Synergistic activity between the delta-opioid agonist SNC80 and amphetamine occurs via a glutamatergic NMDA-receptor dependent mechanism

Neuropharmacology

Volumn 77, Issue , 2014, Pages 19-27

  Bosse, Kelly E ^a,c   Jutkiewicz, Emily M ^a   Schultz Kuszak, Kristin N ^b,d   Mabrouk, Omar S ^b   Kennedy, Robert T ^a,b   Gnegy, Margaret E ^a   Traynor, John R ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MEDIMMUNE   (United States)

Author keywords

Amphetamine; Delta opioid receptor; Dopamine; GABA; Glutamate; SNC80

Indexed keywords

2 HYDROXYSACLOFEN; 4 [ALPHA (4 ALLYL 2,5 DIMETHYL 1 PIPERAZINYL) 3 METHOXYBENZYL] N,N DIETHYLBENZAMIDE; AMPHETAMINE; CALCIUM ION; DELTA OPIATE RECEPTOR; DIZOCILPINE; GLUTAMIC ACID; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN TISSUE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC TRANSMISSION; EXTRACELLULAR SPACE; GABAERGIC TRANSMISSION; HYPERACTIVITY; LOCOMOTION; MALE; NEUROMODULATION; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

AMPHETAMINE; DELTA OPIOID RECEPTOR; DOPAMINE; GABA; GLUTAMATE; SNC80;

AMPHETAMINE; ANALGESICS, OPIOID; ANIMALS; BENZAMIDES; CORPUS STRIATUM; DIZOCILPINE MALEATE; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; DRUG SYNERGISM; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; MOTOR ACTIVITY; PIPERAZINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, OPIOID, DELTA;

EID: 84885447796     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.08.027     Document Type: Article

References (60)

