Antimicrobial photodynamic therapy with decacationic monoadducts and bisadducts of [70]fullerene: In vitro and in vivo studies

Nanomedicine

Volumn 9, Issue 2, 2014, Pages 253-266

  Huang, Liyi ^a,b,c   Wang, Min ^d   Dai, Tianhong ^b,c   Sperandio, Felipe F ^b,e   Huang, Ying Ying ^a,b,c   Xuan, Yi ^b,f   Chiang, Long Y ^d   Hamblin, Michael R ^b,c,g  

^a GUANGXI MEDICAL UNIVERSITY   (China)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d University of Massachusetts Lowell   (United States)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f TUFTS UNIVERSITY   (United States)

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

Author keywords

Antimicrobial photodynamic therapy; Bioluminescence imaging; Deca(tertiaryamino)malonate arm; Hydroxyl radical; Mouse model of burn infection; Singlet oxygen

Indexed keywords

CARBON; FLUORESCEIN; FULLERENE DERIVATIVE; HYDROXYL RADICAL; IODIDE; QUATERNARY AMMONIUM DERIVATIVE; REACTIVE OXYGEN METABOLITE; SINGLET OXYGEN; UNCLASSIFIED DRUG; WATER; [70]FULLERENE;

ABSORPTION SPECTROSCOPY; ACINETOBACTER BAUMANNII; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMICROBIAL THERAPY; ARTICLE; BIOLUMINESCENCE; BURN INFECTION; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; ESCHERICHIA COLI; FEMALE; FOLLOW UP; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; QUANTUM YIELD; SOLUBILITY; STAPHYLOCOCCUS AUREUS; ULTRAVIOLET A RADIATION; WHITE LIGHT;

ACINETOBACTER BAUMANNII; ANIMALS; ANTI-INFECTIVE AGENTS; ESCHERICHIA COLI; FEMALE; FLUORESCENT DYES; FULLERENES; MICE; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; PHOTOCHEMOTHERAPY; REACTIVE OXYGEN SPECIES;

EID: 84896703452     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.13.22     Document Type: Article

References (55)

