Trichophyton rubrum is inhibited by free and nanoparticle encapsulated curcumin by induction of nitrosative stress after photodynamic activation

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Baltazar, Ludmila Matos ^a   Krausz, Aimee E ^a   Souza, Ana Camila Oliveira ^a   Adler, Brandon L ^a   Landriscina, Angelo ^a   Musaev, Tagai ^a   Nosanchuk, Joshua D ^a   Friedman, Adam J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CURCUMIN; NANOPARTICLE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; ANTIFUNGAL AGENT; MICROCAPSULE; PHOTOSENSITIZING AGENT; SCAVENGER;

ANTIFUNGAL ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DERMATOPHYTE; DRUG DETERMINATION; FUNGAL CELL; FUNGUS GROWTH; GROWTH INHIBITION; NANOENCAPSULATION; NITROSATIVE STRESS; NONHUMAN; PHOTODYNAMICS; PROTEIN EXPRESSION; TRICHOPHYTON RUBRUM; CELL LINE; CHEMISTRY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HUMAN; KINETICS; LIGHT; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROCAPSULE; PHAGOCYTOSIS; PHYSIOLOGICAL STRESS; RADIATION RESPONSE; TRICHOPHYTON;

FUNGI; TRICHOPHYTON RUBRUM;

ANTIFUNGAL AGENTS; CAPSULES; CELL LINE; CURCUMIN; FREE RADICAL SCAVENGERS; HUMANS; KINETICS; LIGHT; MICROBIAL SENSITIVITY TESTS; NANOPARTICLES; PHAGOCYTOSIS; PHOTOSENSITIZING AGENTS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; STRESS, PHYSIOLOGICAL; TRICHOPHYTON;

EID: 84925867912     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120179     Document Type: Article

References (54)

