Influence of multidrug efflux systems on methylene blue-mediated photodynamic inactivation of Candida albicans

Journal of Antimicrobial Chemotherapy

Volumn 66, Issue 7, 2011, Pages 1525-1532

  Prates, Renato A ^a   Kato, Ilka T ^a   Ribeiro, Martha S ^a   Tegos, George P ^b,c,d   Hamblin, Michael R ^b,c,e  

^a INSTITUTO DE PESQUISAS ENERGÉTICAS E NUCLEARES   (Brazil)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^e HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

ABC transporters; Major facilitator superfamily; Photodynamic therapy; Photosensitizer; Verapamil

Indexed keywords

ABC TRANSPORTER; INF 271; MAJOR FACILITATOR SUPERFAMILY; MEMBRANE PROTEIN; METHYLENE BLUE; MULTIDRUG EFFLUX SYSTEM; PHOTOSENSITIZING AGENT; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; VERAPAMIL;

ANTIMICROBIAL PHOTODYNAMIC INACTIVATION; ARTICLE; CANDIDA ALBICANS; CELL KILLING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; FUNGICIDAL ACTIVITY; HYPOTHESIS; MUTANT; NONHUMAN; PHOTODYNAMIC THERAPY; PROTEIN EXPRESSION; PROTEIN TRANSPORT; WILD TYPE;

ANTIFUNGAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; CANDIDA ALBICANS; HUMANS; METHYLENE BLUE; MICROBIAL VIABILITY; MICROSCOPY, CONFOCAL; PHOTOSENSITIZING AGENTS;

EID: 79958805967     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkr160     Document Type: Article

References (53)

