μ-opioid receptor endocytosis prevents adaptations in ventral tegmental area gaba transmission induced during naloxone-precipitated morphine withdrawal

Journal of Neuroscience

Volumn 30, Issue 9, 2010, Pages 3276-3286

  Madhavan, Anuradha ^a   He, Li ^a   Stuber, Garret D ^a   Bonci, Antonello ^a,b   Whistler, Jennifer L ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; [ADENOSINE CYCLIC 3',5' (HYDROGENPHOSPHOROTHIOATE)TRIETHYLAMMONIUM]; ADENOSINE 3',5' PHOSPHOROTHIOATE; AMMONIUM DERIVATIVE; CYCLIC AMP; MORPHINE; NALOXONE; OPIATE RECEPTOR; UNCLASSIFIED DRUG; ADENOSINE-3',5'-CYCLIC PHOSPHOROTHIOATE; DRUG DERIVATIVE; MU OPIATE RECEPTOR; NARCOTIC AGENT; NARCOTIC ANTAGONIST; NUCLEOTIDE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DESENSITIZATION; DOPAMINERGIC NERVE CELL; ENDOCYTOSIS; GABAERGIC TRANSMISSION; GROOMING; INTERNEURON; JUMPING; KNOCKOUT MOUSE; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; REARING; TREMOR; VENTRAL TEGMENTUM; WET DOG SHAKES; WILD TYPE; WITHDRAWAL SYNDROME; ADAPTATION; ANIMAL; C57BL MOUSE; CHIMERA; DISEASE MODEL; DRUG ANTAGONISM; DRUG EFFECT; GENE TARGETING; GENETICS; METABOLISM; MORPHINE ADDICTION; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CHIMERA; CYCLIC AMP; DISEASE MODELS, ANIMAL; ENDOCYTOSIS; GAMMA-AMINOBUTYRIC ACID; GENE KNOCK-IN TECHNIQUES; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MORPHINE; MORPHINE DEPENDENCE; NALOXONE; NARCOTIC ANTAGONISTS; NARCOTICS; NEURAL INHIBITION; RECEPTORS, OPIOID, MU; SUBSTANCE WITHDRAWAL SYNDROME; SYNAPTIC TRANSMISSION; THIONUCLEOTIDES; VENTRAL TEGMENTAL AREA;

EID: 77749324825     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4634-09.2010     Document Type: Article

References (37)

