GH-releasing hormone induces cardioprotection in isolated male rat heart via activation of RISK and SAFE pathways

Endocrinology

Volumn 154, Issue 4, 2013, Pages 1624-1635

  Penna, Claudia ^a   Settanni, Fabio ^b   Tullio, Francesca ^a   Trovato, Letizia ^b   Pagliaro, Pasquale ^a   Alloatti, Giuseppe ^c   Ghigo, Ezio ^b   Granata, Riccarda ^b,d  

^a Department of Medical Sciences ^*  (Italy)

^b Division of Endocrinology   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYDECANOIC ACID; ATRACTYLOSIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCOGEN SYNTHASE KINASE 3BETA; GROWTH HORMONE RELEASING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PEPTIDES AND PROTEINS; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REPERFUSION INJURY SALVAGE KINASE; STAT3 PROTEIN; SURVIVOR ACTIVATING FACTOR ENHANCEMENT; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART CONTRACTION; HEART INFARCTION SIZE; HEART PROTECTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; GROWTH HORMONE-RELEASING HORMONE; MALE; MITOCHONDRIA, HEART; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, NEUROPEPTIDE; RECEPTORS, PITUITARY HORMONE-REGULATING HORMONE; SIGNAL TRANSDUCTION;

EID: 84875859728     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2064     Document Type: Article

References (55)