1. Espinel-Ingroff A. Novel antifungal agents, targets or therapeutic strategies for the treatment of invasive fungal diseases: a review of the literature (2005-2009). Rev Iberoam Micol 2009; 26: 15-22.
2. d'Enfert C. Hidden killers: persistence of opportunistic fungal pathogens in the human host. Curr Opin Microbiol 2009; 12: 358-64.
3. Freydiere AM, Guinet R, Boiron P. Yeast identification in the clinical microbiology laboratory: phenotypical methods. Med Mycol 2001; 39: 9-33.
4. Schuetzer-Muehlbauer M, Willinger B, Egner R et al. Reversal of antifungal resistance mediated by ABC efflux pumps from Candida albicans functionally expressed in yeast. Int J Antimicrob Agents 2003; 22: 291-300.
5. Cowen LE, Anderson JB, Kohn LM. Evolution of drug resistance in Candida albicans. Annu Rev Microbiol 2002; 56: 139-65.
6. Pao SS, Paulsen IT, Saier MH Jr. Major facilitator superfamily. Microbiol Mol Biol Rev 1998; 62: 1-34.
7. Tegos GP, Masago K, Aziz F et al. Inhibitors of bacterial multidrug efflux pumps potentiate antimicrobial photoinactivation. Antimicrob Agents Chemother 2008; 52: 3202-9.
8. Dai TH, Tegos GP, Zhiyentayev T et al. Photodynamic therapy for methicillin-resistant Staphylococcus aureus infection in a mouse skin abrasion model. Lasers Surg Med 2010; 42: 38-44.
9. Prates RA, da Silva EG, Yamada AM et al. Light parameters influence cell viability in antifungal photodynamic therapy in a fluence and rate fluence-dependent manner. Laser Physics 2009; 19: 1038-44.
10. Dai T, Huang YY, Hamblin MR. Photodynamic therapy for localized infections-state of the art. Photodiagnosis Photodyn Ther 2009; 6: 170-88.
11. Moan J, Peng Q. An outline of the hundred-year history of PDT. Anticancer Res 2003; 23: 3591-600.
12. Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer 2003; 3: 380-7.
13. Cruess AF, Zlateva G, Pleil AM et al. Photodynamic therapy with verteporfin in age-related macular degeneration: a systematic review of efficacy, safety, treatment modifications and pharmacoeconomic properties. Acta Ophthalmol 2009; 87: 118-32.
14. Hamblin MR, Hasan T. Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci 2004; 3: 436-50.
15. Jori G, Fabris C, Soncin M et al. Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Lasers Surg Med 2006; 38: 468-81.
16. Wainwright M, Phoenix DA, Laycock SL et al. Photobactericidal activity of phenothiazinium dyes against methicillin-resistant strains of Staphylococcus aureus. FEMS Microbiol Lett 1998; 160: 177-81.
17. Wainwright M, Phoenix DA, Marland J et al. A study of photobactericidal activity in the phenothiazinium series. FEMS Immunol Med Microbiol 1997; 19: 75-80.
18. Phoenix DA, Sayed Z, Hussain S et al. The phototoxicity of phenothiazinium derivatives against Escherichia coli and Staphylococcus aureus. FEMS Immunol Med Microbiol 2003; 39: 17-22.
19. Wilson M, Burns T, Pratten J et al. Bacteria in supragingival plaque samples can be killed by low-power laser light in the presence of a photosensitizer. J Appl Bacteriol 1995; 78: 569-74.
20. Romanova NA, Brovko LY, Moore L et al. Assessment of photodynamic destruction of Escherichia coli O157:H7 and Listeria monocytogenes by using ATP bioluminescence. Appl Environ Microbiol 2003; 69: 6393-8.
21. Wong TW, Wang YY, Sheu HM et al. Bactericidal effects of toluidine blue-mediated photodynamic action on Vibrio vulnificus. Antimicrob Agents Chemother 2005; 49: 895-902.
22. Demidova TN, Hamblin MR. Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 2004; 17: 245-54.
23. Wainwright M. The use of dyes in modern biomedicine. Biotech Histochem 2003; 78: 147-55.
24. Demidova TN, Gad F, Zahra T et al. Monitoring photodynamic therapy of localized infections by bioluminescence imaging of genetically engineered bacteria. J Photochem Photobiol B 2005; 81: 15-25.
25. Monfrecola G, Procaccini EM, Bevilacqua M et al. In vitro effect of 5-aminolaevulinic acid plus visible light on Candida albicans. Photochem Photobiol Sci 2004; 3: 419-22.
26. O'Neill JF, Hope CK, Wilson M. Oral bacteria in multi-species biofilms can be killed by red light in the presence of toluidine blue. Lasers Surg Med 2002; 31: 86-90.
27. Garcez AS, Ribeiro MS, Tegos GP et al. Antimicrobial photodynamic therapy combined with conventional endodontic treatment to eliminate root canal biofilm infection. Lasers Surg Med 2007; 39: 59-66.
28. Usacheva MN, Teichert MC, Usachev YM et al. Interaction of the photobactericides methylene blue and toluidine blue with a fluorophore in Pseudomonas aeruginosa cells. Lasers Surg Med 2008; 40: 55-61.
