Photodynamic inactivation of Bacillus spores, mediated by phenothiazinium dyes

Applied and Environmental Microbiology

Volumn 71, Issue 11, 2005, Pages 6918-6925

  Demidova, Tatiana N ^a,b   Hamblin, Michael R ^a,c,d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DYES; PORPHYRINS; TISSUE; TOXICITY;

BACILLUS CEREUS; PHOTODYNAMIC INACTIVATION; VEGETATIVE BACTERIA;

BACTERIA;

1,9 DIMETHYLMETHYLENE BLUE; ANTIINFECTIVE AGENT; BACTERIAL DNA; BENZOPORPHYRIN DERIVATIVE; DYE; METHYLENE BLUE; PHENOTHIAZINE DERIVATIVE; PHOTOSENSITIZING AGENT; POLYLYSINE; PORPHYRIN DERIVATIVE; ROSE BENGAL; TALAPORFIN; TOLONIUM CHLORIDE; UNCLASSIFIED DRUG;

BACTERIUM;

ANTHRAX; ARTICLE; BACILLUS ATROPHAEUS; BACILLUS CEREUS; BACILLUS MEGATERIUM; BACILLUS SUBTILIS; BACILLUS THURINGIENSIS; BACTERIAL MEMBRANE; BACTERIAL SPORE; CELL KILLING; CONCENTRATION RESPONSE; HEAT TOLERANCE; NONHUMAN; PHOTODYNAMICS; RADIOSENSITIVITY; RED LIGHT; SPOROGENESIS; STARVATION; STRESS; SURVIVAL; WOUND INFECTION;

BACILLUS; COLORING AGENTS; LIGHT; METHYLENE BLUE; MICROBIAL SENSITIVITY TESTS; PHENOTHIAZINES; PHOTOSENSITIZING AGENTS; SPORES, BACTERIAL; TOLONIUM CHLORIDE;

BACILLUS (BACTERIUM); BACILLUS ATROPHAEUS; BACILLUS CEREUS; BACILLUS MEGATERIUM; BACILLUS SUBTILIS; BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS);

EID: 32044433726     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.71.11.6918-6925.2005     Document Type: Article

References (61)

