Inhaled NO accelerates restoration of liver function in adults following orthotopic liver transplantation

Journal of Clinical Investigation

Volumn 117, Issue 9, 2007, Pages 2583-2591

  Lang Jr , John D ^a,h   Teng, Xinjun ^b   Chumley, Phillip ^c   Crawford, Jack H ^b,c   Isbell, T Scott ^b   Chacko, Balu K ^b   Liu, Yuliang ^a   Jhala, Nirag ^b   Crowe, D Ralph ^b   Smith, Alvin B ^c   Cross, Richard C ^c   Frenette, Luc ^c   Kelley, Eric E ^d   Wilhite, Diana W ^c   Hall, Cheryl R ^c   Page, Grier P ^e   Fallon, Michael B ^f   Bynon, J Steven ^g   Eckhoff, Devin E ^g   Patel, Rakesh P ^b,e  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f University of Alabama at Birmingham   (United States)

^g Kentucky   (United States)

^h UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITROGEN OXIDE; PLACEBO;

ADULT; AGED; APOPTOSIS; ARTICLE; BLOOD CLOTTING TIME; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; FEMALE; HOSPITALIZATION; HUMAN; HUMAN TISSUE; LIVER FUNCTION; LIVER ISCHEMIA; LIVER TRANSPLANTATION; MALE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTHROMBIN TIME; REPERFUSION INJURY;

ADMINISTRATION, INHALATION; ADULT; AGED; CELL DEATH; FEMALE; HUMANS; LENGTH OF STAY; LIVER; LIVER TRANSPLANTATION; MALE; MIDDLE AGED; NITRIC OXIDE; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 34848888949     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI31892     Document Type: Article

References (41)

