The potential of nitric oxide releasing therapies as antimicrobial agents

Virulence

Volumn 3, Issue 3, 2012, Pages 271-279

  Schairer, David O ^a   Chouake, Jason S ^a   Nosanchuk, Joshua D ^a   Friedman, Adam J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Antibiotic; Antimicrobial; Nanotechnology; Nitric oxide

Indexed keywords

CHITOSAN; CYSTEINE; CYTOCHROME P450; DIAZENIUMDIOLATE DERIVATIVE; DINITROGEN TRIOXIDE; DINITROSYL IRON COMPLEX; IRON COMPLEX; LIPOSOME; MACROGOL; METHIONINE; MYELOPEROXIDASE; NANOPARTICLE; NITRIC OXIDE; NITRITE; NITROGEN DIOXIDE; PEROXYNITRITE; PHENYLALANINE; POLYPROPYLENE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; S NITROSOTHIOL; SODIUM NITRITE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG; VANCOMYCIN; ZEOLITE; ANTIINFECTIVE AGENT;

ABSCESS; ACINETOBACTER BAUMANNII; ANTIMICROBIAL ACTIVITY; BACILLUS CEREUS; BACTERIAL INFECTION; BACTERICIDAL ACTIVITY; BACTERIOSTASIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); DNA ALKYLATION; DNA BINDING; DNA REPAIR; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG RESISTANCE; DRUG STRUCTURE; DRUG SYNTHESIS; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENT CELL; LEISHMANIA; LIPID PEROXIDATION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOLLUSCUM CONTAGIOSUM; MUTAGENESIS; NANOENCAPSULATION; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS PYOGENES; TINEA PEDIS; COMMUNICABLE DISEASE; METABOLISM;

FUNGI; HARNESS;

ANTI-INFECTIVE AGENTS; COMMUNICABLE DISEASES; DRUG DELIVERY SYSTEMS; NITRIC OXIDE;

EID: 84862852281     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.20328     Document Type: Review

References (111)

1. Fang FC. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 1997; 99:2818-25; PMID: 9185502; DOI: 10.1172/JCI119473.
2. Tripathi P, Tripathi P, Kashyap L, Singh V. The role of nitric oxide in inflammatory reactions. FEMS Immunol Med Microbiol 2007; 51:443-52; PMID: 17903207; DOI: 10.1111/j.1574-695X.2007.00329.x.
3. Andreakis N, D'Aniello S, Albalat R, Patti FP, Garcia-Fernàndez J, Procaccini G, et al. Evolution of the nitric oxide synthase family in metazoans. Mol Biol Evol 2011; 28:163-79; PMID: 20639231; DOI: 10.1093/molbev/msq179.
4. Joerink M, Savelkoul HFJ, Wiegertjes GF. Evolutionary conservation of alternative activation of macrophages: structural and functional characterization of arginase 1 and 2 in carp (Cyprinus carpio L.). Mol Immunol 2006; 43:1116-28; PMID: 16257446; DOI: 10.1016/j.molimm.2005.07.022.
5. Privett BJ, Broadnax AD, Bauman SJ, Riccio DA, Schoenfisch MH. Examination of bacterial resistance to exogenous nitric oxide. Nitric Oxide 2012; 26:169-73; PMID: 22349019; DOI: 10.1016/j.niox.2012.02.002.
6. Ghaffari A, Miller CC, McMullin B, Ghahary A. Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide 2006; 14:21-9; PMID: 16188471; DOI: 10.1016/j.niox.2005.08.003.
7. 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; PMID: 18457680; DOI: 10.1016/j.niox.2008.04.003.
8. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 1997; 15:323-50; PMID: 9143691; DOI: 10.1146/annurev.immunol.15.1.323.
9. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001; 2:907-16; PMID: 11577346; DOI: 10.1038/ni1001-907.
