NF-κB-mediated expression of iNOS promotes epithelial defense against infection by Cryptosporidium parvum in neonatal piglets

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 290, Issue 1, 2006, Pages

  Gookin, Jody L ^a   Chiang, Sophia ^a   Allen, Jessica ^a   Armstrong, Martha U ^a   Stauffer, Stephen H ^a   Finnegan, Colleen ^b   Murtaugh, Michael P ^b  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Barrier function; Cryptosporidiosis; Diarrhea; Nitric oxide

Indexed keywords

BROXURIDINE; CHLORINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; N6 (1 IMINOETHYL)LYSINE; NITRIC OXIDE SYNTHASE INHIBITOR; CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; DEHYDRATION; DIARRHEA; DISEASE COURSE; DISEASE SEVERITY; ENZYME INDUCTION; ENZYME LOCALIZATION; ENZYME SPECIFICITY; EPITHELIUM; EPITHELIUM CELL; HYDRATION; IN VIVO STUDY; INFECTION CONTROL; INTESTINE CELL; INTESTINE MUCOSA; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYST; PARASITISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATISTICAL SIGNIFICANCE; SWINE; ANIMAL; BODY WEIGHT; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; ILEUM; IMMUNOLOGY; METABOLISM; NEWBORN; PARASITOLOGY; PATHOLOGY; SWINE DISEASE; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; CHLORIDES; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM PARVUM; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; ILEUM; INTESTINAL MUCOSA; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; SWINE; SWINE DISEASES;

EID: 33644810365     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00460.2004     Document Type: Article

References (53)

