Identification of μ-and κ-opioid receptors as potential targets to regulate parasympathetic, sympathetic, and sensory neurons within rat intracardiac ganglia

Journal of Comparative Neurology

Volumn 518, Issue 18, 2010, Pages 3836-3847

  Mousa, Shaaban A ^a   Shaqura, Mohammed ^a   Schäper, Jörn ^b   Huang, Wei ^a   Treskatsch, Sascha ^a   Habazettl, Helmut ^a   Abdul Khaliq, Hashim ^c   Schäfer, Michael ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

Intracardiac ganglia; Opioid receptors; Parasympathetic; Sensory nerves; Sympathetic

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; KAPPA OPIATE RECEPTOR; MESSENGER RNA; MU OPIATE RECEPTOR; SUBSTANCE P; TYROSINE 3 MONOOXYGENASE; VESICULAR ACETYLCHOLINE TRANSPORTER;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONFOCAL MICROSCOPY; DRUG TARGETING; GANGLION; GENE EXPRESSION; HEART; HEART ATRIUM; HEART MUSCLE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MALE; NERVE CELL NETWORK; NONHUMAN; PARASYMPATHETIC GANGLION; PRIORITY JOURNAL; PROTEIN ANALYSIS; RADIOASSAY; RAT; REAL TIME POLYMERASE CHAIN REACTION; SAMPLING; SENSORY NERVE CELL; SYMPATHETIC GANGLION; WESTERN BLOTTING; ADRENERGIC NERVE; ANIMAL; CYTOLOGY; GENETICS; IMMUNOHISTOCHEMISTRY; INNERVATION; METABOLISM; PARASYMPATHETIC NERVE; WISTAR RAT;

ADRENERGIC FIBERS; ANIMALS; HEART; IMMUNOHISTOCHEMISTRY; MALE; PARASYMPATHETIC FIBERS, POSTGANGLIONIC; RATS; RATS, WISTAR; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU; RNA, MESSENGER; SENSORY RECEPTOR CELLS;

EID: 77955699774     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22427     Document Type: Article

References (62)

