Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-19T05:58:58.931Z Has data issue: false hasContentIssue false

Cannabinoids and Dopamine Receptors' Action on Calcium Current in Rat Neurons

Published online by Cambridge University Press:  02 December 2014

C. Vásquez*
Affiliation:
Centro Universitario de Investigaciones Biomédicas, Universidad de Colima, Colonia Villa de San Sebastián, Colima, Colima, C.P. 28040, México
R. Navarro-Polanco
Affiliation:
Centro Universitario de Investigaciones Biomédicas, Universidad de Colima, Colonia Villa de San Sebastián, Colima, Colima, C.P. 28040, México
G. Hernández
Affiliation:
Facultad de Enfermeria, Universidad de Colima, Colonia Las Viboras, Colima, Colima, C.P. 28040, Mexico
J. Ruiz
Affiliation:
Facultad de Enfermeria, Universidad de Colima, Colonia Las Viboras, Colima, Colima, C.P. 28040, Mexico
D.G. Guerra
Affiliation:
Facultad de Enfermeria, Universidad de Colima, Colonia Las Viboras, Colima, Colima, C.P. 28040, Mexico
L.M. Baltazar
Affiliation:
Facultad de Medicina, Universidad de Colima, Colonia Las Viboras, Colima, Colima, C.P. 28040, Mexico
M. Huerta
Affiliation:
Centro Universitario de Investigaciones Biomédicas, Universidad de Colima, Colonia Villa de San Sebastián, Colima, Colima, C.P. 28040, México
X. Trujillo
Affiliation:
Centro Universitario de Investigaciones Biomédicas, Universidad de Colima, Colonia Villa de San Sebastián, Colima, Colima, C.P. 28040, México
*
Centro Universitario de Investigaciones Biomédicas, Avenida 25 de julio # 965, Universidad de Colima, Colonia Villa de San Sebastián, Colima, Colima, C.P. 28040, México
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Objective:

To study the effects of cannabinoid, glutamate, and dopamine agonists and antagonists on the calcium current in rat sympathetic neurons.

Methods:

Calcium current was recorded using the whole-cell variant of the patch-clamp technique. After expression in neuronal membranes of the cannabinoid CB1, glutamate mGluR2, or dopamine D1 receptor (by microinjection of the relevant receptor's cDNA into the neuron's nucleus) agonists' and antagonists' effects were observed.

Results:

Applications of agonists of the expressed receptor (0.1-10 µM) decreased the calcium current. The calcium current was increased after application of cannabinoid antagonists (AM251 and AM630); these compounds thus act as inverse agonists in this preparation. Glutamate and dopamine antagonists had no effects on the calcium current by themselves. Combined application of cannabinoids and dopamine, but not glutamate, agonists produced a decrement in the calcium current that was bigger than either of the effects seen when one agonist was applied alone.

Conclusions:

These results suggest that cannabinoid with dopamine receptors have an interactive inhibitory effect on the calcium current in this preparation, indicating that within the nervous system, receptor interactions may be important in the regulation of ion-channel functions.

Résumé:

RÉSUMÉ:Objectif:

Étudier les effets d’agonistes et d’antagonistes de cannabinoïdes, du glutamate et de la dopamine sur le courant calcique dans des neurones sympathiques de rat.

Méthodes:

Le courant calcique a été enregistré au moyen de la technique patch-clamp sur cellules intactes. Des effets agonistes et antagonistes ont été observés après expression dans les membranes neuronales du récepteur cannabinoïde de type CB1, du récepteur métabotropique du glutamate mGluR2 ou du récepteurs D1 de la dopamine par micro injection de l’ADNc correspondant au récepteur dans le noyau du neurone.

Résultats:

L’application d’agonistes du récepteur exprimé (0,1 à 10 mmol) diminuait le courant calcique. Le courant calcique était augmenté suite à l’application d’antagonistes cannabinoïdes tels l’AM251 et l’AM630. Ces substances agissent donc comme des agonistes inverses dans cette préparation. Les antagonistes du glutamate et de la dopamine n’avaient pas d’effet sur le courant calcique par eux-mêmes. Une application combinée d’agonistes de cannabinoïdes et de dopamine diminuait davantage le courant calcique que l’application de chacun d’eux seul, ce qui n’était pas le cas des agonistes du glutamate.

