Carbon monoxide increases inducible nos expression that mediates co-induced myocardial damage during ischemia-reperfusion

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 7, 2015, Pages 759-767

  Meyer, Grégory ^a   André, Lucas ^b   Kleindienst, Adrien ^a   Singh, François ^c   Tanguy, Stéphane ^a,d   Richard, Sylvain ^b   Obert, Philippe ^a   Boucher, François ^d   Jover, Bernard ^b   Cazorla, Olivier ^b   Reboul, Cyril ^a  

^a UNIVERSITY OF AVIGNON   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIV GRENOBLE ALPES   (France)

Author keywords

Carbon monoxide; Myocardial infarction; Nitric oxide; Nitric oxide synthase

Indexed keywords

CALCIUM ION; CARBON MONOXIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; REACTIVE OXYGEN METABOLITE; S METHYLISOTHIOUREA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AIR POLLUTANT; ANTIOXIDANT; ENZYME INHIBITOR; NITRIC OXIDE; NOS2 PROTEIN, RAT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; EXCITATION CONTRACTION COUPLING; HEART MUSCLE INJURY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MYOFILAMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; WESTERN BLOTTING; ADVERSE EFFECTS; AIR POLLUTANT; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; EXPOSURE; HEART CONTRACTION; HEART MUSCLE; HEART MUSCLE CELL; METABOLISM; MUSCLE FIBRIL; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PATHOLOGY; PATHOPHYSIOLOGY; TIME; TOXICITY; UPREGULATION; WISTAR RAT;

AIR POLLUTANTS; ANIMALS; ANTIOXIDANTS; CARBON MONOXIDE; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; EXCITATION CONTRACTION COUPLING; INHALATION EXPOSURE; MALE; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOCYTES, CARDIAC; MYOFIBRILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; TIME FACTORS; UP-REGULATION;

EID: 84926383824     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00702.2014     Document Type: Article

References (59)

