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Antimicrobial Mechanisms of Nitric Oxide and Strategies for Developing Nitric Oxide-based Antimicrobial Agents

산화질소가 미생물에 미치는 영향 및 이를 이용한 항균전략

  • Received : 2014.05.07
  • Accepted : 2014.06.14
  • Published : 2014.06.30

Abstract

Nitric oxide (NO), which has been recognized as an integral molecule in maintaining homeostasis, plays an important role in host defense against microbes. NO has diverse antimicrobial mechanisms by directly and/or indirectly interacting with microbes. Under the circumstance that there is an urgent need for a new class of antimicrobial agents due to antibiotic resistance, much effort has been made to develop a NO-based antimicrobial agent. In order to make it possible, strategies to store and release NO in a controlled manner are required because NO has a gaseous property and a very short half-life. In this review, we described NO biochemistry and its mechanisms of antimicrobial activity. In additions, we introduced various NO-releasing systems that improve NO's antimicrobial activity.

인체의 항상성 유지에 필수적인 물질로 알려진 산화질소는 인체를 침입한 미생물로부터 보호하는 면역반응에서 매우 중요한 역할을 담당하고 있다. 산화질소는 미생물에 직간접적으로 작용하여 다양한 기전으로 항균작용을 나타낸다. 항생제의 심각한 내성이 심각한 사회적 문제로 대두되면서 새로운 계열의 항생제 개발이 절실한 시점에서 항균물질로서의 산화질소에 대한 연구가 활발히 진행되고 있다. 하지만 매우 짧은 반감기와 기체분자인 산화질소를 항생제로 이용하기 위해서는 산화질소의 저장과 방출을 제어할 전략 필요하다. 본 총설에서는 산화질소의 체내에서의 생화학적 특성과 항균작용을 나타내는 다양한 기전에 대해 설명하였다. 또한 산화질소 방출을 조절하여 항균작용을 향상시키는 최근의 연구에 대해 알아보았다.

Keywords

References

  1. Amadeu, T.P., Seabra, A.B., de Oliveira, M.G., and Costa, A.M. 2007. S-nitrosoglutathione-containing hydrogel accelerates rat cutaneous wound repair. J. Eur. Acad. Dermatol. Venereol. 21, 629-637.
  2. Assreuy, J., Cunha, F.Q., Epperlein, M., Noronha-Dutra, A., O'Donnell, C.A., Liew, F.Y., and Moncada, S. 1994. Production of nitric oxide and superoxide by activated macrophages and killing of Leishmania major. Eur. J. Immunol. 24, 672-676. https://doi.org/10.1002/eji.1830240328
  3. Beckman, J.S. 1991. The double-edged role of nitric oxide in brain function and superoxide-mediated injury. J. Dev. Physiol. 15, 53-59.
  4. Bhide, M. 2006. Nitric oxide delivery from polymeric wound dressings. University of Akron.
  5. Bogdan, C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2, 907-916. https://doi.org/10.1038/ni1001-907
  6. Bogdan, C. 2011. Regulation of lymphocytes by nitric oxide. Suppression and Regulation of Immune Responses, pp. 375-393. Springer.
  7. Bryan, N.S., Rassaf, T., Maloney, R.E., Rodriguez, C.M., Saijo, F., Rodriguez, J.R., and Feelisch, M. 2004. Cellular targets and mechanisms of nitros(yl)ation: An insight into their nature and kinetics in vivo. Proc. Natl. Acad. Sci. USA 101, 4308-4313. https://doi.org/10.1073/pnas.0306706101
  8. Bryk, R., Griffin, P., and Nathan, C. 2000. Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407, 211-215. https://doi.org/10.1038/35025109
  9. Coates, A.R., Halls, G., and Hu, Y. 2011. Novel classes of antibiotics or more of the same? Br. J. Pharmacol. 163, 184-194. https://doi.org/10.1111/j.1476-5381.2011.01250.x
  10. Coneski, P.N. and Schoenfisch, M.H. 2012. Nitric oxide release: part III. Measurement and reporting. Chem. Soc. Rev. 41, 3753-3758. https://doi.org/10.1039/c2cs15271a
  11. De Groote, M.A. and Fang, F.C. 1995. NO inhibitions: antimicrobial properties of nitric oxide. Clin. Infect. Dis. 21, S162-S165. https://doi.org/10.1093/clinids/21.Supplement_2.S162
  12. De Groote, M.A., Granger, D., Xu, Y., Campbell, G., Prince, R., and Fang, F.C. 1995. Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc. Natl. Acad. Sci. USA 92, 6399-6403. https://doi.org/10.1073/pnas.92.14.6399
  13. de Souza, G.F.P., Yokoyama-Yasunaka, J.K., Seabra, A.B., Miguel, D.C., de Oliveira, M.G., and Uliana, S.R.B. 2006. Leishmanicidal activity of primary S-nitrosothiols against Leishmania major and Leishmania amazonensis: Implications for the treatment of cutaneous leishmaniasis. Nitric Oxide 15, 209-216. https://doi.org/10.1016/j.niox.2006.01.011
  14. Dukelow, A.M., Weicker, S., Karachi, T.A., Razavi, H.M., McCormack, D.G., Joseph, M.G., and Mehta, S. 2002. Effects of nebulized diethylenetetraamine-NONOate in a mouse model of acute Pseudomonas aeruginosa pneumonia. Chest 122, 2127-2136. https://doi.org/10.1378/chest.122.6.2127
  15. Dusse, L.M.S.A., Vieira, L.M., and Carvalho, M.d.G. 2003. Nitric oxide revision. Brazil. J. Arch. Pathol. Lab. Med. 39, 343-350.
