Potentiation of dopamine D1-like receptor signaling by concomitant activation of δ- And μ-opioid receptors in mouse medial prefrontal cortex

Neurochemistry International

Volumn 61, Issue 8, 2012, Pages 1404-1416

  Olianas, Maria C ^a   Dedoni, Simona ^a   Onali, Pierluigi ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Stimulated adenylyl cyclase isoforms; CREB; DA D1 like receptors; Glutamate receptor phosphorylation; Medial prefrontal cortex; Opioid receptors

Indexed keywords

6 CHLORO 2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DELTA OPIATE RECEPTOR; DOPAMINE 1 RECEPTOR; GLUTAMATE RECEPTOR 1; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; GUANOSINE DIPHOSPHATE; LEUCINE ENKEPHALIN; MU OPIATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MALE; MEDIAL PREFRONTAL CORTEX; MOUSE; NERVE CELL CULTURE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ADENYLATE CYCLASE; ANIMALS; BENZAZEPINES; CARRIER PROTEINS; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOPAMINE; DOPAMINE AGONISTS; ENKEPHALIN, LEUCINE; ENZYME ACTIVATION; FRONTAL LOBE; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; MALE; MICE; NERVE TISSUE PROTEINS; NEURONS; OPIOID PEPTIDES; PHOSPHORYLATION; PREFRONTAL CORTEX; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, AMPA; RECEPTORS, DOPAMINE D1; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU;

EID: 84870299438     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.10.005     Document Type: Article

References (80)

