Two delta opioid receptor subtypes are functional in single ventral tegmental area neurons, and can interact with the mu opioid receptor

Alonso, 2013, Minireview: ubiquitination-regulated G protein-coupled receptor signaling and trafficking, Mol. Endocrinol., 27, 558, 10.1210/me.2012-1404 Appelmans, 1986, Sodium ions increase the binding of the antagonist peptide ICI 174864 to the delta-opiate receptor, Neuropeptides, 7, 139, 10.1016/0143-4179(86)90089-2 Badiani, 1995, Ventral tegmental area opioid mechanisms and modulation of ingestive behavior, Brain Res., 670, 264, 10.1016/0006-8993(94)01281-L Bals-Kubik, 1993, Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats, J. Pharmacol. Exp. Ther., 264, 489 Bender, 2010, Dopaminergic modulation of axon initial segment calcium channels regulates action potential initiation, Neuron, 68, 500, 10.1016/j.neuron.2010.09.026 Bozarth, 1987, Neuroanatomical boundaries of the reward-relevant opiate-receptor field in the ventral tegmental area as mapped by the conditioned place preference method in rats, Brain Res., 414, 77, 10.1016/0006-8993(87)91327-8 Calenco-Choukroun, 1991, Opioid delta agonists and endogenous enkephalins induce different emotional reactivity than mu agonists after injection in the rat ventral tegmental area, Psychopharmacol. (Berl), 103, 493, 10.1007/BF02244249 Chang, 2004 Chini, 2009, G-protein-coupled receptors, cholesterol and palmitoylation: facts about fats, J. Mol. Endocrinol., 42, 371, 10.1677/JME-08-0114 Daniels, 2005, Opioid-induced tolerance and dependence in mice is modulated by the distance between pharmacophores in a bivalent ligand series, Proc. Natl. Acad. Sci. U. S. A., 102, 19208, 10.1073/pnas.0506627102 Devine, 1993, Ventral mesencephalic delta opioid receptors are involved in modulation of basal mesolimbic dopamine neurotransmission: an anatomical localization study, Brain Res., 622, 348, 10.1016/0006-8993(93)90843-C Devine, 1993, Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies, J. Pharmacol. Exp. Ther., 266, 1236 Devine, 1993, Mesolimbic dopamine neurotransmission is increased by administration of mu-opioid receptor antagonists, Eur. J. Pharmacol., 243, 55, 10.1016/0014-2999(93)90167-G Devine, 1994, Self-administration of morphine, DAMGO, and DPDPE into the ventral tegmental area of rats, J. Neurosci., 14, 1978, 10.1523/JNEUROSCI.14-04-01978.1994 Drake, 2008, beta-arrestin-biased agonism at the beta2-adrenergic receptor, J. Biol. Chem., 283, 5669, 10.1074/jbc.M708118200 Erbs, 2015, A mu-delta opioid receptor brain atlas reveals neuronal co-occurrence in subcortical networks, Brain Struct. Funct., 220, 677, 10.1007/s00429-014-0717-9 Erspamer, 1989, Deltorphins: a family of naturally occurring peptides with high affinity and selectivity for delta opioid binding sites, Proc. Natl. Acad. Sci. U. S. A., 86, 5188, 10.1073/pnas.86.13.5188 Fallon, 1985, Dynorphin-containing pathways in the substantia nigra and ventral tegmentum: a double labeling study using combined immunofluorescence and retrograde tracing, Neuropeptides, 5, 457, 10.1016/0143-4179(85)90053-8 Farias, 2003, Cardiac enkephalins interrupt vagal bradycardia via delta 2-opioid receptors in sinoatrial node, Am. J. Physiol. Heart Circ. Physiol., 284, H1693, 10.1152/ajpheart.00730.2002 Fenalti, 2014, Molecular control of δ-opioid receptor signalling, Nature, 506, 191, 10.1038/nature12944 Ford, 