10. Durand JL, Mukherjee S, Commodari F, De Souza AP, Zhao D, Machado FS, et al. Role of NO synthase in the development of Trypanosoma cruzi-induced cardiomyopathy in mice. Am J Trop Med Hyg 2009; 80:782-7; PMID: 19407124.
11. Cui X, Besch V, Khaibullina A, Hergen A, Quezado M, Eichacker P, et al. Neuronal nitric oxide synthase deficiency decreases survival in bacterial peritonitis and sepsis. Intensive Care Med 2007; 33:1993-2003; PMID: 17684724; DOI: 10.1007/s00134-007-0814-9.
12. Bogdan C. Regulation of lymphocytes by nitric oxide. Methods Mol Biol 2011; 677:375-93; PMID: 20941622; DOI: 10.1007/978-1-60761-869-0_24.
13. Wink DA, Mitchell JB. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 1998; 25:434-56; PMID: 9741580; DOI: 10.1016/S0891-5849(98)00092-6.
14. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, et al. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 2008; 45:18-31; PMID: 18439435; DOI: 10.1016/j.freeradbiomed.2008.03.020.
15. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 1997; 15:323-50; PMID: 9143691; DOI: 10.1146/annurev.immunol.15.1.323.
16. Jones ML, Ganopolsky JG, Labbé A, Wahl C, Prakash S. Antimicrobial properties of nitric oxide and its application in antimicrobial formulations and medical devices. Appl Microbiol Biotechnol 2010; 88:401-7; PMID: 20680266; DOI: 10.1007/s00253-010-2733-x.
17. Wink DA, Grisham MB, Mitchell JB, Ford PC. Direct and indirect effects of nitric oxide in chemical reactions relevant to biology. In: Lester P, ed. Methods in Enzymology. Vol Volume 268: Academic Press; 1996:12-31.
18. Fang FC. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2004; 2:820-32; PMID: 15378046; DOI: 10.1038/nrmicro1004.
19. Gow AJ, Buerk DG, Ischiropoulos H. A novel reaction mechanism for the formation of S-nitrosothiol in vivo. J Biol Chem 1997; 272:2841-5; PMID: 9006926; DOI: 10.1074/jbc.272.5.2841.
20. Ischiropoulos H, al-Mehdi AB. Peroxynitrite-mediated oxidative protein modifications. FEBS Lett 1995; 364:279-82; PMID: 7758583; DOI: 10.1016/0014-5793(95)00307-U.
21. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, et al. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 1991; 254:1001-3; PMID: 1948068; DOI: 10.1126/science.1948068.
22. Juedes MJ, Wogan GN. Peroxynitrite-induced mutation spectra of pSP189 following replication in bacteria and in human cells. Mutat Res 1996; 349:51-61; PMID: 8569792; DOI: 10.1016/0027-5107(95)00152-2.
23. Maragos CM, Andrews AW, Keefer LK, Elespuru RK. Mutagenicity of glyceryl trinitrate (nitroglycerin) in Salmonella typhimurium. Mutat Res 1993; 298:187-95; PMID: 7678153; DOI: 10.1016/0165-1218(93)90040-K.
24. Laval F, Wink DA, Laval J. A discussion of mechanisms of NO genotoxicity: implication of inhibition of DNA repair proteins. Rev Physiol Biochem Pharmacol 1997; 131:175-91; PMID: 9204692.
25. Laval F, Wink DA. Inhibition by nitric oxide of the repair protein, O6-methylguanine-DNA-methyltransferase. Carcinogenesis 1994; 15:443-7; PMID: 8118926; DOI: 10.1093/carcin/15.3.443.
26. Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, et al. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J Biol Chem 1994; 269:26066-75; PMID: 7929318.
27. Deupree SM, Schoenfisch MH. Morphological analysis of the antimicrobial action of nitric oxide on gram-negative pathogens using atomic force microscopy. Acta Biomater 2009; 5:1405-15; PMID: 19250890; DOI: 10.1016/j.actbio.2009.01.025.
