Role of nitric oxide during rotavirus infection

Journal of Medical Virology

Volumn 78, Issue 7, 2006, Pages 979-985

  Rodríguez Díaz, Jesús ^a,f   Banasaz, Mahanez ^b   Istrate, Claudia ^c   Buesa, Javier ^a   Lundgren, Ove ^d   Espinoza, Felix ^e   Sundqvist, Tommy ^f   Rottenberg, Martin ^g   Svensson, Lennart ^f  

^a UNIVERSITY OF VALENCIA   (Spain)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e National Autonomous University of Nicaragua   (Nicaragua)

^f LINKÖPING UNIVERSITY   (Sweden)

^g KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Diarrhoea; Gastroenteritis; Nitrate; Nitrite

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRATE; NITRIC OXIDE; NITRITE; NONSTRUCTURAL PROTEIN 4; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIARRHEA; DUODENUM; HUMAN; HUMAN CELL; ILEUM; IMMUNE RESPONSE; INTESTINE EPITHELIUM CELL; INTESTINE INNERVATION; JEJUNUM; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRESCHOOL CHILD; ROTAVIRUS; VIRUS INFECTION; VIRUS STRAIN;

ANIMALS; ANIMALS, NEWBORN; BASE SEQUENCE; CASE-CONTROL STUDIES; CELL LINE; GASTROENTERITIS; GLYCOPROTEINS; HUMANS; INFANT; MICE; MICE, INBRED BALB C; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PROSPECTIVE STUDIES; RNA, MESSENGER; ROTAVIRUS; ROTAVIRUS INFECTIONS; TOXINS, BIOLOGICAL; VIRAL NONSTRUCTURAL PROTEINS;

MURINE ROTAVIRUS; ROTAVIRUS;

EID: 33744952454     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.20650     Document Type: Article

References (44)