2006, Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location, J. Neurosci., 26, 2788, 10.1523/JNEUROSCI.4331-05.2006 Fujita, 2015, Heteromers of μ-δ opioid receptors: new pharmacology and novel therapeutic possibilities, Br. J. Pharmacol., 172, 375, 10.1111/bph.12663 Fujita, 2014, Molecular characterization of eluxadoline as a potential ligand targeting mu-delta opioid receptor heteromers, Biochem. Pharmacol., 92, 448, 10.1016/j.bcp.2014.09.015 Gahbauer, 2016, Membrane-mediated Oligomerization of G Protein coupled receptors and its implications for GPCR function, Front. Physiol., 7, 494, 10.3389/fphys.2016.00494 Gomes, 2013, Identification of a μ-δ opioid receptor heteromer-biased agonist with antinociceptive activity, Proc. Natl. Acad. Sci. U. S. A., 110, 12072, 10.1073/pnas.1222044110 Gomes, 2004, A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia, Proc. Natl. Acad. Sci. U. S. A., 101, 5135, 10.1073/pnas.0307601101 Gomes, 2011, G protein-coupled receptor heteromerization: a role in allosteric modulation of ligand binding, Mol. Pharmacol., 79, 1044, 10.1124/mol.110.070847 Gomes, 2000, Heterodimerization of mu and delta opioid receptors: a role in opiate synergy, J. Neurosci., 20, RC110, 10.1523/JNEUROSCI.20-22-j0007.2000 Gupta, 2010, Increased abundance of opioid receptor heteromers after chronic morphine administration, Sci. Signal, 3, ra54, 10.1126/scisignal.2000807 Haberstock-Debic, 2003, Morphine acutely regulates opioid receptor trafficking selectively in dendrites of nucleus accumbens neurons, J. Neurosci., 23, 4324, 10.1523/JNEUROSCI.23-10-04324.2003 Hammond, 1998, Differential effects of intrathecally administered delta and mu opioid receptor agonists on formalin-evoked nociception and on the expression of Fos-like immunoreactivity in the spinal cord of the rat, J. Pharmacol. Exp. Ther., 284, 378 Hasbi, 2007, Trafficking of preassembled opioid mu-delta heterooligomer-Gz signaling complexes to the plasma membrane: coregulation by agonists, Biochemistry, 46, 12997, 10.1021/bi701436w Iegorova, 2010, G-protein-independent modulation of P-type calcium channels by mu-opioids in Purkinje neurons of rat, Neurosci. Lett., 480, 106, 10.1016/j.neulet.2010.06.015 Ishibashi, 1995, Regional difference of high voltage-activated Ca2+ channels in rat CNS neurones, Neuroreport, 6, 1621, 10.1097/00001756-199508000-00008 Jiang, 1991, Differential antagonism of opioid delta antinociception by [D-Ala2,Leu5,Cys6]enkephalin and naltrindole 5'-isothiocyanate: evidence for delta receptor subtypes, J. Pharmacol. Exp. Ther., 257, 1069 Johnson, 1992, Opioids excite dopamine neurons by hyperpolarization of local interneurons, J. Neurosci., 12, 483, 10.1523/JNEUROSCI.12-02-00483.1992 Johnson, 1992, Two types of neurone in the rat ventral tegmental area and their synaptic inputs, J. Physiol., 450, 455, 10.1113/jphysiol.1992.sp019136 Kalivas, 1993, GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area, Neuroscience, 57, 1047, 10.1016/0306-4522(93)90048-K Khaimova, 2004, Opioid receptor subtype antagonists differentially alter GABA agonist-induced feeding elicited from either the nucleus accumbens shell or ventral tegmental area regions in rats, Brain Res., 1026, 284, 10.1016/j.brainres.2004.08.032 Korotkova, 2006, Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat, Eur. J. Neurosci., 23, 2677, 10.1111/j.1460-9568.2006.04792.x Korotkova, 2003, Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins, J. Neurosci., 