28. Abouhamad WN, Manson M, Gibson MM, Higgins CF. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol Microbiol 1991; 5:1035-47; PMID: 1956284; DOI: 10.1111/j.1365-2958.1991.tb01876.x.
29. Morris SL, Hansen JN. Inhibition of Bacillus cereus spore outgrowth by covalent modification of a sulfhydryl group by nitrosothiol and iodoacetate. J Bacteriol 1981; 148:465-71; PMID: 6795179.
30. Kim YM, Bergonia HA, Müller C, Pitt BR, Watkins WD, Lancaster JR. Nitric oxide and intracellular heme. Adv Pharmacol 1995; 34:277-91; PMID: 8562440; DOI: 10.1016/S1054-3589(08)61092-3.
31. Björne H, Weitzberg E, Lundberg JO. Intragastric generation of antimicrobial nitrogen oxides from saliva--physiological and therapeutic considerations. Free Radic Biol Med 2006; 41:1404-12; PMID: 17023267; DOI: 10.1016/j.freeradbiomed.2006.07.020.
32. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 2008; 7:156-67; PMID: 18167491; DOI: 10.1038/nrd2466.
33. Weller R, Price RJ, Ormerod AD, Benjamin N, Leifert C. Antimicrobial effect of acidified nitrite on dermatophyte fungi, Candida and bacterial skin pathogens. J Appl Microbiol 2001; 90:648-52; PMID: 11309079; DOI: 10.1046/j.1365-2672.2001.01291.x.
34. Weller R, Finnen MJ. The effects of topical treatment with acidified nitrite on wound healing in normal and diabetic mice. Nitric Oxide 2006; 15:395-9; PMID: 16731016; DOI: 10.1016/j.niox.2006.04.002.
35. Pacelli R, Wink DA, Cook JA, Krishna MC, DeGraff W, Friedman N, et al. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J Exp Med 1995; 182:1469-79; PMID: 7595217; DOI: 10.1084/jem.182.5.1469.
36. Fang FC. Antimicrobial actions of reactive oxygen species. MBio 2011; 2; PMID: 21896680; DOI: 10.1128/mBio.00141-11.
37. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001; 2:907-16; PMID: 11577346; DOI: 10.1038/ni1001-907.
38. Ghaffari A, Jalili R, Ghaffari M, Miller C, Ghahary A. Efficacy of gaseous nitric oxide in the treatment of skin and soft tissue infections. Wound Repair Regen 2007; 15:368-77; PMID: 17537124; DOI: 10.1111/j.1524-475X.2007.00239.x.
39. Friedman AJ, Blecher K, Schairer D, Tuckman-Vernon C, Nacharaju P, Sanchez D, et al. Improved antimicrobial efficacy with nitric oxide releasing nanoparticle generated S-nitrosoglutathione. Nitric Oxide 2011; 25:381-6; PMID: 21946032; DOI: 10.1016/j.niox.2011.09.001.
40. Englander L, Friedman A. Nitric oxide nanoparticle technology: a novel antimicrobial agent in the context of current treatment of skin and soft tissue infection. J Clin Aesthet Dermatol 2010; 3:45-50; PMID: 20725551.
41. Christman MF, Morgan RW, Jacobson FS, Ames BN. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 1985; 41:753-62; PMID: 2988786; DOI: 10.1016/S0092-8674(85)80056-8.
42. Richardson AR, Dunman PM, Fang FC. The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol Microbiol 2006; 61:927-39; PMID: 16859493; DOI: 10.1111/j.1365-2958.2006.05290.x.
43. Richardson AR, Libby SJ, Fang FC. A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 2008; 319:1672-6; PMID: 18356528; DOI: 10.1126/science.1155207.
44. Hetrick EM. Antimicrobial and wound healing properties of nitric oxide-releasing xerogels and silica nanoparticles. University of North Carolina; 2008.