1. Aberg AM, Abrahamsson P, Johansson G, Haney M, Winso O, Larsson JE. Does carbon monoxide treatment alter cytokine levels after endotoxin infusion in pigs? A randomized controlled study. J Inflamm (Lond) 5: 13, 2008.
2. André L, Boissiere J, Reboul C, Perrier R, Zalvidea S, Meyer G, Thireau J, Tanguy S, Bideaux P, Hayot M, Boucher F, Obert P, Cazorla O, Richard S. Carbon monoxide pollution promotes cardiac remodeling and ventricular arrhythmia in healthy rats. Am J Respir Crit Care Med 181: 587-595, 2010.
3. Andre L, Gouzi F, Thireau J, Meyer G, Boissiere J, Delage M, Abdellaoui A, Feillet-Coudray C, Fouret G, Cristol JP, Lacampagne A, Obert P, Reboul C, Fauconnier J, Hayot M, Richard S, Cazorla O. Carbon monoxide exposure enhances arrhythmia after cardiac stress: involvement of oxidative stress. Basic Res Cardiol 106: 1235-1246, 2011.
4. Bak I, Szendrei L, Turoczi T, Papp G, Joo F, Das DK, de Leiris J, Der P, Juhasz B, Varga E, Bacskay I, Balla J, Kovacs P, Tosaki A. Heme oxygenase-1-related carbon monoxide production and ventricular fibrillation in isolated ischemic/reperfused mouse myocardium. FASEB J 17: 2133-2135, 2003.
5. Bak I, Varadi J, Nagy N, Vecsernyes M, Tosaki A. The role of exogenous carbon monoxide in the recovery of post-ischemic cardiac function in buffer perfused isolated rat hearts. Cell Mol Biol (Noisy-legrand) 51: 453-459, 2005.
6. Barua A, Standen NB, Galinanes M. Dual role of nNOS in ischemic injury and preconditioning. BMC Physiol 10: 15, 2010.
7. Bell ML, Peng RD, Dominici F, Samet JM. Emergency hospital admissions for cardiovascular diseases and ambient levels of carbon monoxide: results for 126 United States urban counties, 1999-2005. Circulation 120: 949-955, 2009.
8. Bolli R, Dawn B, Xuan YT. Role of the JAK-STAT pathway in protection agaInstitutemyocardial ischemia/reperfusion injury. Trends Cardiovasc Med 13: 72-79, 2003.
9. Bredt DS. Endogenous nitric oxide synthesis: biological functions and pathophysiology. Free Radic Res 31: 577-596, 1999.
10. Bye A, Sorhaug S, Ceci M, Hoydal MA, Stolen T, Heinrich G, Tjonna AE, Najjar SM, Nilsen OG, Catalucci D, Grimaldi S, Contu R, Steinshamn S, Condorelli G, Smith GL, Ellingsen O, Waldum H, Wisloff U. Carbon monoxide levels experienced by heavy smokers impair aerobic capacity and cardiac contractility and induce pathological hypertrophy. Inhal Toxicol 20: 635-646, 2008.
11. Carrozza JP Jr, Bentivegna LA, Williams CP, Kuntz RE, Grossman W, Morgan JP. Decreased myofilament responsiveness in myocardial stunning follows transient calcium overload during ischemia and reperfusion. Circ Res 71: 1334-1340, 1992.
12. Cho HJ, Xie QW, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Nathan C. Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med 176: 599-604, 1992.
13. Cuong DV, Kim N, Youm JB, Joo H, Warda M, Lee JW, Park WS, Kim T, Kang S, Kim H, Han J. Nitric oxide-cGMP-protein kinase G signaling pathway induces anoxic preconditioning through activation of ATP-sensitive K+channels in rat hearts. Am J Physiol Heart Circ Physiol 290: H1808-H1817, 2006.
14. Das A, Salloum FN, Xi L, Rao YJ, Kukreja RC. ERK phosphorylation mediates sildenafil-induced myocardial protection agaInstituteischemia-reperfusion injury in mice. Am J Physiol Heart Circ Physiol 296: H1236-H1243, 2009.
15. Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens 18: 655-673, 2000.
16. Farah C, Kleindienst A, Bolea G, Meyer G, Gayrard S, Geny B, Obert P, Cazorla O, Tanguy S, Reboul C. Exercise-induced cardioprotection: a role for eNOS uncoupling and NO metabolites. Basic Res Cardiol 108: 389, 2013.
17. Farah C, Meyer G, Andre L, Boissiere J, Gayrard S, Cazorla O, Richard S, Boucher F, Tanguy S, Obert P, Reboul C. Moderate exercise prevents impaired Ca2+handling in heart of CO-exposed rat: implication for sensitivity to ischemia-reperfusion. Am J Physiol Heart Circ Physiol 299: H2076-H2081, 2010.
18. Forstermann U, Boissel JP, Kleinert H. Expressional control of the ‘constitutive’ isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J 12: 773-790, 1998.
19. Garvey EP, Oplinger JA, Tanoury GJ, Sherman PA, Fowler M, Marshall S, Harmon MF, Paith JE, Furfine ES. Potent and selective inhibition of human nitric oxide synthases. Inhibition by non-amino acid isothioureas. J Biol Chem 269: 26669-26676, 1994.
