Abstract
We have recently shown that a wide range of different inorganic salts can potentiate antimicrobial photo-dynamic inactivation (aPDI) and TiO2-mediated antimicrobial photocatalysis. Potentiation has been shown with azide, bromide, thiocyanate, selenocyanate, and most strongly, with iodide. Here we show that sodium nitrite can also potentiate broad-spectrum aPDI killing of Gram-positive MRSA and Gram-negative Escherichia coli bacteria. Literature reports have previously shown that two photosensitizers (PS), methylene blue (MB) and riboflavin, when excited by broad-band light in the presence of nitrite could lead to tyrosine nitration. Addition of up to 100 mM nitrite gave 6 logs of extra killing in the case of Rose Bengal excited by green light against E. coli, and 2 logs of extra killing against MRSA (eradication in both cases). Comparable results were obtained for other PS (TPPS4 + blue light and MB + red light). Some bacterial killing was obtained when bacteria were added after light using a functionalized fullerene (LC15) + nitrite + blue light, and tyrosine ester amide was nitrated using both “in” and “after” modes with all four PS. The mechanism could involve formation of peroxynitrate by a reaction between superoxide radicals and nitrogen dioxide radicals; formation of the latter species was demonstrated by spin trapping with nitromethane.
Similar content being viewed by others
References
J. O’Neill, Tackling a global health crisis:initial steps, The Review on Antimicrobial Resistance Chaired by Jim O’Neill, 2015.
K. Bush, P. Courvalin, G. Dantas, J. Davies, B. Eisenstein, P. Huovinen, et al., Tackling antibiotic resistance, Nat. Rev. Microbiol., 2011, 9(12), 894–896.
A. P. Castano, T. N. Demidova and M. R. Hamblin, Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization, Photodiagn. Photodyn. Ther., 2004, 1(4), 279–293.
M. da Silva Baptista, J. Cadet, P. Di Mascio, A. A. Ghogare, A. Greer, M. R. Hamblin, et al., Type I and II Photosensitized Oxidation Reactions: Guidelines and Mechanistic Pathways, Photochem. Photobiol., 2017, 93(4), 912–919.
S. K. Sharma, P. Mroz, T. Dai, Y. Y. Huang, T. G. St Denis and M. R. Hamblin, Photodynamic Therapy for Cancer and for Infections: What Is the Difference?, Isr. J. Chem., 2012, 52(8–9), 691–705.
M. R. Hamblin, Potentiation of antimicrobial photodynamic inactivation by inorganic salts, Expert Rev. Anti-Infect. Ther., 2017, 15(11), 1059–1069.
L. Huang, A. El-Hussein, W. Xuan and M. R. Hamblin, Potentiation by potassium iodide reveals that the anionic porphyrin TPPS4 is a surprisingly effective photosensitizer for antimicrobial photodynamic inactivation, J. Photochem. Photobiol., B, 2017, 178, 277–286.
L. Huang, G. Szewczyk, T. Sarna and M. R. Hamblin, Potassium Iodide Potentiates Broad-Spectrum Antimicrobial Photodynamic Inactivation Using Photofrin, ACS Infect. Dis., 2017, 3(4), 320–328.
D. Vecchio, A. Gupta, L. Huang, G. Landi, P. Avci, A. Rodas, et al., Bacterial photodynamic inactivation mediated by methylene blue and red light is enhanced by synergistic effect of potassium iodide, Antimicrob. Agents Chemother., 2015, 59(9), 5203–5212.
X. Wu, Y. Y. Huang, Y. Kushida, B. Bhayana and M. R. Hamblin, Broad-spectrum antimicrobial photocatalysis mediated by titanium dioxide and UVA is potentiated by addition of bromide ion via formation of hypobromite, Free Radicals Biol. Med., 2016, 95, 74–81.
T G. St Denis, D. Vecchio, A. Zadlo, A. Rineh, M. Sadasivam, P. Avci, et al., Thiocyanate potentiates antimicrobial photodynamic therapy: In situ generation of the sulfur trioxide radical anion by singlet oxygen, Free Radicals Biol. Med., 2013, 65C, 800–810.
