Paradoxical potentiation of methylene blue-mediated antimicrobial photodynamic inactivation by sodium azide: Role of ambient oxygen and azide radicals

Free Radical Biology and Medicine

Volumn 53, Issue 11, 2012, Pages 2062-2071

  Huang, Liyi ^a,b,c   St Denis, Tyler G ^b,d   Xuan, Yi ^b,e   Huang, Ying Ying ^a,b,c   Tanaka, Masamitsu ^a,b,c   Zadlo, Andrzej ^f   Sarna, Tadeusz ^f   Hamblin, Michael R ^b,c,g,h  

^a GUANGXI MEDICAL UNIVERSITY   (China)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Howard Hughes Medical Institute   (United States)

^e Tufts University   (United States)

^f NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^g JAGIELLONIAN UNIVERSITY   (Poland)

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

Author keywords

Antimicrobial photodynamic therapy (APDT); Azidyl radical; Hydroxyl radical; Single oxygen; Sodium azide

Indexed keywords

CHLORINE; FERROUS SULFATE; HYDROGEN PEROXIDE; HYPOCHLORITE SODIUM; METHYLENE BLUE; OXYGEN; POLYETHYLENEIMINE; SINGLET OXYGEN; SODIUM AZIDE;

ANTIMICROBIAL PHOTODYNAMIC THERAPY; ARTICLE; BACTERICIDAL ACTIVITY; CONJUGATE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ESCHERICHIA COLI; FENTON REACTION; ILLUMINATION; INCUBATION TIME; NONHUMAN; OXIDATION; PHOTODYNAMIC THERAPY; PHOTOSENSITIZATION; PRIORITY JOURNAL; RED LIGHT; SPIN TRAPPING; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; DRUG SYNERGISM; ESCHERICHIA COLI; FREE RADICALS; HYDROGEN PEROXIDE; IRON; METHYLENE BLUE; MICROBIAL VIABILITY; OXIDATION-REDUCTION; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; REACTIVE OXYGEN SPECIES; SODIUM AZIDE; SODIUM HYPOCHLORITE; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 84868631091     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.09.006     Document Type: Article

References (63)