1. B. Bie, W. Zhu, and Z.Z. Pan Rewarding morphine-induced synaptic function of δ- opioid receptors on central glutamate synapses J. Pharmacol. Exp. Ther. 329 2009 290 296
2. F. Billet, N. Dourmap, and J. Costentin Involvement of corticostriatal glutamatergic terminals in striatal dopamine release elicited by stimulation of delta-opioid receptors Eur. J. Neurosci. 20 2004 2629 2638 (Pubitemid 39573778)
3. F. Billet, J. Costentin, and N. Dourmap Influence of corticostriatal δ-opioid receptors on abnormal involuntary movements induced by L-DOPA in hemiparkinsonian rats Exp. Neurol. 236 2012 339 350
4. K.B. Bosse, E.M. Jutkiewicz, M.E. Gnegy, and J.R. Traynor The selective delta opioid agonist SNC80 enhances amphetamine-mediated efflux of dopamine from rat striatum Neuropharmacology 55 2008 755 762
5. J.J. Bouyer, R.J. Miller, and V.M. Pickel Ultrastructural relation between cortical efferents and terminals containing enkephalin-like immunoreactivity in rat neostriatum Regul. Pept. 8 1984 105 115 (Pubitemid 14131756)
6. M.T. Bowser, and R.T. Kennedy In vivo monitoring of amine neurotransmitters using microdialysis with on-line capillary electrophoresis Electrophoresis 22 2001 3668 3676 (Pubitemid 32998598)
7. 3H]dopamine from striatal slices J. Pharmacol. Exp. Ther. 257 1991 262 270
8. M.R. Brandt, S.S. Negus, N.K. Mello, M.S. Furness, X. Zhang, and K.C. Rice Discriminative stimulus effects of the nonpeptidic delta-opioid agonist SNC80 in rhesus monkeys J. Pharmacol. Exp. Ther. 290 1999 1157 1164 (Pubitemid 29400256)
9. M. Carlsson, and A. Carlsson Interactions between glutamatergic and monoaminergic systems within the basal ganglia - implications for schizophrenia and Parkinson's disease Trends Neurosci. 13 1990 272 276 (Pubitemid 20193457)
10. A.G. Chapman Glutamate receptors in epilepsy Prog. Brain Res. 116 1998 371 383 (Pubitemid 28526947)
11. L. Churchill, and P.W. Kalivas Dopamine depletion produces augmented behavioral responses to a mu- but not a delta-opioid receptor agonist in the nucleus accumbens: lack of a role for receptor upregulation Synapse 11 1992 47 57
12. J.L. Cornish, P. Duffy, and P.W. Kalivas A role for nucleus accumbens glutamate transmission in the relapse to cocaine-seeking behavior Neuroscience 93 1999 1359 1567
13. 2+ dependence of membrane resistance increases evoked by NMDA in hippocampal neurons Brain Res. 311 1984 392 396 (Pubitemid 14023396)
14. G.P. Do Carmo, J.E. Folk, K.C. Rice, E. Chartoff, W.A. Carlezon Jr., and S.S. Negus The selective non-peptidic delta opioid agonist SNC80 does not facilitate intracranial self-stimulation in rats Eur. J. Pharmacol. 604 2009 58 65
15. N. Dourmap, and J. Costentin Involvement of glutamate receptor in the striatal enkephalin-induced dopamine release Eur. J. Pharmacol. 253 1994 R9 R11
16. J.P. Druhan, H. Rajabi, and J. Stewart MK-801 increases locomotor activity without elevating extracellular dopamine levels in the nucleus accumbens Synapse 24 1996 135 146 (Pubitemid 26339306)
17. K.N. Gracy, and V.M. Pickel Ultrastructural immunocytochemical localization of the N-methyl-D-aspartate receptor and tyrosine hydroxylase in the shell of the rat nucleus accumbens Brain Res. 739 1996 169 181 (Pubitemid 26387375)
18. C. Heidbreder, M. Shoaib, and T.S. Shippenberg Differential role of delta-opioid receptors in the development and expression of behavioral sensitization to cocaine Eur. J. Pharmacol. 298 1996 207 216
19. + and A23187 J. Biol. Chem. 263 1988 9292 9297
20. Z.G. Jiang, and R.A. North Pre- and postsynaptic inhibition of opioids in rat striatum J. Neurosci. 12 1992 356 361
21. D.N. Jones, W.D. Bowen, P.S. Portoghese, and S.G. Holtzman Delta-opioid receptor antagonists attenuate motor activity induced by amphetamine but not cocaine Eur. J. Pharmacol. 249 1993 167 177