1. Adams LB, Hibbs JB Jr, Taintor RR, and Krahenbuhl JL. Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii. Role for synthesis of inorganic nitrogen oxides from L-arginine. J Immunol 144: 2725-2729, 1990.
2. Argenzio RA, Lecce J, and Powell DW. Prostanoids inhibit intestinal NaCl absorption in experimental porcine cryptosporidiosis. Gastroenterology 104: 440-447, 1993.
3. Argenzio RA, Liacos JA, Levy ML, Meuten DJ, Lecce JG, and Powell DW. Villous atrophy, crypt hyperplasia, cellular infiltration, and impaired glucose-Na absorption in enteric cryptosporidiosis of pigs. Gastroenterology 98: 1129-1140, 1990.
4. Banan A, Fields JZ, Zhang Y, and Keshavarzian A. iNOS upregulation mediates oxidant-induced disruption of F-actin and barrier of intestinal monolayers. Am J Physiol Gastrointest Liver Physiol 280: G1234-G1246, 2001.
5. Butler DG, Gall DG, Kelly MH, and Hamilton JR. Transmissible gastroenteritis. Mechanisms responsible for diarrhea in an acute viral enteritis in piglets. J Clin Invest 53: 1335-1342, 1974.
6. Chen XM, Levine SA, Splinter PL, Tietz PS, Ganong AL, Jobin C, Gores GJ, Paya CV, and LaRusso NF. Cryptosporidium parvum activates nuclear factor κB in biliary epithelia preventing epithelial cell apoptosis. Gastroenterology 120: 1774-1783, 2001.
7. Dikopoulos N, Nussler AK, Liptay S, Bachem M, Reinshagen M, Stiegler M, Schmid RM, Adler G, and Weidenbach H. Inhibition of nitric oxide synthesis by aminoguanidine increases intestinal damage in the acute phase of rat TNB-colitis. Eur J Clin Invest 31: 234-239, 2001.
8. Eckmann L, Laurent F, Langford TD, Hetsko ML, Smith JR, Kagnoff MF, and Gillin FD. Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J Immunol 164: 1478-1487, 2000.
9. Efron DT, Thornton FJ, Steulten C, Tantry US, Witte MB, Kiyama T, and Barbul A. Expression and function of inducible nitric oxide synthase during rat colon anastomotic healing. J Gastrointest Surg 3: 592-601, 1999.
10. Fang FC. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99: 2818-2825, 1997.
11. Ferraris RP, Villenas SA, and Diamond J. Regulation of brush-border enzyme activities and enterocyte migration rates in mouse small intestine. Am J Physiol Gastrointest Liver Physiol 262: G1047-G1059, 1992.
12. Gookin J, Nordone S, Perryman L, and Argenzio R. Lymphocytes mediate IFN-independent ileal enterocyte iNOS expression in murine cryptosporidiosis (Abstract). Gastroenterology 122: A531, 2002.
13. Gookin JL, Allen J, Chiang S, Duckett L, and Armstrong MU. Local peroxynitrite formation contributes to early control of Cryptosporidium parvum infection. Infect Immun 73: 3929-3936, 2005.
14. Gookin JL, Duckett LL, Armstrong MU, Stauffer SH, Finnegan CP, Murtaugh MP, and Argenzio RA. Nitric oxide synthase stimulates prostaglandin synthesis and barrier function in C. parvum-infected porcine ileum. Am J Physiol Gastrointest Liver Physiol 287: G571-G581, 2004.
15. Gookin JL, Rhoads JM, and Argenzio RA. Inducible nitric oxide synthase mediates early epithelial repair of porcine ileum. Am J Physiol Gastrointest Liver Physiol 283: G157-G168, 2002.
16. Guo FH, De Raeve HR, Rice TW, Stuehr DJ, Thunnissen FB, and Erzurum SC. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc Natl Acad Sci USA 92: 7809-7813, 1995.
17. Hayward AR, Chmura K, and Cosyns M. Interferon-γ is required for innate immunity to Cryptosporidium parvum in mice. J Infect Dis 182: 1001-1004, 2000.
18. Hoffman RA. Intraepithelial lymphocytes coinduce nitric oxide synthase in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 278: G886-G894, 2000.
19. Hoffman RA, Zhang G, Nussler NC, Gleixner SL, Ford HR, Simmons RL, and Watkins SC. Constitutive expression of inducible nitric oxide synthase in the mouse ileal mucosa. Am J Physiol Gastrointest Liver Physiol 272: G383-G392, 1997.
20. Ito Y, Abril ER, Bethea NW, and McCuskey RS. Role of nitric oxide in hepatic microvascular injury elicited by acetaminophen in mice. Am J Physiol Gastrointest Liver Physiol 286: G60-G67, 2004.
21. Itoh Y, Ma FH, Hoshi H, Oka M, Noda K, Ukai Y, Kojima H, Nagano T, and Toda N. Determination and bioimaging method for nitric oxide in biological specimens by diaminofluorescein fluorometry. Anal Biochem 287: 203-209, 2000.
22. Izzo AA, Mascolo N, and Capasso F. Nitric oxide as a modulator of intestinal water and electrolyte transport. Dig Dis Sci 43: 1605-1620, 1998.
23. James SL. Role of nitric oxide in parasitic infections. Microbiol Rev 59: 533-547, 1995.
24. Kalff JC, Schraut WH, Billiar TR, Simmons RL, and Bauer AJ. Role of inducible nitric oxide synthase in postoperative intestinal smooth muscle dysfunction in rodents. Gastroenterology 118: 316-327, 2000.
25. Kuhls TL, Mosier DA, Abrams VL, Crawford DL, and Greenfield RA. Inability of interferon-γ and aminoguanidine to alter Cryptosporidium parvum infection in mice with severe combined immunodeficiency. J Parasitol 80: 480-485, 1994.
26. Kukuruzovic R, Robins-Browne RM, Anstey NM, and Brewster DR. Enteric pathogens, intestinal permeability and nitric oxide production in acute gastroenteritis. Pediatr Infect Dis J 21: 730-739, 2002.
27. Land SC and Rae C. iNOS initiates and sustains metabolic arrest in hypoxic lung adenocarcinoma cells: a mechanism of cell survival in the solid tumor core. Am J Physiol Cell Physiol 289: C918-C933, 2005.