1. Hamblin MR, Jori G. Photodynamic Inactivation of Microbial Pathogens: Medical and Environmental Applications. RSC Publishing, Cambridge, UK (2011).
2. Hamblin MR, Hasan T. Photodynamic therapy: A new antimicrobial approach to infectious d isease Photochem. Photobiol. Sci. 3(5), 436-450 (2004).
3. Hamblin MR, Mroz P. Advances in Photodynamic Therapy: Basic, Translational and Clinical. Artech House, Norwood, MA, USA (2008).
4. Costa L, Faustino MA, Neves MG, Cunha A, Almeida A. Photodynamic inactivation of mammalian viruses and bacteriophages. Viruses 4(7), 1034-1074 (2012).
5. Calzavara-Pinton P, Rossi MT, Sala R, Venturini M. Photodynamic antifungal chemotherapy. Photochem. Photobiol. 88(3), 512-522 (2012).
6. Baptista MS, Wainwright M. Photodynamic antimicrobial chemotherapy (PACT) for the treatm ent of malaria, leishmaniasis and trypanosomiasis. Braz. J. Med. Biol. Res. 44(1), 1-10 (2011).
7. Nordmann P, Poirel L, Toleman MA, Walsh TR. Does broad-spectrum b-lactam resistance due to NDM-1 herald the end of the antibiotic era for treatment of infections caused by Gram-negative bacteria J. Antimicrob. Chemother. 66(4), 689-692 (2011).
8. Yoshikawa TT. Antimicrobial resistance and aging: Beginning of the end of the antibiotic era J. Am. Geriatr. Soc. 50(Suppl. 7), S226-S229 (2002).
9. Bell SG. Antibiotic resistance: Is the end of an era near Neonatal Netw. 22(6), 47-54 (2003).
10. Huang L, Dai T, Hamblin MR. Antimicrobial photodynamic inactivation and photodynamic therapy for infections. Methods Mol. Biol. 635, 155-173 (2010).
11. Sharma SK, Dai T, Kharkwal GB et al. Drug discovery of antimicrobial photosensitizers using animal models. Curr. Pharm. Des. 17, 1303-1319 (2011).
12. Merchat M, Spikes JD, Bertoloni G, Jori G. Studieso n the mechanism of bacteria photosensitization by meso-substituted cationic porphyrins. J. Photochem. Photobiol. B 35(3), 149-157 (1996).
13. Huang L, Huang YY, Mroz P et al. Stable synthetic cati onic bacteriochlorins as selective antimicrobial photosensitizers. Antimicrob. Agents Chemother. 54(9), 3834-3841 (2010).
14. Alves E, Costa L, Carvalho CM et al. Charge effect on the photoinact ivation of Gram-negative and Gram-positive bacteria by cationic meso-substituted porphyrins. BMC Microbiol. 9, 70 (2009).
15. Pereira JB, Carvalho EF, Faustino MA et al. Phthalocyanine thio-pyridi nium derivatives as antibacterial photosensitizers. Photochem. Photobiol. 88(3), 537-547 (2012).
16. Wang M, Huang L, Sharma SK et al. Synthesis and photodynamic effect of new highly photostable decacationically armed [60]-and [70]fullerene decaiodide monoadducts to target pathogenic bacteria and cancer cells. J. Med. Chem. 55(9), 4274-4285 (2012).
17. Arbogast JW, Darmanyan AP, Foote CS e t al. Photophysical properties of C60. J. Phys. Chem. A Mol. Spectrosc. Kinet. Environ. Gen. Theory 95(1), 11-12 (1991).
18. Yamakoshi Y, Umezawa N, Ryu A et al. Active oxygen species generat ed from photoexcited fullerene (C60) as potential medicines: O2-Versus 1O2. J. Am. Chem. Soc. 125(42), 12803-12809 (2003).
19. Mroz P, Tegos GP, Gali H, Wharton T, Sarna T, Hamblin MR. P hotodynamic therapy with fullerenes. Photochem. Photobiol. Sci. 6(11), 1139-1149 (2007).
20. Sharma SK, Chiang LY, Hamblin MR. Photodynamic therapy with fullerenes in vivo: Reality or a dream Nanomedicine (Lond.) 6(10), 1813-1825 (2011).
21. Nakamura E, Isobe H. Functionalized fullerenes in water. The first 10 years of their chemistry, biology, and nanoscience. Acc. Chem. Res. 36(11), 807-815 (2003).
22. Dai T, Lu Z, Huang L et al. Photodynamic therapy for Acinetobacter baumannii burn infections in mice. Antimicrob. Agents Chemother. 53, 3929-3934 (2009).
23. Jett BD, Hatter KL, Huycke MM, Gilmore MS. Simplified agar plate method for quantifying viable bacteria. Biotechniques 23(4), 648-650 (1997).
24. Merlin JL, Azzi S, Lignon D, Ramacci C, Zeghari N, Guillemin F. MTT assays allow quick and reliable measurement of the response of human tumour cells to photodynamic therapy. Eur. J. Cancer 28A(8-9), 1452-1458 (1992).
25. Price M, Reiners JJ, Santiago AM, Kessel D. Monitoring singlet oxygen and hydroxyl radical formation with fluorescent probes during photodynamic therapy. Photochem. Photobiol. 85(5), 1177-1181 (2009).
26. Setsukinai K, Urano Y, Kakinuma K, Majima HJ, Nagano T. Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish speci fic species. J. Biol. Chem. 278(5), 3170-3175 (2003).
27. Zhao B, He YY, Bilski PJ, Chignell CF. Pristine (C60) and hydroxylated [C60(OH)24] fullerene phototoxicity towards HaCaT keratinocyte s: Type I vs type II mechanisms. Chem. Res. Toxicol. 21(5), 1056-1063 (2008).
28. Ashur I, Goldschmidt R, Pinkas I et al. Photocatalytic generation of oxygen radicals by the water-soluble bacteriochlor ophyll derivative WST11, noncovalently bound to serum albumin. J. Phys. Chem. A 113(28), 8027-8037 (2009).