1. Aktan F. 2004. iNOS-mediated nitric oxide production and its regulation. Life Sci 75:639-653.
2. Alderton WK, Cooper CE, Knowles RG. 2001. Nitric oxide synthases: Structure, function and inhibition. Biochem J 357:593-615.
3. Aley KO, McCarter G, Levine JD. 1998. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 18:7008-7014.
4. Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK. 1996. Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 272:101-104.
5. Bi Z, Reiss CS. 1995. Inhibition of vesicular stomatitis virus infection by nitric oxide. J Virol 69:2208-2213.
6. Cezard JP, Duhamel JF, Meyer M, Pharaon I, Bellaiche M, Maurage C, Ginies JL, Vaillant JM, Girardet JP, Lamireau T, Poujol A, Morali A, Sarles J, Olives JP, Whately-Smith C, Audrain S, Lecomte JM. 2001. Efficacy and tolerability of racecadotril in acute diarrhea in children. Gastroenterology 120:799-805.
7. Dong Y, Zeng CQ, Ball JM, Estes MK, Morris AP. 1997. The rotavirus enterotoxin NSP4 mobilizes intracellular calcium in human intestinal cells by stimulating phospholipase C-mediated inositol 1,4,5-trisphosphate production. Proc Natl Acad Sci USA 94:3960-3965.
8. Furchgott RF. 1990. The 1989 Ulf von Euler lecture. Studies on endothelium-dependent vasodilation and the endothelium-derived relaxing factor. Acta Physiol Scand 139:257-270.
9. Garthwaite J. 1991. Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci 14:60-67.
10. Kawashima H, Inage Y, Ogihara M, Kashiwagi Y, Takekuma K, Hoshika A, Mori T, Watanabe Y. 2004. Serum and cerebrospinal fluid nitrite/nitrate levels in patients with rotavirus gastroenteritis induced convulsion. Life Sci 74:1397-1405.
11. Knowles RG, Palacios M, Palmer RM, Moncada S. 1989. Formation of nitric oxide from L-arginine in the central nervous system: A transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci USA 86:5159-5162.
12. Komatsu T, Ireland DD, Chen N, Reiss CS. 1999. Neuronal expression of NOS-1 is required for host recovery from viral encephalitis. Virology 258:389-395.
13. Kordasti S, Sjovall H, Lundgren O, Svensson L. 2004. Serotonin and vasoactive intestinal peptide antagonists attenuate rotavirus diarrhoea. Gut 53:952-957.
14. Kukuruzovic R, Robins-Browne RM, Anstey NM, Brewster DR. 2002. Enteric pathogens, intestinal permeability and nitric oxide production in acute gastroenteritis. Pediatr Infect Dis J 21:730-739.
15. Li Y, Ito N, Suzuki T, Stechschulte DJ, Dileepan KN. 1995. Dexamethasone inhibits nitric oxide-mediated cytotoxicity via effects on both macrophages and target cells. Immunopharmacology 30:177-186.
16. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
17. Lundgren O, Svensson L. 2001. Pathogenesis of rotavirus diarrhea. Microbes Infect 3:1145-1156.
18. Lundgren O, Svensson L. 2003. The enteric nervous system and infectious diarrhea. In: Gray J, editor. Viral gastroenteritis. London: Elsevier. pp 51-67.
19. Lundgren O, Peregrin AT, Persson K, Kordasti S, Uhnoo I, Svensson L. 2000. Role of the enteric nervous system in the fluid and electrolyte secretion of rotavirus diarrhea. Science 287:491-495.
20. MacLean A, Wei XQ, Huang FP, Al-Alem UA, Chan WL, Liew FY. 1998. Mice lacking inducible nitric-oxide synthase are more susceptible to herpes simplex virus infection despite enhanced Th1 cell responses. J Gen Virol 79:825-830.
21. 2+-dependently converts L-arginine into an activator of soluble guanylyl cyclase. Biochem Biophys Res Commun 164:678-685.
22. Michelangeli F, Ruiz MC, del Castillo JR, Ludert JE, Liprandi F. 1991. Effect of rotavirus infection on intracellular calcium homeostasis in cultured cells. Virology 181:520-527.
23. Morris AP, Estes MK. 2001. Microbes and microbial toxins: Paradigms for microbial-mucosal interactions. VIII. Pathological consequences of rotavirus infection and its enterotoxin. Am J Physiol Gastrointest Liver Physiol 281:G303-G310.
24. Offit PA, Clark HF, Kornstein MJ, Plotkin SA. 1984. A murine model for oral infection with a primate rotavirus (simian SA11). J Virol 51:233-236.
25. Osborne MP, Haddon SJ, Spencer AJ, Collins J, Starkey WG, Wallis TS, Clarke GJ, Worton KJ, Candy DC, Stephen J. 1988. An electron microscopic investigation of time-related changes in the intestine of neonatal mice infected with murine rotavirus. J Pediatr Gastroenterol Nutr 7:236-248.
26. Osborne MP, Haddon SJ, Worton KJ, Spencer AJ, Starkey WG, Thornber D, Stephen J. 1991. Rotavirus-induced changes in the microcirculation of intestinal villi of neonatal mice in relation to the induction and persistence of diarrhea. J Pediatr Gastroenterol Nutr 12:111-120.
27. Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI. 2003. Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9:565-572.
28. Ramig RF. 2004. Pathogenesis of intestinal and systemic rotavirus infection. J Virol 78:10213-10220.
29. Reiss CS, Komatsu T. 1998. Does nitric oxide play a critical role in viral infections? J Virol 72:4547-4551.
30. Rodriguez-Diaz J, Lopez-Andujar P, Garcia-Diaz A, Cuenca J, Montava R, Buesa J. 2003. Expression and purification of polyhistidine-tagged rotavirus NSP4 proteins in insect cells. Protein Expr Purif 31:207-212.
31. Rottenberg ME, Castanos-Velez E, de Mesquita R, Laguardia OG, Biberfeld P, Orn A. 1996. Intracellular co-localization of Trypanosoma cruzi and inducible nitric oxide synthase (iNOS): Evidence for dual pathway of iNOS induction. Eur J Immunol 26:3203-3213.
32. Salazar-Lindo E, Santisteban-Ponce J, Chea-Woo E, Gutierrez M. 2000. Racecadotril in the treatment of acute watery diarrhea in children. N Engl J Med 343:463-467.
33. Starkey WG, Collins J, Wallis TS, Clarke GJ, Spencer AJ, Haddon SJ, Osborne MP, Candy DC, Stephen J. 1986. Kinetics, tissue specificity and pathological changes in murine rotavirus infection of mice. J Gen Virol 67:2625-2634.
34. Stuehr DJ, Cho HJ, Kwon NS, Weise MF, Nathan CF. 1991. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase: An FAD- and FMN-containing flavoprotein. Proc Natl Acad Sci USA 88:7773-7777.
35. Sundqvist T, Laurin P, Falth-Magnusson K, Magnusson KE, Stenhammar L. 1998. Significantly increased levels of nitric oxide products in urine of children with celiac disease. J Pediatr Gastroenterol Nutr 27:196-198.
36. Superti F, Amici C, Tinari A, Donelli G, Santoro MG. 1998. Inhibition of rotavirus replication by prostaglandin A: Evidence for a block of virus maturation. J Infect Dis 178:564-568.
37. Svensson L, Uhnoo I, Grandien M, Wadell G. 1986. Molecular epidemiology of rotavirus infections in Uppsala, Sweden, 1981: Disappearance of a predominant electropherotype. J Med Virol 18:101-111.
38. Tafazoli F, Zeng CQ, Estes MK, Magnusson KE, Svensson L. 2001. NSP4 enterotoxin of rotavirus induces paracellular leakage in polarized epithelial cells. J Virol 75:1540-1546.
39. Tamura K, Schemann M, Wood JD. 1993. Actions of nitric oxide-generating sodium nitroprusside in myenteric plexus of guinea pig small intestine. Am J Physiol 265:G887-G893.
40. Tian P, Hu Y, Schilling WP, Lindsay DA, Eiden J, Estes MK. 1994. The nonstructural glycoprotein of rotavirus affects intracellular calcium levels. J Virol 68:251-257.
41. 2+ from the endoplasmic reticulum. J Virol 69:5763-5772.
42. Verdon CP, Burton BA, Prior RL. 1995. Sample pretreatment with nitrate reductase and glucose-6-phosphate dehydrogenase quantitatively reduces nitrate while avoiding interference by NADP+ when the Griess reaction is used to assay for nitrite. Anal Biochem 224:502-508.
43. Vodovotz Y, Kwon NS, Pospischil M, Manning J, Paik J, Nathan C. 1994. Inactivation of nitric oxide synthase after prolonged incubation of mouse macrophages with IFN-gamma and bacterial lipopolysaccharide. J Immunol 152:4110-4118.
44. Wu Z, Milton D, Nybom P, Sjo A, Magnusson KE. 1996. Vibrio cholerae hemagglutinin/protease (HA/protease) causes morphological changes in cultured epithelial cells and perturbs their paracellular barrier function. Microb Pathog 21:111-123.