22. D.N. Jones, and S.G. Holtzman Interaction between opioid antagonists and amphetamine: evidence for mediation by central delta opioid receptors J. Pharmacol. Exp. Ther. 262 1992 638 645
23. E.M. Jutkiewicz, K.C. Rice, and J.H. Woods The delta-opioid receptor agonist SNC80 synergistically enhances the locomotor-activating effects of some psychomotor stimulants, but not direct dopamine agonists in rats J. Pharmacol. Exp. Ther. 324 2008 714 724
24. 35S]GPTgammaS) binding in brain slices from Sprague-Dawley rats J. Pharmacol. Exp. Ther. 312 2005 1314 1320 (Pubitemid 40293795)
25. F.G. Kaddis, N.J. Uretsky, and L.J. Wallace DNQX in the nucleus accumbens inhibits cocaine-induced conditioned place preference Brain Res. 697 1995 76 82
26. P.W. Kalivas The glutamate homeostasis hypothesis of addiction Nat. Rev. Neurosci. 10 2010 561 572
27. P.W. Kalivas, and N.D. Volkow The neural basis of addiction: a pathology of motivation and choice Am. J. Psychiatr. 162 2005 1403 1413 (Pubitemid 41105554)
28. L. Kantor, and M.E. Gnegy Protein kinase C inhibitors block amphetamine-mediated dopamine release in rat striatal slices J. Pharmacol. Exp. Ther. 284 1998 592 598 (Pubitemid 28086646)
29. A.E. Kelley, and L.C. Throne NMDA receptors mediate the behavioral effects of amphetamine infused into the nucleus accumbens Brain Res. Bull. 29 1992 247 254
30. M.O. Krebs, J.M. Desce, M.L. Kemel, G. Gauchy, G. Godeheu, A. Cheramy, and J. Glowinski Glutamatergic control of dopamine release in the rat striatum: evidence for presynaptic N-methyl-D-aspartate receptors on dopaminergic nerve terminals J. Neurochem. 56 1991 81 85 (Pubitemid 21901933)
31. R. Longoni, C. Cadoni, A. Mulas, G. Di Chiara, and L. Spina Dopamine-dependent behavioural stimulation by non-peptide delta opioids BW373U86 and SNC 80: 2. Place-preference and brain microdialysis studies in rats Behav. Pharmacol. 9 1998 9 14 (Pubitemid 28098662)
32. O.S. Mabrouk, M. Marti, S. Salvadori, and M. Morari The novel delta opioid receptor agonist UFP-512 dually modulates motor activity in hemiparkinsonian rats via control of the nigro-thalamic pathway Neuroscience 164 2009 360 369
33. O.S. Mabrouk, M. Volta, M. Marti, and M. Morari Stimulation of delta opioid receptors located in substantia nigra reticulate but not globus pallidus or striatum restores motor activity in 6-hydroxydopamine lesioned rats: new insights into the role of delta receptors in Parkinsonism J. Neurochem. 107 2008 1647 1659
34. K. Menkens, E.J. Bilsky, K.D. Wild, P.S. Portoghese, L.D. Reid, and F. Porreca Cocaine place preference is blocked by the delta-opioid receptor antagonist, naltrindole Eur. J. Pharmacol. 219 1992 345 356
35. B. Moghaddam, R.J. Gruen, R.H. Roth, B.S. Bunney, and R.N. Adams Effect of L-glutamate on the release of striatal dopamine: in vivo dialysis and electrochemical studies Brain Res. 518 1990 55 60 (Pubitemid 20197030)
36. T. Mori, S. Ito, T. Kita, M. Narita, T. Suzuki, and T. Sawaguchi Effects of mu-, delta-, and kappa-opioid receptor agonists on methamphetamine-induced self-injurious behavior in mice Eur. J. Pharmacol. 532 2006 81 87
37. S.S. Negus, M.B. Gatch, N.K. Mello, X. Zhang, and K. Rice Behavioral effects of the delta-selective opioid agonist SNC80 and related compounds in rhesus monkeys J. Pharmacol. Exp. Ther. 286 1998 362 375 (Pubitemid 28318012)
38. W.H. Oertel, G. Riethmuller, E. Mugnaini, D.E. Schmechel, A. Weindl, C. Gramsch, and A. Herz Opioid peptide-like immunoreactivity localized in GABAergic neurons of rat neostriatum and central amygdaloid nucleus Life Sci. 33 1983 73 76 (Pubitemid 14249932)
39. L. Pulvirenti, R. Maldonado-Lopez, and G.F. Koob NMDA receptors in the nucleus accumbens modulate intravenous cocaine but not heroin self-administration in the rat Brain Res. 594 1992 327 330
40. L. Pulvirenti, R. Berrier, M. Kreifeldt, and G.F. Koob Modulation of locomotor activity by NMDA receptors in the nucleus accumbens core and shell regions of the rat Brain Res. 664 1994 231 236 (Pubitemid 24347619)
