The role of β-adrenergic receptors in the cardioprotective effects of beta-preconditioning (βPC)

Cardiovascular Drugs and Therapy

Volumn 25, Issue 1, 2011, Pages 31-46

  Salie, Ruduwaan ^a   Moolman, Johannes A ^a   Lochner, Amanda ^b  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

^b SOUTH AFRICAN MEDICAL RESEARCH COUNCIL   (South Africa)

Author keywords

adrenergic receptors; Gi protein; Infarct size; Mechanical recovery during reperfusion; Protein kinase A

Indexed keywords

1 (2 ETHYLPHENOXY) 3 (1,2,3,4 TETRAHYDRO 1 NAPHTHYLAMINO) 2 PROPANOL OXALATE; 3 ISOPROPYLAMINO 1 (7 METHYL 4 INDANYLOXY) 2 BUTANOL; 4 [2 [[2 (3 CHLOROPHENYL) 2 HYDROXYETHYL]AMINO]PROPYL]PHENOXYACETIC ACID; 5 [2 [[2 HYDROXY 3 [4 (1 METHYL 4 TRIFLUOROMETHYL 2 IMIDAZOLYL)PHENOXY]PROPYL]AMINO]ETHOXY]SALICYLAMIDE; BETA ADRENERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; DENOPAMINE; FORMOTEROL FUMARATE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; ISOPRENALINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE;

ANIMAL TISSUE; ARTICLE; CLINICAL PROTOCOL; CONTROLLED STUDY; ENZYME ACTIVATION; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; ISCHEMIC PRECONDITIONING; ISOLATED HEART; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

A KINASE ANCHOR PROTEINS; ADRENERGIC BETA-AGONISTS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; ETHANOLAMINES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HEART; ISCHEMIC PRECONDITIONING, MYOCARDIAL; ISOPROTERENOL; MALE; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3-KINASES; RATS; RATS, WISTAR; RECEPTORS, ADRENERGIC, BETA;

EID: 79959921178     PISSN: 09203206     EISSN: 15737241     Source Type: Journal    
DOI: 10.1007/s10557-010-6275-3     Document Type: Article