45. Hetrick EM, Shin JH, Paul HS, Schoenfisch MH. Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. Biomaterials 2009; 30:2782-9; PMID: 19233464; DOI: 10.1016/j.biomaterials.2009.01.052.
46. De Groote MA, Fang FC. NO inhibitions: antimicrobial properties of nitric oxide. Clin Infect Dis 1995; 21:S162-5; PMID: 8845445; DOI: 10.1093/clinids/21.Supplement_2.S162.
47. Ghaffari A, Neil DH, Ardakani A, Road J, Ghahary A, Miller CC. A direct nitric oxide gas delivery system for bacterial and mammalian cell cultures. Nitric Oxide 2005; 12:129-40; PMID: 15797841; DOI: 10.1016/j.niox.2005.01.006.
48. Miller C, McMullin B, Ghaffari A, Stenzler A, Pick N, Roscoe D, et al. Gaseous nitric oxide bactericidal activity retained during intermittent high-dose short duration exposure. Nitric Oxide 2009; 20:16-23; PMID: 18789393; DOI: 10.1016/j.niox.2008.08.002.
49. Ghaffari A, Jalili R, Ghaffari M, Miller C, Ghahary A. Efficacy of gaseous nitric oxide in the treatment of skin and soft tissue infections. Wound Repair Regen 2007; 15:368-77; PMID: 17537124; DOI: 10.1111/j.1524-475X.2007.00239.x.
50. Ichinose F, Roberts JD, Zapol WM. Inhaled nitric oxide: a selective pulmonary vasodilator: current uses and therapeutic potential. Circulation 2004; 109:3106-11; PMID: 15226227; DOI: 10.1161/01.CIR.0000134595.80170.62.
51. Angus DC, Clermont G, Watson RS, Linde-Zwirble WT, Clark RH, Roberts MS. Cost-effectiveness of inhaled nitric oxide in the treatment of neonatal respiratory failure in the United States. Pediatrics 2003; 112:1351-60; PMID: 14654609; DOI: 10.1542/peds.112.6.1351.
52. Jones ML, Ganopolsky JG, Labbé A, Prakash S. A novel nitric oxide producing probiotic patch and its antimicrobial efficacy: preparation and in vitro analysis. Appl Microbiol Biotechnol 2010; 87:509-16; PMID: 20300748; DOI: 10.1007/s00253-010-2490-x.
53. Jones M, Ganopolsky JG, Labbé A, Gilardino M, Wahl C, Martoni C, et al. Novel nitric oxide producing probiotic wound healing patch: preparation and in vivo analysis in a New Zealand white rabbit model of ischaemic and infected wounds. Int Wound J 2012;:no-, no; PMID: 22221913; DOI: 10.1111/j.1742-481X.2011.00889.x.
54. Ormerod AD, Copeland P, Hay I, Husain A, Ewen SW. The inflammatory and cytotoxic effects of a nitric oxide releasing cream on normal skin. J Invest Dermatol 1999; 113:392-7; PMID: 10469339; DOI: 10.1046/j.1523-1747.1999.00692.x.
55. Weller R, Ormerod AD, Hobson RP, Benjamin NJ. A randomized trial of acidified nitrite cream in the treatment of tinea pedis. J Am Acad Dermatol 1998; 38:559-63; PMID: 9555794; DOI: 10.1016/S0190-9622(98)70117-3.
56. Ormerod AD, White MI, Shah SAA, Benjamin N. Molluscum contagiosum effectively treated with a topical acidified nitrite, nitric oxide liberating cream. Br J Dermatol 1999; 141:1051-3; PMID: 10606851; DOI: 10.1046/j.1365-2133.1999.03204.x.
