Antiarrhythmic effect of prolonged morphine exposure is accompanied by altered myocardial adenylyl cyclase signaling in rats

Pharmacological Reports

Volumn 64, Issue 2, 2012, Pages 351-359

  Skrabalova, Jitka ^a   Neckar, Jan ^b,c   Hejnova, Lucie ^a   Bartonova, Iveta ^a   Kolar, Frantisek ^b,c   Novotny, Jiri ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^c Centre for Experimental Cardiovascular Research   (Czech Republic)

Author keywords

Adenylyl cyclase; Arrhythmias; G proteins; Morphine; Rat myocardium

Indexed keywords

ADENYLATE CYCLASE; BETA ADRENERGIC RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MORPHINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIARRHYTHMIC ACTIVITY; ARTICLE; BODY WEIGHT; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; HEART INFARCTION SIZE; HEART PROTECTION; HEART VENTRICLE ARRHYTHMIA; HEART WEIGHT; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WISTAR RAT;

EID: 84862209511     PISSN: 22995684     EISSN: 22995684     Source Type: Journal    
DOI: 10.1016/S1734-1140(12)70775-2     Document Type: Article

References (55)

1. Ackerman JM, Womble MD, Moises HC: Multiple effects of long-term morphine treatment on postsynaptic β-adrenergic receptor function in hippocampus: an intracellular analysis. Brain Res, 1994, 656, 309-318. (Pubitemid 24277116)
2. Ammer H, Schulz R: Alterations in the expression of G-proteins and regulation of adenylate cyclase in human neuroblastoma SH-SY5Y cells chronically exposed to low-efficacy ±-opioids. Biochem J, 1993, 295, 263-271. (Pubitemid 23298336)
3. Ammer H, Schulz R: Opioid tolerance/dependence in neuroblastoma x glioma (NG108-15) hybrid cells is associated with a reduction in spontaneous stimulatory receptor activity. FEBS Lett, 2000, 485, 157-162.
4. Berton O, Nestler EJ: New approaches to antidepressant drug discovery: beyond monoamines. Nat Rev Neurosci, 2006, 7, 137-151. (Pubitemid 43151600)
5. Bie B, Peng Y, Zhang Y, Pan ZZ: cAMP-mediated mechanisms for pain sensitization during opioid withdrawal. J Neurosci, 2005, 25, 3824-3832. (Pubitemid 40570415)
6. Bourova L, Vosahlikova M, Kagan D, Dlouha K, Novotny J, Svoboda P: Long-term adaptation to high doses of morphine causes desensitization of μ-OR- and δ-OR-stimulated G-protein response in forebrain cortex but does not decrease the amount of G-protein a subunits. Med Sci Monit, 2010, 16, BR260-270.
7. Clark MJ, Traynor JR: Endogenous regulator of G protein signaling proteins reduce μ-opioid receptor desensitization and down-regulation and adenylyl cyclase tolerance in C6 cells. J Pharmacol Exp Ther, 2005, 312, 809-815. (Pubitemid 40189583)
8. Fabian G, Bozo B, Szikszay M, Horvath G, Coscia CJ, SzucsM: Chronic morphine-induced changes in mu-opioid receptors and G proteins of different subcellular loci in rat brain. J Pharmacol Exp Ther, 2002, 302, 774-780. (Pubitemid 34787247)
9. Frassdorf J, Huhn R, Niersmann C, Weber NC, Schlack W, Preckel B, Hollmann MW: Morphine induces preconditioning via activation of mitochondrial K(Ca) channels. Can J Anaesth, 2010, 57, 767-773.
10. Gintzler AR, Chakrabarti S: Opioid tolerance and the emergence of new opioid receptor-coupled signaling. Mol Neurobiol, 2000, 21, 21-33. (Pubitemid 32289467)
11. Gintzler AR, Chakrabarti S: Post-opioid receptor adaptations to chronic morphine; altered functionality and associations of signaling molecules. Life Sci, 2006, 79, 717-722. (Pubitemid 43975121)
12. He L, Kim JA, Whistler JL: Biomarkers of morphine tolerance and dependence are prevented by morphineinduced endocytosis of a mutant mu-opioid receptor. FASEB J, 2009, 23, 4327-4334.
13. Chakrabarti S, Rivera M, Yan SZ, Tang WJ, Gintzler AR: Chronic morphine augments Gbg/Gsa stimulation of adenylyl cyclase: relevance to opioid tolerance. Mol Pharmacol, 1998, 54, 655-662. (Pubitemid 28480968)
14. Chan MY, Dai S, Ko WW: Effects of morphine on cardiovascular responses to acute myocardial ischaemia in rats. Br J Pharmacol, 1987, 90, 537-543. (Pubitemid 17022600)
