Use of nitric oxide nanoparticulate platform for the treatment of skin and soft tissue infections

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 5, Issue 5, 2013, Pages 502-514

  Kutner, Allison J ^a   Friedman, Adam J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTI-MICROBIAL ACTIVITY; ANTIMICROBIAL ACTION; CONTROLLED RELEASE; MECHANISMS OF RESISTANCES; NANO PARTICULATES; PHYSIOLOGIC FUNCTION; SOFT TISSUE INFECTIONS; STORAGE AND DELIVERY;

MICROORGANISMS;

NITRIC OXIDE;

1 [N (2 AMINOETHYL) N ( AMMONIOETHYL)AMINO]DIAZEN 1 IUM 1,2 DIOLATE; AMINOGUANIDINE; ANTIBIOTIC AGENT; ANTIFUNGAL AGENT; ANTIPARASITIC AGENT; N ACETYL S NITROSOCYSTEINE; NANOPARTICLE; NITRIC OXIDE; NITRITE; ORGANIC NITRATE; PROBIOTIC AGENT; S NITROSOGLUTATHIONE; S NITROSOTHIOL; SILICON DIOXIDE; UNCLASSIFIED DRUG; ZEOLITE;

ACINETOBACTER BAUMANNII; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIFUNGAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ANTIVIRAL ACTIVITY; BURKHOLDERIA CEPACIA; BURN INFECTION; CANDIDA ALBICANS; CHAGAS DISEASE; CONTROLLED RELEASE FORMULATION; CRYPTOCOCCUS NEOFORMANS; CYTOTOXICITY; DENGUE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG STORAGE; DRUG STRUCTURE; HUMAN; IMMUNITY; IMMUNOMODULATION; IN VITRO STUDY; INFECTION RISK; INNATE IMMUNITY; LACTOBACILLUS FERMENTUM; LEISHMANIA; LEISHMANIA MAJOR; LISTERIOSIS; MALARIA FALCIPARUM; MOLECULAR WEIGHT; MOLLUSCUM CONTAGIOSUM; NANOENCAPSULATION; NANOTECHNOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROPIONIBACTERIUM ACNES; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SERRATIA MARCESCENS; SIDE EFFECT; SKIN ABSCESS; SKIN INFECTION; SKIN IRRITATION; SOFT TISSUE INFECTION; STAPHYLOCOCCUS; STREPTOCOCCUS AGALACTIAE; TACHYPHYLAXIS; TINEA PEDIS; TINEA VERSICOLOR; TOXOPLASMA GONDII; TOXOPLASMOSIS; TRICHOPHYTON MENTAGROPHYTES; TRICHOPHYTON RUBRUM; WOUND HEALING; WOUND INFECTION;

ANIMALS; ANTI-INFECTIVE AGENTS; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, BACTERIAL; HUMANS; MICE; NANOPARTICLES; NANOTECHNOLOGY; NITRIC OXIDE; SKIN DISEASES, INFECTIOUS; SOFT TISSUE INFECTIONS; STAPHYLOCOCCAL SKIN INFECTIONS; WOUND HEALING;

EID: 84884815789     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1230     Document Type: Review

References (73)

