Hindlimb ischemia/reperfusion-induced remote injury to the small intestine: Role of inducible nitric-oxide synthase-derived nitric oxide

Journal of Pharmacology and Experimental Therapeutics

Volumn 329, Issue 3, 2009, Pages 919-927

  Katada, Kazuhiro ^a   Bihari, Aurelia ^a   Badhwar, Amit ^a   Yoshida, Norimasa ^c   Yoshikawa, Toshikazu ^c   Potter, Richard F ^a,b   Cepinskas, Gediminas ^a  

^a LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRATE; NITRIC OXIDE; NITRITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; HINDLIMB; ILEUM; INFLAMMATION; INTESTINE FLUID; INTESTINE INJURY; INTESTINE MUCOSA PERMEABILITY; JEJUNUM; LEUKOCYTE MIGRATION; LIMB ISCHEMIA; MALE; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

AMIDINES; ANIMALS; BENZYLAMINES; E-SELECTIN; ENZYME INHIBITORS; EPITHELIAL CELLS; HINDLIMB; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; INTESTINAL MUCOSA; INTESTINE, SMALL; LEUKOCYTES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROVESSELS; NF-KAPPA B; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PERMEABILITY; PEROXIDASE; REPERFUSION INJURY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 66749160461     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.108.148460     Document Type: Article

References (40)

