Delta opioid receptors in brain function and diseases

Pharmacology and Therapeutics

Volumn 140, Issue 1, 2013, Pages 112-120

  Chu Sin Chung, Paul ^a   Kieffer, Brigitte L ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Delta opioid receptor; In vivo; Knockout; Pathology; Pharmacology

Indexed keywords

4 [ALPHA (4 ALLYL 2,5 DIMETHYL 1 PIPERAZINYL) 3 HYDROXYBENZYL] N,N DIETHYLBENZAMIDE; 4 [ALPHA (4 ALLYL 2,5 DIMETHYL 1 PIPERAZINYL) 3 METHOXYBENZYL] N,N DIETHYLBENZAMIDE; ADL 5747; ADL 5859; ADL 5945; ALCOHOL; AZD 2327; BENZODIAZEPINE DERIVATIVE; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; DELTA OPIATE RECEPTOR ANTAGONIST; ENKEPHALINASE INHIBITOR; MORPHINE; MU OPIATE RECEPTOR; NALTRIBEN; NEUROPROTECTIVE AGENT; NP 2; PSYCHOSTIMULANT AGENT; UNCLASSIFIED DRUG;

ADDICTION; ARTICLE; BRAIN DISEASE; BRAIN FUNCTION; CHRONIC PAIN; CLINICAL TRIAL; CONSTIPATION; DRUG ABUSE; EMOTION; EPILEPTOGENESIS; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HYPOXIA; INHIBITION (PSYCHOLOGY); INTRACTABLE PAIN; KNEE OSTEOARTHRITIS; LEARNING; LIVER CELL CARCINOMA; LOCOMOTION; MAJOR DEPRESSION; MOOD DISORDER; MOTOR CONTROL; NEUROPROTECTION; NONHUMAN; PAIN; PARKINSON DISEASE; POSTHERPETIC NEURALGIA; PRIORITY JOURNAL; RECEPTOR BINDING; REWARD; TRANQUILIZING ACTIVITY; X RAY CRYSTALLOGRAPHY;

AMY; AMYGDALA; CA; CAUDATE PUTAMEN NUCLEUS; CEA; CENTRAL NUCLEUS OF THE AMYGDALA; CG; CINGULATE CORTEX; CONDITIONED PLACE AVERSION; CONDITIONED PLACE PREFERENCE; CONTINUOUS ACCESS; CORTEX; CPA; CPP; CPU; CX; DELTA OPIOID RECEPTOR; DOR; EEG; ELECTROENCEPHALOGRAPHY; ENK; ENKEPHALIN; FCX; FRONTAL CORTEX; G PROTEIN COUPLED RECEPTOR; GPCR; HIPP; HIPPOCAMPUS; HYP; HYPOTHALAMUS; I.C.V.; I.P.; I.V.; IA; IN VIVO; INTERMITTENT ACCESS; INTRACEREBROVENTRICULAR; INTRAPERITONEAL; INTRAVENOUS; KNOCKOUT; KO; NACC; NALTRINDOLE; NTI; NUCLEUS ACCUMBENS; OB; OLFACTORY BULB; P.O.; PARAVENTRICULAR NUCLEUS; PATHOLOGY; PERS OS; PHARMACOLOGY; PR; PROGRESSIVE RATIO; PVN; RETROSPLENIAL CORTEX; RS; S.C.; SA; SC; SELF-ADMINISTRATION; SPINAL CORD; SUBCUTANEOUS; TH; THALAMUS; VENTRAL TEGMENTAL AREA; VTA;

ANIMALS; ANOXIA; BRAIN; BRAIN ISCHEMIA; EMOTIONS; EPILEPSY; HUMANS; MOTOR ACTIVITY; OPIOID-RELATED DISORDERS; RECEPTORS, OPIOID, DELTA; REWARD;

EID: 84883753603     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2013.06.003     Document Type: Review

References (130)

1. L.M. Ambrose-Lanci, R.C. Sterling, and E.J. Van Bockstaele Cocaine withdrawal-induced anxiety in females: impact of circulating estrogen and potential use of delta-opioid receptor agonists for treatment J Neurosci Res 88 2008 816 824
2. V. Andre, N. Pineau, J.E. Motte, C. Marescaux, and A. Nehlig Mapping of neuronal networks underlying generalized seizures induced by increasing doses of pentylenetetrazol in the immature and adult rat: a c-Fos immunohistochemical study Eur J Neurosci 10 1998 2094 2106
3. R.D. Baler, and N.D. Volkow Drug addiction: the neurobiology of disrupted self-control Trends Mol Med 12 2006 559 566
4. B.W. Balleine, and A. Dickinson Goal-directed instrumental action: contingency and incentive learning and their cortical substrates Neuropharmacology 37 1998 407 419
5. J.R. Barson, A.J. Carr, J.E. Soun, N.C. Sobhani, P. Rada, and S.F. Leibowitz Opioids in the hypothalamic paraventricular nucleus stimulate ethanol intake Alcohol Clin Exp Res 34 2010 214 222