1. Friedman A, Blecher K, Sanchez D, Tuckman-Vernon C, Gialanella P, Friedman J, Martinez L, Nosanchuk J. Susceptibility of Gram-positive and -negative bacteria to novel nitric oxide-releasing nanoparticle technology. Virulence 2011, 2:217-221.
2. Marra F, Patrick D, Chong M, McKay R, Hoang L, Bowie W. Population-based study of the increased incidence of skin and soft tissue infections and associated antimicrobial use. Antimicrob Agents Chemother 2012, 56:6243-6249.
3. Huttner B, Goossens H, Verheij T, Harbarth S, on behalf of the CHAMP consortium. Characteristics and outcomes of public campaigns aimed at improving the use of antibiotics in outpatients in high-income countries. Lancet Infect Dis 2010, 10:17-31.
4. 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.
5. Lautz T, Raval M, Barsness K. Increasing national burden of hospitalizations for skin and soft tissue infections in children. J Pediatr Surg 2011, 46:1935-1941.
6. Frei C, Makos B, Daniels K, Oramasionwu C. Emergence of community-acquired methicillin-resistant Staphylococcus aureus skin and soft tissue infections as a common cause of hospitalization in United States children. J Pediatr Surg 2010, 45:1967-1974.
7. Miller C, McMullin B, Ghaffari A, Miller J, Stenzler A, Pick N, Roscoe D, Ghahary A, Road J, Av Gay Y. Gaseous nitric oxide bactericidal activity retained during intermittent high-dose short duration exposure. Nitric Oxide 2009, 20:16-23.
8. Privett B, Broadnax A, Bauman S, Riccio D, Schoenfisch MH. Examination of bacterial resistance to exogenous nitric oxide. Nitric Oxide 2012, 26:169-173.
9. Del Rosso J. Wound care in the dermatology office: where are we in 2011? J Am Acad Dermatol 2011, 64:S1-S7.
10. Hetrick EM, Shin JH, Stasko NA, Johnson CB, Wespe DA, Holmuhamedov E, Schoenfisch MH. Bactericidal efficacy of nitric oxide-releasing silica nanoparticles. ACS Nano 2008, 2:235-246.
11. McElhaney-Feser G, Raulli R, Cihlar R. Synergy of nitric oxide and azoles against Candida species in vitro. Antimicrob Agents Chemother 1998, 42:2342-2346.
12. Carpenter A, Slomberg D, Rao K, Schoenfisch M. Influence of scaffold size on bactericidal activity of nitric oxide-releasing silica nanoparticles. ACS Nano 2011, 5:7235-7244.
13. Fang FC. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 1997, 99:2818-2825.
14. Green S, Nacy C. Antimicrobial and immunopathologic effects of cytokine-induced nitric oxide synthesis. Curr Opin Infect Dis 1993, 6:384-396.
15. Schairer D, Chouake J, Nosanchuk J, Friedman A. The potential of nitric oxide releasing therapies as antimicrobial agents. Virulence 2012, 3:271-279.
16. Friedman A, Han G, Navati M, Chacko M, Gunther L, Alfieri A, Friedman J. 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.
17. Cabrales P. Nanoengineering bactericidal nitric oxide therapies. Virulence 2011, 2:185-187.
18. Weller R. Nitric oxide-containing nanoparticles as an antimicrobial agent and enhancer of wound healing. J Invest Dermatol 2009, 129:2335-2337.
19. Shin J, Metzger S, Schoenfisch M. Synthesis of nitric oxide-releasing silica nanoparticles. J Am Chem Soc 2007, 129:4612-4619.
20. Pacelli R, Wink D, Cook JK, Krishna MC, DeGraff W, Friedman N, Tsokos M, Samuni A, Mitchell J. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J Exp Med 1995, 182:1469-1479.
21. Ormerod A, Copeland P, Hay I, Husain A, Ewen S. The inflammatory and cytotoxic effects of a nitric oxide releasing cream on normal skin. J Invest Dermatol 1999, 113:392-397.
22. Medeiros R, Figueiredo C, Passos G, Calixto J. Reduced skin inflammatory response in mice lacking inducible nitric oxide synthase. Biochem Pharmacol 2009, 78:390-395.
23. Friedman A, Friedman J. New biomaterials for the sustained release of nitric oxide: past, present and future. Expert Opin Drug Deliv 2009, 6:1113-1122.
24. Bruch-Gerharz D, Ruzicka T, Kolb-Bachofen V. Nitric oxide in human skin: current status and future prospects. J Invest Dermatol 1998, 110:1-7.
25. Jones ML, Ganopolsky JG, Labbe A, Prakash S. A novel nitric oxide producing probiotic patch and its antimicrobial efficacy: preparation and in vitro analysis. Appl Microbiol Biotechnol 2010, 87:509-516.
26. Ghaffari A, Neil D, Ardakani A, Road J, Ghahary A, Miller C. A direct nitric oxide gas delivery system for bacterial and mammalian cell cultures. Nitric Oxide 2005, 12:129-140.
