Selective inhibition of iNOS attenuates trauma-hemorrhage/resuscitation- induced hepatic injury

Journal of Applied Physiology

Volumn 105, Issue 4, 2008, Pages 1076-1082

  Kan, Wen Hong ^a   Hsu, Jun Te ^a,b   Schwacha, Martin G ^a   Choudhry, Mashkoor A ^a   Raju, Raghavan ^a   Bland, Kirby I ^a   Chaudry, Irshad H ^a,c  

^a Kentucky   (United States)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

Chemokine; Cytokine; Hypoxia inducible factor 1 ; Myeloperoxidase activity

Indexed keywords

3 NITROTYROSINE; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT 1; GLUTATHIONE TRANSFERASE ALPHA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 2; MYELOPEROXIDASE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; N(G) NITROARGININE METHYL ESTER; NITRATE; NITRITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 3-NITROTYROSINE; AMIDINE; BENZYLAMINE DERIVATIVE; CHEMOKINE; CYTOKINE; DRUG DERIVATIVE; ENOS PROTEIN, RAT; ENZYME INHIBITOR; GLUTATHIONE S-TRANSFERASE ALPHA; GLUTATHIONE TRANSFERASE; HIF1A PROTEIN, RAT; ISOENZYME; N (3 (AMINOMETHYL)BENZYL)ACETAMIDINE; N-(3-(AMINOMETHYL)BENZYL)ACETAMIDINE; NOS2 PROTEIN, RAT; PEROXIDASE; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; FLUID RESUSCITATION; HEMORRHAGIC SHOCK; HYPOTENSION; LAPAROTOMY; LIVER DYSFUNCTION; LIVER INJURY; MALE; MEAN ARTERIAL PRESSURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; ANIMAL; BLOOD; BLOOD PRESSURE; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; FLUID THERAPY; INJURY; LIVER; LIVER DISEASE; METABOLISM; PATHOPHYSIOLOGY; RESUSCITATION; SPRAGUE DAWLEY RAT;

AMIDINES; ANIMALS; BENZYLAMINES; BLOOD PRESSURE; CHEMOKINES; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FLUID THERAPY; GLUTATHIONE TRANSFERASE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERCELLULAR ADHESION MOLECULE-1; ISOENZYMES; LIVER; LIVER DISEASES; MALE; NG-NITROARGININE METHYL ESTER; NITRATES; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PEROXIDASE; RATS; RATS, SPRAGUE-DAWLEY; RESUSCITATION; SHOCK, HEMORRHAGIC; TYROSINE; WOUNDS AND INJURIES;

EID: 55449133915     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.90495.2008     Document Type: Article

References (43)