6. K. Befort, M.K. Mahoney, C. Chow, S.J. Hayton, B.L. Kieffer, and M.C. Olmstead Effects of delta opioid receptors activation on a response inhibition task in rats Psychopharmacology (Berl) 214 2011 967 976
7. D. Belin, S. Jonkman, A. Dickinson, T.W. Robbins, and B.J. Everitt Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction Behav Brain Res 199 2009 89 102
8. E. Belkai, J.M. Scherrmann, F. Noble, and C. Marie-Claire Modulation of MDMA-induced behavioral and transcriptional effects by the delta opioid antagonist naltrindole in mice Addict Biol 14 2009 245 252
9. F. Berrendero, A. Plaza-Zabala, L. Galeote, A. Flores, S.A. Bura, and B.L. Kieffer Influence of delta-opioid receptors in the behavioral effects of nicotine Neuropsychopharmacology 37 2012 2332 2344
10. B. Bie, W. Zhu, and Z.Z. Pan Ethanol-induced delta-opioid receptor modulation of glutamate synaptic transmission and conditioned place preference in central amygdala Neuroscience 160 2009 348 358
11. A. Bilkei-Gorzo, K. Michel, F. Noble, B.P. Roques, and A. Zimmer Preproenkephalin knockout mice show no depression-related phenotype Neuropsychopharmacology 32 2007 2330 2337
12. S.K. Billa, Y. Xia, and J.A. Moron Disruption of morphine-conditioned place preference by a delta2-opioid receptor antagonist: study of mu-opioid and delta-opioid receptor expression at the synapse Eur J Neurosci 32 2010 625 631
13. F. Billet, J. Costentin, and N. Dourmap Influence of corticostriatal delta-opioid receptors on abnormal involuntary movements induced by L-DOPA in hemiparkinsonian rats Exp Neurol 236 2012 339 350
14. A.H. Borkowski, D.C. Barnes, D.R. Blanchette, F.X. Castellanos, D.F. Klein, and D.A. Wilson Interaction between delta opioid receptors and benzodiazepines in CO(2)-induced respiratory responses in mice Brain Res 1396 2011 54 59
15. M.E. Brevard, P. Kulkarni, J.A. King, and C.F. Ferris Imaging the neural substrates involved in the genesis of pentylenetetrazol-induced seizures Epilepsia 47 2006 745 754
16. D.C. Broom, J.F. Nitsche, J.E. Pintar, K.C. Rice, J.H. Woods, and J.R. Traynor Comparison of receptor mechanisms and efficacy requirements for delta-agonist-induced convulsive activity and antinociception in mice J Pharmacol Exp Ther 303 2002 723 729
17. R.N. Cardinal, J.A. Parkinson, J. Hall, and B.J. Everitt Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex Neurosci Biobehav Rev 26 2002 321 352
18. D. Chao, and Y. Xia Ionic storm in hypoxic/ischemic stress: can opioid receptors subside it? Prog Neurobiol 90 2010 439 470
19. D. Chao, A. Bazzy-Asaad, G. Balboni, S. Salvadori, and Y. Xia Activation of DOR attenuates anoxic K+ derangement via inhibition of Na+ entry in mouse cortex Cereb Cortex 18 2008 2217 2227
20. D. Chao, G. Balboni, L.H. Lazarus, S. Salvadori, and Y. Xia Na+ mechanism of delta-opioid receptor induced protection from anoxic K+ leakage in the cortex Cell Mol Life Sci 66 2009 1105 1115
21. C. Chavkin The therapeutic potential of kappa-opioids for treatment of pain and addiction Neuropsychopharmacology 36 2011 369 370
22. V.I. Chefer, and T.S. Shippenberg Augmentation of morphine-induced sensitization but reduction in morphine tolerance and reward in delta-opioid receptor knockout mice Neuropsychopharmacology 34 2009 887 898
23. C. Contet, B.L. Kieffer, and K. Befort Mu opioid receptor: a gateway to drug addiction Curr Opin Neurobiol 14 2004 370 378
