Involvement of nitric oxide and its up/down stream molecules in the immunity against parasitic infections

Brazilian Journal of Infectious Diseases

Volumn 13, Issue 6, 2009, Pages 440-448

  Nahrevanian, Hossein ^a  

^a PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Helminth; Immunity; iNOS; Nitric oxide; NO; Parasite; Protozoa

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; GAMMA INTERFERON; IMMUNOGLOBULIN E; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; NITRIC OXIDE SYNTHASE;

AMEBIASIS; ARTICLE; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; CYTOKINE PRODUCTION; ECHINOCOCCUS; FASCIOLA; GENE EXPRESSION; GIARDIA; GRANULOMA; HELMINTHIASIS; HUMAN; INTRACELLULAR KILLING; LEISHMANIA; MACROPHAGE; NEMATODE; NONHUMAN; PARASITOSIS; PLASMODIUM; PROTOZOAL INFECTION; SCHISTOSOMA; SCHIZONT; TAENIA; TOXOCARA; TOXOPLASMA; TOXOPLASMOSIS; TRICHOMONAS; TROPHOZOITE; IMMUNOLOGY; REVIEW; UPREGULATION;

HELMINTHIASIS; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PROTOZOAN INFECTIONS; UP-REGULATION;

EID: 77953926710     PISSN: 14138670     EISSN: None     Source Type: Journal    
DOI: 10.1590/s1413-86702009000600010     Document Type: Article

References (147)

1. Kroncke KD, Fehsel K, Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection: how, why, when, and where? Nitric Oxide: Biology and Chemistry 1997; 1:107-120.
2. Lancaster JRJ. A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1997; 1: 18-30.
3. Nahrevanian H, Dascombe MJ. Reactive nitrogen intermediate (RNI) levels inside and outside Plasmodium infected red blood cells in murine malaria, J Trop Med Parasitol 2003; 26(1):13-19.
4. Ellis G, Adatia I, Yazdanpanah M, Makela SK. Nitrite and nitrate analyses: a clinical biochemistry perspective. Clin Biochem 1998; 31:195-220.
5. Clark IA, Rockett KA, Cowden WB. Possible central role of nitricoxide in conditions clinically similar to cerebral malaria. Lancet 1992; 340:894-896.
6. Nahrevanian H, Dascombe MJ. Nitric oxide and reactive nitrogen intermediates in lethal and nonlethal strains of murine malaria. Parasite Immunol 2001; 23:491-501.
7. Nahrevanian H, Dascombe MJ. Expression of inducible nitric oxide synthase (iNOS) mRNA in target organs of lethal and nonlethal strains of murine malaria, Parasite Immunol 2002; 24(9-10):471-478.
8. Nahrevanian H, Dascombe MJ. Simultaneous increases in immune competent cells and nitric oxide in the spleen during Plasmodium berghei infection in mice. J Microbiol Immunol Infec 2006; 39(1):11-17.
9. Nahrevanian H, Gholizadeh SJ, Farahmand M, Aghighi Z, Assmar M, Abolhassani M. Reactiv enitrogen intermediate production and tolerance variability in different mouse strains after in vivo treatment with lipopolysaccharide from Salmonella abortus equi. J Microbiol Immunol Infec 2005; 38(3):164-168.
10. Nahrevanian H, Gholizadeh J, Farahmand M, Assmar M, Sharifi K, Ayatollahi Mousavi SA, Abolhassani M. Nitric oxide induction as a novel immunoepidemiological target in malaria-infected patients from endemic areas of Islamic Republic of Iran. Scand J Clin Lab Invest 2006; 66(3):201-210.
11. Dascombe MJ, Nahrevanian H. Pharmacological assessment of the role of nitric oxide in mice infected with lethal and nonlethal species of malaria, Parasite Immunol 2003; 25(3):149-159.
12. Nussler AK, Di Silvio M, Billiar TR, Hoffman RA, Geller DA, Selby R, Madariaga J, Simmons RL. Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J Exp Med 1992; 176:261-264.
13. Nahrevanian H. Nitric oxide involvement during malaria infection; Immunological concepts, mechanisms and complexities; A novel review. J Trop Med Parasitol, 2004; 27(2):93-101.
14. Burdon MG, Butler AR, Renton LM. A study of antibacterial activity of nitric oxide donor compounds. In: The biology of nitric oxide, ed. by Moncada S, Stamler J, Gross S, Higgs EA. Portland Press Ltd., London 1996; p.170.
15. Motard A, Landau I, Nussler A, Grau G, Baccam D, Mazier D, Targett GA. The role of reactive nitrogen intermediates in modulation of gametocyte infectivity of rodent malaria parasites. Parasite Immunol 1993; 15:21-26.