1. Urakami, H., and Grisham, M.B. 2006. Divergent roles of superoxide and nitric oxide in reduced-size liver ischemia and reperfusion injury: implications for partial liver transplantation. Pathophysiology. 13:183-193.
2. Jaeschke, H., Smith, C.V., and Mitchell, J.R. 1988. Reactive oxygen species during ischemia-reflow injury in isolated perfused rat liver. J. Clin. Invest. 81:1240-1246.
3. Fondevila, C., Busuttil, R.W., and Kupiec-Weglinski, J.W. 2003. Hepatic ischemia/reperfusion injury - a fresh look. Exp. Mol. Pathol. 74:86-93.
4. Fellstrom, B., et al. 1998. Postischemic reperfusion injury and allograft arteriosclerosis. Transplant Proc. 30:4278-4280.
5. Kupiec-Weglinski, J.W., and Busuttil, R.W. 2005. Ischemia and reperfusion injury in liver transplantation. Transplant Proc. 37:1653-1656.
6. Jaeschke, H., and Hasegawa, T. 2006. Role of neutrophils in acute inflammatory liver injury. Liver Int. 26:912-919.
7. Varadarajan, R., et al. 2004. Nitric oxide in early ischaemia reperfusion injury during human orthotopic liver transplantation. Transplantation. 78:250-256.
8. Duranski, M.R., et al. 2006. Genetic overexpression of eNOS attenuates hepatic ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 291:H2980-H2986.
9. Li, J., and Billiar, T.R. 1999. Nitric oxide. IV. Determinants of nitric oxide protection and toxicity in liver. Am. J. Physiol. 276:G1069-G1073.
10. Griffiths, M.J., and Evans, T.W. 2005. Inhaled nitric oxide therapy in adults. N. Engl. J. Med. 353:2683-2695.
11. Fox-Robichaud, A., et al. 1998. Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J. Clin. Invest. 101:2497-2505.
12. Hataishi, R., et al. 2006. Inhaled nitric oxide decreases infarction size and improves left ventricular function in a murine model of myocardial ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 291:H379-H384.
13. Gianetti, J., et al. 2004. Supplemental nitric oxide and its effect on myocardial injury and function in patients undergoing cardiac surgery with extracorporeal circulation. J. Thorac. Cardiovasc. Surg. 127:44-50.
14. Cannon, R.O., 3rd, et al. 2001. Effects of inhaled nitric oxide on regional blood flow are consistent with intravascular nitric oxide delivery. J. Clin. Invest. 108:279-287. doi:10.1172/JCI200112761.
15. Mathru, M., Huda, R., Solanki, D.R., Hays, S., and Lang, J.D. 2007. Inhaled nitric oxide attenuates reperfusion inflammatory responses in humans. Anesthesiology. 106:275-282.
16. Ng, E.S., et al. 2004. Enhanced S-nitroso-albumin formation from inhaled NO during ischemia/reperfusion. Circ. Res. 94:559-565.
17. Duranski, M.R., et al. 2005. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J. Clin. Invest. 115:1232-1240. doi:10.1172/JCI200522493.
18. Gladwin, M.T., et al. 2006. Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation. Am. J. Physiol. Heart Circ. Physiol. 291:H2026- H2035.
19. Gladwin, M.T., et al. 2005. The emerging biology of the nitrite anion. Nat. Chem. Biol. 1:308-314.
20. Bryan, N.S., et al. 2004. Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo. Proc. Natl. Acad. Sci. U. S. A. 101:4308-4313.
21. McMahon, T.J., and Doctor, A. 2006. Extrapulmonary effects of inhaled nitric oxide: role of reversible S-nitrosylation of erythrocytic hemoglobin. Proc. Am. Thorac. Soc. 3:153-160.
22. Zweier, J.L., and Talukder, M.A. 2006. The role of oxidants and free radicals in reperfusion injury. Cardiovasc. Res. 70:181-190.
23. Jaeschke, H., et al. 1998. Activation of caspase 3 (CPP32)-like proteases is essential for TNF-alpha-induced hepatic parenchymal cell apoptosis and neutrophil-mediated necrosis in a murine endotoxin shock model. J. Immunol. 160:3480-3486.
24. Kawachi, S., et al. 2000. Nitric oxide synthase and postischemic liver injury. Biochem. Biophys. Res. Commun. 276:851-854.
25. Kevil, C.G., et al. 2004. Intercellular adhesion molecule-1 (ICAM-1) regulates endothelial cell motility through a nitric oxide-dependent pathway. J. Biol. Chem. 279:19230-19238.
26. Hussain, M.B., Hobbs, A.J., and MacAllister, R.J. 1999. Autoregulation of nitric oxide-soluble guanylate cyclase-cyclic GMP signalling in mouse thoracic aorta. Br. J. Pharmacol. 128:1082-1088.
27. Gladwin, M.T., Crawford, J.H., and Patel, R.P. 2004. The biochemistry of nitric oxide, nitrite, and hemoglobin: role in blood flow regulation. Free Radic. Biol. Med. 36:707-717.
28. Lundberg, J.O., Weitzberg, E., Cole, J.A., and Benjamin, N. 2004. Nitrate, bacteria and human health. Nat. Rev. Microbiol. 2:593-602.
29. Li, H., Samouilov, A., Liu, X., and Zweier, J.L. 2003. Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrate reduction: evaluation of its role in nitrite and nitric oxide generation in anoxic tissues. Biochemistry. 42:1150-1159.
30. Azizi, F., et al. 2005. Rates of nitric oxide dissociation from hemoglobin. Free Radic. Biol. Med. 39:145-151.
31. Crawford, J.H., et al. 2004. Transduction of NO-bioactivity by the red blood cell in sepsis: novel mechanisms of vasodilation during acute inflammatory disease. Blood. 104:1375-1382.
32. McMahon, T.J., et al. 2002. Nitric oxide in the human respiratory cycle. Nat. Med. 8:711-717.
33. Hunter, C.J., et al. 2004. Inhaled nebulized nitrite is a hypoxia-sensitive NO-dependent selective pulmonary vasodilator. Nat. Med. 10:1122-1127.
34. Pluta, R.M., Dejam, A., Grimes, G., Gladwin, M.T., and Oldfield, E.H. 2005. Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. JAMA. 293:1477-1484.
35. Webb, A., et al. 2004. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proc. Natl. Acad. Sci. U. S. A. 101:13683-13688.
36. Li, H., Samouilov, A., Liu, X., and Zweier, J.L. 2001. Characterization of the magnitude and kinetics of xanthine oxidase-catalyzed nitrite reduction. Evaluation of its role in nitric oxide generation in anoxic tissues. J. Biol. Chem. 276:24482-24489.
37. Zweier, J.L., Wang, P., Samouilov, A., and Kuppusamy, P. 1995. Enzyme-independent formation of nitric oxide in biological tissues. Nat. Med. 1:804-809.
38. Shiva, S., et al. 2006. Ceruloplasmin is a NO oxidase and nitrite synthase that determines endocrine NO homeostasis. Nat. Chem. Biol. 2:486-493.
39. Schopfer, F.J., et al. 2005. Fatty acid transduction of nitric oxide signaling. Nitrolinoleic acid is a hydrophobically stabilized nitric oxide donor. J. Biol. Chem. 280:19289-19297.
40. Bryan, N.S., et al. 2005. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat. Chem. Biol. 1:290-297.
41. Wang, X., et al. 2006. Measurement of nitric oxide levels in the red cell: validation of tri-iodide-based chemiluminescence with acid-sulfanilamide pretreatment. J. Biol. Chem. 281:26994-27002.