Skip to main content
Log in

Prejunctional opioid μ-receptors and adenosine A1-receptors on the sympathetic nerve endings of the rat tail artery interact with the α2-adrenoceptors

  • Published:
Naunyn-Schmiedeberg's Archives of Pharmacology Aims and scope Submit manuscript

Summary

Experiments were designed to study the interaction between prejunctional α2-adrenoceptors and both adenosine and opioid receptors at the postganglionic sympathetic nerve endings innervating the tail artery of the rat. Segments of this vessel were preincubated with [3H]-noradrenaline and then perfused/superfused with [3H]-noradrenaline-free medium. Their perivascular nerves were field stimulated with standard stimulation parameters: 24 pulses at 0.4 Hz, 0.3 ms, 200 mA. In some experiments, the stimulation parameters were adjusted in order to obtain similar reference release values despite the presence of a first release-modulating drug.

The adenosine agonist 5′-N-ethylcarboxamidoadenosine (NECA; 0.3–10 μmol/l) and [D-Ala2,MePhe4,Glyol5]enkephalin (DAGO; 0.3–10 μmol/l) depressed the stimulation-evoked overflow of tritium in a concentration dependent manner. The release-inhibiting effect of both NECA and DAGO was enhanced in the presence of the α2-adrenoceptor antagonist rauwolscine (3 μmol/l) while it was attenuated in the presence of the α2-adrenoceptor agonist 5-bromo-6-[2-imidazolin-2yl-aminol-quinoxaline (UK-14,304; 0.1 μmol/l). These changes occurred both at standard and adjusted stimulation parameters.

These results demonstrate that the prejunctional adenosine A1- and opioid μ-receptors interact with the prejunctional α2-adrenoceptors. The level at which these interactions take place (receptors themselves or transduction mechanisms) as well as the physiological significance of the phenomenon remain to be determined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allgaier C, Hertting G, Kügelgen OV (1987) The adenosine receptor-mediated inhibition of noradrenaline release possibly involves a N-protein and is increased by α2-adrenoceptor blockade. Br J Pharmacol 90:403–412

    Google Scholar 

  • Allgaier C, Daschmann B, Sieverling J, Hertting G (1989a) Presynaptic κ-receptors on noradrenergic nerve terminals couple to G protein and interact with the α2-adrenoceptors. J Neurochem 53:1629–1635

    Google Scholar 

  • Allgaier C, Jäger T, Hertting G (1989 b) Endogenous noradrenaline impairs the prostaglandin-induced inhibition of noradrenaline release. Naunyn-Schmiedeberg's Arch Pharmacol 340:472–474

    Google Scholar 

  • Bals-Kubik R, Shippenberg TS, Herz A (1990) Involvement of central μ and δ opiod receptors in mediating the reinforcing effects of β-endorphin in the rat. Eur J Pharmacol 175:63–69

    Google Scholar 

  • Bruns RF, Lu GH, Pugsley TA (1986) Adenosine receptor subtypes: binding studies. In: Gerlach E, Becker BF (eds) Perspectives in adenosine research. Springer, Berlin Heidelberg New York, pp 59–73

    Google Scholar 

  • Bucher B, Stoclet J-C, Illes P (1988) Further evidence for the existence of a homogenous β-endorphin-sensitive receptor population in the rat tail artery. Eur J Pharmacol 147:305–308

    Google Scholar 

  • Budai D, Duckles SP (1989) Opioid-induced prejunctional inhibition of vasoconstriction in the rabbit ear artery: alpha-2 adrenoceptor activation and external calcium. J Pharmacol Exp Ther 251:497–501

    Google Scholar 

  • Cambridge D (1981) UK-14,304, a potent and selective α2-agonist for the characterisation of α-adrenoceptor subtypes. Eur J Pharmacol 72:413–415

    Google Scholar 

  • Enero MA, Saidman BQ (1977) Possible feed-back inhibition of noradrenaline release by purine compounds. Naunyn-Schmiedeberg's Arch Pharmacol 297:39–46

    Google Scholar 

  • Gan EA, Duckles SP (1988) Comparison of the pre-junctional effect of opioids in the blood vessels of the rabbit. Eur J Pharmacol 158:21–28

    Google Scholar 

  • Garzon J, Schulz R, Herz A (1985) Evidence for the ε-type of opioid receptor in the rat vas deferens. Mol Pharmacol 28:1–9

    Google Scholar 

  • Handa BK, Lane AC, Lord JAI, Morgan BA, Rance MJ, Smith CFC (1981) Analogues of β-LPH61–64 possessing selective agonist activity at μ-opiate receptors. Eur J Pharmacol 70:531–540

    Google Scholar 

  • Hedqvist P (1974) Prostaglandin action on noradrenaline release and mechanical responses in the stimulated guinea pig vas deferens. Acta Physiol Scand 90:86–93

    Google Scholar 

  • Illes P, Nörenberg W (1990) Blockade of α2-adrenoceptors increases opioid μ-receptor-mediated inhibition of the firing rate of rat locus coeruleus neurones. Naunyn-Schmeedberg's Arch Pharmacol 342:490–496

    Google Scholar 

  • Illes P, Bettermann R, Brod I, Bucher B (1987) β-Endorphin-sensitive opioid receptors in the rat tail artery. Naunyn-Schmiedeberg's Arch Pharmacol 335:420–427