24. C.M. Costantino, I. Gomes, S.D. Stockton, M.P. Lim, and L.A. Devi Opioid receptor heteromers in analgesia Expert Rev Mol Med 14 2012 e9
25. R.C. Crist, L.M. Ambrose-Lanci, M. Vaswani, T.K. Clarke, A. Zeng, and C. Yuan Case-control association analysis of polymorphisms in the delta-opioid receptor, OPRD1, with cocaine and opioid addicted populations Drug Alcohol Depend 127 2013 122 128
26. V. David, A. Matifas, S. Gavello-Baudy, L. Decorte, B.L. Kieffer, and P. Cazala Brain regional Fos expression elicited by the activation of mu- but not delta-opioid receptors of the ventral tegmental area: evidence for an implication of the ventral thalamus in opiate reward Neuropsychopharmacology 33 2008 1746 1759
27. Y.L. Duan, S.Y. Wang, Q.W. Zeng, D.S. Su, W. Li, and X.R. Wang Astroglial reaction to delta opioid peptide [D-Ala2, D-Leu5] enkephalin confers neuroprotection against global ischemia in the adult rat hippocampus Neuroscience 192 2011 81 90
28. A. Etkin, T. Egner, and R. Kalisch Emotional processing in anterior cingulate and medial prefrontal cortex Trends Cogn Sci 15 2011 85 93
29. B.J. Everitt, R.N. Cardinal, J.A. Parkinson, and T.W. Robbins Appetitive behavior: impact of amygdala-dependent mechanisms of emotional learning Ann N Y Acad Sci 985 2003 233 250
30. B.J. Everitt, D. Belin, D. Economidou, Y. Pelloux, J.W. Dalley, and T.W. Robbins Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction Philos Trans R Soc Lond B Biol Sci 363 2008 3125 3135
31. S.E. File, P.J. Kenny, and S. Cheeta The role of the dorsal hippocampal serotonergic and cholinergic systems in the modulation of anxiety Pharmacol Biochem Behav 66 2000 65 72
32. D. Filliol, S. Ghozland, J. Chluba, M. Martin, H.W. Matthes, and F. Simonin Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses Nat Genet 25 2000 195 200
33. G.L. Fraser, H. Parenteau, T.M. Tu, J. Ducharme, M.N. Perkins, and P.B. Clarke The effects of delta agonists on locomotor activity in habituated and non-habituated rats Life Sci 67 2000 913 922
34. S. Galandrin, G. Oligny-Longpre, and M. Bouvier The evasive nature of drug efficacy: implications for drug discovery Trends Pharmacol Sci 28 2007 423 430
35. C.J. Gao, J.P. Li, W. Wang, B.C. Lu, L. Niu, and C. Zhu Effects of intracerebroventricular application of the delta opioid receptor agonist [D-Ala2, D-Leu5] enkephalin on neurological recovery following asphyxial cardiac arrest in rats Neuroscience 168 2010 531 542
36. C.J. Gao, L. Niu, P.C. Ren, W. Wang, C. Zhu, and Y.Q. Li Hypoxic preconditioning attenuates global cerebral ischemic injury following asphyxial cardiac arrest through regulation of delta opioid receptor system Neuroscience 202 2012 352 362
37. C. Gaveriaux-Ruff Opiate-induced analgesia: contributions from mu, delta and kappa opioid receptors mouse mutants Curr Pharm Des 2013 (in press)
38. C. Gaveriaux-Ruff, and B.L. Kieffer Delta opioid receptor analgesia: recent contributions from pharmacology and molecular approaches Behav Pharmacol 22 2011 405 414
39. C. Gaveriaux-Ruff, C. Nozaki, X. Nadal, X.C. Hever, R. Weibel, and A. Matifas Genetic ablation of delta opioid receptors in nociceptive sensory neurons increases chronic pain and abolishes opioid analgesia Pain 152 2011 1238 1248
40. S. Ghozland, H.W. Matthes, F. Simonin, D. Filliol, B.L. Kieffer, and R. Maldonado Motivational effects of cannabinoids are mediated by mu-opioid and kappa-opioid receptors J Neurosci 22 2002 1146 1154