  16. Eiserich, J.P., Hristova, M., Cross, C.E., Jones, A.D., Freeman, B.A., Halliwell, B., and van der Vliet, A. 1998. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391, 393-397. https://doi.org/10.1038/34923
  17. Englander, L. and Friedman, A. 2010. Nitric oxide nanoparticle technology: a novel antimicrobial agent in the context of current treatment of skin and soft tissue infection. J. Clin. Aesthet. Dermatol. 3, 45-50.
  18. Espey, M.G., Miranda, K.M., Thomas, D.D., and Wink, D.A. 2001. Distinction between nitrosating mechanisms within human cells and aqueous solution. J. Biol. Chem. 276, 30085-30091. https://doi.org/10.1074/jbc.M101723200
  19. Espey, M.G., Miranda, K.M., Thomas, D.D., Xavier, S., Citrin, D., Vitek, M.P., and Wink, D.A. 2002. A chemical perspective on the interplay between NO, reactive oxygen species, and reactive nitrogen oxide species. Ann. Ny. Acad. Sci. 962, 195-206. https://doi.org/10.1111/j.1749-6632.2002.tb04068.x
  20. Falagas, M.E. and Bliziotis, I.A. 2007. Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? Int. J. Antimicrob. Agents 29, 630-636. https://doi.org/10.1016/j.ijantimicag.2006.12.012
  21. Fang, F.C. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99, 2818-2825. https://doi.org/10.1172/JCI119473
  22. Fernandes, P.D. and Assreuy, J. 1997. Role of nitric oxide and superoxide in Giardia lamblia killing. Braz. J. Med. Biol. Res. 30, 93-99. https://doi.org/10.1590/S0100-879X1997000100015
  23. Friedman, A. and Friedman, J. 2009. New biomaterials for the sustained release of nitric oxide: past, present and future. Expert Opin. Drug Deliv. 6, 1113-1122. https://doi.org/10.1517/17425240903196743
  24. Ghaffari, A., Jalili, R., Ghaffari, M., Miller, C., and Ghahary, A. 2007. Efficacy of gaseous nitric oxide in the treatment of skin and soft tissue infections. Wound Repair Regen. 15, 368-377. https://doi.org/10.1111/j.1524-475X.2007.00239.x
  25. Ghaffari, A., Miller, C.C., McMullin, B., and Ghahary, A. 2006. Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide 14, 21-29.
  26. Ghaffari, A., Neil, D.H., Ardakani, A., Road, J., Ghahary, A., and Miller, C.C. 2005. A direct nitric oxide gas delivery system for bacterial and mammalian cell cultures. Nitric Oxide 12, 129-140. https://doi.org/10.1016/j.niox.2005.01.006
  27. Gorham, F. and Scamman, C. 1934. Papers of Charles V. Chapin. MD New York, Commonwealth Fund.
  28. Halpenny, G.M., Gandhi, K.R., and Mascharak, P.K. 2010. Eradication of pathogenic bacteria by remote delivery of NO via light triggering of nitrosyl-containing materials. Acs Med. Chem. Lett. 1, 180-183. https://doi.org/10.1021/ml1000646
  29. Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E., and Chaudhuri, G. 1987. Endothelium-derived relaxing factor produced and released from artery and vein is nitric-oxide. Proc. Natl. Acad. Sci. USA 84, 9265-9269. https://doi.org/10.1073/pnas.84.24.9265
  30. Ishima, Y., Sawa, T., Kragh-Hansen, U., Miyamoto, Y., Matsushita, S., Akaike, T., and Otagiri, M. 2007. S-Nitrosylation of human variant albumin Liprizzi (R410C) confers potent antibacterial and cytoprotective properties. J. Pharmacol. Exp. Ther. 320, 969-977.