    Google Scholar 

  • Illes P, Rickmann H, Brod I, Bucher B, Stoclet J-C (1989) Subsensitivity of presynaptic adenosine A1-receptors in caudal arteries of spontaneously hypertensive rats. Eur J Pharmacol 174:237–251

    Google Scholar 

  • Jackisch R, Geppert M, Illes P (1986) Characterization of opioid receptors modulating noradrenaline release in the hippocampus of the rabbit. J Neurochem 46:1802–1810

    Google Scholar 

  • Langer SZ (1981) Presynaptic regulation of the release of catecholamines. Pharmacol Rev 32:337–362

    Google Scholar 

  • Limberger N, Späth L, Hölting Th, Starke K (1986) Mutual interaction between presynaptic α2-adrenoceptors and opioid κ-receptors at the noradrenergic axons of rabbit brain cortex. Naunyn-Schmiedeberg's Arch Pharmacol 334:166–171

    Google Scholar 

  • Limberger N, Singer EA, Starke K (1988a) Only activated but not non-activated presynaptic α2-adrenoceptors interfere with neighbouring presynaptic receptor mechanisms. Naunyn-Schmiedeberg's Arch Pharmacol 338:62–67

    Google Scholar 

  • Limberger N, Späth L, Starke K (1988b) Presynaptic α2-adrenoceptor, opioid κ-receptor and adenosine A1-receptor interactions on noradrenaline release in rabbit brain cortex. Naunyn-Schmiedeberg's Arch Pharmacol 338:53–61

    Google Scholar 

  • Lipscombe D, Kongsamut S, Tsien RW (1989) α-Adrenergic inhibition of sympathetic neurotransmitter release mediated by modulation of N-type calcium-channel gating. Nature 340: 639–642

    Google Scholar 

  • Loiacono RE, Rand MJ, Story DF (1985) Interaction between the inhibitory action of acetylcholine and the α-adrenoceptor autoinhibitory feedback system on release of [3H]-noradrenaline from rat atria and rabbit ear artery. Br J Pharmacol 84:697–705

    Google Scholar 

  • Majewski H, Rand MJ (1981) An interaction between prejunctional α-adrenoceptors and prejunctional β-adrenoceptors. Eur J Pharmacol 69:493–498

    Google Scholar 

  • Massingham R, Dubocovich ML, Langer SZ (1980) The role of presynaptic receptors in the cardiovascular actions of N,N-di-n-propyldopamine in the cat and dog. Naunyn-Schmiedeberg's Arch Pharmacol 314:17–28

    Google Scholar 

  • Molderings GJ, Göthert M (1990) Mutual interaction between presynaptic α2-adrenoceptors and 5-HT1B receptors on the sympathetic nerve terminals of the rat inferior vena cava. Naunyn-Schmiedeberg's Arch Pharmacol 341:391–397

    Google Scholar 

  • Paterson SJ, Robson LE, Kosterlitz HW (1983) Classification of opioid receptors. Br Med Bull 39:31–36

    Google Scholar 

  • Ramme D, Illes P, Späth L, Starke K (1986) Blockade of α2-adrenoceptors permits the operation of otherwise silent κ-receptors at the sympathetic axons of rabbit jejunal arteries. Naunyn-Schmiedeberg's Arch Pharmacol 334:48–55

    Google Scholar 

  • Schoffelmeer ANM, Putters J, Mulder AH (1986) Activation of presynaptic α2-adrenoceptors attenuates the inhibitory effect of μ-opioid receptor agonists on noradrenaline release from brain slices. Naunyn-Schmiedeberg's Arch Pharmacol 333:377–380

    Google Scholar 

  • Schoffelmeer ANM, Yao YH, Simon EJ (1989) Cross-linking of human 125I-β-endorphin to a μ-δ opioid receptor complex in rat striatum. Eur J Pharmacol 166:357–358

    Google Scholar 

  • Schulz R, Wüster M, Herz A (1981) Pharmacological characterization of the ε-opiate receptor. J Pharmacol Exp Ther 216:604–606

    Google Scholar 

  • Shook JE, Kazmierski W, Wire WS, Lemcke PK, Hruby VJ, Burks TF (1988) Opioid receptor selectivity of β-endorphin in vitro and in vivo: mu, delta and epsilon receptors. J Pharmacol Exp Ther 246:1018–1025

    Google Scholar 

  • Starke K (1981) Presynaptic receptors. Ann Rev Pharmacol Toxicol 21:7–30

    Google Scholar 

  • Starke K, Göthert M, Kilbinger H (1989) Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol Rev 69:864–989

    Google Scholar 

  • Weitzell R, Tanaka T, Starke K (1979) Pre- and postsynaptic effects of yohimbine stereoisomers on noradrenaline transmission in the pulmonary artery of the rabbit. Naunyn-Schmiedeberg's Arch Pharmacol 308:127–136

    Google Scholar 

  • Williams M (1987) Purine receptors in mammalian tissues: pharmacology and functional significance. Ann Rev Pharmacol Toxicol 27:315–345

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Send offprint requests to B. Bucher at the above address

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bucher, B., Corriu, C. & Stoclet, J.C. Prejunctional opioid μ-receptors and adenosine A1-receptors on the sympathetic nerve endings of the rat tail artery interact with the α2-adrenoceptors. Naunyn-Schmiedeberg's Arch Pharmacol 345, 37–43 (1992). https://doi.org/10.1007/BF00175467

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00175467

Key words

Navigation