41. C. Gianoulakis Endogenous opioids and addiction to alcohol and other drugs of abuse Curr Top Med Chem 9 2009 999 1015
42. R.J. Goody, S.M. Oakley, D. Filliol, B.L. Kieffer, and I. Kitchen Quantitative autoradiographic mapping of opioid receptors in the brain of delta-opioid receptor gene knockout mice Brain Res 945 2002 9 19
43. S. Granier, A. Manglik, A.C. Kruse, T.S. Kobilka, F.S. Thian, and W.I. Weis Structure of the delta-opioid receptor bound to naltrindole Nature 485 2012 400 404
44. C.T. Gross, and N.S. Canteras The many paths to fear Nat Rev Neurosci 13 2012 651 658
45. T.J. Hudzik, C. Maciag, M.A. Smith, R. Caccese, M.R. Pietras, and K.H. Bui Preclinical pharmacology of AZD2327: a highly selective agonist of the delta-opioid receptor J Pharmacol Exp Ther 338 2011 195 204
46. N. Ismayilova, and M. Shoaib Alteration of intravenous nicotine self-administration by opioid receptor agonist and antagonists in rats Psychopharmacology (Berl) 210 2010 211 220
47. H. Javelot, M. Messaoudi, S. Garnier, and C. Rougeot Human opiorphin is a naturally occurring antidepressant acting selectively on enkephalin-dependent delta-opioid pathways J Physiol Pharmacol 61 2010 355 362
48. S.M. Johnson, and S.M. Turner Protecting motor networks during perinatal ischemia: the case for delta-opioid receptors Ann N Y Acad Sci 1198 2010 260 270
49. E.M. Jutkiewicz, S.T. Kaminsky, K.C. Rice, J.R. Traynor, and J.H. Woods Differential behavioral tolerance to the delta-opioid agonist SNC80 ([(+)-4-[(alphaR)-alpha-[(2S,5R)-2,5-dimethyl-4-(2-propenyl)-1-piperazinyl ]-(3-methoxyphenyl)methyl]-N, N-diethylbenzamide) in Sprague-Dawley rats J Pharmacol Exp Ther 315 2005 414 422
50. E.M. Jutkiewicz, K.C. Rice, J.R. Traynor, and J.H. Woods Separation of the convulsions and antidepressant-like effects produced by the delta-opioid agonist SNC80 in rats Psychopharmacology (Berl) 182 2005 588 596
51. E.M. Jutkiewicz, M.G. Baladi, J.E. Folk, K.C. Rice, and J.H. Woods The convulsive and electroencephalographic changes produced by nonpeptidic delta-opioid agonists in rats: comparison with pentylenetetrazol J Pharmacol Exp Ther 317 2006 1337 1348
52. E.M. Jutkiewicz, M.M. Torregrossa, K. Sobczyk-Kojiro, H.I. Mosberg, J.E. Folk, and K.C. Rice Behavioral and neurobiological effects of the enkephalinase inhibitor RB101 relative to its antidepressant effects Eur J Pharmacol 531 2006 151 159
53. T. Kenakin Functional selectivity and biased receptor signaling J Pharmacol Exp Ther 336 2011 296 302
54. R.P. Kesner, and P.E. Gilbert The role of the agranular insular cortex in anticipation of reward contrast Neurobiol Learn Mem 88 2007 82 86
55. I. Kitchen, S.J. Slowe, H.W. Matthes, and B. Kieffer Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene Brain Res 778 1997 73 88
56. P. Kleczkowska, A.W. Lipkowski, D. Tourwe, and S. Ballet Hybrid opioid/non-opioid ligands in pain research Curr Pharm Des 2013 (in press)
57. A.T. Knoll, and W.A. Carlezon Jr. Dynorphin, stress, and depression Brain Res 1314 2010 56 73
58. M. Konig, A.M. Zimmer, H. Steiner, P.V. Holmes, J.N. Crawley, and M.J. Brownstein Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin Nature 383 1996 535 538
59. G.F. Koob, and M. Le Moal Review. Neurobiological mechanisms for opponent motivational processes in addiction Philos Trans R Soc Lond B Biol Sci 363 2008 3113 3123
