μ-opioid receptors are located postsynaptically and endomorphin-1 inhibits voltage-gated calcium currents in premotor cardiac parasympathetic neurons in the rat nucleus ambiguus

Neuroscience

Volumn 116, Issue 2, 2003, Pages 573-582

  Irnaten, M ^a   Aicher, S A ^b   Wang, J ^a   Venkatesan, P ^a   Evans, C ^a   Baxi, S ^a   Mendelowitz, D ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Agatoxin; Baroreflex; Bradycardia; Endomorphin; Heart rate; Vagal

Indexed keywords

CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; ENDOMORPHIN 1; ENDOMORPHIN 2; FLUORESCENT DYE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; PERTUSSIS TOXIN;

AMBIGUUS NUCLEUS; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CELL LABELING; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DENDRITE; DRUG EFFECT; ELECTRON MICROSCOPY; HEART INNERVATION; IMMUNOCYTOCHEMISTRY; NEWBORN; NONHUMAN; PARASYMPATHETIC NERVE CELL; PATCH CLAMP; PERIKARYON; POSTSYNAPTIC POTENTIAL; PREMOTOR CORTEX; PRIORITY JOURNAL; RAT; SYNAPSE;

EID: 0037474055     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00657-7     Document Type: Article

References (40)

1. Aghajanian G.K., Wang Y.Y. Pertussis toxin blocks the outward currents evoked by opiate and alpha 2-agonists in locus coeruleus neurons. Brain Res. 371:1986;390-394.
2. Aicher S.A., Sharma S., Pickel V.M. N-methyl-D-aspartate receptors are present in vagal afferents and their dendritic targets in the nucleus tractus solitarius. Neuroscience. 91:1999;119-132.
3. Aicher S.A., Sharma S., Cheng P.Y., Pickel V.M. The N-methyl-D-aspartate (NMDA) receptor is postsynaptic to substance P-containing axon terminals in the rat superficial dorsal horn. Brain Res. 772:1997;71-81.
4. Aicher SA, Mitchell JL, Sharma S, Mendelowitz D (2001a) distribution of mu-opioid receptors in rat visceral premotor neurons. Neuroscience 115:851-860.
5. Aicher S.A., Schreihofer A.M., Kraus J.A., Sharma S., Milner T.A., Guyenet P.G. Mu-opioid receptors are present in functionally identified sympathoexcitatory neurons in the rat rostral ventrolateral medulla. J Comp Neurol. 433:2001;34-47.
6. Ang K.K., McRitchie R.J., Minson J.B., Llewellyn-Smith I.J., Pilowsky P.M., Chalmers J.P., Arnolda L.F. Activation of spinal opioid receptors contributes to hypotension after hemorrhage in conscious rats. Am J Physiol. 276:1999;H1552-H1558.
7. Arvidsson U., Riedl M., Chakrabarti S., Lee J.H., Nakano A.H., Dado R.J., Loh H.H., Law P.Y., Wessendorf M.W., Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci. 15:1995;3328-3341.
8. Batten T.F. Immunolocalization of putative neurotransmitters innervating autonomic regulating neurons (correction of neurones) of cat ventral medulla. Brain Res Bull. 37:1995;487-506.
9. Beck H., Steffens R., Heinemann U., Elger C.E. Properties of voltage-activated Ca2+ currents in acutely isolated human hippocampal granule cells. J Neurophysiol. 77:1997;1526-1537.
10. Burley J.R., Dolphin A.C. Overlapping selectivity of neurotoxin and dihydropyridine calcium channel blockers in cerebellar granule neurones. Neuropharmacology. 39:2000;1740-1755.
11. Ding Y.Q., Kaneko T., Nomura S., Mizuno N. Immunohistochemical localization of mu-opioid receptors in the central nervous system of the rat. J Comp Neurol. 367:1996;375-402.
12. Eisenberg R.M. DAMGO stimulates the hypothalamo-pituitary-adrenal axis through a mu-2 opioid receptor. J Pharmacol Exp Ther. 266:1993;985-991.
13. Ertel E.A., Campbell K.P., Harpold M.M., Hofmann F., Mori Y., Perez-Reyes E., Schwartz A., Snutch T.P., Tanabe T., Birnbaumer L, Tsien R.W., Catterall W.A. Nomenclature of voltage-gated calcium channels. Neuron. 25:2000;533-535.
14. Evans R.G., Ludbrook J., Potocnik S.J. Intracisternal naloxone and cardiac nerve blockade prevent vasodilatation during simulated haemorrhage in awake rabbits. J Physiol. 409:1989;1-14.
15. Garc I.A.C.J., Valdiosera R., Garc I.U. P-type Ca2+ current in crayfish peptidergic neurones. J Exp Biol. 202:1999;429-440.
16. Hamra M., McNeil R.S., Runciman M., Kunze D.L. Opioid modulation of calcium current in cultured sensory neurons Mu-modulation of baroreceptor input . Am J Physiol. 277:1999;H705-H713.
17. Hayar A., Guyenet P.G. Pre- and postsynaptic inhibitory actions of methionine-enkephalin on identified bulbospinal neurons of the rat RVL. J Neurophysiol. 80:1998;2003-2014.