L. Huang, W. Xuan, A. Zadlo, A. Kozinska, T. Sarna and M. R. Hamblin, Antimicrobial photodynamic inactivation is potentiated by addition of selenocyanate: possible involvement of selenocyanogen?, J. Biophotonics, 2018, 11(8), e201800029.
L. Huang, T. G. St Denis, Y. Xuan, Y. Y. Huang, M. Tanaka, A. Zadlo, et al., Paradoxical potentiation of methylene blue-mediated antimicrobial photodynamic inactivation by sodium azide: role of ambient oxygen and azide radicals, Free Radicals Biol. Med., 2012, 53(11), 2062–2071.
L. Huang, Y. Xuan, Y. Koide, T. Zhiyentayev, M. Tanaka and M. R. Hamblin, Type I and Type II mechanisms of antimicrobial photodynamic therapy: An in vitro study on Gram-negative and Gram-positive bacteria, Lasers Surg. Med., 2012, 44(6), 490–499.
K. R. Kasimova, M. Sadasivam, G. Landi, T. Sarna and M. R. Hamblin, Potentiation of photoinactivation of Gram-positive and Gram-negative bacteria mediated by six phenothiazinium dyes by addition of azide ion, Photochem. Photobiol. Sci., 2014, 13(11), 1541–1548.
R. Yin, M. Wang, Y. Y. Huang, G. Landi, D. Vecchio, L. Y. Chiang, et al., Antimicrobial photodynamic inactivation with decacationic functionalized fullerenes: oxygen independent photokilling in presence of azide and new mechanistic insights, Free Radicals Biol. Med., 2015, 79,14–27.
L. Pecci, G. Montefoschi, A. Antonucci, M. Costa, M. Fontana and D. Cavallini, Formation of nitrotyrosine by methylene blue photosensitized oxidation of tyrosine in the presence of nitrite, Biochem. Biophys. Res. Commun., 2001, 289(1), 305–309.
M. Fontana, C. Blarzino and L. Pecci, Formation of 3-nitro-tyrosine by riboflavin photosensitized oxidation of tyrosine in the presence of nitrite, Amino Acids, 2012, 42(5), 1857–1865.
P. Bilski, C. F. Chignell, J. Szychlinski, A. Borkowski, E. Oleksy and K. Reszka, Photooxidation of organic and inorganic substrates during UV photolysis of nitrite anion in aqueous solution, J. Am. Chem. Soc., 1992, 114, 549–556.
X. Wen, X. Zhang, G. Szewczyk, A. El-Hussein, Y. Y. Huang, T. Sarna, et al., Potassium Iodide Potentiates Antimicrobial Photodynamic Inactivation Mediated by Rose Bengal in In Vitro and In Vivo Studies, Antimicrob. Agents Chemother., 2017, 61(7), pii: e00467-17.
Y. Y. Huang, H. Choi, Y. Kushida, B. Bhayana, Y. Wang and M. R. Hamblin, Broad-Spectrum Antimicrobial Effects of Photocatalysis Using Titanium Dioxide Nanoparticles Are Strongly Potentiated by Addition of Potassium Iodide, Antimicrob. Agents Chemother., 2016, 60(9), 5445–5453.
G. Szewczyk, A. Zadlo, M. Sarna, S. Ito, K. Wakamatsu and T. Sarna, Aerobic photoreactivity of synthetic eumelanins and pheomelanins: generation of singlet oxygen and superoxide anion, Pigm. Cell Melanoma Res., 2016, 29(6), 669–678.
K. J. Reszka, P. Bilski and C. F. Chignell, Spin trapping of nitric oxide by aci anions of nitroalkanes, Nitric Oxide, 2004, 10(2), 53–59.
M. D. Pace, Spin Trapping of Nitrogen Dioxide from Photolysis of Sodium Nitrite, Ammonium Nitrate, Ammonium Dinitramide, and Cyclic Nitramines, J. Phys. Chem., 1994, 98, 6251–6257.