60. G.F. Koob, and N.D. Volkow Neurocircuitry of addiction Neuropsychopharmacology 35 2010 217 238
61. V. Laurent, B. Leung, N. Maidment, and B.W. Balleine Mu- and delta-opioid-related processes in the accumbens core and shell differentially mediate the influence of reward-guided and stimulus-guided decisions on choice J Neurosci 32 2012 1875 1883
62. B. Le Bourdonnec, R.T. Windh, C.W. Ajello, L.K. Leister, M. Gu, and G.H. Chu Potent, orally bioavailable delta opioid receptor agonists for the treatment of pain: discovery of N, N-diethyl-4-(5-hydroxyspiro[chromene-2,4′- piperidine]-4-yl)benzamide (ADL5859) J Med Chem 51 2008 5893 5896
63. B. Le Bourdonnec, R.T. Windh, L.K. Leister, Q.J. Zhou, C.W. Ajello, and M. Gu Spirocyclic delta opioid receptor agonists for the treatment of pain: discovery of N, N-diethyl-3-hydroxy-4-(spiro[chromene-2,4′-piperidine]-4- yl) benzamide (ADL5747) J Med Chem 52 2009 5685 5702
64. J. Le Merrer, J.A. Becker, K. Befort, and B.L. Kieffer Reward processing by the opioid system in the brain Physiol Rev 89 2009 1379 1412
65. J. Le Merrer, A. Plaza-Zabala, C. Del Boca, A. Matifas, R. Maldonado, and B.L. Kieffer Deletion of the delta opioid receptor gene impairs place conditioning but preserves morphine reinforcement Biol Psychiatry 69 2011 700 703
66. J. Le Merrer, L. Faget, A. Matifas, and B.L. Kieffer Cues predicting drug or food reward restore morphine-induced place conditioning in mice lacking delta opioid receptors Psychopharmacology (Berl) 223 2012 99 106
67. J. Le Merrer, X. Rezai, G. Scherrer, J.A. Becker, and B.L. Kieffer Impaired hippocampus-dependent and facilitated striatum-dependent behaviors in mice lacking the delta opioid receptor Neuropsychopharmacology 2013 (in press)
68. J.E. LeDoux Emotion circuits in the brain Annu Rev Neurosci 23 2000 155 184
69. P.E. Lutz, and B.L. Kieffer Opioid receptors: distinct roles in mood disorders Trends Neurosci 2013 (in press)
70. 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
71. A. Manglik, A.C. Kruse, T.S. Kobilka, F.S. Thian, J.M. Mathiesen, and R.K. Sunahara Crystal structure of the micro-opioid receptor bound to a morphinan antagonist Nature 485 2012 321 326
72. E.B. Margolis, H.L. Fields, G.O. Hjelmstad, and J.M. Mitchell Delta-opioid receptor expression in the ventral tegmental area protects against elevated alcohol consumption J Neurosci 28 2008 12672 12681
73. P.W. Marinelli, D. Funk, S. Harding, Z. Li, W. Juzytsch, and A.D. Le Roles of opioid receptor subtypes in mediating alcohol-seeking induced by discrete cues and context Eur J Neurosci 30 2009 671 678
74. M.M. Mas Nieto, S.L. Guen, B.L. Kieffer, B.P. Roques, and F. Noble Physiological control of emotion-related behaviors by endogenous enkephalins involves essentially the delta opioid receptors Neuroscience 135 2005 305 313
75. P.S. Naidu, A.H. Lichtman, C.C. Archer, E.L. May, L.S. Harris, and M.D. Aceto NIH 11082 produces anti-depressant-like activity in the mouse tail-suspension test through a delta-opioid receptor mechanism of action Eur J Pharmacol 566 2007 132 136
76. M. Narita, C. Kaneko, K. Miyoshi, Y. Nagumo, N. Kuzumaki, and M. Nakajima Chronic pain induces anxiety with concomitant changes in opioidergic function in the amygdala Neuropsychopharmacology 31 2006 739 750
77. M. Narita, N. Kuzumaki, C. Kaneko, N. Hareyama, M. Miyatake, and K. Shindo Chronic pain-induced emotional dysfunction is associated with astrogliosis due to cortical delta-opioid receptor dysfunction J Neurochem 97 2006 1369 1378