16. Liew FY, Li Y, Millott S. Tumor necrosis factor-a synergizes with IFN-gamma in mediating killing of Leishmania major through the induction of nitric oxide. J Immunol 1990; 145:4306-4310.
17. Adams B, Hibbs JB, Taintor RR, Krahenbuhl JL. Microbiostatic effect of murine activated macrophages for Toxoplasma gondii. Role for synthesis of inorganic nitrogen oxides from L-arginine. J Immunol 1990; 144:2725-2729.
18. Vincendeau P, Dalouede S. Macrophages cytostatic effect on Trypanosoma musculi involves an L-arginine-dependent mechanism. J Immunol 1991; 146:4338-4343.
19. Gazzinelli RT, Oswald IP, Heiny S, James SL, Sher A. The microbicidal activity of interferon treated macrophages against Trypanosoma cruzi involves an L-arginine-dependent, nitrogen oxide-mediated mechanism inhibitable by interleukin-10 and transforming growth factor-b. Eur J Immunol 1992; 22:2501-2506.
20. Adams LB, Franzblau SG, Vavrin V, Hibbs JRJ, Krahenbuhl JL. Larginine-dependent macrophage effector functions inhibit metabolic activity of Mycobacterium leprae. J Immunol 1991; 147:1642-1646.
21. Denis M. Tumor necrosis factor and granulocytes macrophagescolony stimulating factor stimulate human macrophages to restrict growth of virulent Mycobacterium avium and to kill avirulent M. avium: Killing effector mechanism depends on the generation of reactive nitrogen intermediates. J Leuk Biol 1991; 49:380-387.
22. Cenci E, Romani L, Mencacci A, Spaccapelo R, Schiabbella E, Paccetti P, Bistoni F. Interleukin-4 and interleukin-10 inhibit nitric oxide-dependent macrophage killing of Candida albicans. Eur J Immunol 1993; 23:1034-1038.
23. Gunasegaran K, Xie Q-W, Buller RM, Nathan C, Duarte C, MacMicking JD. Inhibition of viral replication by interferong-induced nitric oxide synthase. Science 1993; 261:1445-1447.
24. Fierro IM, Barja-Fidalgo C, Cunha FQ, Ferreira SH. The involvement of nitric oxide in the anti-Candida albicans activity of rat neutrophils. Immunol 1996; 89:295-300.
25. Malawista SE, Montgomery RR, Van Blaricom G. Evidence for reactive nitrogen intermediates in killing of Staphylococci by human neutrophil cytoplasts. A new microbicidal pathway for polymorphonuclear leukocytes. J Clin Invest 1992; 90:631-636.
26. Pimenta PFP, Dos Santos MAV, De Souza W. Fine structure and cytochemistry of the interaction between Leishmania mexicana amazonensis and rat neutrophils and eosinophils. J Submicrosc Cytol 1987; 19:387-395.
27. Pearson RD, Uydess IL, Chapman SW, Steigbigel RT. Interaction of human eosinophils with Leishmania donovani. Ann Trop Med Parasitol 1987; 81:735-739.
28. Oliveira SHP, Fonseca SG, Romao PRT, Ferreira SH, Cunha FQ. Nitric Oxide Mediates the Microbicidal Activity of Eosinophils. Mem Inst Oswaldo Cruz, Rio de Janeiro, 1997; 92(Suppl.2):233-235.
29. Mayer B. Structure and function of nitric oxide synthase. Nitric Oxide: Biology and Chemistry 1998; 2:390-391.
30. Xu WM, Liu LZ. Nitric oxide: from a mysterious labile factor to the molecule of the Nobel Prize. Recent progress in nitric oxide research. Cell Res 1998; 8:251-258.
31. Baudouin JE, Tachon P. Characterization of a constitutive nitric oxide synthase from normal human keratinocytes. In: The biology of nitric oxide, ed. by Moncada S, Stamler J, Gross S, Higgs EA. Portland Press Ltd., London 1996; p.54.
32. Babu BR, Griffith OW. Design of isoform-selective inhibitors of nitric oxide synthase. Curr Opin Chem Biol 1998; 2:491-500.
33. Bogdan C, Rollinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 2000; 12:64-76.
34. Bogdan C, Rollinghoff M, Diefenbach A. The role of nitric oxide in innate immunity. Immunol Rev 2000; 173:17-26.
35. Park CS, Lee HS, Lee HY, Krishna G. An unprocessed pseudogene of inducible nitric oxide synthase gene in human. Nitric Oxide 1997; 1:294-300.
36. Favre N, Ryffel B, Rudin W. Parasite killing in murine malaria does not require nitric oxide production. Parasitol 1999; 118:139-143.
37. Favre N, Ryffel B, Rudin W. The development of murine cerebral malaria does not require nitric oxide production. Parasitol 1999; 118:135-138.
38. Dugbartey AT, Spellacy FJ, Dugbartey MT. Somatosensory discrimination deficits following pediatric cerebral malaria. Am J Trop Med Hyg 1998; 59:393-396.