1. Adams V, Nehrhoff B, Späte U, Linke A, Schulze PC, Baur A, Gielen S, Hambrecht R, and Schuler G (2002) Induction of iNOS expression in skeletal muscle by IL-1beta and NFkappaB activation: an in vitro and in vivo study. Cardiovasc Res 54:95-104. (Pubitemid 34327940)
2. Avontuur JA, Bruining HA, and Ince C (1995) Inhibition of nitric oxide synthesis causes myocardial ischemia in endotoxemic rats. Circ Res 76:418-425.
3. Balzan S, de Almeida Quadros C, de Cleva R, Zilberstein B, and Cecconello I (2007) Bacterial translocation: overview of mechanisms and clinical impact. J Gastroenterol Hepatol 22:464-471. (Pubitemid 46435001)
4. Binion DG, Rafiee P, Ramanujam KS, Fu S, Fisher PJ, Rivera MT, Johnson CP, Otterson MF, Telford GL, and Wilson KT (2000) Deficient iNOS in inflammatory bowel disease intestinal microvascular endothelial cells results in increased leukocyte adhesion. Free Radic Biol Med 29:881-888.
5. Brown KA, Brain SD, Pearson JD, Edgeworth JD, Lewis SM, and Treacher DF (2006) Neutrophils in development of multiple organ failure in sepsis. Lancet 368:157-169. (Pubitemid 43994173)
6. Carden DL and Granger DN (2000) Pathophysiology of ischaemia-reperfusion injury. J Pathol 190:255-266. (Pubitemid 30141372)
7. Cepinskas G and Wilson JX (2008) Inflammatory response in microvascular endothelium in sepsis: role of oxidants. J Clin Biochem Nutr 42:175-184.
8. Chen LW, Hwang B, Wang JS, Chen JS, and Hsu CM (2004) Hypertonic salineenhanced postburn gut barrier failure is reversed by inducible nitric oxide synthase inhibition. Crit Care Med 32:2476-2484. (Pubitemid 39648231)
9. Deitch EA (1990) The role of intestinal barrier failure and bacterial translocation in the development of systemic infection and multiple organ failure. Arch Surg 125:403-404. (Pubitemid 20079089)
10. Fink MP (2003) Intestinal epithelial hyperpermeability: update on the pathogenesis of gut mucosal barrier dysfunction in critical illness. Curr Opin Crit Care 9:143-151. (Pubitemid 36408134)
11. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, and Knowles RG (1997) 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo. J Biol Chem 272:4959-4963. (Pubitemid 27090046)
12. Grisham MB, Jourd'Heuil D, and Wink DA (1999) Nitric oxide. I. Physiological chemistry of nitric oxide and its metabolites: implications in inflammation. Am J Physiol 276:G315-G321. (Pubitemid 29104144)
13. Han X, Fink MP, Yang R, and Delude RL (2004) Increased iNOS activity is essential for intestinal epithelial tight junction dysfunction in endotoxemic mice. Shock 21:261-270.
14. Hassoun HT, Kone BC, Mercer DW, Moody FG, Weisbrodt NW, and Moore FA (2001) Post-injury multiple organ failure: the role of the gut. Shock 15:1-10. (Pubitemid 33598153)
15. Hickey MJ, Sharkey KA, Sihota EG, Reinhardt PH, Macmicking JD, Nathan C, and Kubes P (1997) Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J 11:955-964. (Pubitemid 27425897)
16. Hierholzer C, Kalff JC, Billiar TR, Bauer AJ, Tweardy DJ, and Harbrecht BG (2004) Induced nitric oxide promotes intestinal inflammation following hemorrhagic shock. Am J Physiol Gastrointest Liver Physiol 286:G225-G233. (Pubitemid 38134033)
17. Hollenberg SM, Guglielmi M, and Parrillo JE (2007) Discordance between microvascular permeability and leukocyte dynamics in septic inducible nitric oxide synthase deficient mice. Crit Care 11:R125.
18. Inoue K, Takahashi T, Uehara K, Shimuzu H, Ido K, Morimatsu H, Omori E, Katayama H, Akagi R, and Morita K (2008) Protective role of heme oxygenase 1 in the intestinal tissue injury in hemorrhagic shock in rats. Shock 29:252-261.
19. Jean-Baptiste E (2007) Cellular mechanisms in sepsis. J Intensive Care Med 22:63-72.
20. Kleinert H, Schwarz PM, and Förstermann U (2003) Regulation of the expression of inducible nitric oxide synthase. Biol Chem 384:1343-1364. (Pubitemid 37508640)
21. Kubes P (2000) Inducible nitric oxide synthase: a little bit of good in all of us. Gut 47:6-9. (Pubitemid 30430403)
22. Lawlor DK, Brock RW, Harris KA, and Potter RF (1999) Cytokines contribute to early hepatic parenchymal injury and microvascular dysfunction after bilateral hindlimb ischemia. J Vasc Surg 30:533-541. (Pubitemid 29441795)
23. Lee CC, Lin NT, Hsu YH, and Chen HI (2005) Inducible nitric oxide synthase inhibition potentiates multiple organ dysfunction induced by endotoxin in conscious rats. J Cardiovasc Pharmacol 45:396-403. (Pubitemid 40627959)
24. Lefer DJ, Jones SP, Girod WG, Baines A, Grisham MB, Cockrell AS, Huang PL, and Scalia R (1999) Leukocyte-endothelial cell interactions in nitric oxide synthasedeficient mice. Am J Physiol 276:H1943-H1950. (Pubitemid 29323478)
25. Leong KG and Karsan A (2000) Signaling pathways mediated by tumor necrosis factor alpha. Histol Histopathol 15:1303-1325.
26. Levy RM, Prince JM, and Billiar TR (2005) Nitric oxide: a clinical primer. Crit Care Med 33:S492-S495. (Pubitemid 41785998)
27. Liu SF and Malik AB (2006) NF-kappa B activation as a pathological mechanism of septic shock and inflammation. Am J Physiol Lung Cell Mol Physiol 290:L622-L645. (Pubitemid 43738989)
28. Lozano FS, Barros MB, García-Criado FJ, and Gomez-Alonso A (2005) Exogenous nitric oxide can control SIRS and downregulate NFkappaB. J Surg Res 124:52-58. (Pubitemid 40269801)
29. Lush CW, Cepinskas G, and Kvietys PR (2003) Regulation of intestinal nuclear factor-kappaB activity and E-selectin expression during sepsis: a role for peroxynitrite. Gastroenterology 124:118-128. (Pubitemid 36055345)
30. Mark LA, Robinson AV, and Schulak JA (2005) Inhibition of nitric oxide synthase reduces renal ischemia/reperfusion injury. J Surg Res 129:236-241. (Pubitemid 41797058)
31. Nagahama S, Korenaga D, Honda M, Inutsuka S, and Sugimachi K (2002) Assessment of the intestinal permeability after a gastrectomy and the oral administration of anticancer drugs in rats: nitric oxide release in response to gut injury. Surgery 131:S92-S97. (Pubitemid 34118622)
32. Naito Y, Takagi T, Ichikawa H, Tomatsuri N, Kuroda M, Isozaki Y, Katada K, Uchiyama K, Kokura S, Yoshida N, et al. (2004) A novel potent inhibitor of inducible nitric oxide inhibitor, ONO-1714, reduces intestinal ischemia-reperfusion injury in rats. Nitric Oxide 10:170-177. (Pubitemid 38668666)
33. Poon BY, Raharjo E, Patel KD, Tavener S, and Kubes P (2003) Complexity of inducible nitric oxide synthase: cellular source determines benefit versus toxicity. Circulation 108:1107-1112. (Pubitemid 37071522)
34. Potoka DA, Nadler EP, Upperman JS, and Ford HR (2002) Role of nitric oxide and peroxynitrite in gut barrier failure. World J Surg 26:806-811. (Pubitemid 36920321)
35. Sanz MJ, Hickey MJ, Johnston B, McCafferty DM, Raharjo E, Huang PL, and Kubes P (2001) Neuronal nitric oxide synthase (NOS) regulates leukocyte-endothelial cell interactions in endothelial NOS deficient mice. Br J Pharmacol 134:305-312. (Pubitemid 32989127)
36. Scott JR, Gray DK, Bihari A, Badhwar A, Zhang X, Shan P, Lee PJ, Chakrabarti S, Harris KA, and Potter RF (2005) Heme oxygenase modulates small intestine leukocyte adhesion following hindlimb ischemia/reperfusion by regulating the expression of intercellular adhesion molecule-1. Crit Care Med 33:2563-2570. (Pubitemid 41682109)
37. Souza DG, Vieira AT, Pinho V, Sousa LP, Andrade AA, Bonjardim CA, McMillan M, Kahn M, and Teixeira MM (2005) NF-kappaB plays a major role during the systemic and local acute inflammatory response following intestinal reperfusion injury. Br J Pharmacol 145:246-254. (Pubitemid 40756529)
38. Suzuki Y, Deitch EA, Mishima S, Lu Q, and Xu D (2000) Inducible nitric oxide synthase gene knockout mice have increased resistance to gut injury and bacterial translocation after an intestinal ischemia-reperfusion injury. Crit Care Med 28:3692-3696.
39. Wunder C, Brock RW, McCarter SD, Bihari A, Harris K, Eichelbrönner O, and Potter RF (2002) Inhibition of haem oxygenase activity increases leukocyte accumulation in the liver following limb ischaemia-reperfusion in mice. J Physiol 540:1013-1021. (Pubitemid 35190170)
40. Yassin MM, Harkin DW, Barros D'Sa AA, Halliday MI, and Rowlands BJ (2002) Lower limb ischemia-reperfusion injury triggers a systemic inflammatory response and multiple organ dysfunction. World J Surg 26:115-121. (Pubitemid 36918828)