1. McGowan, J.E., Jr. Resistance in nonfermenting gram-negative bacteria: multidrug resistance to the maximum. Am. J. Med. 119:S29-S36;discussion S62-S70; 2006.
2. L.C. McDonald Trends in antimicrobial resistance in health care-associated pathogens and effect on treatment Clin. Infect. Dis 42 Suppl. 2 2006 S65 S71
3. T.D. Drews, J.L. Temte, and B.C. Fox Community-associated methicillin-resistant Staphylococcus aureus: review of an emerging public health concern WMJ 105 2006 52 57
4. S.G. Bell Antibiotic resistance: is the end of an era near? Neonatal Netw 22 2003 47 54
5. J.W. Harrison, and T.A. Svec The beginning of the end of the antibiotic era? Part II. Proposed solutions to antibiotic abuse Quintessence Int 29 1998 223 229
6. D. Nathwani, and G.S. Tillotson Vancomycin for Staphylococcus aureus therapy of respiratory tract infections: the end of an era? Int. J. Antimicrob. Agents 21 2003 521 524
7. T.T. Yoshikawa Antimicrobial resistance and aging: beginning of the end of the antibiotic era? J. Am. Geriatr. Soc. 50 2002 S226 S229
8. M.D. Poole Are we facing the end of the antibiotic era? Ear Nose Throat J 72 1993 433
9. R. Kenawy el, S.D. Worley, and R. Broughton The chemistry and applications of antimicrobial polymers: a state-of-the-art review Biomacromolecules 8 2007 1359 1384
10. M.R. Hamblin, and G. Jori Photodynamic inactivation of microbial pathogens: medical and environmental applications 2011 RSC Publishing Cambridge
11. M.R. Hamblin, and T. Hasan Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem. Photobiol. Sci. 3 2004 436 450
12. Z. Malik, H. Ladan, and Y. Nitzan Photodynamic inactivation of gram-negative bacteria: problems and possible solutions J. Photochem. Photobiol. B 14 1992 262 266
13. A. Minnock, D.I. Vernon, J. Schofield, J. Griffiths, J.H. Parish, and S.B. Brown Mechanism of uptake of a cationic water-soluble pyridinium zinc phthalocyanine across the outer membrane of Escherichia coli Antimicrob. Agents Chemother. 44 2000 522 527
14. R.E. Hancock, S.W. Farmer, Z.S. Li, and K. Poole Interaction of aminoglycosides with the outer membranes and purified lipopolysaccharide and OmpF porin of Escherichia coli Antimicrob. Agents Chemother. 35 1991 1309 1314
15. L. Huang, Y.Y. Huang, P. Mroz, G.P. Tegos, T. Zhiyentayev, S.K. Sharma, Z. Lu, T. Balasubramanian, M. Krayer, C. Ruzie, E. Yang, H.L. Kee, C. Kirmaier, J.R. Diers, D.F. Bocian, D. Holten, J.S. Lindsey, and M.R. Hamblin Stable synthetic cationic bacteriochlorins as selective antimicrobial photosensitizers Antimicrob. Agents Chemother. 54 2010 3834 3841
16. L. Huang, M. Terakawa, T. Zhiyentayev, Y.Y. Huang, Y. Sawayama, A. Jahnke, G.P. Tegos, T. Wharton, and M.R. Hamblin Innovative cationic fullerenes as broad-spectrum light-activated antimicrobials Nanomedicine 6 2010 442 452
17. G.P. Tegos, T.N. Demidova, D. Arcila-Lopez, H. Lee, T. Wharton, H. Gali, and M.R. Hamblin Cationic fullerenes are effective and selective antimicrobial photosensitizers Chem. Biol. 12 2005 1127 1135
18. S.P. Denyer, and J.Y. Maillard Cellular impermeability and uptake of biocides and antibiotics in gram-negative bacteria J. Appl. Microbiol. 92 Suppl 2002 35S 45S
19. H. Nikaido Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria Semin. Cell Dev. Biol 12 2001 215 223
20. H. Nikaido Molecular basics of bacterial outer membrane permeability revisited Microbiol. Mol. Biol. Rev. 2003 593 656
21. H.L. Alakomi, A. Paananen, M.L. Suihko, I.M. Helander, and M. Saarela Weakening effect of cell permeabilizers on gram-negative bacteria causing biodeterioration Appl. Environ. Microbiol. 72 2006 4695 4703
22. I.M. Helander, H.L. Alakomi, K. Latva-Kala, and P. Koski Polyethyleneimine is an effective permeabilizer of gram-negative bacteria Microbiology 143 Pt 10 1997 3193 3199
