Colon epithelial cell death in 2,4,6-trinitrobenzenesulfonic acid-induced colitis is associated with increased inducible nitric-oxide synthase expression and peroxynitrite production

Journal of Pharmacology and Experimental Therapeutics

Volumn 297, Issue 3, 2001, Pages 915-925

  Yue, Gang ^a   Lai, Pi Shiang ^a   Yin, Kingsley ^a   Sun, Frank F ^a   Nagele, Robert G ^a   Liu, Xiao ^a   Linask, Kersti K ^a   Wang, Congli ^a   Lin, King Teh ^a   Wong, Patrick Y K ^a  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CYTOKERATIN; MYELOPEROXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE; PROTEIN BAX; PROTEIN BCL 2; SUPEROXIDE; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL DEATH; COLITIS; COLON MUCOSA; CONTROLLED STUDY; ENZYME ACTIVITY; GEL ELECTROPHORESIS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL DEATH; COLITIS; COLON; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; ISOENZYMES; LYSINE; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PEROXIDASE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDES; TRINITROBENZENESULFONIC ACID; TYROSINE;

EID: 0035008079     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (41)

1. Akiba Y, Nakamura M, Oda M, Kimura H, Miura S, Tsuchiya M and Ishii H (1997) Basic fibroblast growth factor increase constitutive nitric oxide synthase during healing of rat gastric ulcer. J Clin Gastroenterol 25 (Suppl 1):S118-S122.
2. Beckman JS and Koppenol WH (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271:C1424-C1437.
3. Beckman JS, Ye YZ, Anderson PG, Chen J, Accavitti MA, Tarpey MM and White CR (1994) Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol Chem Hoppe-Seyler 375:81-88.
4. Bradley PP, Priebat DA, Christensen RD and Rothstein G (1982) Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 78:296-209.
5. Cockrell A, Laroux FS, Jourd'heuil D, Kawachi S, Gray L, van der Heyde H and Grisham MB (1999) Role of inducible nitric oxide synthase in leukocyte extravasation in vivo. Biochem Biophys Res Commun 257:684-686.
6. Dijkstra G, Moshage H, van Dullemen EM, de Jager-Krikken A, Tiebosch AT, Kleibeuker JH, Jansen PL and van Goor H (1998) Expression of nitric oxide synthases and formation of nitrotyrosine and reactive oxygen species in inflammatory bowel disease. J Pathol 186:416-421.
7. Eiserich JP, Cross CE, Jones AD, Halliwell B and van der Vliet A (1996) Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid. J Biol Chem 271:19199-19208.
8. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B and van der Vliet A (1998) Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature (Lond) 391:393-397.
9. Ford H, Watkins S, Reblock K and Rowe M (1997) The role of inflammatory cytokines and nitric oxide in the pathogenesis of necrotizing enterocolitis. J Pediatr Surg 32:275-282.
10. Godkin AJ, De Belder AJ, Villa L, Wong A, Beesley JE, Kane SP and Martin JF (1996) Expression of nitric oxide synthase in ulcerative colitis. Eur J Clin Invest 26:867-872.
11. Green DR and Reed JC (1998) Mitochondria and apoptosis (review). Science (Wash DC) 281:1309-1312.
12. Hall PA, Coates PJ, Ansari B and Hopwood D (1994) Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J Cell Sci 107: 3569-3577.
13. Hughes MN (1999) Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim Biophys Acta 1411:263-272.
14. Iwamoto M, Koji T, Makiyama K, Kobayashi N and Nakane PK (1996) Apoptosis of crypt epithelial cells in ulcerative colitis. J Pathol 180:152-159.
15. Jones BA and Gores GJ (1997) Physiology and pathophysiology of apoptosis in epithelial cells of the liver, pancreas, and intestine. Am J Physiol 273:G1174-G1188.
16. Kim JM, Eckmann L, Savidge TC, Lowe DC, Witthoft T and Kagnoff MF (1998) Apoptosis of human intestinal epithelial cells after bacterial invasion. J Clin Invest 102:1815-1823.
17. Kimura H, Hokari R, Miura S, Shigematsu T, Hirokawa M, Akiba Y, Kurose I, Higuchi H, Fujimori H, Tsuzuki Y, et al. (1998) Increased expression of an inducible isoform of nitric oxide synthase and the formation of peroxynitrite in colonic mucosa of patients with active ulcerative colitis. Gut 42:180-187.
18. Kolios G, Rooney N, Murphy CT, Robertson DA and Westwick J (1998) Expression of inducible nitric oxide synthase activity in human colon epithelial cells: modulation by T lymphocyte derived cytokines. Gut 43:56-63.