23, 7, 10.1523/JNEUROSCI.23-01-00007.2003 Kreil, 1989, Deltorphin, a novel amphibian skin peptide with high selectivity and affinity for delta opioid receptors, Eur. J. Pharmacol., 162, 123, 10.1016/0014-2999(89)90611-0 Kudo, 2014, GABAergic neurons in the ventral tegmental area receive dual GABA/enkephalin-mediated inhibitory inputs from the bed nucleus of the stria terminalis, Eur. J. Neurosci., 39, 1796, 10.1111/ejn.12503 Lamonte, 2002, Analysis of opioid receptor subtype antagonist effects upon mu opioid agonist-induced feeding elicited from the ventral tegmental area of rats, Brain Res., 929, 96, 10.1016/S0006-8993(01)03382-0 Lur, 2015, Glutamate receptor modulation is restricted to synaptic microdomains, Cell Rep., 12, 326, 10.1016/j.celrep.2015.06.029 Manglik, 2012, Crystal structure of the μ-opioid receptor bound to a morphinan antagonist, Nature, 485, 321, 10.1038/nature10954 Mansour, 1995, The cloned mu, delta and kappa receptors and their endogenous ligands: evidence for two opioid peptide recognition cores, Brain Res., 700, 89, 10.1016/0006-8993(95)00928-J Margolis, 2010, Reliability in the identification of midbrain dopamine neurons, PLoS One, 5, e15222, 10.1371/journal.pone.0015222 Margolis, 2008, Delta-opioid receptor expression in the ventral tegmental area protects against elevated alcohol consumption, J. Neurosci., 28, 12672, 10.1523/JNEUROSCI.4569-08.2008 Margolis, 2014, Direct bidirectional μ-opioid control of midbrain dopamine neurons, J. Neurosci., 34, 14707, 10.1523/JNEUROSCI.2144-14.2014 Margolis, 2006, Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex, Proc. Natl. Acad. Sci. U. S. A., 103, 2938, 10.1073/pnas.0511159103 Margolis, 2006, The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?, J. Physiol., 577, 907, 10.1113/jphysiol.2006.117069 Margolis, 2008, Midbrain dopamine neurons: projection target determines action potential duration and dopamine D(2) receptor inhibition, J. Neurosci., 28, 8908, 10.1523/JNEUROSCI.1526-08.2008 Margolis, 2012, Identification of rat ventral tegmental area GABAergic neurons, PLoS One, 7, e42365, 10.1371/journal.pone.0042365 Mattia, 1991, Lack of antinociceptive cross-tolerance between [D-Pen2, D-Pen5]enkephalin and [D-Ala2]deltorphin II in mice: evidence for delta receptor subtypes, J. Pharmacol. Exp. Ther., 258, 583 Mitchell, 2014, Intra-VTA deltorphin, but not DPDPE, induces place preference in ethanol-drinking rats: distinct DOR-1 and DOR-2 mechanisms control ethanol consumption and reward, Alcohol Clin. Exp. Res., 38, 195, 10.1111/acer.12246 Mosberg, 1983, Cyclic penicillamine containing enkephalin analogs display profound delta receptor selectivities, Life Sci., 33, 447, 10.1016/0024-3205(83)90538-6 Nader, 1997, Deprivation state switches the neurobiological substrates mediating opiate reward in the ventral tegmental area, J. Neurosci., 17, 383, 10.1523/JNEUROSCI.17-01-00383.1997 Pasternak, 2001, Incomplete cross tolerance and multiple mu opioid peptide receptors, Trends Pharmacol. Sci., 22, 67, 10.1016/S0165-6147(00)01616-3 Philippart, 2016, Differential somatic Ca2+ channel profile in midbrain dopaminergic neurons, J. Neurosci., 36, 7234, 10.1523/JNEUROSCI.0459-16.2016 Portoghese, 1991, Role of spacer and address components in peptidomimetic delta opioid receptor antagonists related to naltrindole, J. Med. Chem., 34, 1715, 10.1021/jm00109a027 Provasi, 2015, Preferred