15. Chang AP, Dixon WR: Role of plasma catecholamines in eliciting cardiovascular changes seen during naloxone-precipitated withdrawal in conscious, unrestrained morphine-dependent rats. J Pharmacol Exp Ther, 1990, 254, 857-863. (Pubitemid 20303712)
16. Chen Y, Liu J, Yu L: Functional coupling of a mu opioid receptor to G proteins and adenylyl cyclase:Modulation by chronic morphine treatment. Addict Biol, 1996, 1, 49-59. (Pubitemid 126683417)
17. Chen Z, Li T, Zhang B: Morphine postconditioning protects against reperfusion injury in the isolated rat hearts. J Surg Res, 2008, 145, 287-294.
18. Javan M, Ahmadiani A, Motamadi F, Kazemi B: Changes in G proteins genes expression in rat lumbar spinal cord support the inhibitory effect of chronic pain on the development of tolerance to morphine analgesia. Neurosci Res, 2005, 53, 250-256. (Pubitemid 41463778)
19. Jiang X, Shi E, Nakajima Y, Sato S: COX-2 mediates morphine-induced delayed cardioprotection via an iNOS-dependent mechanism. Life Sci, 2006, 78, 2543-2549.
20. Kaplan GB, Sethi RK, McClelland EG, Leite-Morris KA: Regulation of G protein-mediated adenylyl cyclase in striatum and cortex of opiate-dependent and opiate withdrawing mice. Brain Res, 1998, 788, 104-110. (Pubitemid 28202149)
21. Kieffer BL, Evans CJ: Opioid tolerance-in search of the holy grail. Cell, 2002, 108, 587-590. (Pubitemid 34241419)
22. Kindman LA, Kates RE, Ginsburg R: Opioids potentiate contractile response of rabbit myocardium to the β-adrenergic agonist isoproterenol. J Cardiovasc Pharmacol, 1991, 17, 61-67.
23. Law PY, Wong YH, Loh HH: Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol, 2000, 40, 389-430. (Pubitemid 30340688)
24. Lugo-Chinchilla AM, Baez D, Velez M, Ildefonso C, Renaud FL: Altered subcellular signaling in murine peritoneal macrophages upon chronic morphine exposure. J Neuroimmunol, 2006, 176, 86-94. (Pubitemid 44088665)
25. Markiewicz W, Finberg JP, Lichtig C: Morphine increases myocardial infarction size in rats. Anesth Analg, 1982, 61, 843-846. (Pubitemid 12001013)
26. Mattio TG, Kirby ML: Effects of chronic morphine administration on catecholamines and β-adrenergic receptors of the superior cervical ganglion and iris of the rat. Life Sci, 1982, 30, 1435-1442. (Pubitemid 12127788)
27. McPherson BC, Yao Z: Morphine mimics preconditioning via free radical signals and mitochondrial KATP channels in myocytes. Circulation, 2001, 103, 290-295. (Pubitemid 32095417)
28. Minneman KP, Holtzman SG: Morphine dependence and withdrawal without alterations in cerebral b-adrenergic receptor density. Biochem Pharmacol, 1984, 33, 2331-2333. (Pubitemid 14090933)
29. Moises HC, Smith CB: Changes in cortical β-adrenergic receptor density and neuronal sensitivity to norepinephrine accompany morphine dependence and withdrawal. Brain Res, 1987, 400, 110-126. (Pubitemid 17212590)
30. Moises HC, Smith CB: Electrophysiological responsiveness to isoproterenol in rat hippocampal slices correlates with changes in β-adrenergic receptor density induced by chronic morphine treatment. Brain Res, 1989, 485, 67-78. (Pubitemid 19096282)
31. Nalepa I, Zelek-Molik A, Bielawski A, Roman A, Vetulani J: Does the presence of morphine counteract adaptive changes in expression of G-protein a subunits mRNA induced by chronic morphine treatment? Pharmacol Rep, 2007, 59, 34-45. (Pubitemid 46522700)
32. 1D receptors. Eur J Pharmacol, 1999, 368, 259-268.
33. q/11α protein and protein kinase C during the development of sensitization to morphine-induced hyperlocomotion. Neuroscience, 2002, 111, 127-132.
34. Nestler EJ, Berhow MT, Brodkin ES: Molecular mechanisms of drug addiction: adaptations in signal transduction pathways. Mol Psychiatry, 1996, 1, 190-199. (Pubitemid 126441292)
35. Nestler EJ, Erdos JJ, Terwilliger R, Duman RS, Tallman JF: Regulation of G proteins by chronic morphine in the rat locus coeruleus. Brain Res, 1989, 476, 230-239. (Pubitemid 19012591)