39. Granger DL, Hibbs JB. High-output nitric oxide: weapon against infection? Trends Microbiol 1996; 4:46-47.
40. Clark IA, al-Yaman FM, Cowden WB, Rockett KA. Does malarial tolerance, through nitric oxide, explain the low incidence of autoimmune disease in tropical Africa? Lancet 1996; 348:1492-1494.
41. Roitt IM, Brostoff J, Male D. Immunology. 5th edition Mosby Publication, London, 1998; pp.132-133, 235, 246, 247,314.
42. Mellouk S, Green SJ, Nacy CA, Hoffman SL. IFN-gamma inhibits development of Plasmodium berghei exoerythrocytic stages in hepatocytes by an L-arginine-dependent effector echanism. J Immunol 1991; 146:3971-976.
43. Liew FY. Regulation of nitric oxide synthase in macrophages. In: The biology of nitric oxide: 2 Enzymology, Biochemistry and Immunology, ed. by Moncada, S., Stamler, J., Gross, S. & Higgs, E.A. Portland Press, London, UK, 1992; pp.223-229.
44. Fernandes PD, Assreuy J. Role of nitric oxide and superoxide in Giardia lamblia killing. Braz J Med Biol Res 1997; 30:93-99.
45. 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.
46. Taylor-Robinson AW. Nitric oxide can be released as well as scavenged by haemoglobin: relevance to its antimalarial activity. Parasite Immunol 1998; 20:49-50.
47. Mannick EE, Oliver PD, Sadowska-Krowicka H, Miller MJS. Inhibition of inducible nitric oxide synthase reverse endotoxin tolerance in cultured macrophages. In: The biology of nitric oxide, ed. by Moncada, S., Stamler, J., Gross, S. & Higgs, E.A. Portland Press Ltd., London, 1996; p.144.
48. Haswell-Elkins M, Satarug S, Sithithaworn P, Mairiang E, Mairiang P, Elkins D. Nitrate excretion and parasite-specific T lymphocyte responses of humans infected with the liver fluke, Opisthorchis viverrini. In: The biology of nitric oxide: 1 Physiological and clinical aspects, ed. by Moncada, S., Marletta, M.A., Hibbs, JR.J.B. & Higgs, E.A. Portland Press, London, UK, 1992; p.380.
49. Gradoni L, Ascenzi P. Nitric oxide and anti-protozoan chemotherapy. Parassitologia. 2004; 46(1-2):101-103.
50. Stempin CC, Cerban FM. Macrophages and arginase induction as a mechanism for parasite escape. Medicina (B Aires). 2007; 67(6Pt 2):737-746.
51. Ascenzi P, Fasano M, Gradoni L. Do hemoglobin and hemocyanin impair schistosoma killing by no? IUBMB Life. 2002; 53(6):287-8.
52. Zafra R, Jaber JR, Pérez-Ecija RA, Barragán A, Martínez-Moreno A, Pérez J. High iNOS expression in macrophages in canine leishmaniasis is associated with low intracellular parasite burden. Vet Immunol Immunopathol. 2008, 15; 123(3-4):353-359.
53. Panaro MA, Brandonisio O, de Caprariis D, Cavallo P, Cianciulli A, Mitolo V, Otranto D. Canine leishmaniasis in Southern Italy: a role for nitric oxide released from activated macrophages in asymptomatic infection? Parasit Vectors. 2008; 9; 1(1):10.
54. Valdez CA, Saavedra JE, Showalter BM, Davies KM, Wilde TC, Citro ML, Barchi JJ Jr, Deschamps JR, Parrish D, El-Gayar S, Schleicher U, Bogdan C, Keefer LK. Hydrolytic reactivity trends among potential prodrugs of the O2-glycosylated diazeniumdiolate family. Targeting nitric oxide to macrophages for antileishmanial activity. J Med Chem. 2008; 10; 51(13):3961-3970.
55. Soares-Bezerra RJ, da Silva EF, Echevarria A, Gomes-da-Silva L, Cysne-Finkelstein L, Monteiro FP, Leon LL, Genestra M. Effect of mesoionic 4-phenyl-5-(cinnamoyl)-1,3,4- thiadiazolium-2-phenylamine chloride derivative salts on the activities of the nitric oxide synthase and arginase of Leishmania amazonensis. J Enzyme Inhib Med Chem. 2008; 23(3):328-333.
56. Ferreira AS, de Souza MA, Barbosa NR, da Silva SS. Leishmania amazonensis: xylitol as inhibitor of macrophage infection and stimulator of macrophage nitric oxide production. Exp Parasitol. 2008; 119(1):74-79.
57. Linares E, Giorgio S, Augusto O. Inhibition of in vivo leishmanicidal mechanisms by tempol: nitric oxide downregulation and oxidant scavenging. Free Radic Biol Med. 2008; 44(8):1668-1676.