  31. Jo, Y.S., van der Vlies, A.J., Gantz, J., Thacher, T.N., Antonijevic, S., Cavadini, S., Demurtas, D., Stergiopulos, N., and Hubbell, J.A. 2009. Micelles for delivery of nitric oxide. J. Am. Chem. Soc. 131, 14413-14418. https://doi.org/10.1021/ja905123t
  32. Juedes, M.J. and Wogan, G.N. 1996. Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat. Res. 349, 51-61. https://doi.org/10.1016/0027-5107(95)00152-2
  33. Kapadia, M.R., Chow, L.W., Tsihlis, N.D., Ahanchi, S.S., Eng, J.W., Murar, J., Martinez, J., Popowich, D.A., Jiang, Q., Hrabie, J.A., and et al. 2008. Nitric oxide and nanotechnology: a novel approach to inhibit neointimal hyperplasia. J. Vasc. Surg. 47, 173-182. https://doi.org/10.1016/j.jvs.2007.09.005
  34. Kaplan, S.S., Lancaster, J.R., Jr., Basford, R.E., and Simmons, R.L. 1996. Effect of nitric oxide on staphylococcal killing and interactive effect with superoxide. Infect. Immun. 64, 69-76.
  35. Karupiah, G. and Harris, N. 1995. Inhibition of viral replication by nitric oxide and its reversal by ferrous sulfate and tricarboxylic acid cycle metabolites. J. Exp. Med. 181, 2171-2179. https://doi.org/10.1084/jem.181.6.2171
  36. Keefer, L.K. 2005. Nitric oxide (NO)- and nitroxyl (HNO)-generating diazeniumdiolates (NONOates): Emerging commercial opportunities. Curr. Top. Med. Chem. 5, 625-634. https://doi.org/10.2174/1568026054679380
  37. Konter, J., Mollmann, U., and Lehmann, J. 2008. NO-donors. Part 17: Synthesis and antimicrobial activity of novel ketoconazole-NO-donor hybrid compounds. Bioorg. Med. Chem. 16, 8294-8300. https://doi.org/10.1016/j.bmc.2008.05.008
  38. Laval, F., Wink, D., and Laval, J. 1997. A discussion of mechanisms of NO genotoxicty: Implication of inhibition of DNA repair proteins. Rev. Physiol. Biochem. Pharmacol. 131, 175-191.
  39. Laval, F. and Wink, D.A. 1994. Inhibition by nitric oxide of the repair protein, O6-DNA-methyltransferase. Carcinogenesis 15, 443-447. https://doi.org/10.1093/carcin/15.3.443
  40. Laver, J.R., Stevanin, T.M., Messenger, S.L., Lunn, A.D., Lee, M.E., Moir, J.W., Poole, R.K., and Read, R.C. 2010. Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: a novel mechanism of bacterial pathogenesis. FASEB J. 24, 286-295. https://doi.org/10.1096/fj.08-128330
  41. Lepoivre, M., Chenais, B., Yapo, A., Lemaire, G., Thelander, L., and Tenu, J.P. 1990. Alterations of ribonucleotide reductase activity following induction of the nitrite-generating pathway in adenocarcinoma cells. J. Biol. Chem. 265, 14143-14149.
  42. Lepoivre, M., Flaman, J.M., and Henry, Y. 1992. Early loss of the tyrosyl radical in ribonucleotide reductase of adenocarcinoma cells producing nitric oxide. J. Biol. Chem. 267, 22994-23000.
  43. MacMicking, J., Xie, Q.W., and Nathan, C. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15, 323-350. https://doi.org/10.1146/annurev.immunol.15.1.323
  44. Maragos, C.M., Andrews, A., Keefer, L.K., and Elespuru, R.K. 1993. Mutagenicity of glyceryl trinitrate (nitroglycerin) in Salmonella typhimurium. Mutat. Res. 298, 187-195. https://doi.org/10.1016/0165-1218(93)90040-K
  45. Marcinkiewicz, J. 1997. Nitric oxide and antimicrobial activity of reactive oxygen intermediates. Immunopharmacology 37, 35-41. https://doi.org/10.1016/S0162-3109(96)00168-3
  46. McElhaney-Feser, G.E., Raulli, R.E., and Cihlar, R.L. 1998. Synergy of nitric oxide and azoles against Candida species in vitro. Antimicrob. Agents. Chemother. 42, 2342-2346.