1. Adams CA Jr, Hauser CJ, Adams JM, Fekete Z, Xu DZ, Sambol JT, Deitch EA. Trauma-hemorrhage-induced neutrophil priming is prevented by mesenteric lymph duct ligation. Shock 18: 513-517, 2002.
2. Agani FH, Puchowicz M, Chavez JC, Pichiule P, LaManna J. Role of nitric oxide in the regulation of HIF-1α expression during hypoxia. Am J Physiol Cell Physiol 283: C178-C186, 2002.
3. Allen JW, Khetani SR, Johnson RS, Bhatia SN. In vitro liver tissue model established from transgenic mice: role of HIF-1alpha on hypoxic gene expression. Tissue Eng 12: 3135-3147, 2006.
4. Angele MK, Fitzal F, Smail N, Knoferl MW, Schwacha MG, Ayala A, Wang P, Chaudry IH. L-Arginine attenuates trauma-hemorrhage-induced liver injury. Crit Care Med 28: 3242-3248, 2000.
5. Banta S, Yokoyama T, Berthiaume F, Yarmush ML. Effects of dehydroepiandrosterone administration on rat hepatic metabolism following thermal injury. J Surg Res 127: 93-105, 2005.
6. Chen T, Zamora R, Zuckerbraun B, Billiar TR. Role of nitric oxide in liver injury. Curr Mol Med 3: 519-526, 2003.
7. Choudhry MA, Schwacha MG, Hubbard WJ, Kerby JD, Rue LW, Bland KI, Chaudry IH. Gender differences in acute response to trauma-hemorrhage. Shock 24, Suppl 1: 101-106, 2005.
8. Christopherson KS, Bredt DS. Nitric oxide in excitable tissues: physiological roles and disease. J Clin Invest 100: 2424-2429, 1997.
9. Cottart CH, Do L, Blanc MC, Vaubourdolle M, Descamps G, Durand D, Galen FX, Clot JP. Hepatoprotective effect of endogenous nitric oxide during ischemia-reperfusion in the rat. Hepatology 29: 809-813, 1999.
10. Duranski MR, Elrod JW, Calvert JW, Bryan NS, Feelisch M, Lefer DJ. Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 291: H2980-H2986, 2006.
11. Fan J, Li Y, Levy RM, Fan JJ, Hackam DJ, Vodovotz Y, Yang H, Tracey KJ, Billiar TR, Wilson MA. Hemorrhagic shock induces NAD(P)H oxidase activation in neutrophils: role of HMGB1-TLR4 signaling. J Immunol 178: 6573-6580, 2007.
12. Frankel DA, Acosta JA, Anjaria DJ, Porcides RD, Wolf PL, Coimbra R, Hoyt DB. Physiologic response to hemorrhagic shock depends on rate and means of hemorrhage. J Surg Res 143: 276-280, 2007.
13. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, Knowles RG. 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, 1997.
14. He T, Ai M, Zhao XH, Xing YQ. Inducible nitric oxide synthase mediates hypoxia-induced hypoxia-inducible factor-1 alpha activation and vascular endothelial growth factor expression in oxygen-induced retinopathy. Pathobiology 74: 336-343, 2007.
15. Hellwig-Burgel T, Stiehl DP, Wagner AE, Metzen E, Jelkmann W. Review: hypoxia-inducible factor-1 (HIF-1): a novel transcription factor in immune reactions. J Interferon Cytokine Res 25: 297-310, 2005.
16. Hierholzer C, Billiar TR. Molecular mechanisms in the early phase of hemorrhagic shock. Langenbecks Arch Surg 386: 302-308, 2001.
17. Hines IN, Kawachi S, Harada H, Pavlick KP, Hoffman JM, Bharwani S, Wolf RE, Grisham MB. Role of nitric oxide in liver ischemia and reperfusion injury. Mol Cell Biochem 234-235: 229-237, 2002.
18. Hsu JT, Kan WH, Hsieh CH, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH. Mechanism of estrogen-mediated attenuation of hepatic injury following trauma-hemorrhage: Akt-dependent HO-1 up-regulation. J Leukoc Biol 82: 1019-1026, 2007.
19. Ito Y, Abril ER, Bethea NW, 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.
20. Kan W, Zhao KS, Jiang Y, Yan W, Huang Q, Wang J, Qin Q, Huang X, Wang S. Lung, spleen, and kidney are the major places for inducible nitric oxide synthase expression in endotoxic shock: role of p38 mitogen activated protein kinase in signal transduction of inducible nitric oxide synthase expression. Shock 21: 281-287, 2004.
21. Kiang JG, Peckham RM, Duke LE, Shimizu T, Chaudry IH, Tsokos GC. Androstenediol inhibits the trauma-hemorrhage-induced increase in caspase-3 by downregulating the inducible nitric oxide synthase pathway. J Appl Physiol 102: 933-941, 2007.
22. Kobata A, Kotani T, Komatsu Y, Amagase K, Kato S, Takeuchi K. Dual action of nitric oxide in the pathogenesis of ischemia/reperfusion-induced mucosal injury in mouse stomach. Digestion 75: 188-197, 2007.
23. Lefer DJ, Scalia R, Campbell B, Nossuli T, Hayward R, Salamon M, Grayson J, Lefer AM. Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischemia-reperfusion injury in rats. J Clin Invest 99: 684-691, 1997.