58. Wang QH, Liu YJ, Liu J, Chen G, Zheng W, Wang JC, Cao YM. Plasmodium yoelii: Assessment of production and role of nitric oxide during the early stages of infection in susceptible and resistant mice. Exp Parasitol. 2009; 121(3):268-273.
59. Koka S, Lang C, Niemoeller OM, Boini KM, Nicolay JP, Huber SM, Lang F. Influence of NO synthase inhibitor L-NAME on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem. 2008; 21(5-6):481-488.
60. Safeukui I, Vatan R, Dethoua M, Agbo H, Haumont G, Moynet D, Malvy D, Vincendeau P, Mossalayi D, Millet P. A role of IgE and CD23/NO immune pathway in age-related resistance of Lewis rats to Plasmodium berghei Anka? Microbes Infect. 2008; 10(12-13):1411-1416.
61. Yeo TW, Rooslamiati I, Gitawati R, Tjitra E, Lampah DA, Kenangalem E, McNeil YR, Price RN, Anstey NM, Duffull SB. Pharmacokinetics of L-arginine in adults with moderately severe malaria. Antimicrob Agents Chemother. 2008; 52(12):4381-4387.
62. Cramer JP, Nüssler AK, Ehrhardt S, Burkhardt J, Otchwemah RN, Zanger P, Dietz E, Gellert S, Bienzle U, Mockenhaupt FP. Agedependent effect of plasma nitric oxide on parasite density in Ghanaian children with severe malaria. Trop Med Int Health. 2005; 10(7):672-680.
63. Sobolewski P, Gramaglia I, Frangos J, Intaglietta M, van der Heyde HC. Nitric oxide bioavailability in malaria. Trends Parasitol. 2005; 21(9):415-422.
64. Gramaglia I, Sobolewski P, Meays D, Contreras R, Nolan JP, Frangos JA, Intaglietta M, van der Heyde HC. Low nitric oxide bioavailability contributes to the genesis of experimental cerebral malaria. Nat Med. 2006; 12(12):1417-1422.
65. Ostera G, Tokumasu F, Oliveira F, Sa J, Furuya T, Teixeira C, Dvorak J. Plasmodium falciparum: food vacuole localization of nitric oxide-derived species in intraerythrocytic stages of the malaria parasite. Exp Parasitol. 2008; 120(1):29-38.
66. Hunt NH, Golenser J, Chan-Ling T, Parekh S, Rae C, Potter S, Medana IM, Miu J, Ball HJ. Immunopathogenesis of cerebral malaria. Int J Parasitol. 2006; 36(5):569-582.
67. Sobolewski P, Gramaglia I, Frangos JA, Intaglietta M, van der Heyde H. Plasmodium berghei resists killing by reactive oxygen species. Infect Immun. 2005; 73(10):6704-6710.
68. Guillermo LV, DaMatta RA. Nitric oxide inhibition after Toxoplasma gondii infection of chicken macrophage cell lines. Poult Sci. 2004; 83(5):776-782.
69. Nishikawa Y, Kawase O, Vielemeyer O, Suzuki H, Joiner KA, Xuan X, Nagasawa H. Toxoplasma gondii infection induces apoptosis in noninfected macrophages: role of nitric oxide and other soluble factors. Parasite Immunol. 2007; 29(7):375-385.
70. Gutierrez-Escobar AJ, Arenas AF, Villoria-Guerrero Y, Padilla-Londoño JM, Gómez-Marin JE. Toxoplasma gondii: molecular cloning and characterization of a nitric oxide synthase-like protein. Exp Parasitol. 2008; 119(3):358-363.
71. Kang KM, Lee GS, Lee JH, Choi IW, Shin DW, Lee YH. Effects of iNOS inhibitor on IFN-gamma production and apoptosis of splenocytes in genetically different strains of mice infected with Toxoplasma gondii. Korean J Parasitol. 2004; 42(4):175-183.
72. Machado FS, Souto JT, Rossi MA, Esper L, Tanowitz HB, Aliberti J, Silva JS. Nitric oxide synthase-2 modulates chemokine production by Trypanosoma cruzi-infected cardiac myocytes. Microbes Infect. 2008; 10(14-15):1558-1566.
73. Ribeiro DA, Calvi SA, Picka MM, Persi E, de Carvalho TB, Caetano PK, Nagoshi LR, Lima CR, Machado JM, Salvadori DM. DNA damage and nitric oxide synthesis in experimentally infected Balb/c mice with Trypanosoma cruzi. Exp Parasitol. 2007; 116(3):296-301.
74. Nishimura K, Yagi M, Ohnishi Y, Yamasaki S. Cytokine and nitric oxide production by Trypanosoma brucei infection in rats fed polyamine-deficient chow. J Parasitol. 2008; 94(1):107-113.