57. Phillips R, Adjei O, Lucas S, Benjamin N, Wansbrough-Jones M. Pilot randomized double-blind trial of treatment of Mycobacterium ulcerans disease (Buruli ulcer) with topical nitrogen oxides. Antimicrob Agents Chemother 2004; 48:2866-70; PMID: 15273093; DOI: 10.1128/AAC.48.8.2866-2870.2004.
58. Ormerod AD, Shah AA, Li H, Benjamin NB, Ferguson GP, Leifert C. An observational prospective study of topical acidified nitrite for killing methicillin-resistant Staphylococcus aureus (MRSA) in contaminated wounds. BMC Res Notes 2011; 4:458; PMID: 22032298; DOI: 10.1186/1756-0500-4-458.
59. Davidson RN, Yardley V, Croft SL, Konecny P, Benjamin N. A topical nitric oxide-generating therapy for cutaneous leishmaniasis. Trans R Soc Trop Med Hyg 2000; 94:319-22; PMID: 10975011; DOI: 10.1016/S0035-9203(00)90341-9.
60. Daiber A, Wenzel P, Oelze M, Münzel T. New insights into bioactivation of organic nitrates, nitrate tolerance and cross-tolerance. Clin Res Cardiol 2008; 97:12-20; PMID: 17938848; DOI: 10.1007/s00392-007-0588-7.
61. Bátai I, Kerényi M, Tekeres M. The growth of bacteria in intravenous glyceryl trinitrate and in sodium nitroprusside. Anesth Analg 1999; 89:1570-2; PMID: 10589651; DOI: 10.1213/00000539-199912000-00049.
62. Barraud N, Storey MV, Moore ZP, Webb JS, Rice SA, Kjelleberg S. Nitric oxide-mediated dispersal in single-and multi-species biofilms of clinically and industrially relevant microorganisms. Microb Biotechnol 2009; 2:370-8; PMID: 21261931; DOI: 10.1111/j.1751-7915.2009.00098.x.
63. Maragos CM, Morley D, Wink DA, Dunams TM, Saavedra JE, Hoffman A, et al. Complexes of. NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects. J Med Chem 1991; 34:3242-7; PMID: 1956043; DOI: 10.1021/jm00115a013.
64. Miller MR, Megson IL. Recent developments in nitric oxide donor drugs. Br J Pharmacol 2007; 151:305-21; PMID: 17401442; DOI: 10.1038/sj.bjp.0707224.
65. Keefer LK. Nitric oxide (NO)-and nitroxyl (HNO)-generating diazeniumdiolates (NONOates): emerging commercial opportunities. Curr Top Med Chem 2005; 5:625-36; PMID: 16101424; DOI: 10.2174/1568026054679380.
66. Kröncke K-D, Suschek CV. Adulterated effects of nitric oxide-generating donors. J Invest Dermatol 2008; 128:258-60; PMID: 18195740; DOI: 10.1038/sj.jid.5701162.
67. Keefer LK. Progress toward clinical application of the nitric oxide-releasing diazeniumdiolates. Annu Rev Pharmacol Toxicol 2003; 43:585-607; PMID: 12415121; DOI: 10.1146/annurev.pharmtox.43.100901.135831.
68. Tabor H, Tabor CW. Biosynthesis and Metabolism of 1,4-diaminobutane, Spermidine, Spermine, and Related Amines. Advances in Enzymology and Related Areas of Molecular Biology: John Wiley & Sons, Inc.; 2006:203-268.
69. Raulli R, McElhaney-Feser G, Hrabie J, Cihlar R. Antimicrobial properties of nitric oxide using diazeniumdiolates as the nitric oxide donor. Rec Res Devel Microbiol. 2002; 6:177-83.
70. Dukelow AM, Weicker S, Karachi TA, Razavi HM, McCormack DG, Joseph MG, et al. Effects of nebulized diethylenetetraamine-NONOate in a mouse model of acute Pseudomonas aeruginosa pneumonia. Chest 2002; 122:2127-36; PMID: 12475857; DOI: 10.1378/chest.122.6.2127.