1. A. Abeyta, T.S. Dettmer, A. Barnes, D. Vega, M. Carta, N. Gallegos, M. Raymond-Stintz, D.D. Savage, C.F. Valenzuela, and L.C. Saland Delta opioid receptor localization in the rat cerebellum Brain Res. 931 2002 100 105
2. D.J. Anand, and A. Oommen A molecular weight study of the rat brain delta opioid receptor Indian J. Biochem. Biophys. 32 1995 161 165
3. L.P. Baker, M.D. Nielsen, S. Impey, B.M. Hacker, S.W. Posser, M.Y.M. Chan, and D.R. Storm Regulation and immunohistochemical localization of βγ-stimulated adenylyl cyclases in mouse hippocampus J. Neurosci. 19 1999 180 192
4. A.E. Baldwin, K. Sadeghian, and A.E. Kelley Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex J. Neurosci. 22 2002 1063 1071
5. R. Bals-Kubik, A. Ableitner, A. Herz, and T.S. Shippenberg Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats J. Pharmacol. Exp. Ther. 264 1993 489 495
6. L. Bao, S.-X. Jin, C. Zhang, L.-H. Wang, Z.-Z. Xu, F.-X. Zhang, L.-C. Wang, F.-S. Ning, H.-J. Chai, J.-S. Guan, H.-S. Xiao, Z.-Q.D. Xu, C. He, T. Hokfelt, Z. Zhou, and X. Zhang Activation of delta opioid receptors induces receptor insertion and neuropeptide secretion Neuron 37 2003 121 133
7. βγ subunits FASEB J. 12 1998 1019 1025
8. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
9. C.M. Cahill, K.A. McClellan, A. Morinville, C. Hoffert, D. Hubatsch, D. O'Donnell, and A. Beaudet Immunohistochemical distribution of delta opioid receptors in the rat central nervous system: evidence for somatodendritic labelling and antigen-specific cellular compartmentalization J. Comp. Neurol. 440 2001 65 84
10. W.A. Carlezon Jr, R.S. Duman, and E.J. Nestler The many faces of CREB Trends Neurosci. 28 2005 436 445
11. S.Z. Chao, W. Lu, H.-K. Lee, R.L. Hunganir, and M.E. Wolf D1 dopamine receptor stimulation increases GluR1 phosphorylation in postnatal nucleus accumbens cultures J. Neurochem. 81 2002 984 992
12. B. Cheng, and J.T. Williams Increased opioid inhibition of GABA release in nucleus accumbens during morphine withdrawal J. Neurosci. 18 1998 7033 7039
13. P. Cheng, L. Liu-Chen, and V. Pickel Dual ultrastructural immunocytochemical labelling of μ and δ opioid receptors in the superficial layers of the rat cervical spinal cord Brain Res. 778 1997 367 380
14. 50) of an enzymatic reaction Biochem. Pharmacol. 22 1973 3099 3102
15. Y. Chern Regulation of adenylyl cyclase in the central nervous system Cell Signal. 12 2000 195 204
16. D.P. Devine, P. Leone, D. Pocock, and R.A. Wise 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 1993 1236 1246
17. J.A. Esteban, S.-H. Shi, C. Wilson, M. Nuriya, R.L. Huganir, and R. Malinow PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity Nature Neurosci. 6 2003 136 143
18. i protein βγ subunits Nature 356 1992 159 161
19. K.B.J. Franklin, and G. Paxinos The Mouse Brain in Stereotaxic Coordinates second ed. 2001 Academic Press San Diego
20. A.M. Gabilondo, J.J. Meana, and J.A. Garcia-Sevilla Increased density of mu-opioid receptors in the post-mortem brain of suicide victims Brain Res. 682 1995 245 250
21. S. George, T. Fan, Z. Xie, R. Tse, V. Tam, G. Varghese, and B. O'Dowd Oligomerization of μ- and δ-opioid receptors. Generation of novel functional properties J. Biol. Chem. 275 2000 26128 26135
22. J.L. Giacchino, and S.J. Henriksen Opioid effects on activation of neurons in the medial prefrontal cortex Prog. Neuro-Psychopharmacol. Biol. Psych. 22 1998 1157 1178
23. C.E. Glatt, and S.H. Snyder Cloning and expression of an adenylyl cyclase localized to the corpus striatum Nature 361 1993 536 538
24. P.S. Goldman-Rakic, M.S. Lidow, and D.W. Gallager Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complementarity of their subtypes in primate prefrontal cortex J. Neurosci. 10 1990 2125 2138
25. P.S. Goldman-Rakic, E.C. Muly III, and G.V. Williams D1 receptors in prefrontal cells and circuits Brain Res. Rev. 31 2000 295 301
26. I. Gomes, B.A. Jordan, A. Gupta, N. Trapaidze, V. Nagy, and L.A. Devi Heterodimerization of μ and δ opioid receptors: a role in opiate synergy J. Neurosci. 20 2000 RC110
27. I. Gomes, A. Gupta, J. Filipovska, H.H. Szeto, J.E. Pintar, and L.A. Devi A role for heterodimerization of μ and δ opiate receptors in enhancing morphine analgesia Proc. Natl. Acad. Sci. USA 101 2004 5135 5139
28. H. Gurden, M. Takita, and T.M. Jay Essential role of D1 but not D2 receptors in the NMDA receptor-dependent long-term potentiation at hippocampal-prefrontal cortex synapses in vivo J. Neurosci. 20 2000 RC106(1-5)
29. M. Hotte, S. Thuault, F. Lachaise, K.T. Dineley, H.C. Hemmings, A.C. Nairn, and T.M. Jay D1 receptor modulation of memory retrieval performance is associated with changes in pCREB and pDARPP-32 in rat prefrontal cortex Behav. Brain Res. 171 2006 127 133