75. Vieira PM, Francisco AF, de Souza SM, Malaquias LC, Reis AB, Giunchetti RC, Veloso VM, de Lana M, Tafuri WL, Carneiro CM. Trypanosoma cruzi: Serum levels of nitric oxide and expression of inducible nitric oxide synthase in myocardium and spleen of dogs in the acute stage of infection with metacyclic or blood trypomastigotes. Exp Parasitol. 2009; 121(1):76-82.
76. Guiñazú N, Pellegrini A, Carrera-Silva EA, Aoki MP, Cabanillas AM, Gìronés N, Fresno M, Cano R, Gea S. Immunisation with a major Trypanosoma cruzi antigen promotes proinflammatory cytokines, nitric oxide production and increases TLR2 expression. Int J Parasitol. 2007,37(11):1243-1254.
77. Ny L, Li H, Mukherjee S, Persson K, Holmqvist B, Zhao D, Shtutin V, Huang H, Weiss LM, Machado FS, Factor SM, Chan J, Tanowitz HB, Jelicks LA. A magnetic resonance imaging study of intestinal dilation in Trypanosoma cruzi-infected mice deficient in nitric oxide synthase. Am J Trop Med Hyg. 2008; 79(5):760-767.
78. Gookin JL, Allen J, Chiang S, Duckett L, Armstrong MU.Local peroxynitrite formation contributes to early control of Cryptosporidium parvum infection. Infect Immun. 2005; 73(7):3929-3936.
79. Gookin JL, Chiang S, Allen J, Armstrong MU, Stauffer SH, Finnegan C, Murtaugh MP. NF-kappaB-mediated expression of iNOS promotes epithelial defense against infection by Cryptosporidium parvum in neonatal piglets. Am J Physiol Gastrointest Liver Physiol. 2006; 290(1):G164-G174.
80. Leitch GJ, He Q. Arginine-derived nitric oxide reduces fecal oocyst shedding in nude mice infected with Cryptosporidium parvum. Infect Immun. 1994; 62(11):5173-5176.
81. Chen YF, Qin YH, Zheng LL, Dai XD, Ren YX, Nie DP, Cui Y. Experimental treatment using combined Fructus psoraleae and dihydroartemisinin in mouse cryptosporidiosis. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2008; 26(1):67-69.
82. Gookin JL, Duckett LL, Armstrong MU, Stauffer SH, Finnegan CP, Murtaugh MP, Argenzio RA. Nitric oxide synthase stimulates prostaglandin synthesis and barrier function in C. parvuminfected porcine ileum. Am J Physiol Gastrointest Liver Physiol. 2004; 287(3):G571-G581.
83. Leitch GJ, He Q. Reactive nitrogen and oxygen species ameliorate experimental cryptosporidiosis in the neonatal BALB/c mouse model. Infect Immun. 1999; 67(11):5885-5891.
84. Park GC, Ryu JS, Min DY. The role of nitric oxide as an effector of macrophage-mediated cytotoxicity against Trichomonas vaginalis. Korean J Parasitol. 1997; 35(3):189-195.
85. Harris KM, Goldberg B, Biagini GA, Lloyd D. Trichomonas vaginalis and Giardia intestinalis produce nitric oxide and display NOsynthase activity. J Eukaryot Microbiol. 2006; 53 Suppl 1:S182-S183.
86. Sarti P, Fiori PL, Forte E, Rappelli P, Teixeira M, Mastronicola D, Sanciu G, Giuffré A, Brunori M. Trichomonas vaginalis degrades nitric oxide and expresses a flavorubredoxin- like protein: a new pathogenic mechanism? Cell Mol Life Sci. 2004; 61(5):618-623.
87. Yadav M, Dubey ML, Gupta I, Malla N. Nitric oxide radicals in leucocytes and vaginal washes of Trichomonas vaginalis- infected symptomatic and asymptomatic women. Parasitology. 2006; 132(Pt 3):339-343.
88. Eckmann L, Laurent F, Langford TD, Hetsko ML, Smith JR, Kagnoff MF, Gillin FD. Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumendwelling pathogen Giardia lamblia. J Immunol. 2000; 164(3):1478-1487.
89. Li E, Zhou P, Singer SM. Neuronal nitric oxide synthase is necessary for elimination of Giardia lamblia infections in mice. J Immunol. 2006; 176(1):516-521.
90. Bayraktar MR, Mehmet N, Durmaz R. Serum cytokine changes in Turkish children infected with Giardia lamblia with and without allergy: Effect of metronidazole treatment. Acta Trop. 2005; 95(2):116-122.
91. Hernández-Campos ME, Campos-Rodríguez R, Tsutsumi V, Shibayama M, García-Latorre E, Castillo-Henkel C, Valencia-Hernández I. Nitric oxide synthase in Entamoeba histolytica:its effect on rat aortic rings. Exp Parasitol. 2003; 104(3-4):87-95.