71. McElhaney-Feser GE, Raulli RE, Cihlar RL. Synergy of nitric oxide and azoles against Candida species in vitro. Antimicrob Agents Chemother 1998; 42:2342-6; PMID: 9736560.
72. Konter J, Möllmann U, Lehmann J. NO-donors. Part 17: Synthesis and antimicrobial activity of novel ketoconazole-NO-donor hybrid compounds. Bioorg Med Chem 2008; 16:8294-300; PMID: 18710813; DOI: 10.1016/j.bmc.2008.05.008.
73. Nablo BJ, Prichard HL, Butler RD, Klitzman B, Schoenfisch MH. Inhibition of implant-associated infections via nitric oxide release. Biomaterials 2005; 26:6984-90; PMID: 15978663; DOI: 10.1016/j.biomaterials.2005.05.017.
74. Nablo BJ, Rothrock AR, Schoenfisch MH. Nitric oxide-releasing sol-gels as antibacterial coatings for orthopedic implants. Biomaterials 2005; 26:917-24; PMID: 15353203; DOI: 10.1016/j.biomaterials.2004.03.031.
75. Engelsman AF, Krom BP, Busscher HJ, van Dam GM, Ploeg RJ, van der Mei HC. Antimicrobial effects of an NO-releasing poly(ethylene vinylacetate) coating on soft-tissue implants in vitro and in a murine model. Acta Biomater 2009; 5:1905-10; PMID: 19251498; DOI: 10.1016/j.actbio.2009.01.041.
76. Shin JH, Metzger SK, Schoenfisch MH. Synthesis of nitric oxide-releasing silica nanoparticles. J Am Chem Soc 2007; 129:4612-9; PMID: 17375919; DOI: 10.1021/ja0674338.
77. Charville GW, Hetrick EM, Geer CB, Schoenfisch MH. Reduced bacterial adhesion to fibrinogen-coated substrates via nitric oxide release. Biomaterials 2008; 29:4039-44; PMID: 18657857; DOI: 10.1016/j.biomaterials.2008.07.005.
78. Nablo BJ, Schoenfisch MH. In vitro cytotoxicity of nitric oxide-releasing sol-gel derived materials. Biomaterials 2005; 26:4405-15; PMID: 15701369; DOI: 10.1016/j.biomaterials.2004.11.015.
79. Bhide M. Nitric oxide delivery from polymeric wound dressings. The University Of Akron; 2006.
80. Dicks AP, Swift HR, Williams DLH, Butler AR, Al-Sa'doni HH, Cox BG. Identification of Cu+ as the effective reagent in nitric oxide formation from S-nitrosothiols (RSNO). Journal of the Chemical Society, Perkin Transactions 2 1996; 4.
81. Holmes AJ, Williams DLH. Reaction of ascorbic acid with S-nitrosothiols: clear evidence for two distinct reaction pathways. Journal of the Chemical Society, Perkin Transactions 2 2000; 8.
82. Singh RJ, Hogg N, Joseph J, Kalyanaraman B. Mechanism of nitric oxide release from S-nitrosothiols. J Biol Chem 1996; 271:18596-603; PMID: 8702510; DOI: 10.1074/jbc.271.31.18596.
83. Hogg N. Biological chemistry and clinical potential of S-nitrosothiols. Free Radic Biol Med 2000; 28:1478-86; PMID: 10927172; DOI: 10.1016/S0891-5849(00)00248-3.
84. Laver JR, Stevanin TM, Messenger SL, Lunn AD, Lee ME, Moir JW, et al. Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: a novel mechanism of bacterial pathogenesis. FASEB J 2010; 24:286-95; PMID: 19720623; DOI: 10.1096/fj.08-128330.
85. Souza-Lima RA, Cariello AJ, Bispo M, et al. Bactericidal Effect Of Nitric Oxide Donors Against Clinical Isolates From Keratitis. Invest Ophthalmol Vis Sci 2011; 52:5839-41.