1. Adams DJ, Cuevas J. 2004. Electrophysiological properties of intrinsic cardiac neurons. In: Armour JA, Ardell JL, editors. Basic and clinical neurocardiology. New York: Oxford University Press. p 1-60.
2. Adams DJ, Trequattrini C. 1998. Opioid receptor-mediated inhibition of omega-conotoxin GVIA-sensitive calcium channel currents in rat intracardiac neurons. J Neurophysiol 79: 753-762.
3. Bagnol D, Mansour A, Akil H, Watson SJ. 1997. Cellular localization and distribution of the cloned mu and kappa opioid receptors in rat gastrointestinal tract. Neuroscience 81: 579-591.
4. Barry U, Zuo Z. 2005. Opioids: old drugs for potential new applications. Curr Pharm Des 11:1343-1350.
5. Bell SP, Sack MN, Patel A, Opie LH, Yellon DM. 2000. Delta opioid receptor stimulation mimics ischemic preconditioning in human heart muscle. J Am Coll Cardiol 36: 2296-2302.
6. Bolte C, Newman G, Schultz Jel J. 2009. Hypertensive state, independent of hypertrophy, exhibits an attenuated decrease in systolic function on cardiac kappa-opioid receptor stimulation. Am J Physiol Heart Circ Physiol 296: H967-H975.
7. Brack A, Rittner HL, Machelska H, Shaqura M, Mousa SA, Labuz D, Zöllner C, Schäfer M, Stein C. 2004. Endogenous peripheral antinociception in early inflammation is not limited by the number of opioid-containing leukocytes but by opioid receptor expression. Pain 108:67-75.
8. Brumovsky PR, Shi TJ, Matsuda H, Kopp J, Villar MJ, Hökfelt T. 2002. NPY Y1 receptors are present in axonal processes of DRG neurons. Exp Neurol 174:1-10.
9. Christie MJ, Connor M, Vaughan CW, Ingram SL, Bagley EE. 2000. Cellular actions of opioids and other analgesics: implications for synergism in pain relief. Clin Exp Pharmacol Physiol 27:520-523.
10. Coggeshall RE, Zhou S, Carlton SM. 1997. Opioid receptors on peripheral sensory axons. Brain Res 764:126-132.
11. Dalsgaard C-J, Franco-Cereceda A, Saria A, Lundberg JM, Theodorsson-Norheim E, Hokfelt T. 1986. Distribution and origin of substance P and neuropeptide Y-immunoreactive nerves in the guinea-pig heart. Cell Tissue Res 243: 477-485.
12. Deo SH, Barlow MA, Gonzalez L, Yoshishige D, Caffrey JL. 2008. Cholinergic location of delta-opioid receptors in canine atria and SA node. Am J Physiol Heart Circ Physiol 294:H829-H838.
13. Dickson EW, Hogrefe CP, Ludwig PS, Ackermann LW, Stoll LL, Denning GM. 2008. Exercise enhances myocardial ischemic tolerance via an opioid receptor-dependent mechanism. Am J Physiol Heart Circ Physiol 294: H402-H408.
14. Farias M 3rd, Jackson KE, Yoshishige D, Caffrey JL. 2003. Cardiac enkephalins attenuate vagal bradycardia: interactions with NOS-1-cGMP systems in canine sinoatrial node. Am J Physiol Heart Circ Physiol 284:H1693-H1701.
15. Garzón J, Rodríguez-Munõz M, Sánchez- Blázquez P. 005. Morphine alters the selective association between muopioid receptor and specific RGS proteins in mouse periaqueductal gray matter. Neuropharmacology 48: 853-868.
16. Gibbins IL, Furness JB, Costa M. 1987. Pathway-specific patterns of the co-existence of substance P, calcitonin generelated peptide, cholecystokinin and dynorphin in neurons of the dorsal root ganglia of the guinea-pig. Cell Tissue Res 248:417-437.
17. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy SA. 2002. Third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442-5451.
18. Gray AL, Johnson TA, Ardell JL, Massari VJ. 2004. Parasympathetic control of the heart. II. A novel intergangionic intrinsic circuit mediate neural control of the heart rate. J Appl Physiol 96:2273-2278.
19. Gross GJ. 2003. Role of opioids in in acute and delayed preconditioning. J Mol Cell Cardiol 35:709-718.
20. Hardwick JC, Mawe GM, Parsons RL. 1995. Evidence for afferent fiber innervation of parasympathetic neurons of the guinea-pig cardiac ganglion. J Auton Nerv Syst 53:166.
21. Heglind M, Cederberg A, Aquino J, Lucas G, Ernfors P, Enerbäck S. 2005. Lack of the central nervous system-and neural crest-expressed forkhead gene Foxs1 affects motor function and body weight. Mol Cell Biol 25:5616-5625.
22. Heym C, Klimaschewski L, Borghini N, Fischer-Colbrie R. 1994. Immunohistochemistry of small intensely fluorescent (SIF) cells and of SIF cell-associated nerve fibers in the rat superior cervical ganglion. Microsc Res Techniq 29: 143-150.