27. Nacharaju P, Tuckman-Vernon C, Maier KE, Chouake J, Friedman A, Cabrales P, Friedman JM. A nanoparticle delivery vehicle for S-nitroso-N-acetyl cysteine: sustained vascular response. Nitric Oxide 2012, 27:150-160.
28. Cariello A, Bispo P, de Souza G, Pignatari A, de Oliveira M, Hofling-Lima A. Bactericidal effect of S-nitrosothiols against clinical isolates from keratitis. Clin Ophthalmol 2012, 6:1907-1914.
29. De Groote MA, Fang FC. NO inhibitions: antimicrobial properties of nitric oxide. Clin Infect Dis 1995, 21(suppl 2):S162-S165.
30. Weller R, Price R, Ormerod A, Benjamin N, Leifert C. Antimicrobial effect of acidified nitrite on dermatophyte fungi, Candida and bacterial skin pathogens. J Appl Microbiol 2001, 90:648-652.
31. Sanchez D, Nosanchuk J, Friedman A. The purview of nitric oxide nanoparticle therapy in infection and wound healing. Nanomedicine 2012, 7:933-936.
32. Flatley J, Barrett J, Pullman S, Hughes M, Green J, Poole R. Transcriptional responses of Escherichia coli to S-nitrosoglutathione under defined chemostat conditions reveal major changes in methionine biosynthesis. J Biol Chem 2005, 280:10065-10072.
33. Schairer D, Martinez L, Blecher K, Chouake J, Nacharaju P, Gialanella P, Friedman J, Nosanchuk J, Friedman A. Nitric oxide nanoparticles: pre-clinical utility as a therapeutic for intramuscular abscesses. Virulence 2012, 3:62-67.
34. Friedman AJ, Blecher K, Schairer D, Tuckman-Vernon C, Nacharaju P, Sanchez D, Gialanella P, Martinez LR, Friedman JM, Nosanchuk JD. Improved antimicrobial efficacy with nitric oxide releasing nanoparticle generated S-nitrosoglutathione. Nitric Oxide 2011, 25:381-386.
35. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001, 2:907-916.
36. MacLean A, Wei X, Huang F, Al-Alem U, Chan W, Liew F. Mice lacking inducible nitric-oxide synthase are more susceptible to herpes simplex virus infection despite enhanced Th1 cell responses. J Gen Virol 1998, 79:825-830.
37. Fagundes C, Costa V, Cisalpino D, Amaral FS, Souza PR, Souza RS, Ryffel B, Vieira L, Silva T, Atrasheuskaya A, et al. IFN-γ production depends on IL-12 and IL-18 combined action and mediates host resistance to dengue virus infection in a nitric oxide-dependent manner. PLoS One Trop Dis 2011, 5:1449.
38. Zhou X, Potoka D, Boyle P, Nadler E, McGinnis K, Ford H. Aminoguanidine renders inducible nitric oxide synthase knockout mice more susceptible to Salmonella typhimurium infection. FEMS Microbiol Lett 2002, 206:93-97.
39. MacFarlane A, Schwacha M, Eisenstein T. In vivo blockage of nitric oxide with aminoguanidine inhibits immunosuppression induced by an attenuated strain of Salmonella typhimurium, potentiates Salmonella infection, and inhibits macrophage and polymorphonuclear leukocyte influx into the spleen. Infect Immun 1999, 67:891-898.
40. Ghaffari A, Miller CC, McMullin B, Ghahary A. Potential application of gaseous nitric oxide as a topical antimicrobial agent. Nitric Oxide 2006, 14:21-29.
41. Major T, Panmanee W, Mortensen J, Gray L, Hoglen N, Hassett D. Sodium nitrite-mediated killing of the major cystic fibrosis pathogens Pseudomonas aeruginosa, Staphylococcus aureus, and Burkholderia cepacia under anaerobic planktonic and biofilm conditions. Antimicrob Agents Chemother 2010, 54:4671-4677.
42. Chen C, Shi Y, Song J, Qi Q, Gu L, Wang P. Delivery of nitric oxide released from β-Gal-NONOate activation by β-galactosidase and its activity against Escherichia coli. Biol Pharm Bull 2006, 29:1239-1241.
43. MacMicking J, Nathan C, Hom G, Chartrain N, Fletcher D, Trumbauer M, Stevens K, Xie Q, Sokol K, Hutchinson N, et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 1995, 81:641-650.
44. Kawanishi M. Nitric oxide inhibits Epstein-Barr virus DNA replication and activation of latent EBV. Intervirology 1995, 38:206-213.
45. Akerstrom S, Mousavi-Jazi M, Klingstrom J, Leijon M, Lundkvist A, Mirazimi A. Nitric oxide inhibits the replication cycle of severe acute respiratory syndrome coronavirus. J Virol 2005, 79:1966-1969.
46. Wei Z, Wang X, Ning X, Wang Y, Zhang H, Wang D, Chen H, Cui B. Nitric oxide inhibits the replication cycle of porcine parvovirus in vitro. Arch Virol 2009, 154:999-1003.
47. Ormerod A, White MI, Shah SAA, Benjamin N. Molluscum contagiosum effectively treated with a topical acidified nitrite, nitric oxide liberating cream. Br J Dermatol 1999, 141:1051-1053.
