Efflux pump inhibitor potentiates antimicrobial photodynamic inactivation of enterococcus faecalis biofilm

Photochemistry and Photobiology

Volumn 86, Issue 6, 2010, Pages 1343-1349

  Kishen, Anil ^a,c   Upadya, Megha ^b   Tegos, George P ^c,d   Hamblin, Michael R ^c,d,e  

^a UNIVERSITY OF TORONTO   (Canada)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS AFFECTING WATER, MOLECULE OR ION TRANSPORT; METHYLENE BLUE; PHOTOSENSITIZING AGENT; ROSE BENGAL; VERAPAMIL;

ARTICLE; BIOFILM; CONFOCAL MICROSCOPY; DRUG EFFECT; ENTEROCOCCUS FAECALIS; PHOTOCHEMOTHERAPY; PHYSIOLOGY; RADIATION EXPOSURE;

BIOFILMS; ENTEROCOCCUS FAECALIS; MEMBRANE TRANSPORT MODULATORS; METHYLENE BLUE; MICROSCOPY, CONFOCAL; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; ROSE BENGAL; VERAPAMIL;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS;

EID: 78649663234     PISSN: 00318655     EISSN: 17511097     Source Type: Journal    
DOI: 10.1111/j.1751-1097.2010.00792.x     Document Type: Article

References (52)

