Antifungal activity of azole compounds CPA18 and CPA109 against azole-susceptible and -resistant strains of Candida albicans

Journal of Antimicrobial Chemotherapy

Volumn 68, Issue 5, 2013, Pages 1111-1119

  Calabrese, Elena C ^a   Castellano, Sabrina ^a   Santoriello, Marisabella ^a   Sgherri, Cristina ^b   Quartacci, Mike F ^b   Calucci, Lucia ^c   Warrilow, Andrew G S ^d   Lamb, David C ^d   Kelly, Steven L ^d   Milite, Ciro ^a   Granata, Ilaria ^a   Sbardella, Gianluca ^a   Stefancich, Giorgio ^e   Maresca, Bruno ^a   Porta, Amalia ^a  

^a UNIVERSITY OF SALERNO   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c CNR   (Italy)

^d SWANSEA UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF TRIESTE   (Italy)

Author keywords

Drug development; Fungicidal; Resistance; Synergism; Time kill assays

Indexed keywords

ABC TRANSPORTER; ANTIFUNGAL AGENT; FILIPIN; FLUCONAZOLE; MEMBRANE LIPID; MICONAZOLE; PROPIDIUM IODIDE; PYRROLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIFUNGAL ACTIVITY; ARTICLE; BINDING AFFINITY; CANDIDA ALBICANS; DRUG CYTOTOXICITY; DRUG POTENTIATION; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS HYPHAE; GENE SEQUENCE; IMMUNOCOMPROMISED PATIENT; MACROPHAGE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; ANTIFUNGAL AGENTS; AZOLES; CANDIDA ALBICANS; CELL MEMBRANE; CELL SURVIVAL; DRUG SYNERGISM; FILIPIN; HYPHAE; MACROPHAGES; MICE; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; PROPIDIUM; STAINING AND LABELING;

EID: 84877133207     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dks506     Document Type: Article

References (47)