48. de Souza G, Yokoyama-Yasunaka J, Seabra A, Miguel D, De Oliveira M, Uliana S. Leishmanicidal activity of primary S-nitrosothiols against Leishmania major and Leishmania amazonensis: implications for the treatment of cutaneous leishmaniasis. Nitric Oxide 2006, 15:209-216.
49. Zeina B, Banfield C, al-Assad S. Topical glyceryl trinitrate: a possible treatment for cutaneous leishmaniasis. Clin Exp Dermatol 1997, 22:244-245.
50. Augusto O, Linares E, Giorgio S. Possible roles of nitric oxide and peroxynitrite in murine leishmaniasis. Braz J Med Biol Res 1996, 29:853-862.
51. Vespa G, Cunha F, Silva J. Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro. Infect Immun 1994, 62:5177-5182.
52. Rockett K, Awburn M, Cowden W, Clark I. Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun 1991, 59:3280-3283.
53. Tohyama M, Kawakami K, Futenma M, Saito A. Enhancing effect of oxygen radical scavengers on murine macrophage anticryptococcal activity through production of nitric oxide. Clin Exp Immunol 1996, 103:436-441.
54. Alspaugh J, Granger D. Inhibition of Cryptococcus neoformans replication by nitrogen oxides supports the role of these molecules as effectors of macrophage-mediated cytostasis. Infect Immun 1991, 59:2291-2296.
55. Granger D, Hibbs JJ, Perfect J, Durack D. Metabolic fate of l-arginine in relation to microbiostatic capability of murine macrophages. J Clin Invest 1990, 85:264-273.
56. 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, 15:368-377.
57. Weller R, Ormerod A, Hobson R, Benjamin N. A randomized trial of acidified nitrite cream in the treatment of tinea pedis. J Am Acad Dermatol 1998, 38:559-563.
58. Jowkar F, Jamshidzadeh A, Pakniyat S, Namazi M. Efficacy of nitric-oxide liberating cream on pityriasis versicolor. J Dermatolog Treat 2010, 21:93-96.
59. Ormerod A, Shah A, Li H, Benjamin N, Ferguson G, 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.
60. Seabra A, Fitzpatrick A, Paul J, De Oliveira M, Weller R. Topically applied S-nitrosothiol-containing hydrogels as experimental and pharmacological nitric oxide donors in human skin. Br J Dermatol 2004, 151:977-983.
61. Davies K, Wink D, Saavedra J, Keefer L. Chemistry of the diazeniumdiolates. 2. Kinetics and mechanism of dissociation to nitric oxide in aqueous solution. J Am Chem Soc 2001, 123:5473-5481.
62. Keefer L. Nitric oxide (NO)- and nitroxyl (HNO)-generating diazeniumdiolates (NONOates): emerging commercial opportunities. Curr Top Med Chem 2005, 5:625-636.
63. Keefer L. Progress toward clinical application of the nitric oxide-releasing diazeniumdiolates. Annu Rev Pharmacol Toxicol 2003, 43:585-607.
64. Jones M, Ganopolsky J, Labbe A, Gilardino M, Wahl C, Martoni C, Prakash S. 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, 9:330-343.
65. Fox S, Wilkinson T, Wheatley P, Xiao B, Morris R, Sutherland A, Simpson A, Barlow PG, Butler A, Megson I, et al. NO-loaded Zn(2+)-exchanged zeolite materials: a potential bifunctional anti-bacterial strategy. Acta Biomater 2010, 6:1515-1521.
66. Blecher K, Nasir A, Friedman A. The growing role of nanotechnology in combating infectious disease. Virulence 2011, 2:395-401.
67. Han G, Tar M, Kuppam D, Friedman A, Melman A, Friedman J, Davies K. Nanoparticles as a novel delivery vehicle for therapeutics targeting erectile dysfunction. J Sex Med 2010, 7:224-233.
68. 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.
69. Martinez L, Han G, Chacko M, Mihu M, Jacobson M, Gialanella P, Friedman A, Nosanchuk J, Friedman J. Antimicrobial and healing efficacy of sustained release nitric oxide nanoparticles against Staphylococcus aureus skin infection. J Invest Dermatol 2009, 129:2463-2469.
70. 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, 1:62-67.
71. Macherla C, Sanchez DA, Ahmadi MS, Vellozzi EM, Friedman AJ, Nosanchuk JD, Martinez LR. Nitric oxide releasing nanoparticles for treatment of Candida albicans burn infections. Front Microbiol 2012, 3:193.
72. Hetrick EM, Shin JH, Paul HS, Schoenfisch MH. Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. Biomaterials 2009, 30:2782-2789.
73. Chouake J, Schairer D, Kutner A, Sanchez D, Makdisi J, Blecher-Paz K, Nacharaju P, Tuckman-Vernon C, Gialanella P, Friedman J, et al. Nitrosoglutathione generating nitric oxide nanoparticles as an improved strategy for combating Pseudomonas aeruginosa-infected wounds. J Drugs Dermatol 2012, 2:1471-1477.