Concomitant phosphodiesterase 5 inhibition enhances myocardial protection by inhaled nitric oxide in ischemia-reperfusion injurys

Journal of Pharmacology and Experimental Therapeutics

Volumn 356, Issue 2, 2016, Pages 284-292

  Lux, Arpad ^a   Pokreisz, Peter ^b   Swinnen, Melissa ^b   Caluwe, Ellen ^b   Gillijns, Hilde ^b   Szelid, Zsolt ^a   Merkely, Bela ^a   Janssens, Stefan P ^b,c  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; LONG ACTING DRUG; MYELOPEROXIDASE; NITRIC OXIDE; PHOSPHODIESTERASE V; TADALAFIL; TROPONIN I; CARDIOTONIC AGENT; PHOSPHODIESTERASE V INHIBITOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; C57BL 6 MOUSE; CARDITIS; CELL INFILTRATION; CONTROLLED STUDY; CORONARY ARTERY LIGATION; CORONARY REPERFUSION; CYCLIC GMP BLOOD LEVEL; CYCLIC GMP HEART LEVEL; DISEASE SEVERITY; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; ECHOCARDIOGRAPHY; ENZYME INHIBITION; HEART CATHETERIZATION; HEART DILATATION; HEART HEMODYNAMICS; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE ISCHEMIA; HEART MUSCLE NECROSIS; HEART PROTECTION; HEART STROKE VOLUME; HEART VENTRICLE REMODELING; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; TISSUE LEVEL; ANIMAL; C57BL MOUSE; COMBINATION DRUG THERAPY; ECHOGRAPHY; INHALATIONAL DRUG ADMINISTRATION; MYOCARDIAL REPERFUSION INJURY;

ADMINISTRATION, INHALATION; ANIMALS; CARDIOTONIC AGENTS; DRUG THERAPY, COMBINATION; MALE; MICE; MICE, INBRED C57BL; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE; PHOSPHODIESTERASE 5 INHIBITORS;

EID: 84959440386     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.115.227850     Document Type: Article

References (46)