1. Bassetti M, Ansaldi F, Nicolini L et al. Incidence of candidaemia and relationship with fluconazole use in an intensive care unit. J Antimicrob Chemother 2009; 64: 625-9.
2. Gafter-Gvili A, Vidal L, Goldberg E et al. Treatment of invasive candidal infections: systematic review and meta-analysis. Mayo Clin Proc 2008; 83: 1011-21.
3. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 2007; 20: 133-63.
4. Pappas PG, Kauffman CA, Andes D et al. Clinical practice guidelines for the management candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 2009; 48: 503-35.
5. Chen SC-A, Slavin MA, Sorrell TC. Echinocandin antifungal drugs in fungal infections: a comparison. Drugs 2011; 71: 11-41.
6. Aoyama Y, Yoshida Y, Sato R. Yeast cytochrome P-450 catalyzing lanosterol 14a-demethylation. II. Lanosterol metabolism by purified P-45014DM and by intact microsomes. J Biol Chem 1984; 259: 1661-6.
7. Lamb D, Kelly D, Kelly S. Molecular aspects of azole antifungal action and resistance. Drug Resist Update 1999; 2: 390-402.
8. Rogers TR. Antifungal drug resistance: limited data, dramatic impact? Int J Antimicrob Agents 2006; 27: 7-11.
9. Sanglard D, Odds FC. Resistance of Candida species to antifungal agents: molecular mechanisms and clinical consequences. Lancet Infect Dis 2002; 2: 73-85.
10. Mukherjee PK, Sheehan DJ, Hitchcock CA et al. Combination treatment of invasive fungal infections. Clin Microbiol Rev 2005; 18: 163-94.
11. Onyewu C, Blankenship JR, Del Poeta M et al. Ergosterol biosynthesis inhibitors become fungicidal when combined with calcineurin inhibitors against Candida albicans, Candida glabrata, and Candida krusei. Antimicrob Agents Chemother 2003; 47: 956-64.
12. Castellano S, Stefancich G, Ragno R et al. CYP19 (aromatase): exploring the scaffold flexibility for novel selective inhibitors. Bioorg Med Chem 2008; 16: 8349-58.
13. Favre B, Didmon M, Ryder NS. Multiple amino acid substitutions in lanosterol 14a-demethylase contribute to azole resistance in Candida albicans. Microbiology 1999; 145: 2715-25.
14. Kakeya H, Miyazaki Y, Miyazaki H et al. Genetic analysis of azole resistance in the Darlington strain of Candida albicans. Antimicrob Agents Chemother 2000; 44: 2985-90.
15. Nishikawa H, Yamada E, Shibata T et al. Uptake of T-2307, a novel arylamidine, in Candida albicans. J Antimicrob Chemother 2010; 65: 1681-7.
16. Clinical and Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts-Third Edition: Approved Standard M27-A3. CLSI, Wayne, PA, USA, 2008.
17. Klepser ME, Ernst EJ, Lewis RE et al. Influence of test conditions on antifungal time-kill curve results: proposal for standardized methods. Antimicrob Agents Chemother 1998; 42: 1207-12.
18. Lamb DC, Kelly DE, Waterman MR et al. Characteristics of the heterologously expressed human lanosterol 14a-demethylase (other names: P45014DM, CYP51, P45051) and inhibition of the purified human and Candida albicans CYP51 with azole antifungal agents. Yeast 1999; 15: 755-63.
19. Lutz JD, Dixit V, Yeung CK et al. Expression and functional characterization of cytochrome P450 26A1, a retinoic acid hydroxylase. Biochem Pharmacol 2009; 77: 258-68.
20. Morrison JF. Kinetics of the reversible inhibition of enzyme-catalysed reactions by tight-binding inhibitors. Biochim Biophys Acta Enzymol 1969; 185: 269-86.
21. Copeland RA. Evaluation of Enzyme Inhibitors in Drug Discovery. A Guide for Medicinal Chemists and Pharmacologists. Methods of Biochemical Analysis. New York: Wiley-Interscience, 2005.
22. Quan H, Cao Y-Y, Xu Z et al. Potent in vitro synergism of fluconazole and berberine chloride against clinical isolates of Candida albicans resistant to fluconazole. Antimicrob Agents Chemother 2006; 50: 1096-9.
23. Ahmad A, Khan A, Khan LA et al. In vitro synergy of eugenol and methyleugenol with fluconazole against clinical Candida isolates. J Med Microbiol 2010; 59: 1178-84.
24. Canton E, Peman J, Gobernado M et al. Synergistic activities of fluconazole and voriconazole with terbinafine against four Candida species determined by checkerboard, time-kill, and Etest methods. Antimicrob Agents Chemother 2005; 49: 1593-6.
25. Noverr MC, Huffnagle GB. Regulation of Candida albicans morphogenesis by fatty acid metabolites. Infect Immun 2004; 72: 6206-10.
26. Martin SW, Konopka JB. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 2004; 3: 675-84.
27. Li R-K, Cutler JE. A cell surface/plasma membrane antigen of Candida albicans. J Gen Microbiol 1991; 137: 455-64.
28. Sgherri CLM, Salvateci P, Menconi M et al. Interaction between drought and elevated CO2 in the response of alfalfa plants to oxidative stress. J Plant Physiol 2000; 156: 360-6.
29. Quartacci MF, Glišić O, Stevanović B et al. Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration. J Exp Bot 2002; 53: 2159-66.
30. Prigneau O, Porta A, Maresca B. Candida albicans CTN gene family is induced during macrophage infection: homology, disruption and phenotypic analysis of CTN3 gene. Fungal Genet Biol 2004; 41: 783-93.
31. Jefcoate CRE, Gaylor JL, Calabrese RL. Ligand interactions with cytochrome P-450. I. Binding of primary amines. Biochemistry 1969; 8: 3455-63.
32. Jefcoate CR. Measurement of substrate and inhibitor binding to microsomal cytochrome P-450 by optical-difference spectroscopy. In: Fleischer S, Packer L, eds. Methods in Enzymology. New York: Academic Press, 1978; 258-79.
33. Manavathu EK, Cutright JL, Chandrasekar PH. Organism-dependent fungicidal activities of azoles. Antimicrob Agents Chemother 1998; 42: 3018-21.
34. Ha KC, White TC. Effects of azole antifungal drugs on the transition from yeast cells to hyphae in susceptible and resistant isolates of the pathogenic yeast Candida albicans. Antimicrob Agents Chemother 1999; 43: 763-8.
35. Ramani R, Chaturvedi V. Flow cytometry antifungal susceptibility testing of pathogenic yeasts other than Candida albicans and comparison with the NCCLS broth microdilution test. Antimicrob Agents Chemother 2000; 44: 2752-8.
36. Israelachvili JN, Marčelja S, Horn RG. Physical principles of membrane organization. Q Rev Biophys 1980; 13: 121-200.
37. Williams EE. Membrane lipids: what membrane physical properties are conserved during physiochemically-induced membrane restructuring? Am Zool 1998; 38: 280-90.
38. Quartacci MF, Cosi E, Navari-Izzo F. Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 2001; 52: 77-84.
39. Epand RM, Epand RF. Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta Biomembr 2009; 1788: 289-94.
40. Mannock DA, Lewis RNAH, McMullen TPW et al. The effect of variations in phospholipid and sterol structure on the nature of lipid-sterol interactions in lipid bilayer model membranes. Chem Phys Lipids 2010; 163: 403-48.
41. Lupetti A, Danesi R, Campa M et al. Molecular basis of resistance to azole antifungals. Trends Mol Med 2002; 8: 76-81.
42. Singh A, Prasad R. Comparative lipidomics of azole sensitive and resistant clinical isolates of Candida albicans reveals unexpected diversity in molecular lipid imprints. PLoS One 2011; 6: e19266.
43. Parks LW, Casey WM. Physiological implications of sterol biosynthesis in yeast. Annu Rev Microbiol 1995; 49: 95-116.
44. Sharma SC. Implications of sterol structure for membrane lipid composition, fluidity and phospholipid asymmetry in Saccharomyces cerevisiae. FEMS Yeast Res 2006; 6: 1047-51.
45. Abe F, Usui K, Hiraki T. Fluconazole modulates membrane rigidity, heterogeneity, and water penetration into the plasma membrane in Saccharomyces cerevisiae. Biochemistry 2009; 48: 8494-504.
46. Charlier C, Hart E, Lefort A et al. Fluconazole for the management of invasive candidiasis: where do we stand after 15 years? J Antimicrob Chemother 2006; 57: 384-410.
47. Marr KA, Leisenring W, Crippa F et al. Cyclophosphamide metabolism is affected by azole antifungals. Blood 2004; 103: 1557-9.