Conclusions:

Ces résultats suggèrent un effet inhibiteur interactif des récepteurs cannabinoïdes et des récepteurs dopaminergiques sur le courant calcique dans cette préparation. Ceci indique que, dans le système nerveux, l’interaction de récepteurs pourrait être importante dans la régulation des fonctions des canaux ioniques.

Type
Experimental Neurosciences
Copyright
Copyright © The Canadian Journal of Neurological 2005

References

1. Matsuda, LA, Lolait, SJ, Brownstein, MJ, Young, AC, Bonner, TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990; 346: 561564.Google Scholar
2. Gifford, AN, Ashby, CR. Electrically evoked acetylcholine release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. J Pharmacol Exp Ther 1996; 277: 14311436.Google Scholar
3. Katona, I, Sperlágh, B, Sík, A, et al. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999; 19: 45444558.Google Scholar
4. Hoffman, AF, Lupica, CR. Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. J Neurosci 2000; 20: 24702479.Google Scholar
5. Kathmann, M, Bauer, U, Schlicker, E, Gothert, M. Cannabinoid CB1 receptor-mediated inhibition of NMDA- and kainate-stimulated noradrenaline and dopamine release in the brain. Naunyn-Schmiedeberg's Arch Pharmacol 1999; 359: 466470.Google Scholar
6. Nakazi, M, Bauer, U, Nickel, T, Kathmann, M, Schlicker, E. Inhibition of serotonin release in the mouse brain via presynaptic cannabinoid CB1 receptors. Naunyn-Schmiedeberg's Arch Pharmacol 2000; 361: 1924.Google Scholar
7. Kim, DJ, Thayer, SA. Activation of CB1 cannabinoid receptors inhibits neurotransmitter release from identified synaptic sites in rat hippocampal cultures. Brain Res 2000; 852: 398405.Google Scholar
8. Pan, X, Ikeda, SR, Lewis, DL. Rat brain cannabinoid receptor modulates N-type Ca2+ channels in a neuronal expression system. Mol Pharmacol 1996; 49: 707714.Google Scholar
9. Twitchell, W, Brown, S, Mackie, K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 1997; 78: 4350.Google Scholar
10. Mackie, K, Lai, Y, Westenbroek, R, Mitchell, R. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 1995; 15: 65526561.Google Scholar
11. Schweitzer, P. Cannabinoids decrease the K+ M-current in hippocampal CA1 neurons. J Neurosci 2000; 20: 5158.CrossRefGoogle Scholar
12. Bidaut-Rusell, M, Howlett, A. Cannabinoid receptor-regulated cyclic AMP accumulation in the rat striatum. J Neurochem 1991; 57: 17691773.Google Scholar
13. Glass, M, Brotchie, JM, Maneuf, YP. Modulation of neurotransmission by cannabinoids in the basal ganglia. Eur J Neurosci 1997; 9: 199203.Google Scholar
14. Glass, M, Felder, CC. Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors augments cAMP accumulation in striatal neurons: evidence for a Gs linkage to the CB1 receptor. J Neurosci 1997; 17: 53275333.CrossRefGoogle Scholar
15. Rawls, SM, Cowan, A, Tallarida, RJ, Geller, EB, Adler, MV. N-methyl-D-aspartate antagonists and WIN 55212-2 [4,5-dihydro-2-methyl-4(4-morpholinylmethyl)-1(1-naphthalenyl-carbonyl)-6H pyrrolo[3,2,1i,j]quinolin-6-one] a cannabinoid agonist, interact to produce synergistic hypothermia. J Pharmacol Exp Ther 2002; 303: 395402.Google Scholar
16. Doherty, J, Dingledine, R. Functional interactions between cannabinoid and metabotropic glutamate receptors in the central nervous system. Curr Opin Pharmacol 2003; 3: 4653.Google Scholar
17. Hamill, OP, Marty, A, Neher, E, Sakmann, B, Sigworth, FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 1981; 391: 85100.Google Scholar
