciences of the United States of America, 98(6), 3068–3073. doi: 10.1073/pnas.061562898
  • Robert, X., & Gouet, P. (2014). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42(W1, Web Server issue), W320–W324. doi: 10.1093/nar/gku316
  • Sagatova, A. A., Keniya, M. V., Wilson, R. K., Monk, B. C., & Tyndall, J. D. A. (2015). Structural insights into binding of the antifungal drug fluconazole to Saccharomyces cerevisiae lanosterol 14α-demethylase. Antimicrobial Agents and Chemotherapy, 59(8), 4982–4989. doi: 10.1128/AAC.00925-15
  • Schrödinger, L. C. C. (2015). The PyMOL Molecular Graphics System (Version 2.0).
  • Shapiro, R. S., Robbins, N., & Cowen, L. E. (2011). Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiology and Molecular Biology Reviews: MMBR, 75(2), 213–267. doi: 10.1128/MMBR.00045-10
  • Sheng, C., Chen, S., Ji, H., Dong, G., Che, X., Wang, W., … Zhang, W. (2010). Evolutionary trace analysis of CYP51 family: Implication for site-directed mutagenesis and novel antifungal drug design. Journal of Molecular Modeling, 16(2), 279–284. doi: 10.1007/s00894-009-0527-9
  • Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., … Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Molecular Systems Biology, 7(1), 539. doi: 10.1038/msb.2011.75
  • Strushkevich, N., Usanov, S. A., & Park, H.-W. (2010). Structural basis of human CYP51 inhibition by antifungal azoles. Journal of Molecular Biology, 397(4), 1067–1078. doi: 10.1016/j.jmb.2010.01.075
  • Strushkevich, N. V., Harnastai, I. N., & Usanov, S. A. (2010). Mechanism of steroidogenic electron transport: Role of conserved Glu429 in destabilization of CYP11A1-adrenodoxin complex. Biochemistry (Moscow), 75(5), 570–578. doi: 10.1134/S0006297910050056
  • Swope, W. C., Andersen, H. C., Berens, P. H., & Wilson, K. R. (1982). A computer simulation method for the calculation of equilibrium constants for the formation of physical clusters of molecules: Application to small water clusters. The Journal of Chemical Physics, 76(1), 637–649. doi: 10.1063/1.442716
  • Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., … Mackerell, A. D. Jr.(2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31(4), 671–690. doi: 10.1002/jcc.21367
  • Vanommeslaeghe, K., Raman, E. P., & MacKerell, A. D. Jr.(2012). Automation of the CHARMM General Force Field (CGenFF) II: Assignment of bonded parameters and partial atomic charges. Journal of Chemical Information and Modeling, 52(12), 3155–3168. doi: 10.1021/ci3003649
  • Vijayakumar, S., & Das, P. (2019). Structural, molecular motions, and free-energy landscape of Leishmania sterol-14α-demethylase wild type and drug resistant mutant: A comparative molecular dynamics study. Journal of Biomolecular Structure & Dynamics, 37(6), 1477–1493. doi: 10.1080/07391102.2018.1461135
  • Warrilow, A. G., Parker, J. E., Kelly, D. E., & Kelly, S. L. (2013). Azole affinity of sterol 14α-demethylase (CYP51) enzymes from Candida albicans and Homo sapiens. Antimicrobial Agents and Chemotherapy, 57(3), 1352–1360. doi: 10.1128/AAC.02067-12
  • White, T. C., Marr, K. A., & Bowden, R. A. (1998). Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clinical Microbiology Reviews, 11(2), 382–402. doi: 10.1128/CMR.11.2.382

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.