Inhaled nitric oxide decreases infarction size and improves left ventricular function in a murine model of myocardial ischemia-reperfusion injury

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 291, Issue 1, 2006, Pages

  Hataishi, Ryuji ^a   Rodrigues, Ana Clara ^a   Neilan, Tomas G ^a   Morgan, John G ^a   Buys, Emmanuel ^a   Shiva, Sruti ^c   Tambouret, Rosemary ^b   Jassal, Davinder S ^a   Raher, Michael J ^a   Furutani, Elissa ^a   Ichinose, Fumito ^a   Gladwin, Mark T ^c   Rosenzweig, Anthony ^a   Zapol, Warren M ^a   Picard, Michael H ^a   Bloch, Kenneth D ^a   Scherrer Crosbie, Marielle ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Cardiac injury; Murine model; Myocardial infarction

Indexed keywords

CYCLIC GMP; NITRIC OXIDE; NITRITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; DIASTOLE; DRUG EFFECT; ECHOCARDIOGRAPHY; HEART INFARCTION SIZE; HEART INJURY; HEART LEFT VENTRICLE PERFORMANCE; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEMODYNAMIC PARAMETERS; HYPERTENSION; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; SYSTOLE;

ADMINISTRATION, INHALATION; ANIMALS; DISEASE MODELS, ANIMAL; MALE; MICE; MICE, INBRED C57BL; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE; SEVERITY OF ILLNESS INDEX; TREATMENT OUTCOME; VENTRICULAR DYSFUNCTION, LEFT;

EID: 33745698607     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01172.2005     Document Type: Article

References (49)