1. Vermout S, Tabart J, Baldo A, Mathy A, Losson B, Mignon B. Pathogenesis of dermatophytosis. Mycopathologia. 2008;166:267-275. doi: 10.1007/s11046-008-9104-5 PMID: 18478361
2. Gupta AK, Humke S. The prevalence and management of onychomycosis in diabetic patients. Eur J Dermatol. 2000;10:379-384. PMID: 10882947
3. Manzano-Gayosso P, Mendez-Tovar LJ, Hernandez-Hernandez F, Lopez-Martinez R [Antifungal resistance: an emerging problem in Mexico]. Gac Med Mex. 2008;144:23-26. PMID: 18619054
4. Martinez-Rossi NM, Peres NT, Rossi A. Antifungal resistance mechanisms in dermatophytes. Mycopathologia. 2008;166:369-383. doi: 10.1007/s11046-008-9110-7 PMID: 18478356
5. Ghelardi E, Celandroni F, Gueye SA, Salvetti S, Senesi S, Bulgheroni A, et al. Potential of Ergosterol synthesis inhibitors to cause resistance or cross-resistance in Trichophyton rubrum. Antimicrob Agents Chemother. 2014;58:2825-2829. doi: 10.1128/AAC.02382-13 PMID: 24614379
6. Vena GA, Chieco P, Posa F, Garofalo A, Bosco A, Cassano N. Epidemiology of dermatophytoses: retrospective analysis from 2005 to 2010 and comparison with previous data from 1975. New Microbiol. 2012;35:207-213. PMID: 22707134
7. Adimi P, Hashemi SJ, Mahmoudi M, Mirhendi H, Shidfar MR, Emmam M, et al. In-vitro Activity of 10 Antifungal Agents against 320 Dermatophyte Strains Using Microdilution Method in Tehran. Iran J Pharm Res. 2013;12:537-545. PMID: 24250660
8. Coelho LM, Aquino-Ferreira R, Maffei CM, Martinez-Rossi NM. In vitro antifungal drug susceptibilities of dermatophytes microconidia and arthroconidia. J Antimicrob Chemother. 2008;62:758-761. doi: 10.1093/jac/dkn245 PMID: 18552341
9. Donnelly RF, McCarron PA, Tunney MM. Antifungal photodynamic therapy. Microbiol Res. 2008;163:1-12. PMID: 18037279
10. Smijs TG, Pavel S. The susceptibility of dermatophytes to photodynamic treatment with special focus on Trichophyton rubrum. Photochem Photobiol. 2011;87:2-13. doi: 10.1111/j.1751-1097.2010. 00848.x PMID: 21114670
11. Hamblin MR, Hasan T. Photodynamic therapy: a new antimicrobial approach to infectious disease? Photochem Photobiol Sci. 2004;3:436-450. PMID: 15122361
12. Baltazar Lde M, Soares BM, Carneiro HC, Avila TV, Gouveia LF, Souza DG, et al. Photodynamic inhibition of Trichophyton rubrum: in vitro activity and the role of oxidative and nitrosative bursts in fungal death. J Antimicrob Chemother. 2013;68:354-361. doi: 10.1093/jac/dks414 PMID: 23134678
13. Calzavara-Pinton P, Rossi MT, Sala R, Venturini M. Photodynamic antifungal chemotherapy. Photochem Photobiol. 2012;88:512-522. doi: 10.1111/j.1751-1097.2012.01107.x PMID: 22313493
14. Vatansever F, De Melo WC, Avci P, Vecchio D, Sadasivam M, Gupta A, et al. Antimicrobial strategies centered around reactive oxygen species-bactericidal antibiotics, photodynamic therapy, and beyond. FEMS Microbiol Rev. 2013;37:955-989. doi: 10.1111/1574-6976.12026 PMID: 23802986
15. Dai T, Fuchs BB, Coleman JJ, Prates RA, Astrakas C, St Denis TG, et al. Concepts and principles of photodynamic therapy as an alternative antifungal discovery platform. Front Microbiol. 2012;3:120. doi: 10.3389/fmicb.2012.00120 PMID: 22514547
16. Wikene KO, Hegge AB, Bruzell E, Tonnesen HH. Formulation and characterization of lyophilized curcumin solid dispersions for antimicrobial photodynamic therapy (aPDT): studies on curcumin and curcuminoids LII. Drug Dev Ind Pharm. 2014;1-9.
17. Priyadarsini K. Photophysics, photochemistry and photobiology of curcumin: Studies from organic solutions, bio-mimetics and living cells. Journal of Photochemistry and Photobiology C: Photochemistry Reviews. 2009;10:81-95.
18. Hegge AB, Bruzell E, Kristensen S, Tonnesen HH. Photoinactivation of Staphylococcus epidermidis biofilms and suspensions by the hydrophobic photosensitizer curcumin-effect of selected nanocarrier: studies on curcumin and curcuminoides XLVII. Eur J Pharm Sci. 2012;47:65-74. doi: 10.1016/j.ejps. 2012.05.002 PMID: 22609527