1. Ahmad N, Wang Y, Ali AK, and Ashraf M (2009) Long-acting phosphodiesterase-5 inhibitor, tadalafil, induces sustained cardioprotection against lethal ischemic injury. Am J Physiol Heart Circ Physiol 297: H387-H391.
2. Bhatraju P, Crawford J, Hall M, and Lang JD, Jr (2015) Inhaled nitric oxide: Current clinical concepts. Nitric Oxide 50: 114-128.
3. Bloch KD, Ichinose F, Roberts JD, Jr, and Zapol WM (2007) Inhaled NO as a therapeutic agent. Cardiovasc Res 75: 339-348.
4. Carden DL and Granger DN (2000) Pathophysiology of ischaemia-reperfusion injury. J Pathol 190: 255-266.
5. Chen Y-R and Zweier JL (2014) Cardiac mitochondria and reactive oxygen species generation. Circ Res 114: 524-537.
6. Das A, Xi L, and Kukreja RC (2008) Protein kinase G-dependent cardioprotective mechanism of phosphodiesterase-5 inhibition involves phosphorylation of ERK and GSK3b. J Biol Chem 283: 29572-29585.
7. Das A, Durrant D, Salloum FN, Xi L, and Kukreja RC (2015a) PDE5 inhibitors as therapeutics for heart disease, diabetes and cancer. Pharmacol Ther 147: 12-21.
8. Das A, Samidurai A, Hoke NN, Kukreja RC, Salloum FN (2015b) Hydrogen sulfide mediates the cardioprotective effects of gene therapy with PKG-Ia. Basic Res Cardiol 110: 42.
9. Elrod JW, Greer JJM, and Lefer DJ (2007) Sildenafil-mediated acute cardioprotection is independent of the NO/cGMP pathway. Am J Physiol Heart Circ Physiol 292: H342-H347.
10. Ferdinandy P, Danial H, Ambrus I, Rothery RA, and Schulz R (2000) Peroxynitrite is a major contributor to cytokine-induced myocardial contractile failure. Circ Res 87: 241-247.
11. Francis SH, Busch JL, Corbin JD, and Sibley D (2010) cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol Rev 62: 525-563.
12. Garcia-Dorado D, Agulló L, Sartorio CL, and Ruiz-Meana M (2009) Myocardial protection against reperfusion injury: The cGMP pathway. Thromb Haemost 101: 635-642.
13. Gielis JF, Lin JY, Wingler K, Van Schil PEY, Schmidt HH, and Moens AL (2011) Pathogenetic role of eNOS uncoupling in cardiopulmonary disorders. Free Radic Biol Med 50: 765-776.
14. Guazzi M, Vicenzi M, Arena R, and Guazzi MD (2011) PDE5 inhibition with sildenafil improves left ventricular diastolic function, cardiac geometry, and clinical status in patients with stable systolic heart failure: Results of a 1-year, prospective, randomized, placebo-controlled study. Circ Heart Fail 4: 8-17.
15. Hataishi R, Rodrigues AC, Neilan TG, Morgan JG, Buys E, Shiva S, Tambouret R, Jassal DS, Raher MJ, and Furutani E, 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.
16. Heusch G, Boengler K, and Schulz R (2008) Cardioprotection: Nitric oxide, protein kinases, and mitochondria. Circulation 118: 1915-1919.
17. Ichinose F (2013) Improving outcomes after cardiac arrest using NO inhalation. Trends Cardiovasc Med 23: 52-58.
18. Kakkar R, Seitz DP, Kanthan R, Rajala RVS, Radhi JM, Wang X, Pasha MK, Wang R, and Sharma RK (2002) Calmodulin-dependent cyclic nucleotide phosphodiesterase in an experimental rat model of cardiac ischemia-reperfusion. Can J Physiol Pharmacol 80: 59-66.
19. Kass DA, Champion HC, and Beavo JA (2007a) Phosphodiesterase type 5: Expanding roles in cardiovascular regulation. Circ Res 101: 1084-1095.
20. Kass DA, Takimoto E, Nagayama T, and Champion HC (2007b) Phosphodiesterase regulation of nitric oxide signaling. Cardiovasc Res 75: 303-314.
21. Koka S, Aluri HS, Xi L, Lesnefsky EJ, and Kukreja RC (2014) Chronic inhibition of phosphodiesterase 5 with tadalafil attenuates mitochondrial dysfunction in type 2 diabetic hearts: Potential role of NO/SIRT1/PGC-1a signaling. Am J Physiol Heart Circ Physiol 306: H1558-H1568.
22. Koka S, Das A, Zhu S-G, Durrant D, Xi L, and Kukreja RC (2010) Long-acting phosphodiesterase-5 inhibitor tadalafil attenuates doxorubicin-induced cardiomyopathy without interfering with chemotherapeutic effect. J Pharmacol Exp Ther 334: 1023-1030.
23. Kukreja RC, Salloum FN, Das A, Koka S, Ockaili RA, and Xi L (2011) Emerging new uses of phosphodiesterase-5 inhibitors in cardiovascular diseases. Exp Clin Cardiol 16: E30-e35.
24. Liu X, Huang Y, Pokreisz P, Vermeersch P, Marsboom G, Swinnen M, Verbeken E, Santos J, Pellens M, and Gillijns H, et al. (2007) Nitric oxide inhalation improves microvascular flow and decreases infarction size after myocardial ischemia and reperfusion. J Am Coll Cardiol 50: 808-817.