23. Huang MH, Wang HQ, Roeske WR, Birnbaum Y, Wu Y, Yang NP, Lin Y, Ye Y, McAdoo DJ, Hughes MG, Lick SD, Boor PJ, Lui CY, Uretsky BF. 2007. Mediating delta-opioid-initiated heart protection via the beta2-adrenergic receptor: role of the intrinsic cardiac adrenergic cell. Am J Physiol Heart Circ Physiol 293:H376-H384.
24. Ji RR, Rupp F. 1997. Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: relationship to c-fos induction. J Neurosci 17: 1776-1785.
25. Jiménez N, Puig MM, Pol O. 2006. Antiexudative effects of opioids and expression of kappa-and delta-opioid receptors during intestinal inflammation in mice: involvement of nitric oxide. J Pharmacol Exp Ther 316:261-270.
26. Jin-Cheng L, Wen Y, Zhao Y, Quan-Yu Z, Shu-Miao Z, Hai-Tao G, Hui B, Yue-Min W, Xin S, Liang C, Qin C, Shi-Qiang Y, Kaye AD, Ding-Hua Y, Jian-Ming P. 2008. Antiarrhythmiceffects of kappa-opiod receptor and its changes in ischemia and reperfusion. Arch Med Res 39: 483-488.
27. Krajnik M, Schäfer M, Sobanski P, Kowalewski J, Bloch-Boguslawska E, Zylicz Z, Mousa SA. 2010. Enkephalin, its precursor, processing enzymes and receptor as part of a local opioid network throughout the respiratory system of lung cancer patients. Hum Pathol 41:632-642.
28. Krajnik M, Podolec Z, Siekierka M, Sykutera M, Pufal E, Sobanski P, Makarewicz R, Neef C, Punt N, Zylicz Z. 2009. Morphine inhalation by cancer patients: a comparison of different nebulization techniques using pharmacokinetic, spirometric, and gasometric parameters. J Pain Symptom Manag 38:747-757.
29. Ledda F, Mantelli L, Corti V, Fantozzi R. 1984. Inhibition of the cardiac response to sympathetic nerve stimulation byopioid peptides and its potentiation by morphine and methadone. Eur J Pharmacol 102:443-450.
30. Ledda F, Mantelli L, Corti V. 1985. Sensitivity to dynorphin-(1-13) of the presynaptic inhibitory opiate receptors of the guinea-pig heart. Eur J Pharmacol 117:377-380.
31. Mahler DA, Murray JA, Waterman LA, Ward J, Kraemer WJ, Zhang X, Baird JC. 2009. Endogenous opioids modify dyspnoea during treadmill exercise in patients with COPD. Eur Respir J 33:771-777.
32. Mansour A, Burke S, Pavlic RJ, Akil H, Watson SJ. 1996. Immunohistochemical localization of the cloned kappa 1 receptor in the rat CNS and pituitary. Neuroscience 71: 671-690.
33. McMahan UJ, Purves D. 1976. Visual identification of two kinds of nerve cells and their synaptic contacts in a livingautonomic ganglion of the mudpuppy (Necturus maculosus). J Physiol 254:405-425.
34. Montel H, Starke K. 1973. Effects of narcotic analgesics and their antagonists on the rabbit isolated heart and its adrenergic nerves. Br J Pharmacol 49:628-641.
35. Mousa SA, Straub RH, Schäfer M, Stein C. 2007a. Beta-endorphin, Met-enkephalin and corresponding opioid receptors within synovium of patients with joint trauma, osteoarthritis and rheumatoid arthritis. Ann Rheum Dis 66:871-879.
36. Mousa SA, Cheppudira BP, Shaqura M, Fischer O, Hofmann J, Hellweg R, Schäfer M. 2007b. Nerve growth factor governs the enhanced ability of opioids to suppress inflammatory pain. Brain 130:502-513.
37. Mousa SA, Krajnik M, Sobanski P, Kowalewski J, Bloch-Boguslawska E, Zylicz Z, Schäfer M. 2010. Dynorphin expression, processing and receptors in the alveolar macrophages, cancer cells and bronchial epithelium of lung cancer patients. Histol Histopathol 25:755-764.
38. Musha T, Satoh E, Koyanagawa H, Kimura T, Satoh S. 1989. Effects of opioid agonists on sympathetic and parasympathetic transmission to the dog heart. J Pharmacol Exp Ther 250:1087-1091.
39. Papka RE, Urban L. 1987. Distribution, origin and sensitivity to capsaicin of primary afferent substance P-immunoreactive nerves in the heart. Acta Physiol Hung 69:459-468.
40. Pardini BJ, Patel KP, Schmid PG, Lund DD. 1987. Location, distribution and projections of intracardiac ganglion cells in the rat. J Auton Nerv Syst 20:91-101.
41. Puehler W, Zöllner C, Brack A, Shaqura MA, Krause H, Schäfer M, Stein C. 2004. Rapid up-regulation of mu opioid receptor mRNA in dorsal root ganglia in response to peripheralinflammation depends on neuronal conduction, Neuroscience 129:473-479.