1. Isgaard J, Tivesten A, Friberg P, Bengtsson BA. The role of the GH/IGF-I axis for cardiac function and structure. Horm Metab Res. 1999;31:50-54.
2. Cittadini A, Grossman JD, Stromer H, Katz SE, Morgan JP, Douglas PS. Importance of an intact growth hormone/insulin-like growth factor 1 axis for normal post-infarction healing: studies in dwarf rats. Endocrinology. 2001;142:332-338.
3. Nagaya N, Uematsu M, Kojima M, et al. Chronic administration of ghrelin improves left ventricular dysfunction and attenuates development of cardiac cachexia in rats with heart failure. Circulation. 2001;104:1430-1435.
4. Granata R, Isgaard J, Alloatti G, Ghigo E. Cardiovascular actions of the ghrelin gene-derived peptides and growth hormone-releasing hormone. Exp Biol Med (Maywood). 2011;236:505-514.
5. Chang L, Ren Y, Liu X, et al. Protective effects of ghrelin on ischemia/reperfusion injury in the isolated rat heart. J Cardiovasc Pharmacol. 2004;43:165-170.
6. Alloatti G, Arnoletti E, Bassino E, et al. Obestatin affords cardioprotection to the ischemic-reperfused isolated rat heart and inhibits apoptosis in cultures of similarly stressed cardiomyocytes. Am J Physiol Heart Circ Physiol. 2010;299:H470-H481.
7. Hausenloy DJ, Yellon DM. Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection. Heart Fail Rev. 2007; 12:217-234.
8. Tsang A, Hausenloy DJ, Mocanu MM, Yellon DM. Postconditioning: a form of "modified reperfusion" protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res. 2004;95:230-232.
9. Granata R, Trovato L, Gallo MP, et al. Growth hormone-releasing hormone promotes survival of cardiac myocytes in vitro and protects against ischaemia-reperfusion injury in rat heart. Cardiovasc Res. 2009;83:303-312.
10. Kanashiro-Takeuchi RM, Tziomalos K, Takeuchi LM, et al. Cardioprotective effects of growth hormone-releasing hormone agonist after myocardial infarction. Proc Natl Acad Sci USA. 2010;107: 2604-2609.
11. Barabutis N, Schally AV. Growth hormone-releasing hormone: extrapituitary effects in physiology and pathology. Cell Cycle. 2010; 9:4110-4116.
12. Ukkola O. Ghrelin in type 2 diabetes mellitus and metabolic syndrome. Mol Cell Endocrinol. 2011;340:26-28.
13. Kanashiro-Takeuchi RM, Takeuchi LM, Rick FG, et al. Activation of growth hormone releasing hormone (GHRH) receptor stimulates cardiac reverse remodeling after myocardial infarction (MI). Proc Natl Acad Sci USA. 2012;109:559-563.
14. Yang XM, Philipp S, Downey JM, Cohen MV. Postconditioning's protection is not dependent on circulating blood factors or cells but involves adenosine receptors and requires PI3-kinase and guanylyl cyclase activation. Basic Res Cardiol. 2005;100:57-63.
15. Cohen MV, Yang XM, Downey JM. Acidosis, oxygen, and interference with mitochondrial permeability transition pore formation in the early minutes of reperfusion are critical to postconditioning's success. Basic Res Cardiol. 2008;103:464-471.
16. Pagliaro P, Moro F, Tullio F, Perrelli MG, Penna C. Cardioprotective pathways during reperfusion: focus on redox signaling and other modalities of cell signaling. Antioxid Redox Signal. 2011;14: 833-850.
17. Hausenloy DJ, Yellon DM. Cardioprotective growth factors. Cardiovasc Res. 2009;83:179-194.
18. Zhao ZQ, Corvera JS, Halkos ME, Kerendi F, Wang NP, Guyton RA, Vinten-Johansen J. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol. 2003;285:H579-H588.
19. Pagliaro P, Penna C. Cardiac postconditioning. Antioxid Redox Signal. 2010;14:777-779.
20. O'Rourke B. Evidence for mitochondrial K + channels and their role in cardioprotection. Circ Res. 2004;94:420-432.
21. Ong SB, Gustafsson AB. New roles for mitochondria in cell death in the reperfused myocardium. Cardiovasc Res. 2012;94:190-196.
22. Di Lisa F, Menabo R, Canton M, Barile M, Bernardi P. Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem. 2001;276:2571-2575.
23. Yao Y, Li L, Gao C, Shi C. Sevoflurane postconditioning protects chronically-infarcted rat hearts against ischemia-reperfusion injury by activation of pro-survival kinases and inhibition of mitochondrial permeability transition pore opening upon reperfusion. Biol Pharm Bull. 2009;32:1854-1861.
24. Ovize M, Baxter GF, Di Lisa F, et al. Postconditioning and protection from reperfusion injury: where do we stand? Position paper from the Working Group of Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res. 2011;87:406-423.
25. Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R, Young LH. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature. 2008;451:578-582.
26. Young LH. AMP-activated protein kinase conducts the ischemic stress response orchestra. Circulation. 2008;117:832-840.
27. Paiva MA, Goncalves LM, Providencia LA, Davidson SM, Yellon DM, Mocanu MM. Transitory activation of AMPK at reperfusion protects the ischaemic-reperfused rat myocardium against infarction. Cardiovasc Drugs Ther. 2011;24:25-32.
