Knock out of neuronal nitric oxide synthase exacerbates intestinal ischemia/reperfusion injury in mice

Cell and Tissue Research

Volumn 349, Issue 2, 2012, Pages 565-576

  Rivera, Leni R ^a,c   Pontell, Louise ^a   Cho, Hyun Jung ^a   Castelucci, Patricia ^b   Thacker, Michelle ^a   Poole, Daniel P ^a   Frugier, Tony ^a   Furness, John B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Enteric nervous system; Intestine; Ischemia; Mouse; Nitric oxide synthase

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CONTRACTILE PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; ACTIN; NITRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME ACTIVITY; ENZYME ASSAY; FEMALE; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINE ISCHEMIA; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; MUSCLE CONTRACTION; NERVE STIMULATION; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; REPERFUSION INJURY; ANIMAL; C57BL MOUSE; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; SMALL INTESTINE; SMOOTH MUSCLE;

MUS;

ACTINS; ANIMALS; FEMALE; GENE DELETION; INTESTINE, SMALL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; REPERFUSION INJURY;

EID: 84871893379     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-012-1451-3     Document Type: Article

References (45)

1. Bauer AJ, Boeckxstaens GE (2004) Mechanisms of postoperative ileus. Neurogastroenterol Motil 16:54-60
2. Beck PL, Xavier R, Wong J, Ezedi I, Mashimo H, Mizoguchi A, Mizoguchi E, Bhan AK, Podolsky DK (2004) Paradoxical roles of different nitric oxide synthase isoforms in colonic injury. Am J Physiol 286:G137-G147
3. Ferrer-Sueta G, Radi R (2009) Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem Biol 4:161-177
4. Furness JB, Costa M (1979) Projections of intestinal neurons showing immunoreactivity for vasoactive intestinal polypeptide are consistent with these neurons being the enteric inhibitory neurons. Neurosci Lett 15:199-204
5. Furness JB, Kunze WAA, Clerc N (1999) Nutrient tasting and signaling mechanisms in the gut. II. The intestine as a sensory organ: neural, endocrine, and immune responses. Am J Physiol 277: G922-G928
6. Gabella G (1974) Special muscle cells and their innervation in the mammalian small intestine. Cell Tissue Res 153:63-77
7. Granger N, Korthuis RJ (1995) Physiologic mechanisms of postischemic tissue injury. Annu Rev Physiol 57:311-332
8. Grisham MB, Granger DN, Lefer DJ (1998) Modulation of leukocyteendothelial interactions by reactive metabolites of oxygen and nitrogen: relevance to ischemic heart disease. Free Radic Biol Med 25:404-433
9. Hierholzer C, Kalff JC, Audolfsson G, Billiar TR, Tweardy DJ, Bauer AJ (1999) Molecular and functional contractile sequelae of rat intestinal ischemia/reperfusion injury. Transplantation 68:1244-1254
10. Hoffman RA, Zhang G, Nussler NC, Gleixner SL, Ford HR, Simmons RL, Watkins SC (1997) Constitutive expression of inducible nitric oxide synthase in the mouse ileal mucosa. Am J Physiol Gastrointest Liver Physiol 272:G383-G392
11. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC (1993) Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75:1273-1286
12. Kalff JC, Schraut WH, Simmons RL, Bauer AJ (1998a) Surgical manipulation of the gut elicits an intestinal muscularis inflammatory response resulting in postsurgical ileus. Ann Surg 228:652-663
13. Kalff JC, Schwarz NT, Walgenbach KJ, Schraut WH, Bauer AJ (1998b) Leukocytes of the intestinal muscularis: their phenotype and isolation. J Leukoc Biol 63:683-691
14. Kalff JC, Carlos TM, Schraut WH, Billiar TR, Simmons RL, Bauer AJ (1999) Surgically induced leukocytic infiltrates within the rat intestinal muscularis mediate postoperative ileus. Gastroenterology 117:378-387
15. Knowles CH, De Giorgio R, Kapur RP, Bruder E, Farrugia G, Geboes K, Gershon MD, Hutson J, Lindberg G, Martin JE, Meier-Ruge WA, Milla PJ, Smith VV, Vandervinden JM, Veress B, Wedel T (2009) Gastrointestinal neuromuscular pathology: guidelines for histological techniques and reporting on behalf of the Gastro 2009 International Working Group. Acta Neuropathol 118:271-301
16. Kobayashi Y (2010) The regulatory role of nitric oxide in proinflammatory cytokine expression during the induction and resolution of inflammation. J Leukoc Biol 88:1157-1162
17. Kosonen O, Kankaanranta H, Malo-Ranta U, Moilanen E (1999) Nitric oxide-releasing compounds inhibit neutrophil adhesion to endothelial cells. Eur J Pharmacol 382:111-117
18. Kubes P, McCafferty DM (2000) Nitric oxide and intestinal inflammation. Am J Med 109:150-158