1. Akesson, A., S. A. Hedstrom, and T. Ripa. 1991. Bacillus cereus: a significant pathogen in postoperative and post-traumatic wounds on orthopaedic wards. Scand. J. Infect. Dis. 23:71-77.
2. Bakri, S. J., and P. K. Kaiser. 2004. Verteporfin ocular photodynamic therapy. Exp. Opin. Pharmacother. 5:195-203.
3. Burke, S. A., J. D. Wright, M. K. Robinson, B. V. Bronk, and R. L. Warren. 2004. Detection of molecular diversity in Bacillus atrophaeus by amplified fragment length polymorphism analysis. Appl. Environ. Microbiol. 70:2786-2790.
4. Caipo, M. L., S. Duffy, L. Zhao, and D. W. Schaffner. 2002. Bacillus megaterium spore germination is influenced by inoculum size. J. Appl. Microbiol. 92:879-884.
5. Carlin, F., H. Girardin, M. W. Peck, S. C. Stringer, G. C. Barker, A. Martinez, A. Fernandez, P. Fernandez, W. M. Waites, S. Movahedi, F. van Leusden, M. Nauta, R. Moezelaar, M. D. Torre, and S. Litman. 2000. Research on factors allowing a risk assessment of spore-forming pathogenic bacteria in cooked chilled foods containing vegetables: a FAIR collaborative project. Int. J. Food Microbiol. 60:117-135.
6. Cassell, G. H., and J. Mekalanos. 2001. Development of antimicrobial agents in the era of new and reemerging infectious diseases and increasing antibiotic resistance. JAMA 285:601-605.
7. Demidova, T. N., and M. R. Hamblin. 2005. Microbial photoinactivation: effect of cell-photosensitizer binding and cell density. Antimicrob. Agents Chemother. 49:2329-2335.
8. Demidova, T. N., and M. R. Hamblin. 2004. Photodynamic therapy targeted to pathogens. Int. J. Immunopathol. Pharmacol. 17:245-254.
9. Dolmans, D. E., D. Fukumura, and R. K. Jain. 2003. Photodynamic therapy for cancer. Nat. Rev. Cancer 3:380-387.
10. Dougherty, T. J. 2002. An update on photodynamic therapy applications. J. Clin. Laser Med. Surg. 20:3-7.
11. Dougherty, T. J., C. J. Corner, B. W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan, and Q. Peng. 1998. Photodynamic therapy. J. Natl. Cancer Inst. 90:889-905.
12. Dull, P. M., K. E. Wilson, B. Kournikakis, E. A. Whitney, C. A. Boulet, J. Y. Ho, J. Ogston, M. R. Spence, M. M. McKenzie, M. A. Phelan, T. Popovic, and D. Ashford. 2002. Bacillus anthracis aerosolization associated with a contaminated mail sorting machine. Emerg. Infect. Dis. 8:1044-1047.
13. Genest, P. C., B. Setlow, E. Melly, and P. Setlow. 2002. Killing of spores of Bacillus subtilis by peroxynitrite appears to be caused by membrane damage. Microbiology 148:307-314.
14. Gerhardt, P., and S. H. Black. 1961. Permeability of bacterial spores. II. Molecular variables affecting solute permeation. J. Bacteriol. 82:750-760.
15. Gerhardt, P., and E. Ribi. 1964. Ultrastructure of the exosporium enveloping spores of Bacillus cereus. J. Bacteriol. 88:1774-1789.
16. Hamblin, M. R., and T. Hasan. 2004. Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem. Photobiol. Sci. 3:436-450.
17. Hamblin, M. R., D. A. O'Donnell, N. Murthy, C. H. Contag, and T. Hasan. 2002. Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging. Photochem. Photobiol. 75: 51-57.
18. Hamblin, M. R., D. A. O'Donnell, N. Murthy, K. Rajagopalan, N. Michaud, M. E. Sherwood, and T. Hasan. 2002. Polycationic photosensitizer conjugates: effects of chain length and Gram classification on the photodynamic inactivation of bacteria. J. Antimicrob. Chemother. 49:941-951.
19. Hamblin, M. R., T. Zahra, C. H. Contag, A. T. McManus, and T. Hasan. 2003. Optical monitoring and treatment of potentially lethal wound infections in vivo. J. Infect. Dis. 187:1717-1726.
20. Hamouda, T., A. Y. Shih, and J. R. Baker, Jr. 2002. A rapid staining technique for the detection of the initiation of germination of bacterial spores. Lett. Appl. Microbiol. 34:86-90.
21. Hansen, B. M., T. D. Leser, and N. B. Hendriksen. 2001. Polymerase chain reaction assay for the detection of Bacillus cereus group cells. FEMS Microbiol. Lett. 202:209-213.
22. Helgason, E., O. A. Okstad, D. A. Caugant, H. A. Johansen, A. Fouet, M. Mock, I. Hegna, and Kolsto. 2000. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis: one species on the basis of genetic evidence. Appl. Environ. Microbiol. 66:2627-2630.
23. Hoffmaster, A. R., J. Ravel, D. A. Rasko, G. D. Chapman, M. D. Chute, C. K. Marston, B. K. De, C. T. Sacchi, C. Fitzgerald, L. W. Mayer, M. C. Maiden, F. G. Priest, M. Barker, L. Jiang, R. Z. Cer, J. Rilstone, S. N. Peterson, R. S. Weyant, D. R. Galloway, T. D. Read, T. Popovic, and C. M. Fraser. 2004. Identification of anthrax toxin genes in a Bacillus cereus associated with an illness resembling inhalation anthrax. Proc. Natl. Acad. Sci. USA 101:8449-8454.
24. 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.
25. Koshikawa, T., T. C. Beaman, H. S. Pankratz, S. Nakashio, T. R. Corner, and P. Gerhardt. 1984. Resistance, germination, and permeability correlates of Bacillus megaterium spores successively divested of integument layers. J. Bacteriol. 159:624-632.
26. La Duc, M. T., M. Satomi, N. Agata, and K. Venkateswaran. 2004. gyrB as a phylogenetic discriminator for members of the Bacillus anthracis-cereus- thuringiensis group. J. Microbiol. Methods 56:383-394.
27. Lambrechts, S. A., M. C. Aalders, D. H. Langeveld-Klerks, Y. Khayali, and J. W. Lagerberg. 2004. Effect of monovalent and divalent cations on the photoinactivation of bacteria with meso-substituted cationic porphyrins. Photochem. Photobiol. 79:297-302.