References (60)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischaemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124-36. (Pubitemid 17174962)
2. Das M, Das DK. Molecular mechanism of preconditioning. IUBMB Life. 2008;60:199-203.
3. Gross ER, Gross GJ. Ischemic preconditioning and myocardial infarction. An update and perspective. Drug Discov Today Dis Mech. 2007;43:165-74. (Pubitemid 351966334)
4. Asimakis GK, Inners-McBride K, Conti VR, Yang CJ. Transient beta-adrenergic stimulation can precondition the heart against postischaemic contractile dysfunction. Cardiovasc Res. 1994;28:1726-34.
5. Lochner A, Genade S, Tromp E, Podzuweit T, Moolman JA. Ischemic preconditioning and the beta-adrenergic signal transduction pathway. Circulation. 1999;100:958-66. (Pubitemid 29407177)
6. Sanada S, Asanuma H, Tsukamoto O, Minamino T, et al. Protein kinase A as another mediator of ischemic preconditioning independent of protein kinase C. Circulation. 2004;110:51-7. (Pubitemid 38880133)
7. Tong H, Bernstein D, Murphy E, Steenbergen C. The role of β-adrenergic receptor signaling in cardioprotection. FASEB J. 2005;19:983-5. (Pubitemid 40827725)
8. Miyawaki H, Ashraf M. Isoproterenol mimics calcium preconditioning- induced protein against ischemia. Am J Physiol. 1997;272:H927-936.
9. Bristow M, Ginsburg R, Umans V, Fowler M, Minobe W, Rasmussen R, et al. Beta1- and beta2-adrenergic receptor subpopulations in non-failing and failing human ventricular myocardium: coupling of both receptor subtypes to muscle contraction and selective beta1-receptor down-regulation in heart failure. Circ Res. 1986;59:297-309. (Pubitemid 17178124)
10. Rosec B, Gauthier C. β3-adrenoceptors in the cardiovascular system: putative roles in human pathologies. Pharmacol Ther. 2006;111:652-73. (Pubitemid 44137382)
11. Xiao RP. Beta-adrenergic signaling in the heart: dual coupling of the beta2-adrenergic receptor to G(s) and G(i) proteins. Sci STKE RE. 2001;15.
12. Zheng G, Hau QD, Xiao RP. Distinct beta-adrenergic receptor subtype signaling in the heart and their pathophysiological relevance. Sheng Li Xue Bao. 2004;56:1-15.
13. Gauthier C, Tavernier G, Charpentier F, Langin D, Le Marec H. Functional beta3-adrenoceptor in the human heart. J Clin Invest. 1996;98:556-62.
14. Gauthier C, Leblais V, Kobzik L, Trochu JN, Khandoudi N, Bril A, et al. The negative inotropic effect of beta3-adreneceptor stimulation is mediated by activation of a nitric oxide synthase pathway in human ventricle. J Clin Invest. 1998;102:1377-84. (Pubitemid 28467566)
15. Frances C, Nazeyrollas P, Prevast A, Moreau P, Pisani J, Davani S, et al. Role of beta1- and beta2-adrenoceptor subtypes in preconditioning against myocardial dysfunction after ischaemia and reperfusion. J Cardiovasc Pharmacol. 2003;41:396-405. (Pubitemid 36255299)
16. Robinet A, Hoizey G, Millart H. PI3-kinase, protein kinase C and protein kinase A are involved in the trigger phase of beta1-adrenergic preconditioning. Cardiovasc Res. 2005;66:530-42. (Pubitemid 40725765)
17. Mallet RT, Ryon MG, Williams AG, Howard L, Downey HF. Beta (1)-Adrenergic receptor antagonism abrogates the cardioprotective effects of intermittent hypoxia. Bas Res Cardiol. 2006;101:436-46. (Pubitemid 44275877)
18. Lange M, Smul TM, Blomeyer CA, Redel A, Klotz KN, Roewer N, et al. Role of the beta1-adrenergic pathway in anesthetic and ischemic preconditioning against myocardial infarction in the rabbit heart in vivo. Anesthesiology. 2006;105:503-10. (Pubitemid 44310433)
19. Kannengieser GJ, Opie LH, van der Werff TJ. Impaired cardiac work and oxygen uptake after reperfusion of regionally ischemic myocardium. J Mol Cell Cardiol. 1979;11:197-207. (Pubitemid 9119469)
20. Nasa Y, Yabek, Takeo S. Beta-adrenoceptor stimulation-mediated preconditioning-like cardioprotection in perfused rat hearts. J Cardiovasc Pharmacol. 1997;29:436-43. (Pubitemid 27212745)
21. Akahane K, Furukawa Y, Karasawa Y, Ren LM, Chiba S. Pharmacological analysis of positive chrono-and inotropic responses to denopamine (TA-064) in dog cross-circulated atrial and ventricular preparations. Jpn J Pharmacol. 1990;52:69-79. (Pubitemid 20023690)