78. C.K. Nielsen, J.A. Simms, H.B. Pierson, R. Li, S.K. Saini, and S. Ananthan A novel delta opioid receptor antagonist, SoRI-9409, produces a selective and long-lasting decrease in ethanol consumption in heavy-drinking rats Biol Psychiatry 64 2008 974 981
79. C.K. Nielsen, J.A. Simms, R. Li, D. Mill, H. Yi, and A.A. Feduccia Delta-opioid receptor function in the dorsal striatum plays a role in high levels of ethanol consumption in rats J Neurosci 32 2012 4540 4552
80. C. Nozaki, B. Le Bourdonnec, D. Reiss, R.T. Windh, P.J. Little, and R.E. Dolle Delta-opioid mechanisms for ADL5747 and ADL5859 effects in mice: analgesia, locomotion, and receptor internalization J Pharmacol Exp Ther 342 2012 799 807
81. M.C. Olmstead, A.M. Ouagazzal, and B.L. Kieffer Mu and delta opioid receptors oppositely regulate motor impulsivity in the signaled nose poke task PLoS One 4 2009 e4410
82. R. Panetta, and M.T. Greenwood Physiological relevance of GPCR oligomerization and its impact on drug discovery Drug Discov Today 13 2008 1059 1066
83. J.J. Paton, and K. Louie Reward and punishment illuminated Nat Neurosci 15 2012 807 809
84. M.P. Paulus, and M.B. Stein An insular view of anxiety Biol Psychiatry 60 2006 383 387
85. D. Peckys, and G.B. Landwehrmeyer Expression of mu, kappa, and delta opioid receptor messenger RNA in the human CNS: a 33P in situ hybridization study Neuroscience 88 1999 1093 1135
86. J. Peng, S. Sarkar, and S.L. Chang Opioid receptor expression in human brain and peripheral tissues using absolute quantitative real-time RT-PCR Drug Alcohol Depend 124 2012 223 228
87. S.A. Perrine, B.A. Hoshaw, and E.M. Unterwald Delta opioid receptor ligands modulate anxiety-like behaviors in the rat Br J Pharmacol 147 2006 864 872
88. C.L. Pickens, M. Airavaara, F. Theberge, S. Fanous, B.T. Hope, and Y. Shaham Neurobiology of the incubation of drug craving Trends Neurosci 34 2011 411 420
89. A.A. Pradhan, W. Walwyn, C. Nozaki, D. Filliol, E. Erbs, and A. Matifas Ligand-directed trafficking of the delta-opioid receptor in vivo: two paths toward analgesic tolerance J Neurosci 30 2010 16459 16468
90. A.A. Pradhan, K. Befort, C. Nozaki, C. Gaveriaux-Ruff, and B.L. Kieffer The delta opioid receptor: an evolving target for the treatment of brain disorders Trends Pharmacol Sci 32 2011 581 590
91. A.A. Pradhan, M.L. Smith, B.L. Kieffer, and C.J. Evans Ligand-directed signalling within the opioid receptor family Br J Pharmacol 167 2012 960 969
92. J.L. Price, and W.C. Drevets Neural circuits underlying the pathophysiology of mood disorders Trends Cogn Sci 16 2012 61 71
93. S.D. Primeaux, S.P. Wilson, A.J. McDonald, F. Mascagni, and M.A. Wilson The role of delta opioid receptors in the anxiolytic actions of benzodiazepines Pharmacol Biochem Behav 85 2006 545 554
94. I. Racz, B. Schurmann, A. Karpushova, M. Reuter, S. Cichon, and C. Montag The opioid peptides enkephalin and beta-endorphin in alcohol dependence Biol Psychiatry 64 2008 989 997
95. A. Ragnauth, A. Schuller, M. Morgan, J. Chan, S. Ogawa, and J. Pintar Female preproenkephalin-knockout mice display altered emotional responses Proc Natl Acad Sci U S A 98 2001 1958 1963
96. J.F. Randall-Thompson, K.A. Pescatore, and E.M. Unterwald A role for delta opioid receptors in the central nucleus of the amygdala in anxiety-like behaviors Psychopharmacology (Berl) 212 2010 585 595