92. Lin JY, Seguin R, Keller K, Chadee K. Transforming growth factorbeta 1 primes macrophages for enhanced expression of the nitric oxide synthase gene for nitric oxide-dependent cytotoxicity against Entamoeba histolytica. Immunology. 1995; 85(3):400-407.
93. Lin JY, Chadee K. Macrophage cytotoxicity against Entamoeba histolytica trophozoites is mediated by nitric oxide from Larginine. J Immunol. 1992; 148(12):3999-4005.
94. Pacheco-Yepez J, Campos-Rodríguez R, Ventura-Juárez J, Shibayama M, Martínez-Palomo A, Tsutsumi V. Role of nitric oxide in experimental hepatic amebiasis. Arch Med Res. 1997; 28 Spec No: 214-216.
95. Ramírez-Emiliano J, González-Hernández A, Arias-Negrete S. Expression of inducible nitric oxide synthase mRNA and nitricoxide production during the development of liver abscess in hamster inoculated with Entamoeba histolytica. Curr Microbiol. 2005; 50(6):299-308.
96. Pacheco-Yépez J, Campos-Rodríguez R, Shibayama M, Ventura-Juárez J, Serrano-Luna J, Tsutsumi V. Entamoeba histolytica: production of nitric oxide and in situ activity of NADPH diaphorase in amebic liver abscess of hamsters. Parasitol Res. 2001; 87(1):49-56.
97. Ramirez-Emiliano J, Flores-Villavicencio LL, Segovia J, Arias-Negrete S. Nitricoxide participation during amoebic liver abscess development. Medicina (B Aires). 2007; 67(2):167-176.
98. Siman-Tov R, Ankri S. Nitric oxide inhibits cysteine proteinases and alcohol dehydrogenase 2 of Entamoeba histolytica. Parasitol Res. 2003; 89(2):146-149.
99. Wang W, Keller K, Chadee K. Entamoeba histolytica modulates the nitric oxide synthase gene and nitric oxide production by macrophages for cytotoxicity against amoebae and tumour cells. Immunology. 1994; 83(4):601-610.
100. Elnekave K, Siman-Tov R, Ankri S. Consumption of L-arginine mediated by Entamoeba histolytica L-arginase (EhArg) inhibits amoebicidal activity and nitric oxide production by activated macrophages. Parasite Immunol. 2003; 25(11-12):597-608.
101. Jarillo-Luna RA, Campos-Rodríguez R, Tsutsumi V. Entamoeba histolytica: immunohistochemical study of hepatic amoebiasis in mouse. Neutrophils and nitric oxide as possible factors of resistance. Exp Parasitol. 2002; 101(1):40-56.
102. Kohn AB, Lea JM, Moroz LL, Greenberg RM. Schistosoma mansoni: use of a fluorescent indicator to detect nitric oxide and related species in living parasites. Exp Parasitol. 2006; 113(2):130-133.
103. Andrade MA, Siles-Lucas M, Espinoza E, Pérez Arellano JL, Gottstein B, Muro A. Echinococcus multilocularis laminatedlayer components and the E14t 14-3-3 recombinant protein decrease NO production by activated rat macrophages in vitro. Nitric Oxide. 2004; 10(3):150-155.
104. Nacher M, Singhasivanon P, Traore B, Vannaphan S, Gay F, Chindanond D, Franetich JF, Mazier D, Looareesuwan S. Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. Am J Trop Med Hyg. 2002; 66(3):304-309.
105. Ait Aissa S, Amri M, Bouteldja R, Wietzerbin J, Touil-Boukoffa C. Alterations in interferon-gamma and nitric oxide levels in human echinococcosis. Cell Mol Biol (Noisy-le-grand). 2006; 15; 52(1):65-70.
106. Zhu W, Pryor SC, Putnam J, Cadet P, Stefano GB. Opiate alkaloids and nitric oxide production in the nematode Ascaris suum. J Parasitol. 2004; 90(1):15-22.
107. Pfarr KM, Qazi S, Fuhrman JA. Nitric oxide synthase in filariae: demonstration of nitric oxide production by embryos in Brugia malayi and Acanthocheilonema viteae. Exp Parasitol. 2001; 97(4):205-214.
108. Bascal ZA, Montgomery A, Holden-Dye L, Williams RG, Walker RJ. Histochemical mapping of NADPH diaphorase in the nervous system of the parasitic nematode Ascaris suum. Parasitology. 1995; 110 (Pt 5):625-637.
109. Minning DM, Gow AJ, Bonaventura J, Braun R, Dewhirst M, Goldberg DE, Stamler JS. Ascaris haemoglobin is a nitric oxideactivated 'deoxygenase'. Nature. 1999; 401(6752):497-502.