22. Dooley DJ, Bittiger H, Reyman NC. CGP 20712A: a useful tool for quantifying the β1- and β2-adrenoceptors. Eur J Pharmacol. 1986;130:137-9. (Pubitemid 17170862)
23. Spear JF, Prabu SK, Galati D, Raza M, et al. Beta1-Adrenoceptor activation contributes to ischemia-reperfusion damage as well as playing a role in ischemic preconditioning. Am J Physiol. 2007;292:H2459-66. (Pubitemid 47084629)
24. Wang W, Zhu W, Wang S, Crow MT, Xiao RP, Cheng H. Sustained beta1-adrenergic stimulation modulates cardiac contractility by Ca2+/calmodulin signaling pathway. Circ Res. 2004;95:798-806. (Pubitemid 39390582)
25. Benter IF, Juggi JS, Khan I, Yousif MH, Canatan H, Akhtar S. Signal transduction mechanisms involved in cardiac preconditioning: role of Ras-GTPase, Ca2+/calmodulin-dependent protein kinase II an epidermal growth factor receptor. Mol Cell Biochem. 2005;268:175-83. (Pubitemid 40287840)
26. Lange M, Smul TM, Redel A, Lotz C, Jazbutyte V, Schnupp V, et al. Differential role of calcium/calmodulin-dependent protein kinase II in desflurane-induced preconditioning and cardioprotection by metoprolol; Metoprolol blocks desflurane-induced preconditioning. Anesthesiology. 2008;109:72-8.
27. Communal C, Singh K, Sawyer DB, Colucci WS. Opposing effects of beta(1)- and beta(2)-adrenergic receptors on cardiac myocyte apoptosis: role of a pertussis toxin-sensitive G protein. Circulation. 1999;100:2210-2.
28. Kaumann AJ, Sanders L, Lynham JA, Bartel S, Kuschel M, Karczewski P, et al. Beta-2 adrenoceptor activation by zinterol causes protein phosphorylation, contractile effects and relaxant effects through a cAMP pathway in human atrium. Mol Cell Biochem. 1996;163-164:113-23.
29. Anderson GP. Formoterol: pharmacology, molecular basis of agonism, and mechanism of long duration of a highly potent and selective β2-adrenoceptor agonist bronchodilator. Life Sci. 1993;52:2145-60.
30. Naline E, Zhang Y, Qian Y, Mairon N, Anderson GP, et al. Relaxant effects and durations of action of formoterol and salmeterol on the isolated human bronchus. Eur Respir J. 1994;7:914-20. (Pubitemid 24153592)
31. Gauthier C, Tavernier G, Trochu JN, Leblais V, Laurent K, Langin D, et al. Interspecies differences in the cardiac negative inotropic effects of beta(3)-adrenoceptor agonists. J Pharmacol Exp Therapeut. 1999;2:689-93.
32. Barbier J, Mouas C, Rannou-Bekono F, Carrè F. Existence of beta (3)-adrenoceptors in rat heart: functional implications. Clin Exp Pharmacol Physiol. 2007;34:796-8. (Pubitemid 47013488)
33. Murphy KT, Bundgaard H, Clausen T. Beta3-adrenoceptor agonist stimulation of the Na+, K+-pump in rat skeletal muscle is mediated by beta-2- rather than beta3-adrenoceptors. Br J Pharmacol. 2006;149:635-46. (Pubitemid 44748056)
34. Daaka Y, Luttrell LM, Lefkowitz R. Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature. 1997;390:88-91. (Pubitemid 27494762)
35. Zamah AM, Delahunty M, Luttrell LM, Lefkowitz RJ. Protein kinase A-mediated phosphorylation of the beta2-adrenergic receptor regulates its coupling to Gs and Gi. Demonstration in a reconstituted system. J Biol Chem. 2002;277:31249-56. (Pubitemid 34970833)
36. Zhu WZ, Zheng M, Koch WJ, Lefkowitz RJ, Kobilka BK, Xiao RP. Dual modulation of cell survival and cell death by beta(2)-adrenergic signaling in adult mouse cardiac myocytes. Proc Natl Acad Sci. 2001;98:1607-12. (Pubitemid 32165546)
37. Martin NP, Whalen EJ, Zamah MA, Pierce KL, Lefkowitz RJ. PKA-mediated phosphorylation of the β1-adrenergic receptor promotes Gs/Gi switching. Cell Signal. 2004;16:1397-403. (Pubitemid 39277504)
38. Moolman JA, Hartley S, van Wyk J, Marais E, Lochner A. Inhibition of myocardial apoptosis by ischaemia and beta-adrenergic preconditioning is dependent on p38MAPK. Cardiovasc Drugs Ther. 2006;20:13-25.
39. Critz SD, Cohen MV, Downey JM. Mechanisms of acetylcholine-and bradykinin-induced preconditioning. Vasc Pharm. 2005;42:201-9.
40. Gjertsen BT, Mellgren G, Otten A, et al. Novel (Rp)-cAMPs analogs as tools for inhibition of cAMPkinase in cell culture. Basal cAMPkinase activity modulates interleukin-1beta action. J Biol Chem. 1995;270:20599-607.
41. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Agullo L, Pina P, Soler-Soler J. Ischemic preconditioning attenuates calpain-mediated degradation of structural proteins through a protein kinase A-dependent mechanism. Cardiovasc Res. 2004;64:105-14. (Pubitemid 39208927)
42. Marais E, Genade S, Salie R, Huisamen B, Maritz S, Moolman JA, et al. The temporal relationship between p38MAPK and HSP27 activation in ischaemic and pharmacological preconditioning. Bas Res Cardiol. 2005;100:35-47. (Pubitemid 40069105)
43. Sichelschmidt OJ, Hahnefeld C, Hohlfeld T, Herberg FW, Schrör K. Trapidil protrects ischemic hearts from reperfusion injury by stimulating PKA II activity. Cardiovasc Res. 2003;58:602-10. (Pubitemid 36694446)
44. Dong JM, Leung T, Manser E, LimL. cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and Rho kinase ROKalpha. J Biol Chem. 1998;273:22554-62. (Pubitemid 28399823)
45. Hamid SA, Bower HS, Baxter GF. Rho kinase activation plays a major role as mediator of irreversible injury in reperfused myocardium. Am J Physiol. 2007;292:H 2590-2606.
46. Manganello JM, Huang JS, Kozasa T, Voyno-Yasenetskaya TA, Le Breton GC. Protein kinase A-mediated phosphorylation of the Galpha13 switch I region alters Galphabetagamma13-G protein-coupled receptor complex and inhibits Rho activation. J Biol Chem. 2003;278:124-130. (Pubitemid 36043553)
47. Shimokawa H. Rho-kinase as a novel therapeutic target in treatment of cardiovascular diseases. J Cardiovasc Pharmacol. 2002;39:319-27. (Pubitemid 34175055)
48. Juhaszova M, Zorov DB, Kin SH, Pepe S, Fu Q, Fishbein KW, et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest. 2004;113:1535-49. (Pubitemid 39071677)
49. Lange M, Redel A, Lotz C, Smul TM, Blomeyer C, Frank A, et al. Desflurane-induced postconditioning is mediated by β-adrenergic signaling. Anesthesiology. 2009;110:516-28.
50. Xiao RP, Zhu W, Zheng M, Chakir K, Bond R, Lakatta EG, et al. Subtype-specific beta-adrenoceptor signaling pathways in the heart and their potential clinical implications. Trends Pharmacol Sci. 2004;25:358-65. (Pubitemid 38829489)
51. Slezak J, Buchwalow IB, Schulze W, Karzewski P, Wallukat G, Samoilova VE, et al. Cellular control of nitric oxide synthase expression and activity in rat cardiomyocytes. Antioxid Redox Signal. 2004;6:345-52. (Pubitemid 38332592)
52. Lochner A, Marais E, Genade S, Moolman JA. Nitric oxide: a trigger for classic preconditioning? Am J Physiol Heart Circ Physiol. 2000;279:H2752-65. (Pubitemid 32005864)
53. Cohen MV, Yang XM, Downey JM. Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis ofmany infarct-sparing strategies. Cardiovasc Res. 2006;70:231-9. (Pubitemid 44316808)
54. Balligand J-L. Regulation of cardiac β-adrenergic response by nitric oxide. Cardiovasc Res. 1999;43:607-20. (Pubitemid 29369259)
55. Moens AL, Yang R, Watts VL, Barouch LA. Beta 3-adrenoceptor regulation of nitric oxide in the cardiovascular system. J Mol Cell Cardiol. 2010;48:1088-95.
56. Lafontan M. Differential recruitment and differential regulation by physiological amines of fat cell beta-1, beta-2 and beta-3 adrenergic receptors expressed in native fat cells and in transfected cell lines. Cell Signal. 1994;6:363-92.
57. Cohen MV, Yang X-M, Downey JM. Smaller infarct after preconditioning does not predict extent of early functional improvement of reperfused heart. Am J Physiol. 1999;277:H1754-61.
58. Jenkins DP, Bugsley WB, Yellon DM. Ischaemic preconditioning in a model of global ischaemia: infarct size limitation, but no reduction of stunning. J Mol Cell Cardiol. 1995;27:1623-32.
59. Lochner A, Genade S, Moolman JA. Ischemic preconditioning: infarct size is a more reliable endpoint than functional recovery. Bas Res Cardiol. 2003;98:337-46. (Pubitemid 37107661)
60. Penna C, Tullio F, Merlino A, Moro F, Raimondo S, Rastaldo R, et al. Postconditioning cardioprotection against infarct size and post-ischemic systolic dysfunction is influenced by gender. Bas Res Cardiol. 2009;104:390-402.