29. Lewis K. Multidrug resistance: versatile drug sensors of bacterial cells. Curr Biol 1999; 9: R403-7.
30. Tegos G, Stermitz FR, Lomovskaya O et al. Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob Agents Chemother 2002; 46: 3133-41.
31. Tegos GP, Anbe M, Yang C et al. Protease-stable polycationic photosensitizer conjugates between polyethyleneimine and chlorin(e6) for broad-spectrum antimicrobial photoinactivation. Antimicrob Agents Chemother 2006; 50: 1402-10.
32. Nobile CJ, Andes DR, Nett JE et al. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2006; 2: e63.
33. Otzen T, Wempe EG, Kunz B et al. Folate-synthesizing enzyme system as target for development of inhibitors and inhibitor combinations against Candida albicans-synthesis and biological activity of new 2,4-diaminopyrimidines and 4′-substituted 4-aminodiphenyl sulfones. J Med Chem 2004; 47: 240-53.
34. Watkins WJ, Lemoine RC, Chong L et al. Quinazolinone fungal efflux pump inhibitors. Part 2: In vitro structure-activity relationships of (N-methyl-piperazinyl)-containing derivatives. Bioorg Med Chem Lett 2004; 14: 5133-7.
35. Lemoine RC, Glinka TW, Watkins WJ et al. Quinazolinone-based fungal efflux pump inhibitors. Part 1: Discovery of an (N-methylpiperazine)-containing derivative with activity in clinically relevant Candida spp. Bioorg Med Chem Lett 2004; 14: 5127-31.
36. Sanglard D, Ischer F, Monod M et al. Susceptibilities of Candida albicans multidrug transporter mutants to various antifungal agents and other metabolic inhibitors. Antimicrob Agents Chemother 1996; 40: 2300-5.
37. Barchiesi F, Arzeni D, Del Prete MS et al. Fluconazole susceptibility and strain variation of Candida albicans isolates from HIV-infected patients with oropharyngeal candidosis. J Antimicrob Chemother 1998; 41: 541-8.
38. Sanglard D, Ischer F, Calabrese D et al. The ATP binding cassette transporter gene CgCDR1 from Candida glabrata is involved in the resistance of clinical isolates to azole antifungal agents. Antimicrob Agents Chemother 1999; 43: 2753-65.
39. Bruno VM, Mitchell AP. Regulation of azole drug susceptibility by Candida albicans protein kinase CK2. Mol Microbiol 2005; 56: 559-73.
40. Tegos GP, Hamblin MR. Phenothiazinium antimicrobial photosensitizers are substrates of bacterial multidrug resistance pumps. Antimicrob Agents Chemother 2006; 50: 196-203.
41. Kaatz GW. Bacterial efflux pump inhibition. Curr Opin Investig Drugs 2005; 6: 191-8.
42. Jett BD, Hatter KL, Huycke MM et al. Simplified agar plate method for quantifying viable bacteria. BioTechniques 1997; 23: 648-50.
43. Ball DJ, Luo Y, Kessel D et al. The induction of apoptosis by a positively charged methylene blue derivative. J Photochem Photobiol B 1998; 42: 159-63.
44. Pfaller MA, Burmeister L, Bartlett MS et al. Multicenter evaluation of four methods of yeast inoculum preparation. J Clin Microbiol 1988; 26: 1437-41.
45. Ragas X, Sanchez-Garcia D, Ruiz-Gonzalez R et al. Cationic porphycenes as potential photosensitizers for antimicrobial photodynamic therapy. J Med Chem 2010; 53: 7796-803.
46. Huang L, Huang YY, Mroz P et al. Stable synthetic cationic bacteriochlorins as selective antimicrobial photosensitizers. Antimicrob Agents Chemother 2010; 54: 3834-41.
47. Donnelly RF, McCarron PA, Tunney MM et al. Potential of photodynamic therapy in treatment of fungal infections of the mouth. Design and characterisation of a mucoadhesive patch containing toluidine blue O. J Photochem Photobiol B 2007; 86: 59-69.
48. Giroldo LM, Felipe MP, de Oliveira MA et al. Photodynamic antimicrobial chemotherapy (PACT) with methylene blue increases membrane permeability in Candida albicans. Lasers Med Sci 2009; 24: 109-12.
49. Demidova TN, Hamblin MR. Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 2005; 49: 2329-35.
50. Sampaio P, Nogueira E, Loureiro AS et al. Increased number of glutamine repeats in the C-terminal of Candida albicans Rlm1p enhances the resistance to stress agents. Antonie Van Leeuwenhoek 2009; 96: 395-404.
51. Markham PN, Westhaus E, Klyachko K et al. Multiple novel inhibitors of the NorA multidrug transporter of Staphylococcus aureus. Antimicrob Agents Chemother 1999; 43: 2404-8.
52. Pina-Vaz C, Rodrigues AG, Costa-de-Oliveira S et al. Potent synergic effect between ibuprofen and azoles on Candida resulting from blockade of efflux pumps as determined by FUN-1 staining and flow cytometry. J Antimicrob Chemother 2005; 56: 678-85.
53. Stringaro A, Molinari A, Calcabrini A et al. Detection of human P-glycoprotein-like molecule in azole-resistant Candida albicans from HIV+ patients. Microb Drug Resist 2002; 8: 235-44.