19. Tonnesen HH, De Vries H, Karlsen J, Beijersbergen Van Henegouwen G. Studies on curcumin and curcuminoids. IX: Investigation of the photobiological activity of curcumin using bacterial indicator systems. J Pharm Sci. 1987;76:371-373. PMID: 3309256
20. Haukvik T, Bruzell E, Kristensen S, Tonnesen HH. Photokilling of bacteria by curcumin in different aqueous preparations. Studies on curcumin and curcuminoids XXXVII. Pharmazie. 2009;64:666-673. PMID: 19947170
21. Hegge AB, Nielsen TT, Larsen KL, Bruzell E, Tonnesen HH. Impact of curcumin supersaturation in antibacterial photodynamic therapy-effect of cyclodextrin type and amount: studies on curcumin and curcuminoides XLV. J Pharm Sci. 2012;101:1524-1537. doi: 10.1002/jps.23046 PMID: 22228150
22. Hegge AB, Andersen T, Melvik JE, Bruzell E, Kristensen S, Tonnesen HH. Formulation and bacterial phototoxicity of curcumin loaded alginate foams for wound treatment applications: studies on curcumin and curcuminoides XLII. J Pharm Sci. 2011;100:174-185. doi: 10.1002/jps.22263 PMID: 20575064
23. Dahl TA, McGowan WM, Shand MA, Srinivasan VS. Photokilling of bacteria by the natural dye curcumin. Arch Microbiol. 1989;151:183-185. PMID: 2655550
24. Araujo NC, Fontana CR, Bagnato VS, Gerbi ME. Photodynamic antimicrobial therapy of curcumin in biofilms and carious dentine. Lasers Med Sci. 2013;30:393-9.
25. Dovigo LN, Carmello JC, De Souza Costa CA, Vergani CE, Brunetti IL, Bagnato VS, et al. Curcuminmediated photodynamic inactivation of Candida albicans in a murine model of oral candidiasis. Med Mycol. 2013;51:243-251. doi: 10.3109/13693786.2012.714081 PMID: 22934533
26. Dovigo LN, Pavarina AC, Ribeiro AP, Brunetti IL, Costa CA, Jacomassi DP, et al. Investigation of the photodynamic effects of curcumin against Candida albicans. Photochem Photobiol. 2011;87:895-903. doi: 10.1111/j.1751-1097.2011.00937.x PMID: 21517888
27. Perni S, Prokopovich P, Pratten J, Parkin IP, Wilson M. Nanoparticles: their potential use in antibacterial photodynamic therapy. Photochem Photobiol Sci. 2011;10:712-720. doi: 10.1039/c0pp00360c PMID: 21380441
28. Bruzell EM, Morisbak E, Tonnesen HH. Studies on curcumin and curcuminoids. XXIX. Photoinduced cytotoxicity of curcumin in selected aqueous preparations. Photochem Photobiol Sci. 2005;4:523-530. PMID: 15986060
29. Singh R, Kristensen S, Tonnesen HH. Influence of cosolvents, ionic strength and the method of sample preparation on the solubilization of curcumin by Pluronics and HP-gamma-cyclodextrin. Studies of curcumin and curcuminoids, XLIV. Pharmazie. 2012;67:131-142. PMID: 22512083
30. Santos DA, Barros ME, Hamdan JS. Establishing a method of inoculum preparation for susceptibility testing of Trichophyton rubrum and Trichophyton mentagrophytes. J Clin Microbiol. 2006;44:98-101. PMID: 16390955
31. Friedman AJ, Han G, Navati MS, Chacko M, Gunther L, Alfieri A, et al. Sustained release nitric oxide releasing nanoparticles: characterization of a novel delivery platform based on nitrite containing hydrogel/glass composites. Nitric Oxide. 2008;19:12-20. doi: 10.1016/j.niox.2008.04.003 PMID: 18457680
32. Narayanan A, Kehn-Hall K, Senina S, Lundberg L, Van Duyne R, Guendel I, et al. Curcumin inhibits Rift Valley fever virus replication in human cells. J Biol Chem. 2012;287:33198-33214. PMID: 22847000
33. Krausz AE, Adler BL, Cabral V, Navati M, Doerner J, Charafeddine RA, et al. Curcumin-encapsulated nanoparticles as innovative antimicrobial and wound healing agent. Nanomedicine. 2014;11:195-206. doi: 10.1016/j.nano. 2014.09.004 PMID: 25240595
34. Institute CaLS. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. CLSI, Wayne, PA. 2008.
35. Guimaraes AJ, Frases S, Gomez FJ, Zancope-Oliveira RM, Nosanchuk JD. Monoclonal antibodies to heat shock protein 60 alter the pathogenesis of Histoplasma capsulatum. Infect Immun. 2009;77:1357-1367. doi: 10.1128/IAI.01443-08 PMID: 19179416