42. Puehler W, Rittner HL, Mousa SA, Brack A, Krause H, Stein C, Schäfer M. 2006. Interleukin-1 beta contributes to the upregulation of kappa opioid receptor mrna in dorsal root ganglia in response to peripheral inflammation. Neuroscience 141:551-1100.
43. Samaco RC, Mandel-Brehm C, Chao HT, Ward CS, Fyffe-Maricich SL, Ren J, Hyland K, Thaller C, Maricich SM, Humphreys P, Greer JJ, Percy A, Glaze DG, Zoghbi HY, Neul JL. 2009. Loss of MeCP2 in aminergic neurons causes cell-autonomous defects in neurotransmitter synthesis and specific behavioral abnormalities. Proc Natl Acad Sci U S A 106:21966-21971.
44. Sampaio KN, Mauad H, Spyer KM, Ford TW. 2003. Differential chronotropic and dromotropic responses to focal stimulation of cardiac vagal ganglia in the rat. Exp Physiol 88: 315-327.
45. Schäfer M. 2010. Mechanisms of actions of opioids. In: Evers AS, Maze M, editors. Anesthetic pharmacology: physiologic principles and clinical practice. New York: Cambridge University Press (in press).
46. Schultz JE, Gross GJ. 2001. Opioids and cardioprotection. Pharmacol Ther 89:123-137.
47. Schulz S, Schreff M, Nüss D, Gramsch C, Höllt V. 1996. Nociceptin/orphanin FQ and opioid peptides show overlapping distribution but not co-localization in pain-modulatory brain regions. Neuroreport 7:3021-3025.
48. Shaqura MA, Zöllner C, Mousa SA, Stein C, Schäfer M. 2003. Characterization of mu opioid receptor binding and G protein coupling in rat hypothalamus, spinal cord, and primary afferent neurons during inflammatory pain. J Pharmacol Exp Ther 308:712-718.
49. Singh S, Johnson PI, Lee RE, Orfei E, Lonchyna VA, Sullivan HJ, Montoya A, Tran H, Wehrmacher WH, Wurster RD. 1996. Topography of cardiac ganglia in the adult human heart. J Thorac Cardiovasc Surg 112:943-953.
50. Starke K, Schöffel E, Illes P. 1985. The sympathetic axons innervating the sinus node of the rabbit possess presynaptic opioid kappa-but not mu-or delta-receptors. Naunyn Schmiedebergs Arch Pharmacol 329:206-209.
51. Steele PA, Gibbins IL, Morris JL, Mayer B. 1994. Multiple populations of neuropeptide-containing intrinsic neurons in the guinea-pig heart. Neuroscience 62:241-250.
52. Steele PA, Aromataris EC, Riederer BM. 1996. Endogenous opioid peptides in parasympathetic, sympathetic and sensory nerves in the guinea-pig heart. Cell Tissue Res 284:331-339.
53. Ventura C, Pintus G, Tadolini B. 1998. Opioid peptide gene expression in the myocardial cell. Trends Cardiovasc Med 8:102-110.
54. Verma-Gandhu M, Verdu EF, Bercik P, Blennerhassett PA, Al-Mutawaly N, Ghia JE, Collins SM. 2007. Visceral pain perception is determined by the duration of colitis and associated neuropeptide expression in the mouse. Gut 56:358-364.
55. Weems HB, Chalecka-Franaszek E, Côté TE. 1996. Solubilization of high-affinity, guanine nucleotide-sensitive mu-opioid receptors from rat brain membranes. J Neurochem 66: 1042-1050.
56. Wilson SP, Klein RL, Chang KJ, Gasparis MS, Viveros OH, Yang WH. 1980. Are opioid peptides co-transmitters in noradrenergic vesicles of sympathetic nerves? Nature 288: 707-709.
57. Wittert G, Hope P, Pyle D. 1996. Tissue distribution of opioid receptor gene expression in the rat. Biochem Biophys Res Commun 218:877-881.
58. Wong-Dusting HK, Rand MJ. 1985. Effect of [D-Ala2,Met5]enkephalinamide and [D-Ala2,D-Leu5]enkephalin on cholinergic and noradrenergic neurotransmission in isolated atria. Eur J Pharmacol 111:65-72.
59. Yasuhara O, Aimi Y, Matsuo A, Kimura H. 2008. Distribution of a splice variant of choline acetyltransferase in the trigeminal ganglion and brainstem of the rat: comparison with calcitonin gene-related peptide and substance P. J Comp Neurol 509:436-448.
60. Zimlichman R, Gefel D, Eliahou H, Matas Z, Rosen B, Gass S, Ela C, Eilam Y, Vogel Z, Barg J. 1996. Expression of opioid receptors during heart ontogeny in normotensive and hypertensive rats. Circulation 93:1020-1025.
61. Zöllner C, Shaqura MA, Bopaiah CP, Mousa S, Stein C, Schafer M. 2004. Painful inflammation-induced increase in muopioid receptor binding and G-protein coupling in primary afferent neurons. Mol Pharmacol 64:202-210.
62. Zöllner C, Mousa SA, Fischer O, Rittner HL, Shaqura M, Brack A, Shakibaei M, Binder W, Urban F, Stein C, Schäfer M. 2008. Chronic morphine use does not induce peripheral tolerance in a rat model of inflammatory pain. J Clin Invest 118:1065-1073.