28. Lawson LD and Powell DW. Bradykinin-stimulated eicosanoid synthesis and secretion by rabbit ileal components. Am J Physiol Gastrointest Liver Physiol 252: G783-G790, 1987.
29. Leitch GJ and He Q. Arginine-derived nitric oxide reduces fecal oocyst shedding in nude mice infected with Cryptosporidium parvum. Infect Immun 62: 5173-5176, 1994.
30. Leitch GJ and He Q. Reactive nitrogen and oxygen species ameliorate experimental cryptosporidiosis in the neonatal BALB/c mouse model. Infect Immun 67: 5885-5891, 1999.
31. Lin JY and Chadee K. Macrophage cytotoxicity against Entamoeba histolytica trophozoites is mediated by nitric oxide from L-arginine. J Immunol 148: 3999-4005, 1992.
32. McCafferty DM, Mudgett JS, Swain MG, and Kubes P. Inducible nitric oxide synthase plays a critical role in resolving intestinal inflammation. Gastroenterology 112: 1022-1027, 1997.
33. McCartney-Francis NL, Song X, Mizel DE, and Wahl SM. Selective inhibition of inducible nitric oxide synthase exacerbates erosive joint disease. J Immunol 166: 2734-2740, 2001.
34. McCole DF, Eckmann L, Laurent F, and Kagnoff MF. Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infect Immun 68: 1710-1713, 2000.
35. Mele R, Gomez Morales MA, Tosini F, and Pozio E. Cryptosporidium parvum at different developmental stages modulates host cell apoptosis in vitro. Infect Immun 72: 6061-6067, 2004.
36. Menconi MJ, Unno N, Smith M, Aguirre DE, and Fink MP. Nitric oxide donor-induced hyperpermeability of cultured intestinal epithelial monolayers: role of superoxide radical, hydroxyl radical, and peroxynitrite. Biochim Biophys Acta 1425: 189-203, 1998.
37. Miller MJ, Thompson JH, Zhang XJ, Sadowska-Krowicka H, Kakkis JL, Munshi UK, Sandoval M, Rossi JL, Eloby-Childress S, Beckman JS, et al. Role of inducible nitric oxide synthase expression and peroxynitrite formation in guinea pig ileitis. Gastroenterology 109: 1475-1483, 1995.
38. Oswald IP and James SL. Nitrogen oxide in host defense against parasites. Methods 10: 8-14, 1996.
39. Pampusch MS, Bennaars AM, Harsch S, and Murtaugh MP. Inducible nitric oxide synthase expression in porcine immune cells. Vet Immunol Immunopathol 61: 279-289, 1998.
40. Payne D and Kubes P. Nitric oxide donors reduce the rise in reperfusion-induced intestinal mucosal permeability. Am J Physiol Gastrointest Liver Physiol 265: G189-G195, 1993.
41. Pollok RC, Farthing MJ, Bajaj-Elliott M, Sanderson IR, and McDonald V. Interferon γ induces enterocyte resistance against infection by the intracellular pathogen Cryptosporidium parvum. Gastroenterology 120: 99-107, 2001.
42. Quintana E, Hernandez C, Alvarez-Barrientos A, Esplugues JV, and Barrachina MD. Synthesis of nitric oxide in postganglionic myenteric neurons during endotoxemia: implications for gastric motor function in rats. FASEB J 18: 531-533, 2004.
43. Resta-Lenert S and Barrett KE. Enteroinvasive bacteria alter barrier and transport properties of human intestinal epithelium: role of iNOS and COX-2. Gastroenterology 122: 1070-1087, 2002.
44. Salzman AL, Menconi MJ, Unno N, Ezzell RM, Casey DM, Gonzalez PK, and Fink MP. Nitric oxide dilates tight junctions and depletes ATP in cultured Caco-2BBe intestinal epithelial monolayers. Am J Physiol Gastrointest Liver Physiol 268: G361-G373, 1995.
45. Schwartz D, Schwartz IF, Gnessin E, Wollman Y, Chernichovsky T, Blum M, and Iaina A. Differential regulation of glomerular arginine transporters (CAT-1 and CAT-2) in lipopolysaccharide-treated rats. Am J Physiol Renal Physiol 284: F788-F795, 2003.
46. Singer II, Kawka DW, Scott S, Weidner JR, Mumford RA, Riehl TE, and Stenson WF. Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 111: 871-885, 1996.
47. Unno N, Menconi MJ, Smith M, Aguirre DE, and Fink MP. Hyperpermeability of intestinal epithelial monolayers is induced by NO: effect of low extracellular pH. Am J Physiol Gastrointest Liver Physiol 272: G923-G934, 1997.
48. Unno N, Wang H, Menconi MJ, Tytgat SH, Larkin V, Smith M, Morin MJ, Chavez A, Hodin RA, and Fink MP. Inhibition of inducible nitric oxide synthase ameliorates endotoxin-induced gut mucosal barrier dysfunction in rats. Gastroenterology 113: 1246-1257, 1997.
49. Vallance BA, Deng W, De Grado M, Chan C, Jacobson K, and Finlay BB. Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect Immun 70: 6424-6435, 2002.
50. Wu G, Knabe DA, Flynn NE, Yan W, and Flynn SP. Arginine degradation in developing porcine enterocytes. Am J Physiol Gastrointest Liver Physiol 271: G913-G919, 1996.
51. Yamasaki K, Edington HD, McClosky C, Tzeng E, Lizonova A, Kovesdi I, Steed DL, and Billiar TR. Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J Clin Invest 101: 967-971, 1998.
52. Ye JF, Zheng XX, and Xu LX. Real-time detection of nitric oxide in cultured rat aorta endothelial cells induced by shear stress. Acta Biochim Biophys Sin 35: 296-300, 2003.
53. Yue G, Lai PS, Yin K, Sun FF, Nagele RG, Liu X, Linask KK, Wang C, Lin KT, and Wong PY. Colon epithelial cell death in 2,4,6-trinitro-benzenesulfonic acid-induced colitis is associated with increased inducible nitric-oxide synthase expression and peroxynitrite production. J Pharmacol Exp Ther 297: 915-925, 2001.