97. J.M. Richard, D.C. Castro, A.G. Difeliceantonio, M.J. Robinson, and K.C. Berridge Mapping brain circuits of reward and motivation: in the footsteps of Ann Kelley Neurosci Biobehav Rev 2013 (in press)
98. T.W. Robbins, and B.J. Everitt Neurobehavioural mechanisms of reward and motivation Curr Opin Neurobiol 6 1996 228 236
99. A.J. Roberts, L.H. Gold, I. Polis, J.S. McDonald, D. Filliol, and B.L. Kieffer Increased ethanol self-administration in delta-opioid receptor knockout mice Alcohol Clin Exp Res 25 2001 1249 1256
100. S.M. Rodrigues, J.E. LeDoux, and R.M. Sapolsky The influence of stress hormones on fear circuitry Annu Rev Neurosci 32 2009 289 313
101. A. Saitoh, Y. Kimura, T. Suzuki, K. Kawai, H. Nagase, and J. Kamei Potential anxiolytic and antidepressant-like activities of SNC80, a selective delta-opioid agonist, in behavioral models in rodents J Pharmacol Sci 95 2004 374 380
102. A. Saitoh, Y. Yoshikawa, K. Onodera, and J. Kamei Role of delta-opioid receptor subtypes in anxiety-related behaviors in the elevated plus-maze in rats Psychopharmacology (Berl) 182 2005 327 334
103. A. Saitoh, A. Sugiyama, T. Nemoto, H. Fujii, K. Wada, and J. Oka The novel delta opioid receptor agonist KNT-127 produces antidepressant-like and antinociceptive effects in mice without producing convulsions Behav Brain Res 223 2011 271 279
104. D.S. Sauriyal, A.S. Jaggi, and N. Singh Extending pharmacological spectrum of opioids beyond analgesia: multifunctional aspects in different pathophysiological states Neuropeptides 45 2011 175 188
105. S. Scarpellini Cda, L.H. Gargaglioni, L.G. Branco, and K.C. Bicego Role of preoptic opioid receptors in the body temperature reduction during hypoxia Brain Res 1286 2009 66 74
106. G. Scherrer, P. Tryoen-Toth, D. Filliol, A. Matifas, D. Laustriat, and Y.Q. Cao Knockin mice expressing fluorescent delta-opioid receptors uncover G protein-coupled receptor dynamics in vivo Proc Natl Acad Sci U S A 103 2006 9691 9696
107. G. Scherrer, N. Imamachi, Y.Q. Cao, C. Contet, F. Mennicken, and D. O'Donnell Dissociation of the opioid receptor mechanisms that control mechanical and heat pain Cell 137 2009 1148 1159
108. T.S. Shippenberg The dynorphin/kappa opioid receptor system: a new target for the treatment of addiction and affective disorders? Neuropsychopharmacology 34 2009 247
109. T.S. Shippenberg, A. LeFevour, and V.I. Chefer Targeting endogenous mu- and delta-opioid receptor systems for the treatment of drug addiction CNS Neurol Disord Drug Targets 7 2008 442 453
110. T.S. Shippenberg, V.I. Chefer, and A.C. Thompson Delta-opioid receptor antagonists prevent sensitization to the conditioned rewarding effects of morphine Biol Psychiatry 65 2009 169 174
111. D. Simmons, and D.W. Self Role of mu- and delta-opioid receptors in the nucleus accumbens in cocaine-seeking behavior Neuropsychopharmacology 34 2009 1946 1957
112. F. Simonin, K. Befort, C. Gaveriaux-Ruff, H. Matthes, V. Nappey, and B. Lannes The human delta-opioid receptor: genomic organization, cDNA cloning, functional expression, and distribution in human brain Mol Pharmacol 46 1994 1015 1021
113. F. Simonin, O. Valverde, C. Smadja, S. Slowe, I. Kitchen, and A. Dierich Disruption of the kappa-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal EMBO J 17 1998 886 897