19. Kubes P, Suzuki M, Granger DN (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88:4651-4655
20. Kurose I, Kubes P, Wolf R, Anderson DC, Paulson J, Miyasada M, Granger DN (1993) Inhibition of nitric oxide production. Mechanisms of vascular albumin leakage. Circ Res 73:164-171
21. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568
22. Livingston EH, Passaro EP Jr (1990) Postoperative ileus. Dig Dis Sci 35:121-132
23. Love S (1999) Oxidative stress in brain ischemia. Brain Pathol 9:119-131
24. Lubbers T, Buurman W, Luyer M (2010) Controlling postoperative ileus by vagal activation. World J Gastroenterol 16:1683-1687
25. Luo CC, Chen HM, Chiu CH, Lin JN, Chen JC (2001) Effect of NG-nitro-L-arginine methyl ester on intestinal permeability following intestinal ischemia-reperfusion injury in a rat model. Biol Neonate 80:60-63
26. Mallick IH, Yang W, Winslet MC, Seifalian AM (2004) Ischemia reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci 49:1359-1377
27. Massberg S, Messmer K (1998) The nature of ischemia/reperfusion injury. Transplant Proc 30:4217-4223
28. Masuda E, Kawano S, Nagano K, Tsuji S, Takei Y, Tsujii M, Oshita M, Michida T, Kobayashi I, Nakama A, Fusamoto H, Kamada T (1995) Endogenous nitric oxide modulates ethanol-induced gastric mucosal injury in rats. Gastroenterology 108:58-64
29. McCafferty DM, Miampamba M, Sihota E, Sharkey KA, Kubes P (1999) Role of inducible nitric oxide synthase in trinitrobenzene sulphonic acid induced colitis in mice. Gut 45:864-873
30. Miller MJS, Munshi UK, Sadowska Krowicka H, Kakkis JL, Zhang XJ, Eloby-Childress S, Clark DA (1994) Inhibition of calciumdependent nitric oxide synthase causes ileitis and leukocytosis in guinea pigs. Dig Dis Sci 39:1185-1192
31. Moro MA, Cárdenas A, Hurtado O, Leza JC, Lizasoain I (2004) Role of nitric oxide after brain ischaemia. Cell Calcium 36:265-275
32. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767-801
33. Payne D, Kubes P (1993) Nitric oxide donors reduce the rise in reperfusion-induced intestinal mucosal permeability. Am J Physiol Gastrointest Liver Physiol 265:G189-G195
34. Pfeiffer CJ, Qiu BS (1995) Effects of chronic nitric oxide synthase inhibition on TNB-induced colitis in rats. J Pharm Pharmacol 47:827-832
35. Pique JM, Whittle BJR, Esplugues JV (1989) The vasodilator role of endogenous nitric oxide in the rat gastric microcirculation. Eur J Pharmacol 174:293-296
36. Pontell L, Sharma P, Rivera LR, Thacker M, Tan YH, Brock JA, Furness JB (2011) Damaging effects of ischemia/reperfusion on intestinal muscle. Cell Tissue Res 343:411-419
37. Qu X-W, Wang H, De Plaen IG, Rozenfeld RA, Hsueh W (2001) Neuronal nitric oxide synthase (NOS) regulates the expression of inducible NOS in rat small intestine via modulation of nuclear factor kappa B. FASEB J 15:439-446
38. Rivera LR, Thacker M, Castelucci P, Bron R, Furness JB (2009) The reactions of specific neuron types to intestinal ischemia in the guinea pig enteric nervous system. Acta Neuropathol 118:261-270
39. Rivera LR, Poole DP, Thacker M, Furness JB (2011a) The involvement of nitric oxide synthase neurons in enteric neuropathies. Neurogastroenterol Motil 23:980-988
40. Rivera LR, Thacker M, Pontell L, Cho H-J, Furness JB (2011b) Deleterious effects of intestinal ischemia/reperfusion injury in the mouse enteric nervous system are associated with protein nitrosylation. Cell Tissue Res 344:111-123
41. Taha MO, Miranda-Ferreira R, Fagundes AL, Fagundes DJ, Simões RS, Santos JM, Souza PDF, Júnior ISO, Marchini A, Gomes IT, Monteiro HP, Mendonça LO, Caricati-Neto A (2010) Effects of Lnitro-arginine methyl ester, an inhibitor of nitric oxide biosynthesis, on intestinal ischemia/reperfusion injury in rabbits. Transplant Proc 42:457-460
42. Togashi H, Sasaki M, Frohman E, Taira E, Ratan RR, Dawson TM, Dawson VL (1997) Neuronal (type I) nitric oxide synthase regulates nuclear factor κB activity and immunologic (type II) nitric oxide synthase expression. Proc Natl Acad Sci USA 94:2676-2680
43. Torihashi S, Horowitz B, Pollock JS, Ward SM, Xue C, Kobayashi S, Sanders KM (1996) Expression of nitric oxide synthase in mucosal cells of the canine colon. Histochem Cell Biol 105:33-41
44. Türler A, Kalff JC, Heeckt P, Abu-Elmagd KM, Schraut WH, Bond GJ, Moore BA, Brünagel G, Bauer AJ (2002) Molecular and functional observations on the donor intestinal muscularis during human small bowel transplantation. Gastroenterology 122:1886-1897
45. Woodruff TM, Thundyil J, Tang S-C, Sobey CG, Taylor SM, Arumugam TV (2011) Pathophysiology, treatment, and animal and cellular models of human ischemic stroke. Mol Neurodegener 6:1-19