C. Lambert, T. Sarna and T. G. Truscott, Rose bengal radicals and their reactivity, J. Chem. Soc., Faraday Trans., 1990, 86, 3879–3882.
T. Nauser and W. H. Koppenol, The Rate Constant of the Reaction of Superoxide with Nitrogen Monoxide: Approaching the Diffusion Limit, J. Phys. Chem. A, 2002, 106, 4084–4086.
T. Loegager and K. Sehested, Formation and decay of peroxynitric acid: a pulse radiolysis study, J. Phys. Chem., 1993, 97, 10047–10052.
J. Zielonka, A. Sikora, M. Hardy, J. Joseph, B. P. Dranka and B. Kalyanaraman, Boronate probes as diagnostic tools for real time monitoring of peroxynitrite and hydroperoxides, Chem. Res. Toxicol., 2012, 25(9), 1793–1799.
N. Ieda, H. Nakagawa, T. Peng, D. Yang, T. Suzuki and N. Miyata, Photocontrollable peroxynitrite generator based on, N-methyl-N-nitrosoaminophenol for cellular application, J. Am. Chem. Soc., 2012, 134(5), 2563–2568.
L. Huang, W. Xuan, T. Sarna and M. R. Hamblin, Comparison of thiocyanate and selenocyanate for potentiation of antimicrobial photodynamic therapy, J. Biophotonics, 2018, e201800092.
L. Huang, W. Xuan, A. Zadlo, A. Kozinska, T. Sarna and M. R. Hamblin, Antimicrobial photodynamic inactivation is potentiated by the addition of selenocyanate: Possible involvement of selenocyanogen?, J. Biophotonics, 2018, e201800029.
T. Loegager and K. Sehested, Formation and decay of peroxynitrous acid: a pulse radiolysis study, J. Phys. Chem., 1993, 97, 6664–6669.
L. P. Olson, M. D. Bartberger and K. N. Houk, Peroxynitrate and peroxynitrite: a complete basis set investigation of similarities and differences between these NOx species, J. Am. Chem. Soc., 2003, 125(13), 3999–4006.
K. N. Houk, K. R. Condorski and W. A. Pryor, Radical and Concertaed Mechanisms in Oxidations of Amines, Sulfides, and Alkenes by Peroxynitrite, Peroxynitrous Acid, and the Peroxynitrite−CO2 Adduct: Density Functional Theory Transition Structures and Energetics, J. Am. Chem. Soc., 1996, 118, 13002–13006.
S. Vayssie and H. Elias, Fast Oxidation of Organic Sulfides by Hydrogen Peroxide by In Situ Generated Peroxynitrous Acid, Angew. Chem., Int. Ed. Engl., 1998, 37(15), 2088–2090.
H. K. Dahle, Nitrite as a food additive, NIPH Ann., 1979, 2(2), 17–24.
M. C. Matallana Gonzalez, M. J. Martinez-Tome and M. E. Torija Isasa, Nitrate and nitrite content in organically cultivated vegetables, Food Addit. Contam., Part B, 2010, 3(1), 19–29.
V. E. Nossaman, B. D. Nossaman and P. J. Kadowitz, Nitrates and nitrites in the treatment of ischemic cardiac disease, Cardiol. Rev., 2010, 18(4), 190–197.
J. Tenovuo, The biochemistry of nitrates, nitrites, nitrosamines and other potential carcinogens in human saliva, J. Oral Pathol., 1986, 15(6), 303–307.
A. Butler, Nitrites and nitrates in the human diet: Carcinogens or beneficial hypotensive agents?, J. Ethnopharmacol., 2015, 167, 105–107.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Huang, YY., Rajda, P.J., Szewczyk, G. et al. Sodium nitrite potentiates antimicrobial photodynamic inactivation: possible involvement of peroxynitrate. Photochem Photobiol Sci 18, 505–515 (2019). https://doi.org/10.1039/c8pp00452h
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/c8pp00452h