1. Castano, A. P., T. N. Demidova, and, M. R. Hamblin, (2004) Mechanisms in photodynamic therapy: Part one-Photosensitizers, photochemistry and cellular localization. Photodiagn. Photodyn. Ther. 1, 279-293.
2. Henney, J. E., (2000) From the Food and Drug Administration. JAMA 283, 2779.
3. Bressler, N. M., and, S. B. Bressler, (2000) Photodynamic therapy with verteporfin (Visudyne): Impact on ophthalmology and visual sciences. Invest. Ophthalmol. Vis. Sci. 41, 624-628.
4. Boehncke, W. H., T. Elshorst-Schmidt, and, R. Kaufmann, (2000) Systemic photodynamic therapy is a safe and effective treatment for psoriasis. Arch. Dermatol. 136, 271-272.
5. Trauner, K. B., and, T. Hasan, (1996) Photodynamic treatment of rheumatoid and inflammatory arthritis. Photochem. Photobiol. 64, 740-750.
6. Rockson, S. G., D. P. Lorenz, W. F. Cheong, and, K. W. Woodburn, (2000) Photoangioplasty: An emerging clinical cardiovascular role for photodynamic therapy. Circulation 102, 591-596.
7. Jenkins, M. P., G. A. Buonaccorsi, M. Raphael, I. Nyamekye, J. R. McEwan, S. G. Bown, and, C. C. Bishop, (1999) Clinical study of adjuvant photodynamic therapy to reduce restenosis following femoral angioplasty. Br. J. Surg. 86, 1258-1263.
8. Wainwright, M., (1998) Photodynamic antimicrobial chemotherapy (PACT). J. Antimicrob. Chemother. 42, 13-28.
9. Malik, Z., J. Hanania, and, Y. Nitzan, (1990) Bactericidal effects of photoactivated porphyrins-An alternative approach to antimicrobial drugs. J. Photochem. Photobiol. B Biol. 5, 281-293.
10. Hamblin, M. R., and, T. Hasan, (2004) Photodynamic therapy: A new antimicrobial approach to infectious disease? Photochem. Photobiol. Sci. 3, 436-450.
11. Gad, F., T. Zahra, T. Hasan, and, M. R. Hamblin, (2004) Effects of growth phase and extracellular slime on photodynamic inactivation of gram-positive pathogenic bacteria. Antimicrob. Agents Chemother. 48, 2173-2178.
12. Bhatti, M., A. MacRobert, S. Meghji, B. Henderson, and, M. Wilson, (1998) A study of the uptake of toluidine blue O by Porphyromonas gingivalis and the mechanism of lethal photosensitization. Photochem. Photobiol. 68, 370-376.
13. Wainwright, M., D. A. Phoenix, S. L. Laycock, D. R. Wareing, and, P. A. Wright, (1998) Photobactericidal activity of phenothiazinium dyes against methicillin-resistant strains of Staphylococcus aureus. FEMS Microbiol. Lett. 160, 177-181.
14. Usacheva, M. N., M. C. Teichert, and, M. A. Beil, (2001) Comparison of the methylene blue and toluidine blue photobactericidal efficacy against gram-positive and gram-negative microorganisms. Lasers Surg. Med. 29, 165-173.
15. Zeina, B., J. Greenman, W. M. Purcell, and, B. Das, (2001) Killing of cutaneous microbial species by photodynamic therapy. Br. J. Dermatol. 144, 274-278.
16. O'Neill, J., M. Wilson, and, M. Wainwright, (2003) Comparative antistreptococcal activity of photobactericidal agents. J. Chemother. 15, 329-334.
17. Wainwright, M., (2003) The use of dyes in modern biomedicine. Biotech. Histochem. 78, 147-155.
18. Poole, K., (2005) Efflux-mediated antimicrobial resistance. J. Antimicrob. Chemother. 56, 20-51.
19. Borges-Walmsley, M. I., and, A. R. Walmsley, (2001) The structure and function of drug pumps. Trends Microbiol. 9, 71-79.
20. Lewis, K., (1999) Versatile drug sensors of bacterial cells. Curr. Biol. 9, 403-407.
21. Tegos, G., F. R. Stermitz, O. Lomovskaya, and, K. Lewis, (2002) Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob. Agents Chemother. 46, 3133-3141.
22. Tegos, G. P., and, M. R. Hamblin, (2006) Phenothiazinium antimicrobial photosensitizers are substrates of bacterial multidrug resistance pumps. Antimicrob. Agents Chemother. 50, 196-203.
23. Tegos, G. P., K. Masago, F. Aziz, A. Higginbotham, F. R. Stermitz, and, M. R. Hamblin, (2008) Inhibitors of bacterial multidrug efflux pumps potentiate antimicrobial photoinactivation. Antimicrob. Agents Chemother. 52, 3202-3209.
24. Prince, A. S., (2002) Biofilm, antimicrobial resistance, and airway infection. N. Engl. J. Med. 347, 1110-1111.
25. Anderl, J. N., M. J. Franklin, and, P. S. Stewart, (2000) Role of antibiotic penetration limitation in Klebsiella Pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44, 1818-1824.
26. George, S., and, A. Kishen, (2008) Augmenting the antibiofilm efficacy of advanced noninvasive light activated disinfection with emulsified oxidizer and oxygen carrier. J. Endod. 34, 1119-1123.
27. Fimple, J. L., C. R. Fontana, F. Foschi, K. Ruggiero, X. Song, T. C. Pagonis, A. C. Tanner, R. Kent, A. G. Doukas, P. P. Stashenko, and, N. S. Soukos, (2008) Photodynamic treatment of endodontic polymicrobial infection in vitro. J. Endod. 34, 728-734.