supramolecular organization and dimer interfaces of opioid receptors from simulated self-association, PLoS Comput. Biol., 11, e1004148, 10.1371/journal.pcbi.1004148 Ragnauth, 1997, Evaluation of opioid receptor subtype antagonist effects in the ventral tegmental area upon food intake under deprivation, glucoprivic and palatable conditions, Brain Res., 767, 8, 10.1016/S0006-8993(97)00539-8 Rozenfeld, 2007, Receptor heterodimerization leads to a switch in signaling: beta-arrestin2-mediated ERK activation by mu-delta opioid receptor heterodimers, FASEB J., 21, 2455, 10.1096/fj.06-7793com Schiller, 1993, TIPP[psi]: a highly potent and stable pseudopeptide delta opioid receptor antagonist with extraordinary delta selectivity, J. Med. Chem., 36, 3182, 10.1021/jm00073a020 Sesack, 1992, Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions, J. Neurosci., 12, 1335, 10.1523/JNEUROSCI.12-04-01335.1992 Shippenberg, 1995, Involvement of the mesolimbic dopamine system in mediating the aversive effects of opioid antagonists in the rat, Behav. Pharmacol., 6, 99, 10.1097/00008877-199503000-00001 Shippenberg, 1987, Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists, Brain Res., 436, 169, 10.1016/0006-8993(87)91571-X Sofuoglu, 1991, Differential antagonism of delta opioid agonists by naltrindole and its benzofuran analog (NTB) in mice: evidence for delta opioid receptor subtypes, J. Pharmacol. Exp. Ther., 257, 676 Sofuoglu, 1993, 7-Benzylidenenaltrexone (BNTX): a selective delta 1 opioid receptor antagonist in the mouse spinal cord, Life Sci., 52, 769, 10.1016/0024-3205(93)90240-4 Strasser, 2015, Modulation of GPCRs by monovalent cations and anions, Naunyn Schmiedeb. Arch. Pharmacol., 388, 363, 10.1007/s00210-014-1073-2 Swanson, 1982, The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat, Brain Res. Bull., 9, 321, 10.1016/0361-9230(82)90145-9 van Rijn, 2009, The delta(1) opioid receptor is a heterodimer that opposes the actions of the delta(2) receptor on alcohol intake, Biol. Psychiatry, 66, 777, 10.1016/j.biopsych.2009.05.019 Vickery, 2016, Structural mechanisms of voltage Sensing in G Protein-coupled receptors, Structure, 24, 997, 10.1016/j.str.2016.04.007 Vošahlíková, 2011, The influence of monovalent cations on trimeric G protein G(i)1α activity in HEK293 cells stably expressing DOR-G(i)1α (Cys(351)-Ile(351)) fusion protein, Physiol. Res., 60, 541, 10.33549/physiolres.932096 Wanat, 2008, Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih, J. Physiol., 586, 2157, 10.1113/jphysiol.2007.150078 Williams, 2014, CRF-R2 and the heterosynaptic regulation of VTA glutamate during reinstatement of cocaine seeking, J. Neurosci., 34, 10402, 10.1523/JNEUROSCI.0911-13.2014 Williams, 2001, Cellular and synaptic adaptations mediating opioid dependence, Physiol. Rev., 81, 299, 10.1152/physrev.2001.81.1.299 Wisler, 2014, Recent developments in biased agonism, Curr. Opin. Cell Biol., 27, 18, 10.1016/j.ceb.2013.10.008 Zaki, 1996, Opioid receptor types and subtypes: the delta receptor as a model, Annu. Rev. Pharmacol. Toxicol., 36, 379, 10.1146/annurev.pa.36.040196.002115 Zhang, 2010, In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area, Neuropharmacology, 59, 431, 10.1016/j.neuropharm.2010.06.004 Zheng, 2013, Posttranslation modification of G protein-coupled receptor in relationship to biased agonism, Methods Enzymol., 522, 391, 10.1016/B978-0-12-407865-9.00018-2