1. Adrie C, Bloch KD, Moreno PR, Hurford WE, Guerrero JL, Holt R, Zapol WM, Gold HK, and Semigran MJ. Inhaled nitric oxide increases coronary artery patency after thrombolysis. Circulation 94: 1919-1926, 1996.
2. Ambrosio G and Tritto I. Reperfusion injury: experimental evidence and clinical implications. Am Heart J 138: S69-S75, 1999.
3. Anonymous. GISSI-3: effects of lisinopril and transdermal glyceryl trinitrate singly and together on 6-week mortality and ventricular function after acute myocardial infarction. Gruppo Italiano per lo Studio della Sopravvivenza nell'infarto Miocardico. Lancet 343: 1115-1122, 1994.
4. Anonymous. ISIS-4: a randomised factorial trial assessing early oral captopril, oral mononitrate, and intravenous magnesium sulphate in 58,050 patients with suspected acute myocardial infarction. Fourth International Study of Infarct Survival Collaborative Group. Lancet 345: 669-685, 1995.
5. Chello M, Mastroroberto P, Marchese AR, Maltese G, Santangelo E, and Amantea B. Nitric oxide inhibits neutrophil adhesion during experimental extracorporeal circulation. Anesthesiology 89: 443-448, 1998.
6. Chollet-Martin S, Gatecel C, Kermarrec N, Gougerot-Pocidalo MA, and Payen DM. Alveolar neutrophil functions and cytokine levels in patients with the adult respiratory distress syndrome during nitric oxide inhalation. Am J Respir Crit Care Med 153: 985-990, 1996.
7. Clancy RM, Leszczynska-Piziak J, and Abramson SB. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest 90: 1116-1121, 1992.
8. Cope JT, Banks D, Laubach VE, Binns OA, King RC, Richardson RM, Shockey KS, Tribble CG, and Kron IL. Sodium nitroprusside exacerbates myocardial ischemia-reperfusion injury. Ann Thorac Surg 64: 1656-1659, 1997.
9. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO III, and Gladwin MT. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505, 2003.
10. Dejam A, Hunter CJ, Pelletier MM, Hsu LL, Machado RF, Shiva S, Power GG, Kelm M, Gladwin MT, and Schechter AN. Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood 106: 734-739, 2005.
11. 2 radicals during reperfusion after prolonged myocardial ischemia. Am J Physiol Heart Circ Physiol 280: H2649-H2657, 2001.
12. Duranski MR, Greer JJM, Dejam A, Sathya J, Hogg N, Langston W, Patel RP, Yet SF, Wang X, Kevil CG, Gladwin MT, and Lefer DJ. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. J Clin Invest 115: 1232-1240, 2005.
13. Fox-Robichaud A, Payne D, Hasan SU, Ostrovsky L, Fairhead T, Reinhardt P, and Kubes P. Inhaled NO as a viable antiadhesive therapy for ischemia/reperfusion injury of distal microvascular beds. J Clin Invest 101: 2497-2505, 1998.
14. Fujii H, Ichimori K, Hoshiai K, and Nakazawa H. Nitric oxide inactivates NADPH oxidase in pig neutrophils by inhibiting its assembling process. J Biol Chem 272: 32773-32778, 1997.
15. Gasic AC, McGuire G, Krater S, Farhood AI, Goldstein MA, Smith CW, Entman ML, and Taylor AA. Hydrogen peroxide pretreatment of perfused canine vessels induces ICAM-1- and CD18-dependent neutrophil adherence. Circulation 84: 2154-2166, 1991.
16. Gianetti J, Del Sarto P, Bevilacqua S, Vassalle C, De Filippis R, Kacila M, Farneti PA, Clerico A, Glauber M, and Biagini A. 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, 2004.
17. Groves PH, Lewis MJ, Cheadle HA, and Penny WJ. SIN-1 reduces platelet adhesion and platelet thrombus formation in a porcine model of balloon angioplasty. Circulation 87: 590-597, 1993.
18. Gryglewski RJ, Palmer RM, and Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320: 454-456, 1986.
19. Hogman M, Frostell C, Arnberg H, Sandhagen B, and Hedenstierna G. Prolonged bleeding time during nitric oxide inhalation in the rabbit. Acta Physiol Scand 151: 125-129, 1994.
20. Ichinose F, Roberts JD, and Zapol WM. Inhaled nitric oxide: a selective pulmonary vasodilator: current uses and therapeutic potential. Circulation 109: 3106-3111, 2004.
21. Johnson G III, Tsao PS, and Lefer AM. Cardioprotective effects of authentic nitric oxide in myocardial ischemia with reperfusion. Crit Care Res 19: 244-252, 1991.
22. Jugdutt BI and Khan MI. Effect of prolonged nitrate therapy on left ventricular remodeling after canine acute myocardial infarction. Circulation 89: 2297-2307, 1994.
23. Jugdutt BI and Warnica JW. Intravenous nitroglycerin therapy to limit myocardial infarct size, expansion, and complications. Effect of timing, dosage, and infarct location. Circulation 78: 906-919, 1988.
24. Kubes P, Suzuki M, and Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88: 4651-4655, 1991.
25. Lee JS, Adrie C, Jacob HJ, Roberts JD Jr, Zapol WM, and Bloch KD. Chronic inhalation of nitric oxide inhibits neointimal formation after balloon-induced arterial injury. Circ Res 78: 337-342, 1996.
26. Lefer AM, Siegfried MR, and Ma XL. Protection of ischemia-reperfusion injury by sydnonimine NO donors via inhibition of neutrophil-endothelium interaction. J Cardiovasc Pharmacol 22 Suppl 7: S27-S33, 1993.