41. S.M. Rawls, and J.F. McGinty Kappa opioid and muscarinic receptors inhibit the calcium-dependent component of 4-aminopyridine-evoked glutamate release from striatal synaptosomes J. Neurochem. 73 1999 1058 1065 (Pubitemid 29395462)
42. S.M. Rawls, and J.F. McGinty Delta opioid receptors regulate calcium-dependent, amphetamine-evoked glutamate levels in the rat striatum: an in vivo microdialysis study Brain Res. 861 2000 269 304
43. 3H]dopamine release from rat striatum: an in vitro model for glutamate actions J. Neurochem. 32 1979 1539 1545 (Pubitemid 9163996)
44. J.K. Rowlett, and R.D. Spealman Opioid enhancement of the discriminative stimulus effects of cocaine: evidence for involvement of mu and delta opioid receptors Psychopharmacology 140 1998 217 224 (Pubitemid 28538482)
45. S. Schenk, A. Valadez, C.M. Worley, and C. McNamara Blockade of the acquisition of cocaine self-administration by the NMDA antagonist MK-801 (dizocilpine) Behav. Pharmacol. 4 1993 652 659 (Pubitemid 24002280)
46. S.R. Sesack, and V.M. Pickel In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other Brain Res. 527 1990 266 279 (Pubitemid 20290606)
47. T.S. Shippenberg, R. Bals-Kubik, and A. Herz Motivational properties of opioids: evidence that an activation of delta-receptors mediates reinforcement processes Brain Res. 436 1987 234 239 (Pubitemid 18003562)
48. T.S. Shippenberg, and C. Heidbreder The delta-opioid receptor antagonist naltrindole prevents sensitization to the conditioned rewarding effects of cocaine Eur. J. Pharmacol. 280 1995 55 61
49. I. Smolders, N. De Klippel, S. Sarre, G. Ebinger, and Y. Michotte Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat Eur. J. Pharmacol. 284 1995 83 91
50. P. Song, O.S. Mabrouk, N.D. Hershey, and R.T. Kennedy In vivo neurochemical monitoring using benzoyl chloride derivatization and liquid chromatography-mass spectrometry Anal. Chem. 84 2012 412 419
51. R. Spanagel, A. Herz, and T.S. Shippenberg The effects of opioid peptides on dopamine release in the nucleus accumbens: an in vivo microdialysis study J. Neurochem. 55 1990 1734 1740
52. T. Suzuki, M. Tsuji, T. Mori, M. Misawa, and H. Nagase The effects of dopamine D1 and D2 receptor antagonists on the rewarding effects of delta 1 and delta 2 opioid receptor agonists in mice Pyschopharmacology 124 1996 211 218 (Pubitemid 26130532)
53. T. Suzuki, T. Mori, M. Tsuji, M. Misawa, and H. Nagase The role of delta-opioid receptors in the discriminative stimulus properties of a low dose of methamphetamine Eur. J. Pharmacol. 331 1997 1 8 (Pubitemid 27312404)
54. 5-enkephalin J. Neurosci. 18 1998 1923 1933 (Pubitemid 28103100)
55. F.I. Tarazi, A. Campbell, S.K. Yeghiayan, and R.J. Baldessarini Localization of ionotropic glutamate receptors in caudate-putamen and nucleus accumbens septi of rat brain: comparison of NMDA, AMPA, and kainite receptors Synapse 30 1998 227 235 (Pubitemid 28376382)
56. 2+ influx causes rapid translocation of protein kinase C to membranes. Studies of the effects of secretagogues in adrenal chromaffin cells J. Biol. Chem. 263 1988 18873 18879 (Pubitemid 19016346)
57. M. Ueda, K. Sugimoto, T. Oyama, Y. Kuraishi, and M. Satoh Opioidergic inhibition of capsaicin-evoked release of glutamate from rat spinal dorsal horn slices Neuropharmacology 34 1995 303 308
58. 2+ uptake and glutamate release in rat cerebral cortex in primary culture J. Neurochem. 68 1997 517 524 (Pubitemid 27044710)
59. J.K. Wang Presynaptic glutamate receptors modulate dopamine release from striatal synaptosomes J. Neurochem. 57 1991 819 822
60. D.L. Willins, L.J. Wallace, D.D. Miller, and N.J. Uretsky Alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainite receptor antagonists in the nucleus accumbens and ventral pallidum decrease the hypermotility response to psychostimulant drugs J. Pharmacol. Exp. Ther. 260 1992 1145 1151