1. Abbadie C, Pasternak GW (2001) Differential in vivo internalization of MOR-1 and MOR-1C by morphine. Neuroreport 12:3069 -3072.
2. Alvarez VA, Arttamangkul S, Dang V, Salem A, Whistler JL, Von Zastrow M, Grandy DK, Williams JT (2002) mu-Opioid receptors: ligand-dependent activation of potassium conductance, desensitization, and internalization. J Neurosci 22:5769-5776.
3. Bagley EE, Gerke MB, Vaughan CW, Hack SP, Christie MJ (2005) GABA transporter currents activated by protein kinase A excite midbrain neurons during opioid withdrawal. Neuron 45:433- 445.
4. Baumeister AA, Anticich TG, Hebert G, Hawkins MF, Nagy M (1989) Evidence that physical dependence on morphine is mediated by the ventral midbrain. Neuropharmacology 28:1151-1157.
5. Bonci A, Williams JT (1997) Increased probability of GABA release during withdrawal from morphine. J Neurosci 17:796-803.
6. Cruz HG, Berton F, Sollini M, Blanchet C, Pravetoni M, Wickman K, Lüscher C (2008) Absence and rescue of morphine withdrawal in GIRK/Kir3 knock-out mice. J Neurosci 28:4069-4077.
7. Duman RS, Tallman JF, Nestler EJ (1988) Acute and chronic opiateregulation of adenylate cyclase in brain: specific effects in locus coeruleus. J Pharmacol Exp Ther 246:1033-1039.
8. Duttaroy A, Yoburn BC (1995) The effect of intrinsic efficacy on opioid tolerance. Anesthesiology 82:1226 -1236.
9. Finn AK, Whistler JL (2001) Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32:829-839.
10. Grace AA, Onn SP (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463-3481.
11. Grecksch G, Bartzsch K, Widera A, Becker A, Hollt V, Koch T (2006) Development of tolerance and sensitization to different opioid agonists in rats. Psychopharmacology (Berl) 186:177-184.
12. He L, Whistler JL (2005) An opiate cocktail that reduces morphine tolerance and dependence. Curr Biol 15:1028 -1033.
13. He L, Fong J, von Zastrow M, Whistler JL (2002) Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell 108:271-282.
14. Johnson SW, North RA (1992a) Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450:455- 468.
15. Johnson SW, North RA (1992b) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483- 488.
16. Kaplan GB, Sethi RK, McClelland EG, Leite-Morris KA (1998) Regulation of G protein-mediated adenylyl cyclase in striatum and cortex of opiatedependent and opiate withdrawing mice. Brain Res 788:104 -110.
17. Keith DE, Murray SR, Zaki PA, Chu PC, Lissin DV, Kang L, Evans CJ, von ZastrowM (1996) Morphine activates opioid receptors without causing their rapid internalization. J Biol Chem 271:19021-19024.
18. Keith DE, Anton B, Murray SR, Zaki PA, Chu PC, Lissin DV, Monteillet-Agius G, Stewart PL, Evans CJ, von Zastrow M (1998) mu-Opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in the mammalian brain. Mol Pharmacol 53:377-384.
19. Kim JA, Bartlett S, He L, Nielsen CK, Chang AM, Kharazia V, Waldhoer M, Ou CJ, Taylor S, Ferwerda M, Cado D, Whistler JL (2008) Morphineinduced receptor endocytosis in a novel knockin mouse reduces tolerance and dependence. Curr Biol 18:129 -135.
20. Koch T, Schulz S, Pfeiffer M, Klutzny M, Schröder H, Kahl E, Höllt V (2001) C-terminal splice variants of the mouse mu-opioid receptor differ in morphine-induced internalization and receptor resensitization. J Biol Chem 276:31408 -31414.
21. Laviolette SR, Gallegos RA, Henriksen SJ, van der Kooy D (2004) Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat Neurosci 7:160 -169.
22. Maldonado R, Stinus L, Gold LH, Koob GF (1992) Role of different brain structures in the expression of the physical morphine withdrawal syndrome. J Pharmacol Exp Ther 261:669-677.
23. Nestler EJ (2004) Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol Sci 25:210 -218.
24. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
25. Phillips AG, LePiane FG (1980) Reinforcing effects of morphine microinjection into the ventral tegmental area. Pharmacol Biochem Behav 12:965-968.
26. Rasmussen K, Beitner-Johnson DB, Krystal JH, Aghajanian GK, Nestler EJ (1990) Opiate withdrawal and the rat locus coeruleus: behavioral, electrophysiological, and biochemical correlates. J Neurosci 10:2308 -2317.
27. Schulteis G, Markou A, Gold LH, Stinus L, Koob GF (1994) Relative sensitivity to naloxone of multiple indices of opiate withdrawal: a quantitative dose-response analysis. J Pharmacol Exp Ther 271:1391-1398.
28. Sheu MJ, Sribanditmongkol P, Santosa DN, Tejwani GA (1995) Inhibition of morphine tolerance and dependence by diazepam and its relation to cyclic AMP levels in discrete rat brain regions and spinal cord. Brain Res 675:31-37.
29. Stinus L, Le Moal M, Koob GF (1990) Nucleus accumbens and amygdala are possible substrates for the aversive stimulus effects of opiate withdrawal. Neuroscience 37:767-773.
30. Trafton JA, Abbadie C, Marek K, Basbaum AI (2000) Postsynaptic signaling via the μ-opioid receptor: responses of dorsal horn neurons to exogenous opioids and noxious stimulation. J Neurosci 20:8578-8584.
31. Vargas-Perez H, Kee RT, Walton CH, Hansen DM, Razavi R, Clarke L, Bufalino MR, Allison DW, Steffensen SC, van der Kooy D (2009) Ventral tegmental area BDNF induces an opiate-dependent-like reward state in naive rats. Science 324:1732-1734.
32. Walker EA, Young AM (2001) Differential tolerance to antinociceptive effects of mu opioids during repeated treatment with etonitazene, morphine, or buprenorphine in rats. Psychopharmacology (Berl) 154:131-142.
33. Whistler JL, Chuang HH, Chu P, Jan LY, von ZastrowM (1999) Functional dissociation of mu opioid receptor signaling and endocytosis: implications for the biology of opiate tolerance and addiction. Neuron 23:737-746.
34. 2+ channels. J Neurosci 15:4124-4132.
35. Williams JT, Christie MJ, Manzoni O (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81:299 -343.
36. Wise RA (1989) Opiate reward: sites and substrates. Neurosci Biobehav Rev 13:129 -133.
37. Yu Y, Zhang L, Yin X, Sun H, Uhl GR, Wang JB (1997) Mu opioid receptor phosphorylation, desensitization, and ligand efficacy. J Biol Chem 272: 28869-28874.