86. Marcinkiewicz J. Nitric oxide and antimicrobial activity of reactive oxygen intermediates. Immunopharmacology 1997; 37:35-41; PMID: 9285242; DOI: 10.1016/S0162-3109(96)00168-3.
87. Richie JP, Skowronski L, Abraham P, Leutzinger Y. Blood glutathione concentrations in a large-scale human study. Clin Chem 1996; 42:64-70; PMID: 8565235.
88. Bryan NS, Rassaf T, Maloney RE, Rodriguez CM, Saijo F, Rodriguez JR, et al. Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo. Proc Natl Acad Sci U S A 2004; 101:4308-13; PMID: 15014175; DOI: 10.1073/pnas.0306706101.
89. de Souza GFP, Yokoyama-Yasunaka JKU, Seabra AB, Miguel DC, de Oliveira MG, Uliana SRB. Leishmanicidal activity of primary S-nitrosothiols against Leishmania major and Leishmania amazonensis: implications for the treatment of cutaneous leishmaniasis. Nitric Oxide 2006; 15:209-16; PMID: 16527502; DOI: 10.1016/j.niox.2006.01.011.
90. Vespa GN, Cunha FQ, Silva JS. Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro. Infect Immun 1994; 62:5177-82; PMID: 7523307.
91. Rockett KA, Awburn MM, Cowden WB, Clark IA. Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun 1991; 59:3280-3; PMID: 1879941.
92. Cariello AJ, de Souza GFP, Foronda AS, Yu MCZ, Hofling-Lima AL, de Oliveira MG. In vitro amoebicidal activity of S-nitrosoglutathione and S-nitroso-N-acetylcysteine against trophozoites of Acanthamoeba castellanii. J Antimicrob Chemother 2010; 65:588-91; PMID: 20085996; DOI: 10.1093/jac/dkp485.
93. Ishima Y, Sawa T, Kragh-Hansen U, Miyamoto Y, Matsushita S, Akaike T, et al. S-Nitrosylation of human variant albumin Liprizzi (R410C) confers potent antibacterial and cytoprotective properties. J Pharmacol Exp Ther 2007; 320:969-77; PMID: 17135341; DOI: 10.1124/jpet.106.114959.
94. López-Jaramillo P, Ruano C, Rivera J, Terán E, Salazar-Irigoyen R, Esplugues JV, et al. Treatment of cutaneous leishmaniasis with nitric-oxide donor. Lancet 1998; 351:1176-7; PMID: 9643692; DOI: 10.1016/S0140-6736(05)79119-4.
95. Wheatley PS, Butler AR, Crane MS, Fox S, Xiao B, Rossi AG, et al. NO-releasing zeolites and their antithrombotic properties. J Am Chem Soc 2006; 128:502-9; PMID: 16402837; DOI: 10.1021/ja0503579.
96. Fox S, Wilkinson TS, Wheatley PS, Xiao B, Morris RE, Sutherland A, et al. NO-loaded Zn(2+)-exchanged zeolite materials: a potential bifunctional anti-bacterial strategy. Acta Biomater 2010; 6:1515-21; PMID: 19861185; DOI: 10.1016/j.actbio.2009.10.038.
97. Narin G, Albayrak ÇB, Ülkü S. Antibacterial and bactericidal activity of nitric oxide-releasing natural zeolite. Appl Clay Sci 2010; 50:560-8; DOI: 10.1016/j.clay.2010.10.013.
98. Jin Y, Lohstreter S, Pierce DT, et al. Silica Nanoparticles with Continuously Tunable Sizes: Synthesis and Size Effects on Cellular Contrast Imaging. Chemistry of Materials. 2008; 20:4411-9; DOI: 10.1021/cm8007478.