20. Guo Y, Stein AB, Wu WJ, Zhu X, Tan W, Li Q, Bolli R. Late preconditioning induced by NO donors, adenosine A1 receptor agonists, and δ1-opioid receptor agonists is mediated by iNOS. Am J Physiol Heart Circ Physiol 289: H2251-H2257, 2005.
21. Han W, Fu S, Wei N, Xie B, Li W, Yang S, Li Y, Liang Z, Huo H. Nitric oxide overproduction derived from inducible nitric oxide synthase increases cardiomyocyte apoptosis in human atrial fibrillation. Int J Cardiol 130: 165-173, 2008.
22. Hu A, Jiao X, Gao E, Koch WJ, Sharifi-Azad S, Grunwald Z, Ma XL, Sun JZ. Chronic beta-adrenergic receptor stimulation induces cardiac apoptosis and aggravates myocardial ischemia/reperfusion injury by provoking inducible nitric-oxide synthase-mediated nitrative stress. J Pharmacol Exp Ther 318: 469-475, 2006.
23. Hu Z, Chen J, Wei Q, Xia Y. Bidirectional actions of hydrogen peroxide on endothelial nitric-oxide synthase phosphorylation and function: cocommitment and interplay of Akt and AMPK. J Biol Chem 283: 25256-25263, 2008.
24. Khan M, Mohan IK, Kutala VK, Kotha SR, Parinandi NL, Hamlin RL, Kuppusamy P. Sulfaphenazole protects heart agaInstituteischemiareperfusion injury and cardiac dysfunction by overexpression of iNOS, leading to enhancement of nitric oxide bioavailability and tissue oxygenation. Antioxid Redox Signal 11: 725-738, 2009.
25. Kusuoka H, Porterfield JK, Weisman HF, Weisfeldt ML, Marban E. Pathophysiology and pathogenesis of stunned myocardium. Depressed Ca2+activation of contraction as a consequence of reperfusion-induced cellular calcium overload in ferret hearts. J Clin Invest 79: 950-961, 1987.
26. Layland J, Li JM, Shah AM. Role of cyclic GMP-dependent protein kinase in the contractile response to exogenous nitric oxide in rat cardiac myocytes. J Physiol 540: 457-467, 2002.
27. Li D, Qu Y, Tao L, Liu H, Hu A, Gao F, Sharifi-Azad S, Grunwald Z, Ma XL, Sun JZ. Inhibition of iNOS protects the aging heart agaInstitutebeta-adrenergic receptor stimulation-induced cardiac dysfunction and myocardial ischemic injury. J Surg Res 131: 64-72, 2006.
28. Lokuta AJ, Maertz NA, Meethal SV, Potter KT, Kamp TJ, Valdivia HH, Haworth RA. Increased nitration of sarcoplasmic reticulum Ca2+-ATPase in human heart failure. Circulation 111: 988-995, 2005.
29. Massion PB, Balligand JL. Modulation of cardiac contraction, relaxation and rate by the endothelial nitric oxide synthase (eNOS): lessons from genetically modified mice. J Physiol 546: 63-75, 2003.
30. Meyer G, Andre L, Tanguy S, Boissiere J, Farah C, Lopez-Lauri F, Gayrard S, Richard S, Boucher F, Cazorla O, Obert P, Reboul C. Simulated urban carbon monoxide air pollution exacerbates rat heart ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 298: H1445-H1453, 2010.
31. Mou YA, Reboul C, Andre L, Lacampagne A, Cazorla O. Late exercise training improves non-uniformity of transmural myocardial function in rats with ischaemic heart failure. Cardiovasc Res 81: 555-564, 2009.
32. Mukhopadhyay P, Rajesh M, Batkai S, Kashiwaya Y, Hasko G, Liaudet L, Szabo C, Pacher P. Role of superoxide, nitric oxide, and peroxynitrite in doxorubicin-induced cell death in vivo and in vitro. Am J Physiol Heart Circ Physiol 296: H1466-H1483, 2009.
33. Mungrue IN, Gros R, You X, Pirani A, Azad A, Csont T, Schulz R, Butany J, Stewart DJ, Husain M. Cardiomyocyte overexpression of iNOS in mice results in peroxynitrite generation, heart block, and sudden death. J Clin Invest 109: 735-743, 2002.
34. Mungrue IN, Stewart DJ, Husain M. The Janus faces of iNOS. Circ Res 93: e74, 2003.
35. Niu X, Watts VL, Cingolani OH, Sivakumaran V, Leyton-Mange JS, Ellis CL, Miller KL, Vandegaer K, Bedja D, Gabrielson KL, Paolocci N, Kass DA, Barouch LA. Cardioprotective effect of beta-3 adrenergic receptor agonism: role of neuronal nitric oxide synthase. J Am Coll Cardiol 59: 1979-1987, 2012.
36. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424, 2007.
37. Petroff MG, Kim SH, Pepe S, Dessy C, Marban E, Balligand JL, Sollott SJ. Endogenous nitric oxide mechanisms mediate the stretch dependence of Ca2+release in cardiomyocytes. Nat Cell Biol 3: 867-873, 2001.
38. Rastaldo R, Pagliaro P, Cappello S, Penna C, Mancardi D, Westerhof N, Losano G. Nitric oxide and cardiac function. Life Sci 81: 779-793, 2007.