24. Liu TH, Robinson EK, Helmer KS, West SD, Castaneda AA, Chang L, Mercer DW. Does upregulation of inducible nitric oxide synthase play a role in hepatic injury? Shock 18: 549-554, 2002.
25. Lopez A, Lorente JA, Steingrub J, Bakker J, McLuckie A, Willatts S, Brockway M, Anzueto A, Holzapfel L, Breen D, Silverman MS, Takala J, Donaldson J, Arneson C, Grove G, Grossman S, Grover R. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit Care Med 32: 21-30, 2004.
26. Mateo J, Garcia-Lecea M, Cadenas S, Hernandez C, Moncada S. Regulation of hypoxia-inducible factor-1alpha by nitric oxide through mitochondria-dependent and -independent pathways. Biochem J 376: 537-544, 2003.
27. McKim SE, Gabele E, Isayama F, Lambert JC, Tucker LM, Wheeler MD, Connor HD, Mason RP, Doll MA, Hein DW, Arteel GE. Inducible nitric oxide synthase is required in alcohol-induced liver injury: studies with knockout mice. Gastroenterology 125: 1834-1844, 2003.
28. Menezes JM, Hierholzer C, Watkins SC, Billiar TR, Peitzman AB, Harbrecht BG. The modulation of hepatic injury and heat shock expression by inhibition of inducible nitric oxide synthase after hemorrhagic shock. Shock 17: 13-18, 2002.
29. Natarajan R, Jones DG, Fisher BJ, Wallace TJ, Ghosh S, Fowler AA, III. Hypoxia inducible factor-1: regulation by nitric oxide in posthypoxic microvascular endothelium. Biochem Cell Biol 83: 597-607, 2005.
30. Nowicki MJ, Shi D, Cai Z, Bishop PR, May WL. Developmental expression of endothelial nitric oxide synthase (eNOS) in the rat liver. Pediatr Res 54: 732-738, 2003.
31. Ozturk H, Aldemir M, Dokucu AI, Yagmur Y, Kilinc N, Sahin AH. The nitric oxide donor molsidomine prevents ischemia/reperfusion injury of the adult rat small intestine. Pediatr Surg Int 19: 305-308, 2003.
32. Petersson J, Schreiber O, Steege A, Patzak A, Hellsten A, Phillipson M, Holm L. eNOS involved in colitis-induced mucosal blood flow increase. Am J Physiol Gastrointest Liver Physiol 293: G1281-G1287, 2007.
33. Shimizu T, Tani T, Endo Y, Hanasawa K, Tsuchiya M, Kodama M. Elevation of plasma peptidoglycan and peripheral blood neutrophil activation during hemorrhagic shock: plasma peptidoglycan reflects bacterial translocation and may affect neutrophil activation. Crit Care Med 30: 77-82, 2002.
34. Shiratori Y, Ohmura K, Hikiba Y, Matsumura M, Nagura T, Okano K, Kamii K, Omata M. Hepatocyte nitric oxide production is induced by Kupffer cells. Dig Dis Sci 43: 1737-1745, 1998.
35. Szalay L, Shimizu T, Suzuki T, Yu HP, Choudhry MA, Schwacha MG, Rue LW III, Bland KI, Chaudry IH. Estradiol improves cardiac and hepatic function after trauma-hemorrhage: role of enhanced heat shock protein expression. Am J Physiol Regul Integr Comp Physiol 290: R812-R818, 2006.
36. Takamatsu Y, Shimada K, Yamaguchi K, Kuroki S, Chijiiwa K, Tanaka M. Inhibition of inducible nitric oxide synthase prevents hepatic, but not pulmonary, injury following ischemia-reperfusion of rat liver. Dig Dis Sci 51: 571-579, 2006.
37. Taylor BS, Alarcon LH, Billiar TR. Inducible nitric oxide synthase in the liver: regulation and function. Biochemistry (Mosc) 63: 766-781, 1998.
38. Tsung A, Sahai R, Tanaka H, Nakao A, Fink MP, Lotze MT, Yang H, Li J, Tracey KJ, Geller DA, Billiar TR. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J Exp Med 201: 1135-1143, 2005.
39. Wahl SM, Cartney-Francis N, Chan J, Dionne R, Ta L, Orenstein JM. Nitric oxide in experimental joint inflammation. Benefit or detriment? Cells Tissues Organs 174: 26-33, 2003.
40. Wang FS, Kuo YR, Wang CJ, Yang KD, Chang PR, Huang YT, Huang HC, Sun YC, Yang YJ, Chen YJ. Nitric oxide mediates ultrasound-induced hypoxia-inducible factor-1alpha activation and vascular endothelial growth factor-A expression in human osteoblasts. Bone 35: 114-123, 2004.
41. Wray GM, Millar CG, Hinds CJ, Thiemermann C. Selective inhibition of the activity of inducible nitric oxide synthase prevents the circulatory failure, but not the organ injury/dysfunction, caused by endotoxin. Shock 9: 329-335, 1998.
42. Yin JH, Yang DI, Ku G, Hsu CY. iNOS expression inhibits hypoxia-inducible factor-1 activity. Biochem Biophys Res Commun 279: 30-34, 2000.
43. Zhang L, Looney CG, Qi WN, Chen LE, Seaber AV, Stamler JS, Urbaniak JR. Reperfusion injury is reduced in skeletal muscle by inhibition of inducible nitric oxide synthase. J Appl Physiol 94: 1473-1478, 2003.