23. I.M. Helander, K. Latva-Kala, and K. Lounatmaa Permeabilizing action of polyethyleneimine on Salmonella typhimurium involves disruption of the outer membrane and interactions with lipopolysaccharide Microbiology 144 Pt 2 1998 385 390
24. G.A. Kostenich, I.N. Zhuravkin, and E.A. Zhavrid Experimental grounds for using chlorin e6 in the photodynamic therapy of malignant tumors J. Photochem. Photobiol. B 22 1994 211 217
25. M.R. Hamblin, D.A. O'Donnell, N. Murthy, K. Rajagopalan, N. Michaud, M.E. Sherwood, and T. Hasan Polycationic photosensitizer conjugates: effects of chain length and gram classification on the photodynamic inactivation of bacteria J. Antimicrob. Chemother. 49 2002 941 951
26. N.S. Soukos, L.A. Ximenez-Fyvie, M.R. Hamblin, S.S. Socransky, and T. Hasan Targeted antimicrobial photochemotherapy Antimicrob. Agents Chemother. 42 1998 2595 2601
27. G.P. Tegos, M. Anbe, C. Yang, T.N. Demidova, M. Satti, P. Mroz, S. Janjua, F. Gad, and M.R. Hamblin Protease-stable polycationic photosensitizer conjugates between polyethyleneimine and chlorin(e6) for broad-spectrum antimicrobial photoinactivation Antimicrob. Agents Chemother. 50 2006 1402 1410
28. T.N. Demidova, and M.R. Hamblin Effect of cell-photosensitizer binding and cell density on microbial photoinactivation Antimicrob. Agents Chemother. 49 2005 2329 2335
29. F. Gad, T. Zahra, T. Hasan, and M.R. Hamblin Effects of growth phase and extracellular slime on photodynamic inactivation of gram-positive pathogenic bacteria Antimicrob. Agents Chemother. 48 2004 2173 2178
30. T. Dai, G.P. Tegos, Z. Lu, L. Huang, T. Zhiyentayev, M.J. Franklin, D.G. Baer, and M.R. Hamblin Photodynamic therapy for Acinetobacter baumannii burn infections in mice Antimicrob. Agents Chemother. 53 2009 3929 3934
31. M.R. Hamblin, D.A. O'Donnell, N. Murthy, C.H. Contag, and T. Hasan Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging Photochem. Photobiol. 75 2002 51 57
32. M.R. Hamblin, T. Zahra, C.H. Contag, A.T. McManus, and T. Hasan Optical monitoring and treatment of potentially lethal wound infections in vivo J. Infect. Dis. 187 2003 1717 1725
33. L. Huang, Y. Xuan, Y. Koide, T. Zhiyentayev, M. Tanaka, M.R. Hamblin, and I. Type and Type II mechanisms of antimicrobial photodynamic therapy: an in vitro study on gram-negative and gram-positive bacteria Lasers Surg. Med. 44 2012 490 499
34. S. Sabbahi, Z. Alouini, M. Jemli, and A. Boudabbous The role of reactive oxygen species in Staphylococcus aureus photoinactivation by methylene blue Water Sci. Technol. 58 2008 1047 1054
35. Y. Harada, K. Suzuki, M. Hashimoto, K. Tsukagoshi, and H. Kimoto Chemiluminescence from singlet oxygen that was detected at two wavelengths and effects of biomolecules on it Talanta 77 2009 1223 1227
36. K. Tsukagoshi, K. Fukumoto, K. Noda, R. Nakajima, K. Yamashita, and H. Maeda Chemiluminescence from singlet oxygen under laminar flow condition in a micro-channel Anal. Chim. Acta 570 2006 202 206
37. C. Merli, E. Petrucci, A. Da Pozzo, and M. Pernetti Fenton-type treatment: state of the art Ann. Chim 93 2003 761 770
38. 2) by azide anion in solvent mixtures Photochem. Photobiol. 74 2001 760 764
39. A. Tavares, S.R. Dias, C.M. Carvalho, M.A. Faustino, J.P. Tome, M.G. Neves, A.C. Tome, J.A. Cavaleiro, A. Cunha, N.C. Gomes, E. Alves, and A. Almeida Mechanisms of photodynamic inactivation of a gram-negative recombinant bioluminescent bacterium by cationic porphyrins Photochem. Photobiol. Sci. 10 2011 1659 1669
40. G.R. Buettner, and R.P. Mason Spin-trapping methods for detecting superoxide and hydroxyl free radicals in vitro and in vivo Methods Enzymol 186 1990 127 133
41. P. Mroz, A. Pawlak, M. Satti, H. Lee, T. Wharton, H. Gali, T. Sarna, and M.R. Hamblin Functionalized fullerenes mediate photodynamic killing of cancer cells: type I versus type II photochemical mechanism Free Radic. Biol. Med. 43 2007 711 719