39. Razavi HM, Hamilton JA, Feng Q. Modulation of apoptosis by nitric oxide: implications in myocardial ischemia and heart failure. Pharmacol Ther 106: 147-162, 2005.
40. Saini-Chohan HK, Dhalla NS. Attenuation of ischemia-reperfusioninduced alterations in intracellular Ca2+in cardiomyocytes from hearts treated with N-acetylcysteine and N-mercaptopropionylglycine. Can J Physiol Pharmacol 87: 1110-1119, 2009.
41. Seddon M, Shah AM, Casadei B. Cardiomyocytes as effectors of nitric oxide signalling. Cardiovasc Res 75: 315-326, 2007.
42. Spurgeon HA, duBell WH, Stern MD, Sollott SJ, Ziman BD, Silverman HS, Capogrossi MC, Talo A, Lakatta EG. Cytosolic calcium and myofilaments in single rat cardiac myocytes achieve a dynamic equilibrium during twitch relaxation. J Physiol 447: 83-102, 1992.
43. Stoyanovsky D, Murphy T, Anno PR, Kim YM, Salama G. Nitric oxide activates skeletal and cardiac ryanodine receptors. Cell Calcium 21: 19-29, 1997.
44. Talukder MA, Zweier JL, Periasamy M. Targeting calcium transport in ischaemic heart disease. Cardiovasc Res 84: 345-352, 2009.
45. Thom SR, Ischiropoulos H. Mechanism of oxidative stress from low levels of carbon monoxide. Res Rep Health Eff Institute1-19; discussion 21-17, 1997.
46. Umar S, van der Laarse A. Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart. Mol Cell Biochem 333: 191-201, 2010.
47. Umar S, van der Laarse A. Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart. Mol Cell Biochem 333: 191-201, 2010.
48. Varadi J, Lekli I, Juhasz B, Bacskay I, Szabo G, Gesztelyi R, Szendrei L, Varga E, Bak I, Foresti R, Motterlini R, Tosaki A. Beneficial effects of carbon monoxide-releasing molecules on post-ischemic myocardial recovery. Life Sci 80: 1619-1626, 2007.
49. Walker LM, Walker PD, Imam SZ, Ali SF, Mayeux PR. Evidence for peroxynitrite formation in renal ischemia-reperfusion injury: studies with the inducible nitric oxide synthase inhibitor L-N(6)-(1-Iminoethyl)lysine. J Pharmacol Exp Ther 295: 417-422, 2000.
50. Wang XL, Liu HR, Tao L, Liang F, Yan L, Zhao RR, Lopez BL, Christopher TA, Ma XL. Role of iNOS-derived reactive nitrogen species and resultant nitrative stress in leukocytes-induced cardiomyocyte apoptosis after myocardial ischemia/reperfusion. Apoptosis 12: 1209-1217, 2007.
51. Weidinger A, Mullebner A, Paier-Pourani J, Banerjee A, Miller I, Lautherbock L, Duvigneau JC, Skulachev VP, Redl H, Kozlov A. Vicious iNOS-mitochondrial ROS cycle accelerates inflammatory response and causes liver injury in rats. Antioxid Redox Signal. 2014 Nov 3. [Epub ahead of print].
52. West MB, Rokosh G, Obal D, Velayutham M, Xuan YT, Hill BG, Keith RJ, Schrader J, Guo Y, Conklin DJ, Prabhu SD, Zweier JL, Bolli R, Bhatnagar A. Cardiac myocyte-specific expression of inducible nitric oxide synthase protects agaInstituteischemia/reperfusion injury by preventing mitochondrial permeability transition. Circulation 118: 1970-1978, 2008.
53. Wildhirt SM, Suzuki H, Horstman D, Weismuller S, Dudek RR, Akiyama K, Reichart B. Selective modulation of inducible nitric oxide synthase isozyme in myocardial infarction. Circulation 96: 1616-1623, 1997.
54. Xia Y. Superoxide generation from nitric oxide synthases. Antioxid Redox Signal 9: 1773-1778, 2007.
55. Xu L, Eu JP, Meissner G, Stamler JS. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279: 234-237, 1998.
56. Xu S, Ying J, Jiang B, Guo W, Adachi T, Sharov V, Lazar H, Menzoian J, Knyushko TV, Bigelow D, Schoneich C, Cohen RA. Detection of sequence-specific tyrosine nitration of manganese SOD and SERCA in cardiovascular disease and aging. Am J Physiol Heart Circ Physiol 290: H2220-H2227, 2006.
57. Zhao X, Chen YR, He G, Zhang A, Druhan LJ, Strauch AR, Zweier JL. Endothelial nitric oxide synthase (NOS3) knockout decreases NOS2 induction, limiting hyperoxygenation and conferring protection in the postischemic heart. Am J Physiol Heart Circ Physiol 292: H1541-H1550, 2007.
58. Zhen J, Lu H, Wang XQ, Vaziri ND, Zhou XJ. Upregulation of endothelial and inducible nitric oxide synthase expression by reactive oxygen species. Am J Hypertens 21: 28-34, 2008.
59. Zuckerbraun BS, Chin BY, Bilban M, d’Avila JC, Rao J, Billiar TR, Otterbein LE. Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. FASEB J 21: 1099-1106, 2007.