99. Carpenter AW, Slomberg DL, Rao KS, Schoenfisch MH. Influence of scaffold size on bactericidal activity of nitric oxide-releasing silica nanoparticles. ACS Nano 2011; 5:7235-44; PMID: 21842899; DOI: 10.1021/nn202054f.
100. Hetrick EM, Shin JH, Paul HS, Schoenfisch MH. Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. Biomaterials 2009; 30:2782-9; PMID: 19233464; DOI: 10.1016/j.biomaterials.2009.01.052.
101. Ray A, Friedman BA, Friedman JM. Trehalose glass-facilitated thermal reduction of metmyoglobin and methemoglobin. J Am Chem Soc 2002; 124:7270-1; PMID: 12071726; DOI: 10.1021/ja0201348.
102. Navati MS, Friedman JM. Sugar-derived glasses support thermal and photo-initiated electron transfer processes over macroscopic distances. J Biol Chem 2006; 281:36021-8; PMID: 17005567; DOI: 10.1074/jbc.M606866200.
103. Rabea EI, Badawy MET, Stevens CV, Smagghe G, Steurbaut W. Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 2003; 4:1457-65; PMID: 14606868; DOI: 10.1021/bm034130m.
104. Cabrales P, Han G, Roche C, Nacharaju P, Friedman AJ, Friedman JM. Sustained release nitric oxide from long-lived circulating nanoparticles. Free Radic Biol Med 2010; 49:530-8; PMID: 20460149; DOI: 10.1016/j.freeradbiomed.2010.04.034.
105. Friedman A, Blecher K, Sanchez D, Tuckman-Vernon C, Gialanella P, Friedman JM, et al. Susceptibility of Gram-positive and-negative bacteria to novel nitric oxide-releasing nanoparticle technology. Virulence 2011; 2:217-21; PMID: 21577055; DOI: 10.4161/viru.2.3.16161.
106. Friedman AJ, Blecher K, Schairer D, Tuckman-Vernon C, Nacharaju P, Sanchez D, et al. Improved antimicrobial efficacy with nitric oxide releasing nanoparticle generated S-nitrosoglutathione. Nitric Oxide 2011; 25:381-6; PMID: 21946032; DOI: 10.1016/j.niox.2011.09.001.
107. Martinez LR, Han G, Chacko M, Mihu MR, Jacobson M, Gialanella P, et al. Antimicrobial and healing efficacy of sustained release nitric oxide nanoparticles against Staphylococcus aureus skin infection. J Invest Dermatol 2009; 129:2463-9; PMID: 19387479; DOI: 10.1038/jid.2009.95.
108. Han G, Martinez LR, Mihu MR, Friedman AJ, Friedman JM, Nosanchuk JD. Nitric oxide releasing nanoparticles are therapeutic for Staphylococcus aureus abscesses in a murine model of infection. PLoS One 2009; 4:e7804; PMID: 19915659; DOI: 10.1371/journal.pone.0007804.
109. Mihu MR, Sandkovsky U, Han G, Friedman JM, Nosanchuk JD, Martinez LR. The use of nitric oxide releasing nanoparticles as a treatment against Acinetobacter baumannii in wound infections. Virulence 2010; 1:62-7; PMID: 21178416; DOI: 10.4161/viru.1.2.10038.
110. Schairer D, Martinez LR, Blecher K, Chouake J, Nacharaju P, Gialanella P, et al. Nitric oxide nanoparticles: Pre-clinical utility as a therapeutic for intramuscular abscesses. Virulence 2012; 3:62-7; PMID: 22286699; DOI: 10.4161/viru.3.1.18816.
111. Han G, Nguyen LN, Macherla C, Chi Y, Friedman JM, Nosanchuk JD, et al. Nitric oxide-releasing nanoparticles accelerate wound healing by promoting fibroblast migration and collagen deposition. Am J Pathol 2012; 180:1465-73; PMID: 22306734; DOI: 10.1016/j.ajpath.2011.12.013.