30. P. Huang, C. Chen, S.D. Mague, J.A. Blendy, and L.-Y. Liu-Chen A common single polymorphism A118G of the μ opioid receptor alters its N-glycosylation and protein stability Biochem. J. 441 2012 379 386
31. S.E. Hyman, R.C. Malenka, and E.J. Nestler Neural mechanisms of addiction: the role of reward-related learning and memory Annu. Rev. Neurosci. 29 2006 565 598
32. S.L. Ingram, and J.T. Williams Opioid inhibition of Ih via adenylyl cyclase Neuron 13 1994 179 186
33. T. Iwamoto, S. Okumura, K. Iwatsubo, J.I. Kawabe, K. Ohtsu, I. Sakai, Y. Hashimoto, A. Izumitani, K. Sango, K. Ajiki, Y. Toya, S. Umemura, Y. Goshima, N. Arai, S.F. Vatner, and Y. Ishikawa Motor dysfunction in type 5 adenylyl cyclase-null mice J. Biol. Chem. 278 2003 16936 16940
34. T.M. Jay Dopamine: a potential substrate for synaptic plasticity and memory mechanisms Prog. Neurobiol. 69 2003 375 390
35. J.R. Juhasz, A. Hasbi, A.J. Rashid, C.H. So, S.R. George, and B.F. O'Dowd Mu-opioid receptor heterooligomer formation with the dopamine D1 receptor as directly visualized in living cells Eur. J. Pharmacol. 581 2008 235 243
36. K.-S. Kim, K.-W. Lee, K.W. Lee, J.-Y. Im, J.Y. Yoo, S.-W. Kim, J.-K. Lee, E.J. Nestler, and P.-L. Han Adenylyl cyclase 5 (AC5) is an essential mediator of morphine action Proc. Natl. Acad. Sci. USA 103 2006 3908 3913
37. B.M. Kivell, D.J. Day, F.J. McDonald, and J.H. Miller Mu and delta opioid receptor immunoreactivity and mu receptor regulation in brainstem cells cultured from late fetal and early postnatal rats Dev. Brain Res. 149 2004 9 19
38. M.S. Kruse, J. Premont, M.-O. Krebs, and T.M. Jay Interaction of dopamine D1 with NMDA NR1 receptors in rat prefrontal cortex Eur. Neuropsychopharm. 19 2009 296 304
39. K.-W. Lee, J.-H. Hong, I.Y. Choi, Y. Che, J.-K. Lee, S.-D. Yang, C.-W. Song, H.S. Kang, J.-H. Lee, J.S. Noh, H.-S. Shin, and P.-L. Han Impaired D2 dopamine receptor function in mice lacking type 5 adenylyl cyclase J. Neurosci. 22 2002 7931 7940
40. H.K. Lee, K. Takamiya, J.S. Han, H. Man, C.H. Kim, G. Rumbaugh, S. Yu, L. Ding, C. He, R.S. Petralia, R.J. Wenthold, M. Gallagher, and R.L. Huganir Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory Cell 112 2003 631 643
41. B.E. Lonze, and D.D. Ginty Function and regulation of CREB family transcription factors in the nervous system Neuron 35 2002 605 623
42. H.-Y. Man, Y. Sekine-Aizawa, and R.L. Huganir Regulation of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit Proc Natl. Acad. Sci. USA 104 2007 3579 3584
43. A. Mansour, S. Burke, R.J. Pavlic, H. Akil, and S.J. Watson Immunohistochemical localization of the cloned κ1 receptor in the rat CNS and pituitary Neurosci. 71 1996 671 690
44. A. Mansour, C.A. Fox, H. Akil, and S.J. Watson Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications Trends Neurosci. 18 1995 22 29
45. E.B. Margolis, H. Lock, V.I. Chefer, T.S. Shippenberg, G.O. Hjelmstad, and H.L. Fields κ-Opioids selectively control dopaminergic neurons projecting to the prefrontal cortex Proc. Natl. Acad. Sci. USA 103 2006 2938 2942
46. M. Narita, Y. Matsushima, K. Niikura, M. Narita, S. Takagi, K. Nakahara, K. Kurahashi, M. Abe, M. Saeki, M. Asato, S. Imai, K. Ikeda, N. Kuzumaki, and T. Suzuki Implication of dopaminergic projection from the ventral tegmental area to the anterior cingulated cortex in μ-opioid-induced place preference Addict. Biol. 15 2010 434 447
47. M.B. Noel, and A. Gratton Electrochemical evidence of increased dopamine transmission in prefrontal cortex and nucleus accumbens elicited by ventral tegmental mu-opioid receptor activation in freely behaving rats Synapse 21 1995 110 122
48. M.C. Olianas, D. Concas, and P. Onali Agonist activity of naloxone benzoylhydrazone at recombinant and native opioid receptors Br. J. Pharmacol. 147 2006 360 370
49. M.C. Olianas, and P. Onali Mediation by G protein βγ subunits of the opioid stimulation of adenylyl cyclase activity in rat olfactory bulb Biochem. Pharmacol. 57 1999 649 652
50. P. Onali, A. Ingianni, and M.C. Olianas Dual coupling of opioid receptor-like (ORL1) receptors to adenylyl cyclase in the different layers of the rat main olfactory bulb J. Neurochem. 77 2001 1520 1530
51. P. Onali, and M.C. Olianas Naturally occurring opioid receptor agonists stimulate adenylate cyclase activity in rat olfactory bulb Mol. Pharmacol. 39 1991 436 441
52. 2-adrenergic receptors in rat brain Proc. Natl. Acad. Sci. USA 81 1984 1585 1589
53. P. Schmidt, C. Schmolke, F. Musshoff, M. Menzen, C. Prohaska, and B. Madea Area-specific increased density of μ-opioid receptor immunoreactive neurons in the cerebral cortex of drug-related fatalities Forensic Sci. Int. 133 2003 204 211
54. A.N. Schoffelmeer, F. Hogenboom, and A.H. Mulder Inhibition of dopamine-sensitive adenylate cyclase by opioids: possible involvement of physically associated mu- and delta-opioid receptors Naunyn-Schmiedeberg's Arch. Pharmacol. 335 1987 278 284