18. Pan, X, Ikeda, SR, Lewis, DL. SR 141716A acts as an inverse agonist to increase neuronal voltage-dependent Ca2+ currents by reversal of tonic CB1 cannabinoid receptor activity. Mol Pharmacol 1998; 54: 10641072.Google Scholar
19. Bouaboula, M, Perrachon, S, Milligan, L, et al. A selective inverse agonist for central cannabinoid receptor inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1. Evidence for a new model of receptor/ligand interactions. J Biol Chem 1997; 272: 2233022339.CrossRefGoogle ScholarPubMed
20. Landsman, RS, Burkey, TH, Consroe, P, Roeske, WR, Yamamura, HI. SR 141716A is an inverse agonist at the human cannabinoid CB1 receptor. Eur J Pharmacol 1997; 334: R1-R2.Google Scholar
21. MacLennan, SJ, Reynen, PH, Kwan, J, Bonhaus, DW. Evidence for inverse agonism of SR 141716A at human recombinant cannabinoid CB1 and CB2 receptors. Br J Pharmacol 1998; 124:619622.CrossRefGoogle ScholarPubMed
22. McAllister, SD, Griffin, G, Satin, LS, Abood, ME. Cannabinoid receptors can activate and inhibit G protein-coupled inwardly rectifying potassium channels in a xenopus oocyte expression system. J Pharmacol Exp Ther 1999; 291: 618626.Google Scholar
23. Bigornia, L, Allen, CN, Jan, CR, et al. D2 dopamine receptors modulate calcium channel currents and catecholamine secretion in bovine adrenal chromaffin cells. J Pharmacol Exp Ther 1990; 252: 586592.Google Scholar
24. Pfeiffer-Linn, C, Lasater, EM. Dopamine modulates in a differential fashion T and L-type calcium currents in bass retinal horizontal cells. J Gen Physiol 1993; 102: 277294.Google Scholar
25. Osipenko, ON, Varnai, O, Mike, A, Spät, A, Bici, E. Dopamine blocks T-type calcium channels in cultured rat adrenal glomerulosa cells. Endocrinology 1994; 134: 511514.CrossRefGoogle ScholarPubMed
26. Surmeier, DJ, Bargas, J, Hemmings, HC Jr, Nairn, AC, Greengard, P. Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron 1995; 14: 385397.Google Scholar
27. Drolet, P, Bilodeau, L, Chorvatova, A, et al. Inhibition of the T-type Ca2+ current by the dopamine D1 receptor in rat adrenal glomerulosa cells: requirement of the combined action of the Gßy protein subunit and cyclic adenosine 3',5'-monophosphate. Mol Endocrinol 1997; 11: 503514.Google Scholar
28. Ikeda, SR, Lovinger, DM, McCool, BA, Lewis, DL. Heterologous expression of metabotropic glutamate receptors in adult rat sympathetic neurons: subtype-specific coupling to ion channels. Neuron 1995; 14: 10291038.Google Scholar
29. Knoflach, F, Woltering, T, Adam, G, Mutel, V, Kemp, JA. Pharmacological properties of native metabotropic glutamate receptors in freshly dissociated Golgi cells of the rat cerebellum. Neuropharmacology 2001; 40: 163169.Google Scholar
30. Chen, WP, Kirchgessner, AL. Activation of group II mGlu receptors inhibits voltage-gated Ca2+ currents in myenteric neurons. Am J Physiol Gastrointest Liver Physiol 2002; 283: G1282-G1289.Google Scholar
31. Plummer, MR, Logothetis, DE, Hess, P. Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron 1989; 2: 14531463.Google Scholar
32. Ikeda, SR. Double-pulse calcium channel current facilitation in adult rat sympathetic neurons. J Physiol 1991; 439: 181214.Google Scholar
33. Barret, CF, Rittenhouse, AR. Modulation of N-type calcium channel activity by G-proteins and protein kinase C. J Gen Physiol 2000; 115: 277286.CrossRefGoogle Scholar
34. Herkenham, M, Lynn, AB, Johnson, MR, et al. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 1991; 11: 563583.Google Scholar