18. Hsu S.M., Raine L. Protein A, avidin, and biotin in immunohistochemistry. J Histochem Cytochem. 29:1981;1349-1353.
19. Kamei J., Zushida K., Ohsawa M., Nagase H. The antinociceptive effects of endomorphin-1 and endomorphin-2 in diabetic mice. Eur J Pharmacol. 391:2000;91-96.
20. Kwok E.H., Dun N.J. Endomorphins decrease heart rate and blood pressure possibly by activating vagal afferents in anesthetized rats. Brain Res. 803:1998;204-207.
21. Larsson K.P., Olsen U.B., Hansen A.J. Nociceptin is a potent inhibitor of N-type Ca(2+) channels in rat sympathetic ganglion neurons. Neurosci Lett. 296:2000;121-124.
22. Laubie M., Schmitt H. Indication for central vagal endorphinergic control of heart rate in dogs. Eur J Pharmacol. 71:1981;401-409.
23. Laubie M., Schmitt H., Vincent M. Vagal bradycardia produced by microinjections of morphine-like drugs into the nucleus ambiguus in anaesthetized dogs. Eur J Pharmacol. 59:1979;287-291.
24. Loewy A., Spyer K. Central regulation of autonomic functions. 1990;Oxford University Press, London.
25. Mansour A., Fox C.A., Thompson R.C., Akil H., Watson S.J. mu-Opioid receptor mRNA expression in the rat CNS Comparison to mu-receptor binding . Brain Res. 643:1994;245-265.
26. Meir A., Ginsburg S., Butkevich A., Kachalsky S.G., Kaiserman I., Ahdut R., Demirgoren S., Rahamimoff R. Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol Rev. 79:1999;1019-1088.
27. Mendelowitz D. Firing properties of identified parasympathetic cardiac neurons in nucleus ambiguus. Am J Physiol. 271:1996;H2609-H2614.
28. Milner T.A., Okada J., Pickel V.M. Monosynaptic input from Leu5-enkephalin-immunoreactive terminals to vagal motor neurons in the nucleus ambiguus Comparison with the dorsal motor nucleus of the vagus . J Comp Neurol. 353:1995;391-406.
29. Morilak D.A., Somogyi P., McIlhinney R.A., Chalmers J. An enkephalin-containing pathway from nucleus tractus solitarius to the pressor area of the rostral ventrolateral medulla of the rabbit. Neuroscience. 31:1989;187-194.
30. Nomura S., Ding Y.Q., Kaneko T., Li J.L., Mizuno N. Localization of mu-opioid receptor-like immunoreactivity in the central components of the vagus nerve A light and electron microscope study in the rat . Neuroscience. 73:1996;277-286.
31. Ohnishi M., Kirkman E., Marshall H.W., Little R.A. Morphine blocks the bradycardia associated with severe hemorrhage in the anesthetized rat. Brain Res. 763:1997;39-46.
32. Pfeiffer-Linn C.L., Lasater E.M. Whole cell and single-channel properties of a unique voltage-activated sustained calcium current identified in teleost retinal horizontal cells. J Neurophysiol. 75:1996;609-619.
33. Sakurada S., Hayashi T., Yuhki M., Orito T., Zadina J.E., Kastin A.J., Fujimura T., Murayama K., Sakurada C., Narita T., Narita M., Suzuki T., Tan-no K., Tseng L.F. Differential antinociceptive effects induced by intrathecally administered endomorphin-1 and endomorphin-2 in the mouse. Eur J Pharmacol. 427:2001;203-210.
34. Venkatesan P., Wang J., Evans C., Irnaten M., Mendelowitz D. Endomorphin -2 inhibits GABAergic inputs to cardiac parasympathetic neurons in the nucleus ambiguus. Neuroscience. 111:2002;699-705.
35. Venkatesan P., Wang J., Evans C., Irnaten M., Mendelowitz D. Nociceptin inhibits gamma-aminobutyric acidergic inputs to cardiac parasympathetic neurons in the nucleus ambiguus. J Pharmacol Exp Ther. 300:2002;78-82.
36. Wang J., Irnaten M., Mendelowitz D. Agatoxin-IVA-sensitive calcium channels mediate the presynaptic and postsynaptic nicotinic activation of cardiac vagal neurons. J Neurophysiol. 85:2001;164-168.
37. Wimpey T.L., Chavkin C. Opioids activate both an inward rectifier and a novel voltage-gated potassium conductance in the hippocampal formation. Neuron. 6:1991;281-289.
38. Wright S.N., Brodwick M.S., Bittner G.D. Presynaptic calcium currents at voltage-clamped excitor and inhibitor nerve terminals of crayfish. J Physiol. 496:(Pt 2):1996;347-361.
39. Xiao R.P., Spurgeon H.A., Capogrossi M.C., Lakatta E.G. Stimulation of opioid receptors on cardiac ventricular myocytes reduces L type Ca2+ channel current. J Mol Cell Cardiol. 25:1993;661-666.
40. Zamir N., Palkovits M., Brownstein M. Distribution of immunoreactive Met-enkephalin-Arg6-Gly7-Leu8 and Leu-enkephalin in discrete regions of the rat brain. Brain Res. 326:1985;1-8.