25. Lukowski R, Krieg T, Rybalkin SD, Beavo J, and Hofmann F (2014) Turning on cGMP-dependent pathways to treat cardiac dysfunctions: Boom, bust, and beyond. Trends Pharmacol Sci 35: 404-413.
26. MacArthur PH, Shiva S, and Gladwin MT (2007) Measurement of circulating nitrite and S-nitrosothiols by reductive chemiluminescence. J Chromatogr B Analyt Technol Biomed Life Sci 851: 93-105.
27. McAlindon E, Bucciarelli-Ducci C, Suleiman MS, and Baumbach A (2015) Infarct size reduction in acute myocardial infarction. Heart 101: 155-160.
28. McMahon TJ 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.
29. Mika D, Leroy J, Vandecasteele G, and Fischmeister R (2012) PDEs create local domains of cAMP signaling. J Mol Cell Cardiol 52: 323-329.
30. Nagasaka Y, Fernandez BO, Garcia-Saura MF, Petersen B, Ichinose F, Bloch KD, Feelisch M, and Zapol WM (2008) Brief periods of nitric oxide inhalation protect against myocardial ischemia-reperfusion injury. Anesthesiology 109: 675-682.
31. Nagasaka Y, Buys ES, Spagnolli E, Steinbicker AU, Hayton SR, Rauwerdink KM, Brouckaert P, Zapol WM, and Bloch KD (2011) Soluble guanylate cyclase-a1 is required for the cardioprotective effects of inhaled nitric oxide. Am J Physiol Heart Circ Physiol 300: H1477-H1483.
32. Neye N, Enigk F, Shiva S, Habazettl H, Plesnila N, Kuppe H, Gladwin MT, and Kuebler WM (2012) Inhalation of NO during myocardial ischemia reduces infarct size and improves cardiac function. Intensive Care Med 38: 1381-1391.
33. Pacher P, Nagayama T, Mukhopadhyay P, Bátkai S, and Kass DA (2008) Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 3: 1422-1434.
34. Redfield MM, Chen HH, Borlaug BA, Semigran MJ, Lee KL, Lewis G, LeWinter MM, Rouleau JL, Bull DA, and Mann DL, et al.; RELAX Trial (2013) Effect of phosphodiesterase-5 inhibition on exercise capacity and clinical status in heart failure with preserved ejection fraction: A randomized clinical trial. JAMA 309: 1268-1277.
35. Salloum FN, Abbate A, Das A, Houser J-E, Mudrick CA, Qureshi IZ, Hoke NN, Roy SK, Brown WR, and Prabhakar S, et al. (2008) Sildenafil (Viagra) attenuates ischemic cardiomyopathy and improves left ventricular function in mice. Am J Physiol Heart Circ Physiol 294: H1398-H1406.
36. Salloum FN, Chau VQ, Hoke NN, Abbate A, Varma A, Ockaili RA, Toldo S, and Kukreja RC (2009) Phosphodiesterase-5 inhibitor, tadalafil, protects against myocardial ischemia/reperfusion through protein-kinase g-dependent generation of hydrogen sulfide. Circulation 120(11, Suppl)S31-S36.
37. Salloum FN, Chau VQ, Hoke NN, and Kukreja RC (2014) Tadalafil prevents acute heart failure with reduced ejection fraction in mice. Cardiovasc Drugs Ther 28: 493-500.
38. Schumacker PT (2013) Nitric oxide quenches the fire in heart mitochondria. Nat Med 19: 666-667.
39. Sesti C, Florio V, Johnson EG, and Kloner RA (2007) The phosphodiesterase-5 inhibitor tadalafil reduces myocardial infarct size. Int J Impot Res 19: 55-61.
40. Szabó C, Ischiropoulos H, and Radi R (2007) Peroxynitrite: Biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6: 662-680.
41. Terpolilli NA, Kim S-W, Thal SC, Kataoka H, Zeisig V, Nitzsche B, Klaesner B, Zhu C, Schwarzmaier S, and Meissner L, et al. (2012) Inhalation of nitric oxide prevents ischemic brain damage in experimental stroke by selective dilatation of collateral arterioles. Circ Res 110: 727-738.
42. Tsai EJ and Kass DA (2009) Cyclic GMP signaling in cardiovascular pathophysiology and therapeutics. Pharmacol Ther 122: 216-238.
43. Vandeput F, Krall J, Ockaili R, Salloum FN, Florio V, Corbin JD, Francis SH, Kukreja RC, and Movsesian MA (2009) cGMP-hydrolytic activity and its inhibition by sildenafil in normal and failing human and mouse myocardium. J Pharmacol Exp Ther 330: 884-891.
44. Vinten-Johansen J (2004) Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury. Cardiovasc Res 61: 481-497.
45. Yang BK, Vivas EX, Reiter CD, and Gladwin MT (2003) Methodologies for the sensitive and specific measurement of S-nitrosothiols, iron-nitrosyls, and nitrite in biological samples. Free Radic Res 37: 1-10.
46. Yellon DM and Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357: 1121-1135.