114. S.J. Slowe, F. Simonin, B. Kieffer, and I. Kitchen Quantitative autoradiography of mu-, delta- and kappa1 opioid receptors in kappa-opioid receptor knockout mice Brain Res 818 1999 335 345
115. J.S. Smith, J.K. Zubieta, J.C. Price, J.E. Flesher, I. Madar, and J.R. Lever Quantification of delta-opioid receptors in human brain with N1′-([11C]methyl) naltrindole and positron emission tomography J Cereb Blood Flow Metab 19 1999 956 966
116. J. Solati, M.R. Zarrindast, and A.A. Salari Dorsal hippocampal opioidergic system modulates anxiety-like behaviors in adult male Wistar rats Psychiatry Clin Neurosci 64 2010 634 641
117. H.W. Steenland, X.Y. Li, and M. Zhuo Predicting aversive events and terminating fear in the mouse anterior cingulate cortex during trace fear conditioning J Neurosci 32 2012 1082 1095
118. T. Suzuki, M. Tsuji, T. Mori, M. Misawa, T. Endoh, and H. Nagase Effect of the highly selective and nonpeptide delta opioid receptor agonist TAN-67 on the morphine-induced place preference in mice J Pharmacol Exp Ther 279 1996 177 185
119. C.I. Svensson, Y. Rew, S. Malkmus, P.W. Schiller, J.P. Taulane, and M. Goodman Systemic and spinal analgesic activity of a delta-opioid-selective lanthionine enkephalin analog J Pharmacol Exp Ther 304 2003 827 832
120. M.M. Torregrossa, E.M. Jutkiewicz, H.I. Mosberg, G. Balboni, S.J. Watson, and J.H. Woods Peptidic delta opioid receptor agonists produce antidepressant-like effects in the forced swim test and regulate BDNF mRNA expression in rats Brain Res 1069 2006 172 181
121. R.M. van Rijn, and J.L. Whistler The delta(1) opioid receptor is a heterodimer that opposes the actions of the delta(2) receptor on alcohol intake Biol Psychiatry 66 2009 777 784
122. R.M. van Rijn, D.I. Brissett, and J.L. Whistler Dual efficacy of delta opioid receptor selective ligands for ethanol drinking and anxiety J Pharmacol Exp Ther 335 2010 133 139
123. R.M. van Rijn, J.L. Whistler, and M. Waldhoer Opioid-receptor-heteromer- specific trafficking and pharmacology Curr Opin Pharmacol 10 2010 73 79
124. R. Vergura, G. Balboni, B. Spagnolo, E. Gavioli, D.G. Lambert, and J. McDonald Anxiolytic- and antidepressant-like activities of H-Dmt-Tic-NH-CH(CH2- COOH)-Bid (UFP-512), a novel selective delta opioid receptor agonist Peptides 29 2008 93 103
125. S.J. Ward, and D.C. Roberts Microinjection of the delta-opioid receptor selective antagonist naltrindole 5′-isothiocyanate site specifically affects cocaine self-administration in rats responding under a progressive ratio schedule of reinforcement Behav Brain Res 182 2007 140 144
126. H. Wu, D. Wacker, M. Mileni, V. Katritch, G.W. Han, and E. Vardy Structure of the human kappa-opioid receptor in complex with JDTic Nature 485 2012 327 332
127. Y. Zhu, M.A. King, A.G. Schuller, J.F. Nitsche, M. Reidl, and R.P. Elde Retention of supraspinal delta-like analgesia and loss of morphine tolerance in delta opioid receptor knockout mice Neuron 24 1999 243 252
128. M. Zhu, M.W. Li, X.S. Tian, X.M. Ou, C.Q. Zhu, and J.C. Guo Neuroprotective role of delta-opioid receptors against mitochondrial respiratory chain injury Brain Res 1252 2009 183 191
129. M. Zhu, M. Li, F. Yang, X. Ou, Q. Ren, and H. Gao Mitochondrial ERK plays a key role in delta-opioid receptor neuroprotection against acute mitochondrial dysfunction Neurochem Int 59 2011 739 748
130. C. Zollner, and C. Stein Opioids Handb Exp Pharmacol 2007 31 63