28. Soukos, N. S., P. S. Chen, J. T. Morris, K. Ruggiero, A. D. Abernethy, S. Som, F. Foschi, S. Doucette, L. L. Bammann, C. R. Fontana, A. G. Doukas, and, P. P. Stashenko, (2006) Photodynamic therapy for endodontic disinfection. J. Endod. 32, 979-984.
29. Garcez, A. S., M. S. Ribeiro, G. P. Tegos, S. C. Núñez, A. O. Jorge, and, M. R. Hamblin, (2007) Antimicrobial photodynamic therapy combined with conventional endodontic treatment to eliminate root canal biofilm infection. Lasers Surg. Med. 39, 59-66.
30. Fernández-Guerrero, M. L., L. Herrero, M. Bellver, I. Gadea, R. F. Roblas, and, M. De Górgolas, (2002) Nosocomial enterococcal endocarditis: A serious hazard for hospitalized patients with enterococcal bacteraemia. J. Intern. Med. 252, 510-515.
31. Karmarkar, M. G., E. S. Gershom, and, P. R. Mehta, (2004) Enterococcal infections with special reference to phenotypic characterization & drug resistance. Indian J. Med. Res. 119, 22-25.
32. Sandoe, J. A., I. R. Witherden, J. H. Cove, J. Heritage, and, M. H. Wilcox, (2003) Correlation between enterococcal biofilm formation in vitro and medical-device-related infection potential in vivo. J. Med. Microbiol. 52, 547-550.
33. Huycke, M. M., D. F. Sahm, and, M. S. Gilmore, (1998) Multiple-drug resistant enterococci: The nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4, 239-249.
34. Toledo-Arana, A., J. Valle, C. Solano, M. J. Arrizubieta, C. Cucarella, M. Lamata, B. Amorena, J. Leiva, J. R. Penadés, and, I. Lasa, (2001) The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Appl. Environ. Microbiol. 67, 4538-4545. (Pubitemid 33646082)
35. Mohamed, J. A., W. Huang, S. R. Nallapareddy, F. Teng, and, B. E. Murray, (2004) Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 72, 3658-3663.
36. Tendolkar, P. M., A. S. Baghdayan, M. S. Gilmore, and, N. Shankar, (2004) Enterococcal surface protein, Esp, enhances biofilm formation by Enterococcus faecalis. Infect. Immun. 72, 6032-6039.
37. Hancock, L. E., and, M. Perego, (2004) The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186, 5629-5639.
38. Pillai, S. K., G. Sakoulas, G. M. Eliopoulos, R. C. Moellering Jr, B. E. Murray, and, R. T. Inouye, (2004) Effects of glucose on fsr-mediated biofilm formation in Enterococcus faecalis. J. Infect. Dis. 190, 967-970.
39. Kristich, C. J., Y. H. Li, D. G. Cvitkovitch, and, G. M. Dunny, (2004) Esp-independent biofilm formation by Enterococcus faecalis. J. Bacteriol. 186, 154-163.
40. Molander, A., C. Reit, G. Dahlen, and, T. Kvist, (1998) Microbiological status of root-filled teeth with apical periodontitis. Int. Endod. J. 31, 1-7.
41. Dahlen, G., W. Samuelsson, A. Molander, and, C. Reit, (2000) Identification and antimicrobial susceptibility of enterococci isolated from the root canal. Oral Microbiol. Immunol. 15, 309-312.
42. Portenier, I., M. T. Tuomos, T. Waltimo, and, M. Haapasalo, (2003) Enterococcus faecalis-The root canal survivor and "star" in post-treatment disease. Endod. Top. 6, 135.
43. Jett, B. D., K. L. Hatter, M. M. Huycke, and, M. S. Gilmore, (1997) Simplified agar plate method for quantifying viable bacteria. BioTechniques 23, 648-650.
44. Thrower, Y., R. J. Pinney, and, M. Wilson, (1997) Susceptibilities of Actinobacillus actinomycetemcomitans biofilms to oral antiseptics. J. Med. Microbiol. 46, 425-429.
45. Wilson, M., (1996) Susceptibility of oral bacterial biofilms to antimicrobial agents. J. Med. Microbiol. 44, 79-87.
46. Desai, M., T. Bühler, P. H. Weller, and, M. R. Brown, (1998) Increasing resistance of planktonic and biofilm cultures of Burkholderia cepacia to ciprofloxacin and ceftazidime during exponential growth. J. Antimicrob. Chemother. 42, 153-160.
47. Dunne W. Jr.M., E. O. Mason Jr, and, S. L. Kaplan, (1993) Diffusion of rifampin and vancomycin through a Staphylococcus epidermidis biofilm. Antimicrob. Agents Chemother. 37, 2522-2526.
48. Kvist, M., V. Hancock, and, P. Klemm, (2008) Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl. Environ. Microbiol. 74, 7376-7382.
49. Zhang, L., and, T. F. Mah, (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J. Bacteriol. 190, 4447-4452.
50. Jonas, B. M., B. E. Murray, and, G. M. Weinstock, (2001) Characterization of emeA, a NorA homolog and multidrug resistance efflux pump, in Enterococcus faecalis. Antimicrob. Agents Chemother. 45, 3574-3579.
51. Higgins, C. F., (1992) ABC transporters: From microorganisms to man. Annu. Rev. Cell Biol. 8, 67-113.
52. Safa, A. R., (1988) Photoaffinity labeling of the multidrug-resistance- related P-glycoprotein with photoactive analogs of verapamil. Proc. Natl Acad. Sci. USA 85, 7187-7191.