19. Lin KT, Xue JY, Nomen M, Spur B and Wong PY-K (1995) Peroxynitrite-induced apoptosis in HL-60 cells. J Biol Chem 270:16487-16490.
20. McCafferty DM, Miampamba M, Sihota E, Sharkey KA and Kubes P (1999) Role of inducible nitric oxide synthase in trinitrolbenzene sulphonic acid induced colitis in mice. Gut 45:864-873.
21. McCafferty DM, Mudgett JS, Swain MG and Kubes P (1997) Inducible nitric oxide synthase plays a critical role in resolving intestinal inflammation. Gastroenterology 112:1022-1027.
22. McNaughton WK, Lowe SS and Gushing K (1998) Role of nitric oxide in inflammation-induced suppression of secretion in a mouse model of acute colitis. Am J Physiol 275:G1353-G1360.
23. Miller MJ, Sadowska-Krowicka H, Chotinaruemol S, Kakkis JL and Clark DA (1993) Amelioration of chronic ileitis by inducible nitric oxide synthase inhibition. J Pharmacol Exp Ther 264:11-16.
24. Miller MJ, Thompson JH, Zhang XJ, Sadowska-Krowicka H, Kakkis JL, Munshi UK, Sandoval M, Rossi JL, Eloby-Childress S and Beckman JS (1995) Role of inducible nitric oxide synthase expression and peroxynitrite formation in guinea pig ileitis. Gastroenterology 109:1475-1483.
25. Pfeiffer CJ and Qiu BS (1995) Effects of chronic nitric oxide synthase inhibition of TNB-induced colitis in rats. J Pharm Pharmacol 47:827-832.
26. Rachmilewitz D, Karmeli F, Okon E and Bursztyn M (1995) Experimental colitis is ameliorated by inhibition of nitric oxide synthase activity. Gut 37:247-255.
27. Rachmilewitz D, Stamler JS, Karmeli F, Mullins ME, Singel DJ, Loscalzo J, Xavier RJ and Podolsky DK (1993) Peroxynitrite-induced rat colitis - a new model of colonic inflammation. Gastroenterology 105:1681-1688.
28. Sandoval M, Liu X, Mannick EE, Clark DA and Miller MJ (1997) Peroxynitrite-induced apoptosis in human intestinal epithelial cells is attenuated by mesalamine. Gastroenterology 113:1480-1488.
29. Schwartz D, Mendonca M, Schwartz I, Xia Y, Satriano J, Wilson CB and Blantz RC (1997) Inhibition of constitutive nitric oxide synthase (NOS) by nitric oxide generated by inducible NOS after lipopolysaccharide administration provokes renal dysfunction in rats. J Clin Invest 100:439-448.
30. Singer II, Kawka DW, Scott S, Weidner JR, Mumford RA, Riehl TE and Stenson WF (1996) Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 111:871-885.
31. Slomiany BL, Piotrowski J and Slomiany A (1999) Gastric mucosal inflammatory responses to Helicobacter pylori lipopolysaccharide: down-regulation of nitric oxide synthase-2 and caspase-3 by sulglycotide. Biochem Biophys Res Commun 261:15-20.
32. Squadrito GL and Pryor WA (1995) The formation of peroxynitrite in vivo from nitric oxide and superoxide. Chem-Biol Interact 96:203-206.
33. Sträter J, Koretz K, Günthert AR and Möller P (1995) In situ detection of enterocytic apoptosis in normal colonic mucosa and in familial adnomatous polyposis. Gut 37:819-825.
34. Sträter J, Wellisch I, Riedl S, Walczak H, Koretz K, Tandara A, Krammer PH and Moller P (1997) CD95 (APO-1/Fas)-mediated apoptosis in colon epithelial cells; a possible role in ulcerative colitis. Gastroenterology 113:160-167.
35. Sun Z, Wang X, Wallen R, Deng X, Du X, Hallberg E and Andersson R (1998) The influence of apoptosis on intestinal barrier integrity in rats. Scand J Gastroenterol 33:415-422.
36. Szabo C (1996) DNA strand breakage and activation of poly-ADP ribosyltransferase: a cytotoxic pathway triggered by peroxynitrite. Free Radic Biol Med 21:855-869.
37. Yin K, Hock CE, Lai PS, Ross J and Yue G (1999) Role of interferon-gamma in lung inflammation following cecal ligation and puncture in rats. Shock 12:215-221.
38. Yue G, Sun FF, Dunn C, Yin K and Wong PY (1996) The 21-aminosteroid tirilazad mesylate can ameliorate inflammatory bowel disease in rats. J Pharmacol Exp Ther 276:265-270.
39. Zingarelli B, Cuzzocrea S, Szabo C and Salzman AL (1998) Mercaptoethylguanidine, a combined inhibitor of nitric oxide synthase and peroxynitrite scavenger, reduces trinitrobenzene sulfonic acid-induced colonie damage in rats. J Pharmacol Exp Ther 287:1048-1055.
40. Zingarelli B, Szabo C and Salzman AL (1999a) Reduced oxidative and nitrosative damage in murine experimental colitis in the absence of inducible nitric oxide synthase. Gut 45:199-209.
41. Zingarelli B, Szabo C and Salzman AL (1999b) Blockade of poly(ADP-ribose) synthetase inhibits neutrophil recruitment, oxidant generation, and mucosal injury in murine colitis. Gastroenterology 116:335-345.