35. Sanudo-Pena, MC, Walker, JM. Effects of intrapallidal cannabinoids on rotational behavior in rats: interactions with the dopaminergic system. Synapse 1998; 28: 2732.Google Scholar
36. Sanudo-Pena, MC, Patrick, SL, Patrick, RL, Walker, JM. Effects of intranigral cannabinoids on rotational behavior in rats: interactions with the dopaminergic system. Neurosci Lett 1996; 206: 2124.Google Scholar
37. Ferraro, L, Tomasini, MC, Gessa, GL, et al. The cannabinoid receptor agonist WIN 55,212-2 regulates glutamate transmission in rat cerebral cortex: an in vivo and in vitro study. Cereb Cortex 2001; 11: 728733.Google Scholar
38. Barbara, JG, Auclair, N, Roisin, MP, et al. Direct and indirect interactions between cannabinoid CB1 receptor and group II metabotropic glutamate receptor signaling in layer V pyramidal neurons from the rat prefrontal cortex. Eur J Neurosci 2003; 17: 981990.Google Scholar
39. Pertwee, R, Griffin, G, Fernando, S. AM630, a competitive cannabinoid receptor antagonist. Life Sci 1995; 56: 19491955.Google Scholar
40. Ross, RA, Brockie, HC, Stevenson, LA, et al. Agonist-inverse agonist characterization at CB1 and CB2 cannabinoid receptors of L759633, L759656, and AM630. Br J Pharmacol 1999; 126:665672.Google Scholar
41. Costa, T, Ogino, Y, Munson, PJ, Onaran, HO, Rodbard, D. Drug efficacy at guanine nucleotide-binding regulatory protein-linked receptors: thermodynamic interpretation of negative antagonism and of receptor activity in the absence of ligand. Mol Pharmacol 1992; 41: 549560.Google Scholar
42. Chidiac, P, Hebert, TE, Valiquette, M, Dennis, M, Bouvier, M. Inverse agonist activity of β-adrenergic antagonists. Mol Pharmacol 1994; 45: 490499.Google Scholar
43. Samama, P, Pei, G, Costa, T, Cotecchia, S, Lefkowitz, RJ. Negative antagonists promote an inactive conformation of the β2-adrenergic receptor. Mol Pharmacol 1994; 45: 390394.Google Scholar
44. Zhou, X, Galligan, JJ. Non-additive interaction between nicotinic cholinergic and P2X purine receptors in guinea-pig enteric neurons in culture. J Physiol 1998; 513: 685697.Google Scholar
45. Schiffmann, SN, Lledo, P-M, Vincent, J-D: Dopamine D1 receptor modulates the voltage gated sodium current in rat striatal neurons through a protein kinase A. J Physiol 1995; 483: 95107.Google Scholar
46. Rodriguez de Fonseca, F, Martin Calderon, JL, Mechoulam, R, Navarro, M. Repeated stimulation of D1 dopamine receptors enhances (-)-11-hydroxy-delta8-tetrahydrocannabinol-dimethyl-heptyl-induced catalepsy in male rats. Neuroreport 1994; 5: 761765.Google Scholar
47. Jarrahian, A, Watts, VJ, Barker, EL. D2 dopamine receptors modulate Ga-subunit coupling of the CB1 cannabinoid receptor. J Pharmacol Exp Ther 2004; 308: 880886.Google Scholar
48. Sanudo-Pena, MC, Force, M, Tsou, K, Miller, AS, Walker, JM. Effects of intrastriatal cannabinoids on rotational behavior in rats: interactions with the dopaminergic system. Synapse 1998; 30: 221226.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
49. Giuffrida, A, Parsons, LH, Kerr, TM, et al. Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 1999; 2: 358363.Google Scholar
50. Cichewicz, DL, Martin, ZL, Smith, FL, Welch, SP. Enhancement of μ opioid antinociception by oral A9-tetrahydrocannabinol: dose-response analysis and receptor identification. J Pharmacol Exp Ther 1999; 289: 859867.Google Scholar
51. Fan, SF, Yazulla, S. Inhibitory interaction of cannabinoid CB1 receptor and dopamine D2 receptor agonists on voltage-gated currents of goldfish cones. Vis Neurosci 2004; 21: 6977.Google Scholar