42. Y. Vakrat-Haglili, L. Weiner, V. Brumfeld, A. Brandis, Y. Salomon, B. McLlroy, B.C. Wilson, A. Pawlak, M. Rozanowska, T. Sarna, and A. Scherz The microenvironment effect on the generation of reactive oxygen species by Pd-bacteriopheophorbide J. Am. Chem. Soc. 127 2005 6487 6497
43. Y. Noda, and M. Mankura Inhibitory effect of antioxidants on hydroxyl radical generation from methylguanidine: an ESR study Neurochem. Res. 34 2009 734 738
44. A. Keszler, B. Kalyanaraman, and N. Hogg Comparative investigation of superoxide trapping by cyclic nitrone spin traps: the use of singular value decomposition and multiple linear regression analysis Free Radic. Biol. Med 35 2003 1149 1157
45. 2 peroxidizing systems J. Biol. Chem. 260 1985 4003 4006
46. S.L. Hempel, G.R. Buettner, D.A. Wessels, G.M. Galvan, and Y.Q. O'Malley Extracellular iron (II) can protect cells from hydrogen peroxide Arch. Biochem. Biophys. 330 1996 401 408
47. G.V. Buxton, C.L. Greenstock, W.P. Helman, and A.B. Ross Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (. OH/. O-) in aqueous solution J. Phys. Chem. Ref. Data 17 1988 513 534
48. G.R. Buettner, and R.D. Hall Superoxide, hydrogen peroxide and singlet oxygen in hematoporphyrin derivative-cysteine, -NADH and -light systems Biochim. Biophys. Acta 923 1987 501 507
49. T. Sarna Properties and function of the ocular melanin - a photobiophysical view J. Photochem. Photobiol. B 12 1992 215 258
50. J.A. Farrington, and E.J. Land Swallow, A. J. The one-electron reduction potentials of NAD Biochim. Biophys. Acta 590 1980 273 276
51. E.J. Land Swallow, A. J. One-electron reactions in biochemical systems as studied by pulse radiolysis. V. Cytochrome c Arch. Biochem. Biophys. 145 1971 365 372
52. T. Ohno, and N.N. Lichtin Electron transfer in the quenching of triplet methylene blue by complexes of iron(II) J. Am. Chem. Soc. 102 1980 4636 4643
53. G.G. Carvalho, M.P. Felipe, and M.S. Costa The photodynamic effect of methylene blue and toluidine blue on Candida albicans is dependent on medium conditions J. Microbiol. 47 2009 619 623
54. T. Maisch, C. Bosl, R.M. Szeimies, N. Lehn, and C. Abels Photodynamic effects of novel XF porphyrin derivatives on prokaryotic and eukaryotic cells Antimicrob. Agents Chemother. 49 2005 1542 1552
55. B. Bose, and A. Dube Photodynamic efficacy of chlorin p6: a pH dependent study in aqueous and lipid environment J. Photochem. Photobiol. B 93 2008 32 35
56. A.M. Sugar, R.S. Chahal, E. Brummer, and D.A. Stevens The iron-hydrogen peroxide-iodide system is fungicidal: activity against the yeast phase of Blastomyces dermatitidis J. Leukoc. Biol. 36 1984 545 548
57. Z. Alfassi, A. Harriman, R. Huie, S. Mosseri, and P. Neta The redox potential of the azide/azidyl couple J. Phys. Chem. 91 1987 2120 2122
58. X. Shen, J. Lind, and G. Merenyi One-electron oxidation of indoles and acid-base properties of the indoyl radicals J. Phys. Chem. 91 1987 4403 4406
59. G. Bottu The effect of quenchers on the chemiluminescence of luminol and lucigenin J. Biolumin. Chemilumin 3 1989 59 65
60. P. Wardman Reduction potentialsof one-electron couples involving free radicals in aqueous solution J. Phys. Chem. Ref. Data 18 1989 1639 1755
61. P.B. Roberts Enhanced radiation damage to the erythrocyte membrane in the presence of azide and other anions Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med 35 1979 561 570
62. E.J. Land, and W.A. Prutz Reaction of azide radicals with amino acids and proteins Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med 36 1979 75 83
63. I. Ali, N. Sakhnini, and I. Naseem Hemolysis of human red blood cells by riboflavin-Cu(II) system: enhancement by azide Biochemistry (Mosc.) 70 2005 1011 1014