110. Bascal ZA, Cunningham JM, Holden-Dye L, O'Shea M, Walker RJ. Characterization of a putative nitric oxide synthase in the neuromuscular system of the parasitic nematode, Ascaris suum. Parasitology. 2001; 122(Pt 2):219-231
111. Pfarr KM, Fuhrman JA. Brugia malayi: localization of nitric oxide synthase in a lymphatic filariid. Exp Parasitol. 2000; 94(2):92-98.
112. Espinoza EY, Pérez-Arellano JL, Carranza C, Collía F, Muro A. In vivo inhibition of inducible nitric oxide synthase decreases lung injury induced by Toxocara canis in experimentally infected rats. Parasite Immunol. 2002; 24(11-12):511-520.
113. Demirci C, Gargili A, Kandil A, Cetinkaya H, Uyaner I, Boynuegri B, Gumustas MK. Inhibition of inducible nitric oxide synthase in murine visceral larva migrans: effects on lung and liver damage. Chin J Physiol. 2006; 49(6):326-334.
114. Fan CK, Lin YH, Hung CC, Chang SF, Su KE. Enhanced inducible nitric oxide synthase expression and nitrotyrosine accumulation in experimental granulomatous hepatitis caused by Toxocara canis in mice. Parasite Immunol. 2004; 26(6-7):273-281.
115. Lin SM, Liao CW, Lin YH, Lee CC, Kao TC, Fan CK. Inducible nitric oxide synthase inhibition influenced granuloma formation with suppressed collagen expression in myositis caused by Toxocara canis in mice. Parasitol Res. 2008; 102(4):577-585.
116. Gargili A, Demirci C, Kandil A, Cetinkaya H, Atukeren P, Gümüotao MK. In vivo inhibition of inducible nitric oxide and evaluation of the brain tissue damage induced by Toxocara canis larvae in experimentally infected mice. Chin J Physiol. 2004; 47(4):189-196.
117. Elwakil HS, Ali NM, Talaat RM, Osman WM. Impact of experimental duel infections with Schistosoma mansoni and Echinoccocus granulosus on hepatic histopathology. J Egypt Soc Parasitol. 2007; 37(3 Suppl):1175-1188.
118. Salim EI, Morimura K, Menesi A, El-Lity M, Fukushima S, Wanibuchi H. Elevated oxidative stress and DNA damage and repair levels in urinary bladder carcinomas associated with schistosomiasis. Int J Cancer. 2008; 123(3):601-608.
119. Long XC, Li YL, Ruppel A. Expression of inducible nitric oxide synthase in the livers of mice infected with Schistosoma japonicum. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2004; 22(3):157-159.
120. Hirata M, Hirata K, Kage M, Zhang M, Hara T, Fukuma T. Effect of nitric oxide synthase inhibition on Schistosoma japonicum egg-induced granuloma formation in the mouse liver. Parasite Immunol. 2001; 23(6):281-289.
121. Balemba OB, Mortensen K, Semuguruka WD, Hay-Schmidt A, Johansen MV, Dantzer V. Neuronal nitric oxide synthase activity is increased during granulomatous inflammation in the colon and caecum of pigs infected with Schistosoma japonicum. Auton Neurosci. 2002; 99(1):1-12.
122. Abdallahi OM, Bensalem H, Diagana M, De Reggi M, Gharib B. Inhibition of nitric oxide synthase activity reduces liver injury in murine schistosomiasis. Parasitology. 2001; 122(Pt 3):309-315.
123. Hesse M, Modolell M, La Flamme AC, Schito M, Fuentes JM, Cheever AW, Pearce EJ, Wynn TA. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of Larginine metabolism. J Immunol. 2001; 167(11):6533-6544.
124. Abo-Shousha S, Khalil SS, Rashwan EA. Oxygen free radical and nitric oxide production in single or combined human schistosomiasis and fascioliasis. J Egypt Soc Parasitol. 1999; 29(1):149-156.
125. Sibille P, Tliba O, Boulard C. Early and transient cytotoxic response of peritoneal cells from Fasciola hepatica-infected rats. Vet Res. 2004; 35(5):573-584.
126. Sadeghi-Hashjin G, Naem S. Parasiticidal effects of peroxynitrite on ovine liver flukes in vitro. J Helminthol. 2001; 75(1):73-76.
127. Piedrafita D, Parsons JC, Sandeman RM, Wood PR, Estuningsih SE, Partoutomo S, Spithill TW. Antibody-dependent cellmediated cytotoxicity to newly excysted juvenile Fasciola hepatica in vitro is mediated by reactive nitrogen intermediates. Parasite Immunol. 2001; 23(9):473-482.
128. Cervi L, Rossi G, Cejas H, Masih DT. Fasciola hepatica-induced immune suppression of spleen mononuclear cell proliferation: role of nitric oxide. Clin Immunol Immunopathol. 1998; 87(2):145-154.