28. Lacerda L, Somers S, Opie LH, Lecour S. Ischaemic postconditioning protects against reperfusion injury via the SAFE pathway. Cardiovasc Res. 2009;84:201-208.
29. Goodman MD, Koch SE, Fuller-Bicer GA, Butler KL. Regulating RISK: a role for JAK-STAT signaling in postconditioning? Am J Physiol Heart Circ Physiol. 2008;295:H1649-H1656.
30. Hausenloy DJ, Lecour S, Yellon DM. Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: two sides of the same coin. Antioxid Redox Signal. 2011;14:893-907.
31. Penna C, Mancardi D, Rastaldo R, Losano G, Pagliaro P. Intermittent activation of bradykinin B2 receptors and mitochondrial KATP channels trigger cardiac postconditioning through redox signaling. Cardiovasc Res. 2007;75:168-177.
32. Penna C, Rastaldo R, Mancardi D, et al. Post-conditioning induced cardioprotection requires signaling through a redox-sensitive mechanism, mitochondrial ATP-sensitive K + channel and protein kinase C activation. Basic Res Cardiol. 2006;101:180-189.
33. Cohen MV, Yang XM, Downey JM. The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation. 2007;115:1895-1903.
34. Hausenloy DJ, Ong SB, Yellon DM. The mitochondrial permeability transition pore as a target for preconditioning and postconditioning. Basic Res Cardiol. 2009;104:189-202.
35. Penna C, Pasqua T, Perrelli MG, Pagliaro P, Cerra MC, Angelone T. Postconditioning with glucagon like peptide-2 reduces ischemia/reperfusion injury in isolated rat hearts: role of survival kinases and mitochondrial KATP channels. Basic Res Cardiol. 2012;107:272.
36. Mir SA, Chatterjee A, Mitra A, Pathak K, Mahata SK, Sarkar S. Inhibition of signal transducer and activator of transcription 3 (STAT3) attenuates interleukin-6 (IL-6)-induced collagen synthesis and resultant hypertrophy in rat heart. J Biol Chem. 2012;287: 2666-2677.
37. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121-1135.
38. Gao F, Gao E, Yue TL, et al. Nitric oxide mediates the antiapoptotic effect of insulin in myocardial ischemia-reperfusion: the roles of PI3-kinase, Akt, and endothelial nitric oxide synthase phosphorylation. Circulation. 2002;105:1497-1502.
39. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Aktdependent phosphorylation. Nature. 1999;399:601-605.
40. Frascarelli S, Ghelardoni S, Ronca-Testoni S, Zucchi R. Effect of ghrelin and synthetic growth hormone secretagogues in normal and ischemic rat heart. Basic Res Cardiol. 2003;98:401-405.
41. Freixa X, Bellera N, Ortiz-Perez JT, et al. Ischaemic postconditioning revisited: lack of effects on infarct size following primary percutaneous coronary intervention. Eur Heart J. 2012;33:103-112.
42. Sorensson P, Saleh N, Bouvier F, et al. Effect of postconditioning on infarct size in patients with ST elevation myocardial infarction. Heart. 2010;96:1710-1715.
43. Gelpi RJ, Morales C, Cohen MV, Downey JM. Xanthine oxidase contributes to preconditioning's preservation of left ventricular developed pressure in isolated rat heart: developed pressure may not be an appropriate end-point for studies of preconditioning. Basic Res Cardiol. 2002;97:40-46.
44. Siejka A, Schally AV, Barabutis N. Activation of Janus kinase/signal transducer and activator of transcription 3 pathway by growth hormone-releasing hormone. Cell Mol Life Sci. 2010;67:959-964.
45. Forbes RA, Steenbergen C, Murphy E. Diazoxide-induced cardioprotection requires signaling through a redox-sensitive mechanism. Circ Res. 2001;88:802-809.
46. Ivanes F, Rioufol G, Piot C, Ovize M. Postconditioning in acute myocardial infarction patients. Antioxid Redox Signal. 2011;14: 811-820.
47. Nichols CG. KATP channels as molecular sensors of cellular metabolism. Nature. 2006;440:470-476.
48. Ruderman NB, Cacicedo JM, Itani S, et al. Malonyl-CoA and AMPactivated protein kinase (AMPK): possible links between insulin resistance in muscle and early endothelial cell damage in diabetes. Biochem Soc Trans. 2003;31:202-206.
49. Chen ZP, Mitchelhill KI, Michell BJ, et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999;443:285-289.
50. Li J, Hu X, Selvakumar P, et al. Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am J Physiol Endocrinol Metab. 2004;287:E834-E841.
51. Godecke A, Heinicke T, Kamkin A, et al. Inotropic response to β-adrenergic receptor stimulation and anti-adrenergic effect of ACh in endothelial NO synthase-deficient mouse hearts. J Physiol. 2001; 532:195-204.
52. Sivaraman V, Mudalagiri NR, Di Salvo C, et al. Postconditioning protects human atrial muscle through the activation of the RISK pathway. Basic Res Cardiol. 2007;102:453-459.
53. Juhaszova M, Zorov DB, Yaniv Y, Nuss HB, Wang S, Sollott SJ. Role of glycogen synthase kinase-3β in cardioprotection. Circ Res. 2009;104:1240-1252.
54. Juhaszova M, Zorov DB, Kim SH, et al. Glycogen synthase kinase-3β mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest. 2004;113: 1535-1549.
55. Kiaris H, Chatzistamou I, Papavassiliou AG, Schally AV. Growth hormone-releasing hormone: not only a neurohormone. Trends Endocrinol Metab. 2011;22:311-317.