29. Dabrowski JM, Arnaut LG, Pereira MM et al. Combined effects of singlet oxygen and hyd roxyl radical in photodynamic therapy with photostable bacteriochlorins: Evidence from intracellular fluorescence and increased photodynamic efficacy in vitro. Free Radic. Biol. Med. 52(7), 1188-1200 (2012).
30. Riggs JE, Sun YP. Optical limiting properties of [60]fullerene and methano[60]fullerene derivative in solution versus in polymer matrix: The role of bimolecular processes and a consistent nonlinear absorption mechanism. J. Phys. Chem. A 103, 485-495 (1999).
31. Gupta AK, Rohatgi-Mukherjee KK. Solvent effect on photosensitized oxidation of iodide ion by anthracene sulphonates. Photochem. Photobiol. 27, 539-543 (1978).
32. Huang L, Xuan Y, Koide Y, Zhiyentayev T, Tanaka M, Hamblin MR. Type I and type II mechanisms of antimicrobial photodynamic therapy: An in vitro study on Gram-negative and Gram-positive bacteria. Lasers Surg. Med. 44(6), 490-499 (2012).
33. Dahl TA, Midden WR, Hartman PE. Comparison of killing of Gram-negative and Gram-positive bacteria by pure singlet oxygen. J. Bacteriol. 171(4), 2188-2194 (1989).
34. Sabbahi S, Alouini Z, Jemli M, Boudabbous A. The role of reactive oxygen species in Staphylococcus aureus photoinactivation by methylene blue. Water Sci. Technol. 58(5), 1047-1054 (2008).
35. Vakrat-Haglili Y, Weiner L, Brumfeld V et al. The microenvironment effect on the generation of reactive oxygen species by Pd-bacteriopheophorbide. J. Am. Chem. Soc. 127(17), 6487-6497 (2005).
36. Valduga G, Bertoloni G, Reddi E, Jori G. Effect of extracellularly generated singlet oxygen on Gram-positive and Gram-negative bacteria. J. Photochem. Photobiol. B 21(1), 81-86 (1993).
37. Ragas X, Dai T, Tegos GP, Agut M, Nonell S, Hamblin MR. Photodynamic inactivation of Acinetobacter baumannii using phenothiazinium dyes: In-vitro and in-vivo studies. Lasers Surg. Med. 42(5), 384-390 (2010).
38. Dai T, Tegos GP, Lu Z et al. Photodynamic therapy for Acinetobacter baumannii burn infections in mice. Antimicrob. Agents Chemother. 53(9), 3929-3934 (2009).
39. Nitzan Y, A shkenazi H. Photoinactivation of Acinetobacter baumannii and Escherichia coli B by a cationic hydrophilic porphyrin at various light wavelengths. Curr. Microbiol. 42(6), 408-414 (2001).
40. Nitzan Y, Balz am-Sudakevitz A, Ashkenazi H. Eradication of Acinetobacter baumannii by photosensitized agents in vitro. J. Photochem. Photobiol. B 42(3), 211-218 (1998).
41. Martin JP, Logsdon N. The role of ox ygen radicals in dye-mediated photodynamic effects in Escherichia coli B. J. Biol. Chem. 262(15), 7213-7219 (1987).
42. Maisch T, Baier J, Franz B et al. The role of singlet oxygen and oxygen conc entration in photodynamic inactivation of bacteria. Proc. Natl Acad. Sci. USA 104(17), 7223-7228 (2007).
43. Huang L, St Denis TG, Xuan Y et al. Paradoxical potentiation of methylene blue-mediated antimicrobial photodynamic inactivation by sodium azide: Role of ambient oxygen and azide radicals. Free Radic. Biol. Med. 53(11), 2062-2071 (2012).
44. Mang R, Krutmann J. UVA-1 phototherapy. Photodermatol. Photoimmunol. Photomed. 21(2), 103-108 (2005).
45. Tegos GP, Demidova TN, Arcila-Lopez D et al. Cationic fullerenes are effective and selective antimicrobial photosensitizers. Chem. Biol. 12(10), 1127-1135 (2005).
46. Huang L, Terakawa M, Zhiyentayev T et al. Innovative cationic fullerenes as broad-spectrum light-activated antimicrobials. Nanomedicine 6(3), 442-452 (2010).
47. Mizuno K, Zhiyentayev T, Huang L et al. Antimicrobial photodynamic therapy with functionalized fullerenes: Quantitative structure-activity relationships. J. Nanomedic. Nanotechnol. 2(2), 109-117 (2011).
48. Sharma BR. Infection in patients with severe burns: Causes and prevention thereof. Infect. Dis. Clin. North Am. 21(3), 745-759, ix (2007).
49. Ollstein RN, McDonald C. Topical and systemic antimicrobial agents in burns. Ann. Plast. Surg. 5(5), 386-392 (1980).
50. Saffle JR. Closure of the excised burn wound: Temporary skin substitutes. Clin. Plast. Surg. 36(4), 627-641 (2009).
51. Kang CI, Kim SH, Park WB et al. Bloodstream infections caused by antibiotic-resistant Gram-negative bacilli: Risk factors for mortality and impact of inappropria te initial antimicrobial therapy on outcome. Antimicrob. Agents Chemother. 49(2), 760-766 (2005).
52. Dai T, Huang YY, Sharma SK, Hashmi JT, Kurup DB, Hamblin MR. To pical antimicrobials for burn wound infections. Recent Pat. Antiinfect. Drug Discov. 5(2), 124-151 (2010).
53. Keen EF 3rd, Robinson BJ, Hospenthal DR et al. Incidence and bacteriology of burn i nfections at a military burn center. Burns 36(4), 461-468 (2010).
54. Asadollahi P, Akbari M, Soroush Set al. Antimicrobial resistance patterns and their encoding genes among Acinetobacter baumannii strains isolated from burned patients. Burns 38(8), 1198-1203 (2012).
55. Lu Z, Dai T, Huang L et al. Photodynamic therapy with a cationic functionalized fullerene rescues mice f rom fatal wound infections. Nanomedicine (UK) 5(10), 1525-1533 (2010).