Opioid modulation of GABA release in the rat inferior colliculus
Tóm tắt
The inferior colliculus, which receives almost all ascending and descending auditory signals, plays a crucial role in the processing of auditory information. While the majority of the recorded activities in the inferior colliculus are attributed to GABAergic and glutamatergic signalling, other neurotransmitter systems are expressed in this brain area including opiate peptides and their receptors which may play a modulatory role in neuronal communication. Using a perfusion protocol we demonstrate that morphine can inhibit KCl-induced release of [3H]GABA from rat inferior colliculus slices. DAMGO ([D-Ala(2), N-Me-Phe(4), Gly(5)-ol]-enkephalin) but not DADLE ([D-Ala2, D-Leu5]-enkephalin or U69593 has the same effect as morphine indicating that μ rather than δ or κ opioid receptors mediate this action. [3H]GABA release was diminished by 16%, and this was not altered by the protein kinase C inhibitor bisindolylmaleimide I. Immunostaining of inferior colliculus cryosections shows extensive staining for glutamic acid decarboxylase, more limited staining for μ opiate receptors and relatively few neurons co-stained for both proteins. The results suggest that μ-opioid receptor ligands can modify neurotransmitter release in a sub population of GABAergic neurons of the inferior colliculus. This could have important physiological implications in the processing of hearing information and/or other functions attributed to the inferior colliculus such as audiogenic seizures and aversive behaviour.
Tài liệu tham khảo
Jones EG: Chemically defined parallel pathways in the monkey auditory system. Ann N Y Acad Sci. 2003, 999: 218-33. 10.1196/annals.1284.033.
Musiek FE, Hoffman DW: An introduction to the functional neurochemistry of the auditory system. Ear Hear. 1990, 11: 395-402.
McAlpine D, Palmer AR: Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J Neurosci. 2002, 22: 1443-1453.
Pollak GD, Burger RM, Park TJ, Klug A, Bauer EE: Roles of inhibition for transforming binaural properties in the brainstem auditory system. Hear Res. 2002, 168: 60-78. 10.1016/S0378-5955(02)00362-3.
Garcia-Cairasco N: A critical review on the participation of inferior colliculus in acoustic-motor and acoustic-limbic networks involved in the expression of acute and kindled audiogenic seizures. Hear Res. 2002, 168: 208-22. 10.1016/S0378-5955(02)00371-4.
Troncoso AC, Osaki MY, Mason S, Borelli KG, Brandao ML: Apomorphine enhances conditioned responses induced by aversive stimulation of the inferior colliculus. Neuropsychopharmacology. 2003, 28: 284-91. 10.1038/sj.npp.1300034.
Kalyuzhny AE, Dooyema J, Wessendorf MW: Opioid-and GABA(A)-receptors are co-expressed by neurons in rat brain. Neuroreport. 2000, 11: 2625-2628.
Mackay KB, McCulloch J: Distribution of effects of the kappa-opioid agonist CI-977 on cerebral glucose utilization in rat brain. Brain Res. 1994, 642: 160-168. 10.1016/0006-8993(94)90918-0.
DePaoli AM, Hurley KM, Yasada K, Reisine T, Bell G: Distribution of kappa opioid receptor mRNA in adult mouse brain: an in situ hybridization histochemistry study. Mol Cell Neurosci. 1994, 5: 327-335. 10.1006/mcne.1994.1039.
Gouarderes C, Tellez S, Tafani JA, Zajac JM: Quantitative autoradiographic mapping of delta-opioid receptors in the rat central nervous system using [125I][D.Ala2]deltorphin-I. Synapse. 1993, 13: 231-240.
Mansour A, Fox CA, Thompson RC, Akil H, Watson SJ: mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res. 1994, 643: 245-265.
Jordan BA, Cvejic S, Devi LA: Opioids and their complicated receptor complexes. Neuropsychopharmacology. 2000, 23 (4 Suppl): S5-S18. 10.1016/S0893-133X(00)00143-3.
Calo' G, Rizzi A, Bigoni R, Guerrini R, Salvadori S, Regoli D: Pharmacological profile of nociceptin/orphanin FQ receptors. Clin Exp Pharmacol Physiol. 2002, 29: 223-228. 10.1046/j.1440-1681.2002.03633.x.
Miller RJ: Presynaptic receptors. Annu Rev Pharmacol Toxicol. 1998, 38: 201-227. 10.1146/annurev.pharmtox.38.1.201.
Vaughan CW, Ingram SL, Connor MA, Christie MJ: How opioids inhibit GABA-mediated neurotransmission. Nature. 1997, 390: 611-614. 10.1038/37610.
Capogna M, Gahwiler BH, Thompson SM: Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J Physiol. 1993, 470: 539-558.
Phansuwan-Pujito P, Saleema L, Mukda S, Tongjaroenbuangam W, Jutapakdeegul N, Casalotti SO, Forge A, Dodson H, Govitrapong P: The opioid receptors in inner ear of different stages of postnatal rats. Hear Res. 2003, 184: 1-10. 10.1016/S0378-5955(03)00163-1.
Jongkamonwiwat N, Phansuwan-Pujito P, Sarapoke P, Chetsawang B, Casalotti SO, Forge A, Dodson H, Govitrapong P: The presence of opioid receptors in rat inner ear. Hear Res. 2003, 181: 85-93. 10.1016/S0378-5955(03)00175-8.
Lefkowitz RJ, Caron MG: Ciba-Geigy award for outstanding research. Regulation of adrenergic receptor function by phosphorylation. J Mol Cell Cardiol. 1986, 18: 885-895.
Tang H, Shirai H, Inagami T: Inhibition of protein kinase C prevents rapid desensitization of type 1B angiotensin II receptor. Circ Res. 1995, 77: 239-48.
Mela F, Marti M, Ulazzi L, Vaccari E, Zucchini S, Trapella C, Salvadori S, Beani L, Bianchi C, Morari M: Pharmacological profile of nociceptin/orphanin FQ receptors regulating 5-hydroxytryptamine. Eur J Neurosci. 2004, 19: 1317-1324. 10.1111/j.1460-9568.2004.03220.x.
Smith FL, Javed RR, Elzey MJ, Dewey WL: The expression of a high level of morphine antinociceptive tolerance in mice involves both PKC and PKA. Brain Res. 2003, 985: 78-88. 10.1016/S0006-8993(03)03170-6.
Liu JG, Anand KJ: Protein kinases modulate the cellular adaptations associated with opioid tolerance and dependence. Brain Res Brain Res Rev. 2001, 38: 1-19. 10.1016/S0165-0173(01)00057-1.
Rodriguez JJ, Mackie K, Pickel VM: Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat Caudate putamen nucleus. J Neurosci. 2001, 21: 823-33.
Muzio L, DiBenedetto B, Stoykova A, Boncinelli E, Gruss P, Mallamaci A: Conversion of cerebral cortex into basal ganglia in Emx2(-/-) Pax6(Sey/Sey) double-mutant mice. Nat Neurosci. 2002, 5: 737-745.
Neal MJ, Cunningham JR, Dent Z: Modulation of extracellular GABA levels in the retina by activation of glial P2X-purinoceptors. Br J Pharmacol. 1998, 124: 317-22.