55. J.K. Seamans, and C.R. Yang The principal features and mechanisms of dopamine modulation in the prefrontal cortex Prog. Neurobiol. 74 2004 1 57
56. R.E. See Dopamine D1 receptor antagonism in the prelimbic cortex blocks the reinstatement of heroin-seeking in an animal model of relapse Int. J. Neuropsychopharmacol. 12 2009 431 436
57. A.J. Silva, J.H. Kogan, P.W. Frankland, and S. Kida CREB and memory Annu. Rev. Neurosci. 21 1998 127 148
58. G.L. Snyder, A.A. Fienberg, R.L. Hunganir, and P. Greengard A dopamine/D1 receptor/protein kinase A/dopamine- and cAMP-regulated phosphoprotein (Mr 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor J. Neurosci. 18 1998 10297 10303
59. G.L. Snyder, P.B. Allen, A.A. Fienberg, C.G. Valle, R.L. Hunganir, A.C. Nairn, and P. Greengard Regulation of phosphorylation of the GluR1 AMPA receptor in the neostriatum by dopamine and psychostimulants in vivo J. Neurosci. 20 2000 4480 4488
60. X. Sun, Y. Zhao, and M.E. Wolf Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons J. Neurosci. 25 2005 7342 7351
61. R.K. Sunahara, and R. Taussig Isoforms of mammalian adenylyl cyclase: Multiplicities of signaling Mol. Interv. 2 2002 168 184
62. A.L. Svingos, and E.E.O. Colago κ-Opioid and NMDA glutamate receptors are differentially targeted within rat medial prefrontal cortex Brain Res. 946 2002 262 271
63. K. Taki, T. Kaneko, and N. Mizuno A group of cortical interneurons expressing μ-opioid receptor-like immunoreactivity: a double immunofluorescence study in the rat cerebral cortex Neurosci. 98 2000 221 231
64. E. Tanaka, and R.A. North Opioid actions on rat anterior cingulate cortex neurons in vitro J. Neurosci. 14 1994 1106 1113
65. A.M. Thierry, S. Pirot, Y. Gioanni, and J. Glowinski Dopamine function in the prefrontal cortex Adv. Pharmacol. 42 1998 717 720
66. K.Y. Tseng, and P. O'Donnell Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms J. Neurosci. 24 2004 5131 5139
67. T.M. Tzschentke Pharmacology and behavioural pharmacology of the mesocortical dopamine system Prog. Neurobiol. 63 2001 241 320
68. A.S. Undieh Pharmacology of signaling induced by dopamine D1-like receptor activation Pharmacol. Ther. 128 2010 37 60
69. B.J. Van Vliet, A.H. Mulder, and A.N.M. Schoffelmeer μ-Opioid receptors mediate the inhibitory effect of opioids on dopamine-sensitive adenylate cyclase in primary cultures of rat neostriatal neurons J. Neurochem. 55 1990 1274 1280
70. S. Vijayraghavan, M. Wang, S.G. Birnbaum, G.V. Williams, and A.F.T. Arnsten Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory Nat. Neurosci. 10 2007 376 384
71. B.A. Vogt, R.G. Wiley, and E.L. Jensen Localization of mu and delta opioid receptors to anterior cingulate afferents and projection neurons and input/output model of mu regulation Exp. Neurol. 135 1995 83 92
72. D.W. Volk, P.V. Radchenkova, E.M. Walker, E.J. Sengupta, and D.A. Lewis Cortical opioid markers in schizophrenia and across postnatal development Cereb. Cortex. 2011
73. P.M. Wall, and C. Messier U-69,593 microinjection in the infralimbic cortex reduces anxiety and enhances spontaneous alternation memory in mice Brain Res. 856 2000 259 280
74. J.T. Williams, M.J. Christie, and O. Manzoni Cellular and synaptic adaptations mediating opioid dependence Pharmacol. Rev. 81 2001 299 343
75. G. Witkowski, and P. Szulczyk Opioid μ receptor activation inhibits sodium currents in prefrontal cortical neurons via a protein kinase A- and C-dependent mechanism Brain Res. 1094 2006 92 106
76. J. Yang, Q. Teng, M.E. Garrity-Moses, S. MacClelland 3rd, T. Federici, E. Carlton, J. Riley, and N.M. Boulis Reversible unilateral nigrostriatal pathway inhibition induced through expression of adenovirus-mediated clostridial light chain gene in the substantia nigra Neuromol. Med. 9 2007 276 284
77. M. Yoshimura, H. Ikeda, and B. Tabakoff μ-Opioid receptors inhibit dopamine-stimulated activity of type V adenylyl cyclase but enhance dopamine-stimulated activity of type VII adenylyl cyclase Mol. Pharmacol. 50 1996 4351
78. G. Zalsman, A. Molcho, Y. Huang, A. Dwork, S. Li, and J.J. Mann Postmortem μ opioid receptor binding in suicide victims and controls J. Neural. Transm. 112 2005 949 954
79. Z.Q. Zhao, Y.-J. Gao, Y.-G. Sun, C.-S. Zhao, R.W. Gereau IV, and Z.-F. Chen Central serotonergic neurons are differentially required for opioid analgesia but not for morphine tolerance or morphine reward Proc. Natl. Acad. Sci. USA 104 2007 14519 14524
80. J.K. Zubieta, T.A. Ketter, J.A. Bueller, Y. Xu, M.R. Kilbourn, E.A. Young, and R.A. Koeppe Regulation of human affective responses by anterior cingulated and limbic μ-opioid neurotransmission Arch. Gen. Psychiatry 60 2003 1145 1153