28. Lauro, F. M., P. Pretto, L. Covolo, G. Jori, and G. Bertoloni. 2002. Photo-inactivation of bacterial strains involved in periodontal diseases sensitized by porphycene-polylysine conjugates. Photochem. Photobiol. Sci. 1:468-470.
29. Melly, E., A. E. Cowan, and P. Setlow. 2002. Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. J. Appl. Microbiol. 93:316-325.
30. Menezes, S., M. A. Capella, and L. R. Caldas. 1990. Photodynamic action of methylene blue: repair and mutation in Escherichia coli. J. Photochem. Photobiol. B 5:505-517.
31. Mock, M., and A. Fouet. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671.
32. Nicholson, W. L., and P. Setlow. 1990. Dramatic increase in negative super-helicity of plasmid DNA in the forespore compartment of sporulating cells of Bacillus subtilis. J. Bacteriol. 172:7-14.
33. Nishihara, T., Y. Takubo, E. Kawamata, T. Koshikawa, J. Ogaki, and M. Kondo. 1989. Role of outer coat in resistance of Bacillus megaterium spore. J. Biochem. (Tokyo) 106:270-273.
34. O'Neill, J., M. Wilson, and M. Wainwright. 2003. Comparative antistreptococcal activity of photobactericidal agents. J. Chemother. 15:329-334.
35. Palop, A., G. C. Rutherford, and R. E. Marquis. 1998. Inactivation of enzymes within spores of Bacillus megaterium ATCC 19213 by hydroperoxides. Can. J. Microbiol. 44:465-470.
36. Phoenix, D. A., Z. Sayed, S. Hussain, F. Harris, and M. Wainwright. 2003. The phototoxicity of phenothiazinium derivatives against Escherichia coli and Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 39:17-22.
37. Russell, A. D. 1990. Bacterial spores and chemical sporicidal agents. Clin. Microbiol. Rev. 3:99-119.
38. Russell, A. D. 2003. Similarities and differences in the responses of microorganisms to biocides. J. Antimicrob. Chemother. 52:750-763.
39. Sagripanti, J. L., and A. Bonifacino. 1996. Comparative sporicidal effects of liquid chemical agents. Appl. Environ. Microbiol. 62:545-551.
40. Schafer, M., C. Schmitz, R. Facius, G. Horneck, B. Milow, K. H. Funken, and J. Ortner. 2000. Systematic study of parameters influencing the action of Rose Bengal with visible light on bacterial cells: comparison between the biological effect and singlet-oxygen production. Photochem. Photobiol. 71: 514-523.
41. Setlow, P. 2000. Resistance of bacterial spores, p. 217-230. In G. Storz and R. Hengge-Aronis (ed.), Bacterial stress responses. ASM Press, Washington, D.C.
42. 2 and ascorbic acid. Appl. Environ. Microbiol. 70:2535-2539.
43. Smijs, T. G., and H. J. Schuitmaker. 2003. Photodynamic inactivation of the dermatophyte Trichophyton rubrum. Photochem. Photobiol. 77:556-560.
44. Soukos, N. S., L. A. Ximenez-Fyvie, M. R. Hamblin, S. S. Socransky, and T. Hasan. 1998. Targeted antimicrobial photochemotherapy. Antimicrob. Agents Chemother. 42:2595-2601.
45. Sudakin, D. L. 2003. Biopesticides. Toxicol. Rev. 22:83-90.
46. Teichert, M. C., J. W. Jones, M. N. Usacheva, and M. A. Biel. 2002. Treatment of oral candidiasis with methylene blue-mediated photodynamic therapy in an immunodeficient murine model. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 93:155-160.
47. Trannoy, L. L., J. W. Lagerberg, T. M. Dubbelman, H. J. Schuitmaker, and A. Brand. 2004. Positively charged porphyrins: a new series of photosensitizers for sterilization of RBCs. Transfusion 44:1186-1196.
48. Usacheva, M. N., M. C. Teichert, and M. A. Biel. 2001. Comparison of the methylene blue and toluidine blue photobactericidal efficacy against gram-positive and gram-negative microorganisms. Lasers Surg. Med. 29:165-173.
49. Usacheva, M. N., M. C. Teichert, and M. A. Biel. 2003. The interaction of lipopolysaccharides with phenothiazine dyes. Lasers Surg. Med. 33:311-319.
50. Usacheva, M. N., M. C. Teichert, and M. A. Biel. 2003. The role of the methylene blue and toluidine blue monomers and dimers in the photoinactivation of bacteria. J. Photochem. Photobiol. B 71:87-98.
51. Wainwright, M. 1998. Photodynamic antimicrobial chemotherapy (PACT). J. Antimicrob. Chemother. 42:13-28.
52. 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.
53. Wainwright, M., D. A. Phoenix, J. Marland, D. R. Wareing, and F. J. Bolton. 1997. A study of photobactericidal activity in the phenothiazinium series. FEMS Immunol. Med. Microbiol. 19:75-80.
54. Wainwright, M., D. A. Phoenix, T. E. Smillie, and D. R. Wareing. 2001. Phenothiaziniums as putative photobactericidal agents for red blood cell concentrates. J. Chemother. 13:503-509.
55. Whitney, E. S., M. E. Beatty, T. H. Taylor, Jr., R. Weyant, J. Sobel, M. J. Arduino, and D. A. Ashford. 2003. Inactivation of Bacillus anthracis spores. Emerg. Infect. Dis. 9:623-627.
56. Wiencek, K. M., N. A. Klapes, and P. M. Foegeding. 1990. Hydrophobicity of Bacillus and Clostridium spores. Appl. Environ. Microbiol. 56:2600-2605.
57. Wilson, M. 1994. Bactericidal effect of laser light and its potential use in the treatment of plaque-related diseases. Int. Dent. J. 44:181-189.
58. Wilson, M., and C. Yianni. 1995. Killing of methicillin-resistant Staphylococcus aureus by low-power laser light. J. Med. Microbiol. 42:62-66.
59. Yoshikawa, T. T. 2002. Antimicrobial resistance and aging: beginning of the end of the antibiotic era? J. Am. Geriatr. Soc. 50:S226-S229.
60. Young, S. B., and P. Setlow. 2004. Mechanisms of Bacillus subtilis spore resistance to and killing by aqueous ozone. J. Appl. Microbiol. 96:1133-1142.
61. 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.