36. Baltazar Lde M, Santos PC, Paula TP, Rachid MA, Cisalpino PS, Souza DG, et al. IFN-gamma impairs Trichophyton rubrum proliferation in a murine model of dermatophytosis through the production of IL-1beta and reactive oxygen species. Med Mycol. 2014;52:293-302. doi: 10.1093/mmy/myt011 PMID: 24577006
37. Santos DA, Hamdan JS. In vitro antifungal oral drug and drug-combination activity against onychomycosis causative dermatophytes. Med Mycol. 2006;44:357-362. PMID: 16772230
38. Moghadamtousi ZS, Kadir HA, Hassandarvish P, Tajik H, Abubakar S, Zandi K. A Review on Antibacterial, Antiviral, and Antifungal Activity of Curcumin. Biomed Res Int. 2014:186864.
39. Apisariyakul A, Vanittanakom N, Buddhasukh D. Antifungal activity of turmeric oil extracted from Curcuma longa (Zingiberaceae). J Ethnopharmacol. 1995;49:163-169. PMID: 8824742
40. Wuthi-Udomlert M, Grisanapan W, Luanratana O, Caichompoo W. Antifungal activity of Curcuma longa grown in Thailand. Southeast Asian J Trop Med Public Health. 2000;31:178-182. PMID: 11414453
41. Gold MH, Rao J, Goldman MP, Bridges TM, Bradshaw VL, Boring MM, et al. A multicenter clinical evaluation of the treatment of mild to moderate inflammatory acne vulgaris of the face with visible blue light in comparison to topical 1% clindamycin antibiotic solution. J Drugs Dermatol. 2005;4:64-70. PMID: 15696987
42. Kleinpenning MM, Smits T, Frunt MH, Van Erp PE, Van De Kerkhof PC, Gerritsen RM. Clinical and histological effects of blue light on normal skin. Photodermatol Photoimmunol Photomed. 2010;26:16-21. doi: 10.1111/j.1600-0781.2009.00474.x PMID: 20070834
43. Liebmann J, Born M, Kolb-Bachofen V. Blue-light irradiation regulates proliferation and differentiation in human skin cells. J Invest Dermatol. 2010;130:259-269. doi: 10.1038/jid.2009.194 PMID: 19675580
44. Godley BF, Shamsi FA, Liang FQ, Jarrett SG, Davies S, Boulton M. Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem. 2005;280:21061-21066. PMID: 15797866
45. Wataha JC, Lockwood PE, Lewis JB, Rueggeberg FA, Messer RL. Biological effects of blue light from dental curing units. Dent Mater. 2004;20:150-157. PMID: 14706798
46. Hegge AB, Vukicevic M, Bruzell E, Kristensen S, Tonnesen HH. Solid dispersions for preparation of phototoxic supersaturated solutions for antimicrobial photodynamic therapy (aPDT): Studies on curcumin and curcuminoides L. Eur J Pharm Biopharm. 2013;83:95-105. doi: 10.1016/j.ejpb.2012.09.011 PMID: 23085330
47. Shen L, Ji HF, Zhang HY. A TD-DFT study on triplet excited-state properties of curcumin and its implications in elucidating the photosensitizing mechanisms of the pigment. Chem Phys Lett. 2005;409:300-303.
48. Schairer DO, Chouake JS, Nosanchuk JD, Friedman AJ. The potential of nitric oxide releasing therapies as antimicrobial agents. Virulence. 2012;3:271-279. doi: 10.4161/viru.20328 PMID: 22546899
49. De Groote MA, Fang FC. NO inhibitions: antimicrobial properties of nitric oxide. Clin Infect Dis. 1995;21:S162-165. PMID: 8845445
50. Fang FC. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest. 1997;99:2818-2825. PMID: 9185502
51. Radi R, Cassina A, Hodara R. Nitric oxide and peroxynitrite interactions with mitochondria. Biol Chem. 2002;383:401-409. PMID: 12033431
52. Buytaert E, Dewaele M, Agostinis P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim Biophys Acta. 2007;1776:86-107. PMID: 17693025
53. Sharma M, Manoharlal R, Puri N, Prasad R. Antifungal curcumin induces reactive oxygen species and triggers an early apoptosis but prevents hyphae development by targeting the global repressor TUP1 in Candida albicans. Biosci Rep. 2010;30:391-404. doi: 10.1042/BSR20090151 PMID: 20017731
54. Rotta I, Sanchez A, Goncalves PR, Otuki MF, Correr CJ. Efficacy and safety of topical antifungals in the treatment of dermatomycosis: a systematic review. Br J Dermatol. 2012;166:927-933. doi: 10. 1111/j.1365-2133.2012.10815.x PMID: 22233283