  47. Melkova, Z. and Esteban, M. 1995. Inhibition of vaccinia virus DNA replication by inducible expression of nitric oxide synthase. J. Immunol. 155, 5711-5718.
  48. Miller, M.R. and Megson, I.L. 2007. Recent developments in nitric oxide donor drugs. Br. J. Pharmacol. 151, 305-321.
  49. Murad, F. 2006. Shattuck Lecture. Nitric oxide and cyclic GMP in cell signaling and drug development. N. Engl. J. Med. 355, 2003-2011. https://doi.org/10.1056/NEJMsa063904
  50. Nablo, B.J., Rothrock, A.R., and Schoenfisch, M.H. 2005. Nitric oxide-releasing sol-gels as antibacterial coatings for orthopedic implants. Biomaterials 26, 917-924. https://doi.org/10.1016/j.biomaterials.2004.03.031
  51. Nablo, B.J. and Schoenfisch, M.H. 2005. In vitro cytotoxicity of nitric oxide-releasing sol-gel derived materials. Biomaterials 26, 4405-4415. https://doi.org/10.1016/j.biomaterials.2004.11.015
  52. Nguyen, T., Brunson, D., Crespi, C.L., Penman, B.W., Wishnok, J.S., and Tannenbaum, S.R. 1992. DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. USA 89, 3030-3034. https://doi.org/10.1073/pnas.89.7.3030
  53. Outterson, K., Samora, J.B., and Keller-Cuda, K. 2007. Will longer antimicrobial patents improve global public health? Lancet Infect. Dis. 7, 559-566. https://doi.org/10.1016/S1473-3099(07)70188-3
  54. Pacelli, R., Wink, D.A., Cook, J.A., Krishna, M.C., DeGraff, W., Friedman, N., Tsokos, M., Samuni, A., and Mitchell, J.B. 1995. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J. Exp. Med. 182, 1469-1479. https://doi.org/10.1084/jem.182.5.1469
  55. Privett, B.J., Broadnax, A.D., Bauman, S.J., Riccio, D.A., and Schoenfisch, M.H. 2012. Examination of bacterial resistance to exogenous nitric oxide. Nitric Oxide 26, 169-173. https://doi.org/10.1016/j.niox.2012.02.002
  56. Pryor, W.A., Church, D.F., Govindan, C.K., and Crank, G. 1982. Oxidation of thiols by nitric-oxide and nitrogen-dioxide - synthetic utility and toxicological implications. J. Org. Chem. 47, 156-159. https://doi.org/10.1021/jo00340a038
  57. Raulli, R., McElhaney-Feser, G., Hrabie, J., and Cihlar, R. 2002. Antimicrobial properties of nitric oxide using diazeniumdiolates as the nitric oxide donor. Rec. Res. Devel. Microbiol. 6, 177-183.
  58. Riccio, D.A., Dobmeier, K.P., Hetrick, E.M., Privett, B.J., Paul, H.S., and Schoenfisch, M.H. 2009. Nitric oxide-releasing S-nitrosothiol-modified xerogels. Biomaterials 30, 4494-4502. https://doi.org/10.1016/j.biomaterials.2009.05.006
  59. Rubbo, H., Radi, R., Trujillo, M., Telleri, R., Kalyanaraman, B., Barnes, S., Kirk, M., and Freeman, B.A. 1994. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol. Chem. 269, 26066-26075.
  60. Saraiva, J., Marotta-Oliveira, S.S., Cicillini, S.A., Eloy Jde, O., and Marchetti, J.M. 2011. Nanocarriers for nitric oxide delivery. J. Drug. Deliv. 2011, 936438.