129. Kanazawa T, Asahi H, Hata H, Mochida K, Kagei N, Stadecker MJ. Arginine-dependent generation of reactive nitrogen intermediates is instrumental in the in vitro killing of protoscoleces of Echinococcus multilocularis by activated macrophages. Parasite Immunol. 1993; 15(11):619-623.
130. Li FR, Shi YE, Shi DZ, Vuitton DA, Craig PS. Kinetic analysis of cytokines and immunoglobulin G subclass in BALB/c mice infected with Echinococcus alveolaris. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi. 2003; 21(6):357-360.
131. Dai WJ, Gottstein B. Nitric oxide-mediated immunosuppression following murine Echinococcus multilocularis infection. Immunology. 1999; 97(1):107-116.
132. Dai WJ, Waldvogel A, Jungi T, Stettler M, Gottstein B. Inducible nitric oxide synthase deficiency in mice increases resistance to chronic infection with Echinococcus multilocularis. Immunology. 2003; 108(2):238-244.
133. Amri M, Aissa SA, Belguendouz H, Mezioug D, Touil-Boukoffa C. In vitro antihydatic action of IFN-gamma is dependent on the nitric oxide pathway. J Interferon Cytokine Res. 2007; 27(9):781-787.
134. Touil-Boukoffa C, Bauvois B, Sancéau J, Hamrioui B, Wietzerbin J. Production of nitric oxide (NO) in human hydatidosis: relationship between nitrite production and interferon-gamma levels. Biochimie. 1998; 80(8-9):739-744.
135. Alonso-Trujillo J, Rivera-Montoya I, Rodríguez-Sosa M, Terrazas LI. Nitric oxide contributes to host resistance against experimental Taenia crassiceps cysticercosis. Parasitol Res. 2007; 100(6):1341-1350.
136. Shuttleworth CW, Sweeney KM, Sanders KM. Evidence that nitric oxide acts as an inhibitory neurotransmitter supplying taenia from the guinea-pig caecum. Br J Pharmacol. 1999; 127(6):1495-1501.
137. Knudsen MA, Tøttrup A. A possible role of the L-arginine-nitric oxide pathway in the modulation of cholinergic transmission in the guinea-pig taenia coli. Br J Pharmacol. 1992; 107(3):837-841.
138. Caballero-Alomar C, Santos C, Lopez D, Mitjavila MT, Puig-Parellada P. Sources and implications of basal nitric oxide in spontaneous contractions of guinea pig taenia caeci. Am J Physiol Gastrointest Liver Physiol. 2003; 285(4):G747-G753.
139. Connelly L, Palacios-Callender M, Ameixa C, Moncada S, Hobbs AJ. Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 2001; 166:3873-3881.
140. Honda K, Kobayashi H, Hataishi R, Hirano S, Fukuyama N, Nakazawa H, Tomita T. Inhaled nitric oxide reduces tyrosine nitration after lipopolysaccharide instillation into lungs of rats. Am J Respir Crit Care Med 1999; 160:678-688.
141. Rodriguez D, Keller AC, Faquim-Mauro EL, de Macedo MS, Cunha FQ, Lefort J, Vargaftig BB, Russo M. Bacterial lipopolysaccharide signaling through toll-like receptor 4 suppresses asthma-like responses via nitric oxide synthase 2 activity. J Immunol 2003; 171:1001-1008.
142. Castro Keller A, Rodriguez D, Russo M. Nitric oxide paradox in asthma. Mem Inst Osw Cruz, Rio de Janeiro 2005; 100(Suppl. 1):19-23.
143. Nahrevanian H, Gholizadeh J, Farahmand M, Assmar M: Patterns of co-association of C-reactive protein and nitric oxide in malaria in endemic areas of Iran. Mem Inst Osw Cruz, 2008; 103(1):39-44.
144. Nahrevanian H: Immune effector mechanisms of nitric oxide pathway in malaria: Cytotoxicity versus cytoprotection. Braz J Infec Dis, 2006; 10(4):283-292.
145. Nahrevanian H, Farahmand M, Aghighi Z, Assmar M, Amirkhani A: Pharmacological evaluation of anti-leishmanial activity by in vivo nitric oxide modulation in Balb/c mice infected with Leishmania major MRHO/IR/75/ER; An Iranian strain of cutaneous leishmaniasis. Exp Parasitol, 2007; 116(3): 233-240.
146. Nahrevanian H, Amini M: Nitric oxide functions; an emphasis on its diversity in infectious diseases. Iranian J Basic Med Sci, 2009; 11(4): 197-204.
147. Nahrevanian H, Dascombe MJ. The role of nitric oxide and its up/ downstream molecules in malaria: cytotoxic or preventive? Southeast Asian J Trop Med Publ Health 2003; 34(S2):44-50.