27. Lefer DJ, Nakanishi K, Johnston WE, and Vinten-Johansen J. Antineutrophil and myocardial protecting actions of a novel nitric oxide donor after acute myocardial ischemia and reperfusion of dogs. Circulation 88: 2337-2350, 1993.
28. Lewis MS, Whatley RE, Cain P, McIntyre TM, Prescott SM, and Zimmerman GA. Hydrogen peroxide stimulates the synthesis of platelet-activating factor by endothelium and induces endothelial cell-dependent neutrophil adhesion. J Clin Invest 82: 2045-2055, 1988.
29. Ma XL, Lopez BL, Liu GL, Christopher TA, and Ischiropoulos H. Peroxynitrite aggravates myocardial reperfusion injury in the isolated perfused rat heart. Cardiovasc Res 36: 195-204, 1997.
30. Ma XL, Weyrich AS, Lefer DJ, Buerke M, Albertine KH, Kishimoto TK, and Lefer AM. Monoclonal antibody to L-selectin attenuates neutrophil accumulation and protects ischemic reperfused cat myocardium. Circulation 88: 649-658, 1993.
31. Mahmarian JJ, Moye LA, Chinoy DA, Sequeira RF, Habib GB, Henry WJ, Jain A, Chaitman BR, Weng CS, Morales-Ballejo H, and Pratt CM. Transdermal nitroglycerin patch therapy improves left ventricular function and prevents remodeling after acute myocardial infarction: results of a multicenter prospective randomized, double-blind, placebo-controlled trial. Circulation 97: 2017-2024, 1998.
32. Mori E, Haramaki N, Ikeda H, and Imaizumi T. Intra-coronary administration of L-arginine aggravates myocardial stunning through production of peroxynitrite in dogs. Cardiovasc Res 40: 113-123, 1998.
33. Muhs BE, Gagne P, Plitas G, Shaw JP, and Shamamian P. Experimental hindlimb ischemia leads to neutrophil-mediated increases in gastrocnemius MMP-2 and -9 activity: a potential mechanism for ischemia-induced MMP activation. J Surg Res 117: 249-254, 2004.
34. Neviere R, Guery B, Mordon S, Zerimech F, Charre S, Wattel F, and Chopin C. Inhaled NO reduces leukocyte-endothelial cell interactions and myocardial dysfunction in endotoxemic rats. Am J Physiol Heart Circ Physiol 278: H1783-H1790, 2000.
35. Ng ES, Jourd'heuil D, McCord JM, Hernandez D, Yasui M, Knight D, and Kubes P. Enhanced S-nitroso-albumin formation from inhaled NO during ischemia/reperfusion. Circ Res 94: 559-565, 2004.
36. Rezkalla SH and Kloner RA. No-reflow phenomenon. Circulation 105: 656-662, 2002.
37. Roberts JD Jr, Roberts CT, Jones RC, Zapol WM, and Bloch KD. Continuous nitric oxide inhalation reduces pulmonary arterial structural changes, right ventricular hypertrophy, and growth retardation in the hypoxic newborn rat. Circ Res 76: 215-222, 1995.
38. Rodrigues AC, Hataishi R, Ichinose F, Bloch KD, Derumeaux G, Picard MH, and Scherrer-Crosbie M. Relationship of systolic dysfunction to area at risk and infarction size after ischemia-reperfusion in mice. J Am Soc Echocardiogr 17: 948-953, 2004.
39. Sato Y, Walley KR, Klut ME, English D, D'Yachkova Y, Hogg JC, and van Eeden SF. Nitric oxide reduces the sequestration of polymorphonuclear leukocytes in lung by changing deformability and CD18 expression. Am J Respir Crit Care Med 159: 1469-1476, 1999.
40. Scherrer-Crosbie M, Ullrich R, Bloch KD, Nakajima H, Aretz HT, Lindsey ML, Vançon AC, Huang PL, Lee RT, Zapol WM, and Picard MH. Nitric oxide synthase 3 limits left ventricular remodeling after myocardial infarction in mice. Circulation 104: 1286-1291, 2001.
41. Schulz R, Kelm M, and Heusch G. Nitric oxide in myocardial ischemia/reperfusion injury. Cardiovasc Res 61: 402-413, 2004.
42. Semigran MJ, Cockrill BA, Kacmarek R, Thompson BT, Zapol WM, Dec GW, and Fifer MA. Hemodynamic effects of inhaled nitric oxide in heart failure. J Am Coll Cardiol 24: 982-988, 1994.
43. Sheridan FM, Cole PG, and Ramage D. Leukocyte adhesion to the coronary microvasculature during ischemia and reperfusion in an in vivo canine model. Circulation 93: 1784-1787, 1996.
44. Stamler JS, Jaraki O, Osborne J, Simon DI, Keaney J, Vita J, Singel D, Valeri CR, and Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 89: 7674-7677, 1992.
45. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, and Piantadosi CA. Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-2037, 1997.
46. Troncy E, Francoeur M, Salazkin I, Yang F, Charbonneau M, Leclerc G, Vinay P, and Blaise G. Extra-pulmonary effects of inhaled nitric oxide in swine with and without phenylephrine. Br J Anaesth 79: 631-640, 1997.
47. Ullrich R, Scherrer-Crosbie M, Bloch KD, Ichinose F, Nakajima H, Picard MH, Zapol WM, and Quezado ZMN. Congenital deficiency of nitric oxide synthase 2 protects against endotoxin-induced myocardial dysfunction in mice. Circulation 102: 1440-1446, 2000.
48. Wennmalm A, Benthin G, Edlund A, Jungersten L, Kieler-Jensen N, Lundin S, Westfelt UN, Petersson AS, and Waagstein F. Metabolism and excretion of nitric oxide in humans. An experimental and clinical study. Circ Res 73: 1121-1127, 1993.
49. Yang BK, Vivas EX, Reiter CD, and Gladwin MT. Methodologies for the sensitive and specific measurement of S-nitrosothiols, iron-nitrosyls, and nitrite in biological samples. Free Radic Res 37: 1-10, 2003.