  61. Scatena, R., Bottoni, P., Pontoglio, A., and Giardina, B. 2010. Pharmacological modulation of nitric oxide release: new pharmacological perspectives, potential benefits and risks. Curr. Med. Chem. 17, 61-73. https://doi.org/10.2174/092986710789957841
  62. Seabra, A.B. and Duran, N. 2010. Nitric oxide-releasing vehicles for biomedical applications. J Mater. Chem. 20, 1624-1637. https://doi.org/10.1039/b912493b
  63. Seabra, A.B., Martins, D., Simoes, M.M., da Silva, R., Brocchi, M., and de Oliveira, M.G. 2010. Antibacterial nitric oxide-releasing polyester for the coating of blood-contacting artificial materials. Artif. Organs. 34, E204-214. https://doi.org/10.1111/j.1525-1594.2010.00998.x
  64. Seabra, A.B., Pankotai, E., Feher, M., Somlai, A., Kiss, L., Biro, L., Szabo, C., Kollai, M., de Oliveira, M.G., and Lacza, Z. 2007. S-nitrosoglutathione-containing hydrogel increases dermal blood flow in streptozotocin-induced diabetic rats. Br. J. Dermatol. 156, 814-818. https://doi.org/10.1111/j.1365-2133.2006.07718.x
  65. Shin, J.H., Metzger, S.K., and Schoenfisch, M.H. 2007. Synthesis of nitric oxide-releasing silica nanoparticles. J. Am. Chem. Soc. 129, 4612-4619. https://doi.org/10.1021/ja0674338
  66. Singh, R.J., Hogg, N., Joseph, J., and Kalyanaraman, B. 1996. Mechanism of nitric oxide release from S-nitrosothiols. J. Biol. Chem. 271, 18596-18603. https://doi.org/10.1074/jbc.271.31.18596
  67. Souza-Lima Sr, R.A., Cariello, A.J., Bispo Sr, M., De Souza Sr, G., De Oliveira, M., Hofling-Lima, A.L., and Pignatari, A. 2011. Bactericidal effect of nitric oxide donors against clinical isolates from keratitis. Invest. Ophtalmol. Vis. Sci. 52, 5839.
  68. Spellberg, B., Powers, J.H., Brass, E.P., Miller, L.G., and Edwards, J.E., Jr. 2004. Trends in antimicrobial drug development: implications for the future. Clin. Infect. Dis. 38, 1279-1286. https://doi.org/10.1086/420937
  69. Stadler, J., Trockfeld, J., Schmalix, W.A., Brill, T., Siewert, J.R., Greim, H., and Doehmer, J. 1994. Inhibition of cytochromes P4501A by nitric oxide. Proc. Natl. Acad. Sci. USA 91, 3559-3563. https://doi.org/10.1073/pnas.91.9.3559
  70. Thomas, D.D., Ridnour, L.A., Isenberg, J.S., Flores-Santana, W., Switzer, C.H., Donzelli, S., Hussain, P., Vecoli, C., Paolocci, N., Ambs, S., and et al. 2008. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic. Biol. Med. 45, 18-31. https://doi.org/10.1016/j.freeradbiomed.2008.03.020
  71. Wang, J., Teng, Y.H., Hao, Y., Oh-Lee, J., and Mohanty, D.K. 2009. Preparation and properties of polyamines: part II-controlled and sustained release of nitric oxide (NO) from nitrosated polymers. Polym. J. 41, 715-725. https://doi.org/10.1295/polymj.PJ2008335
  72. Wang, P.G., Xian, M., Tang, X., Wu, X., Wen, Z., Cai, T., and Janczuk, A.J. 2002. Nitric oxide donors: chemical activities and biological applications. Chem. Rev. 102, 1091-1134. https://doi.org/10.1021/cr000040l
  73. Wei, X.Q., Charles, I.G., Smith, A., Ure, J., Feng, G.J., Huang, F.P., Xu, D., Muller, W., Moncada, S., and Liew, F.Y. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375, 408-411. https://doi.org/10.1038/375408a0
  74. Wennmalm, A. 1994. Endothelial nitric oxide and cardiovascular disease. J. Intern. Med. 235, 317-327. https://doi.org/10.1111/j.1365-2796.1994.tb01081.x
  75. Wink, D.A. and Mitchell, J.B. 1998. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25, 434-456. https://doi.org/10.1016/S0891-5849(98)00092-6
  76. Wink, D.A., Nims, R.W., Darbyshire, J.F., Christodoulou, D., Hanbauer, I., Cox, G.W., Laval, F., Laval, J., and Cook, J.A. 1994. Reaction kinetics for nitrosation of cysteine and glutathione in aerobic nitric oxide solutions at neutral pH. Insights into the fate and physiological effects of intermediates generated in the NO/O2 reaction. Chem. Res. Toxicol. 7, 519-525. https://doi.org/10.1021/tx00040a007
  77. Wink, D.A., Osawa, Y., Darbyshire, J.F., Jones, C.R., Eshenaur, S.C., and Nims, R.W. 1993. Inhibition of cytochromes P450 by nitric oxide and a nitric oxide-releasing agent. Arch. Biochem. Biophys. 300, 115 -123. https://doi.org/10.1006/abbi.1993.1016
  78. Wink, D.A., Ridnour, L.A., Hussain, S.P., and Harris, C.C. 2008. The reemergence of nitric oxide and cancer. Nitric Oxide 19, 65-67.
  79. Witte, M.B. and Barbul, A. 2002. Role of nitric oxide in wound repair. Am. J. Surg. 183, 406-412. https://doi.org/10.1016/S0002-9610(02)00815-2