36. Nichols CB, Rossow CF, Navedo MF, Westenbroek RE, Catterall WA, Santana LF, McKnight GS: Sympathetic stimulation of adult cardiomyocytes requires association of AKAP5 with a subpopulation of L-type calcium channels. Circ Res, 2010, 107, 747-756.
37. Novotny J, Bourova L, Malkova O, Svoboda P, Kolar F: G proteins, β-adrenoreceptors and β-adrenergic responsiveness in immature and adult rat ventricular myocardium: influence of neonatal hypo- and hyperthyroidism. J Mol Cell Cardiol, 1999, 31, 761-772. (Pubitemid 29201546)
38. Parolaro D, Rubino T, Gori E, Massi P, Bendotti C, Patrini G, Marcozzi C, Parenti M: In situ hybridization reveals specific increases in Gas and Gao mRNA in discrete brain regions of morphine-tolerant rats. Eur J Pharmacol, 1993, 244, 211-222. (Pubitemid 23051243)
39. Peart JN, Gross ER, Gross GJ: Opioid-induced preconditioning: recent advances and future perspectives. Vascul Pharmacol, 2005, 42, 211-218. (Pubitemid 40726324)
40. Peart JN, Gross GJ: Chronic exposure to morphine produces a marked cardioprotective phenotype in aged mouse hearts. Exp Gerontol, 2004, 39, 1021-1026. (Pubitemid 38952882)
41. Peart JN, Hoe LE, Gross GJ, Headrick JP: Sustained ligand-activated preconditioning via d-opioid receptors. J Pharmacol Exp Ther, 2011, 336, 274-281.
42. 2+ handling and arrhythmogenesis. Circ Res, 2011, 108, 871-883.
43. Przewłocka B, Lasoń W, Przewłocki R: The effect of chronic morphine and cocaine administration on the Gs and Go protein messenger RNA levels in the rat hippocampus. Neuroscience, 1994, 63, 1111-1116.
44. Rabadan JV, Milanes MV, Laorden ML: Effects of chronic morphine treatment on catecholamines content and mechanical response in the rat hearts. J Pharmacol Exp Ther, 1997, 280, 32-37. (Pubitemid 27171384)
45. Randich A, Thurston CL, Ludwig PS, Timmerman MR, Gebhart GF: Antinociception and cardiovascular responses produced by intravenous morphine: the role of vagal afferents. Brain Res, 1991, 543, 256-270.
46. Rivera M, Gintzler AR: Differential effect of chronic morphine on mRNA encoding adenylyl cyclase isoforms: relevance to physiological sequela of tolerance/dependence. Brain Res Mol Brain Res, 1998, 54, 165-169. (Pubitemid 28119173)
47. Seo JJ, Lee JW, Lee WK, Hong JT, Lee CK, Lee MK, Oh KW: Inhibitory effects of ginseng total saponin on up-regulation of cAMP pathway induced by repeated administration of morphine. Arch Pharm Res, 2008, 31, 167-170.
48. Shi E, Jiang X, Bai H, Gu T, Chang Y, Wang J: Cardioprotective effects of morphine on rat heart suffering from ischemia and reperfusion. Chin Med J (Engl), 2003, 116, 1059-1062. (Pubitemid 36975160)
49. Schallmach E, Steiner D, Vogel Z: Adenylyl cyclase type II activity is regulated by two different mechanisms: implications for acute and chronic opioid exposure. Neuropharmacology, 2006, 50, 998-1005. (Pubitemid 43794904)
50. Schultz JE, Hsu AK, Gross GJ: Morphine mimics the cardioprotective effect of ischemic preconditioning via a glibenclamide-sensitive mechanism in the rat heart. Circ Res, 1996, 78, 1100-1104.
51. Steiner D, Avidor-Reiss T, Schallmach E, Saya D, Vogel Z: Inhibition and superactivation of the calcium-stimulated isoforms of adenylyl cyclase: role of Gbg dimers. J Mol Neurosci, 2005, 27, 195-203. (Pubitemid 41356400)
52. Walker MJ, Curtis MJ, Hearse DJ, Campbell RW, Janse MJ, Yellon DM, Cobbe SM et al.: The Lambeth Conventions: guidelines for the study of arrhythmias in ischaemia infarction, and reperfusion. Cardiovasc Res, 1988, 22, 447-455.
53. Watts VJ: Molecular mechanisms for heterologous sensitization of adenylate cyclase. J Pharmacol Exp Ther, 2002, 302, 1-7.
54. Zhao H, Loh HH, Law PY: Adenylyl cyclase superactivation induced by long-term treatment with opioid agonist is dependent on receptor localized within lipid rafts and is independent of receptor internalization. Mol Pharmacol, 2006, 69, 1421-1432.
55. Zuurbier CJ, Eerbeek O, Meijer AJ: Ischemic preconditioning, insulin, and morphine all cause hexokinase redistribution. Am J Physiol Heart Circ Physiol, 2005, 289, H496-499. (Pubitemid 40934137)