Functional selectivity and time-dependence of μ-opioid receptor desensitization at nerve terminals in the mouse ventral tegmental area

British Journal of Pharmacology

Volumn 172, Issue 2, 2015, Pages 469-481

  Lowe, J D ^a,b   Bailey, C P ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

desensitization; GPCR kinase (GRK); morphine; nerve terminal; opiate; opioid; PKC; tolerance; ventral tegmental area (VTA)

Indexed keywords

MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; PROTEIN KINASE C; 4 AMINOBUTYRIC ACID RECEPTOR; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; METENKEPHALIN; MORPHINE; NARCOTIC ANALGESIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; CELL BODY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; GABAERGIC SYSTEM; INCUBATION TIME; MALE; MOUSE; NERVE ENDING; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR DOWN REGULATION; REVIEW; SIGNAL TRANSDUCTION; VENTRAL TEGMENTUM; WHOLE CELL PATCH CLAMP; ACTION POTENTIAL; AGONISTS; ANIMAL; C57BL MOUSE; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; IN VITRO STUDY; PHYSIOLOGY;

ACTION POTENTIALS; ANALGESICS, OPIOID; ANIMALS; DOPAMINERGIC NEURONS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; ENKEPHALIN, METHIONINE; GABAERGIC NEURONS; IN VITRO TECHNIQUES; MALE; MICE, INBRED C57BL; MORPHINE; PROTEIN KINASE C; RECEPTORS, OPIOID, MU; VENTRAL TEGMENTAL AREA;

EID: 84920156138     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12605     Document Type: Review

References (55)

1. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G Protein-Coupled Receptors. Br J Pharmacol 170: 1459-1581.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Catterall WA, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: Ion Channels. Br J Pharmacol 170: 1607-1651.
3. Alvarez VA, Arttamangkul S, Dang V, Salem A, Whistler JL, Von Zastrow M, et al. (2002). mu-Opioid receptors: ligand-dependent activation of potassium conductance, desensitization, and internalization. J Neurosci 13: 5769-5776.
4. Arden JR, Segredo V, Wang Z, Lameh J, Sadee W, (1995). Phosphorylation and agonist-specific intracellular trafficking of an epitope-tagged mu-opioid receptor expressed in HEK 293 cells. J Neurochem 65: 1636-1645.
5. 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.
6. Bailey CP, Couch D, Johnson E, Griffiths K, Kelly E, Henderson G, (2003). Mu-opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine. J Neurosci 23: 10515-10520.
7. Bailey CP, Kelly E, Henderson G, (2004). Protein kinase C activation enhances morphine-induced rapid desensitization of mu-opioid receptors in mature rat locus ceruleus neurons. Mol Pharmacol 66: 1592-1598.
8. Bailey CP, Oldfield S, Llorente J, Caunt CJ, Teschemacher AG, Roberts L, et al. (2009). Involvement of PKC alpha and G-protein-coupled receptor kinase 2 in agonist-selective desensitization of mu-opioid receptors in mature brain neurons. Br J Pharmacol 158: 157-164.
9. Bergevin A, Girardot D, Bourque MJ, Trudeau LE, (2002). Presynaptic mu-opioid receptors regulate a late step of the secretory process in rat ventral tegmental area GABAergic neurons. Neuropharmacology 42: 1065-1078.
10. Blanchet C, Lüscher C, (2002). Desensitization of mu-opioid receptor-evoked potassium currents: initiation at the receptor, expression at the effector. Proc Natl Acad Sci U S A 99: 4674-4679.
11. Blanchet C, Sollini M, Luscher C, (2003). Two distinct forms of desensitisation of G-protein coupled inwardly rectifying potassium currents evoked by alkaloid and peptide μ-opioid receptor agonists. Mol Cell Neurosci 24: 517-523.
12. Bonci A, Williams JT, (1997). Increased probability of GABA release during withdrawal from morphine. J Neurosci 17: 796-803.
13. Bozarth MA, Wise RA, (1981). Intracranial self-administration of morphine into the ventral tegmental area in rats. Life Sci 28: 551-555.
14. Cameron DL, Wessendorf MW, Williams JT, (1997). A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids. Neuroscience 77: 155-166.
15. Chieng B, Azriel Y, Mohammadi S, Christie MJ, (2011). Distinct cellular properties of identified dopaminergic and GABAergic neurons in the mouse ventral tegmental area. J Physiol 589: 3775-3787.
16. Christie MJ, Williams JT, North RA, (1987). Cellular mechanisms of opioid tolerance: studies in single brain neurons. Mol Pharmacol 32: 633-638.
17. Doll C, Konietzko J, Poll F, Koch T, Hollt V, Schulz S, (2011). Agonist-selective patterns of μ-opioid receptor phosphorylation revealed by phosphosite-specific antibodies. Br J Pharmacol 164: 298-307.
18. Feng B, Li Z, Wang JB, (2011). Protein kinase C-mediated phosphorylation of the μ-opioid receptor and its effects on receptor signaling. Mol Pharmacol 79: 768-775.
19. Fyfe LW, Cleary DR, Macey TA, Morgan MM, Ingram SL, (2010). Tolerance to the antinociceptive effect of morphine in the absence of short-term presynaptic desensitization in rat periaqueductal gray neurons. J Pharmacol Exp Ther 335: 674-680.
20. Grecksh G, Just S, Pierstorff C, Imhof AK, Gluck L, Doll C, et al. (2011). Analgesic tolerance to high-efficacy agonists but not to morphine is diminished in phosphorylation-deficient S375A μ-opioid receptor knock-in mice. J Neurosci 31: 13890-13896.
21. Harris GC, Williams JT, (1991). Transient homologous mu-opioid receptor desensitization in rat locus coeruleus neurons. J Neurosci 11: 2574-2581.
22. Jalabert M, Bourdy R, Courtin J, Veinante P, Manzoni OJ, Barrot M, et al. (2011). Neuronal circuits underlying acute morphine action on dopamine neurons. Proc Natl Acad Sci U S A 108: 16446-16450.
23. Jin W, Lu Z, (1999). Synthesis of a stable form of tertiapin: a high-affinity inhibitor for inward-rectifier K+ channels. Biochemistry 38: 14286-14293.
24. Johnson EA, Oldfield S, Braksator E, Gonzalez-Cuello A, Couch D, Hall KJ, et al. (2006). Agonist-selective mechanisms of mu-opioid receptor desensitization in human embryonic kidney 293 cells. Mol Pharmacol 70: 676-685.
25. Johnson SW, North RA, (1992a). Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12: 483-488.
26. Johnson SW, North RA, (1992b). Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450: 455-468.
27. Kelly E, Bailey CP, Henderson G, (2008). Agonist-selective mechanisms of GPCR desensitization. Br J Pharmacol 153 (Suppl. 1): S379-S388.
28. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
29. Koch T, Schulz S, Pfeiffer M, Klutzny M, Schroder H, Kahl E, et al. (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.
30. Kovoor A, Celver JP, Wu A, Chavkin C, (1998). Agonist induced homologous desensitization of mu-opioid receptors mediated by G protein-coupled receptor kinases is dependent on agonist efficacy. Mol Pharmacol 54: 704-711.
31. Law PY, Erickson LJ, El-Kouhen R, Dicker L, Solberg J, Wang W, et al. (2000). Receptor density and recycling affect the rate of agonist-induced desensitization of mu-opioid receptor. Mol Pharmacol 58: 388-398.
32. Levitt ES, Williams JT, (2012). Morphine desensitization and cellular tolerance are distinguished in rat locus ceruleus neurons. Mol Pharmacol 82: 983-992.
33. Llorente J, Lowe JD, Sanderson HS, Tsisanova E, Kelly E, Henderson G, et al. (2012). μ-Opioid receptor desensitization: homologous or heterologous? Eur J Neurosci 36: 3636-3642.
34. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
35. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T, (2006). Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10: 839-850.
36. Margolis EB, Lock H, Hjelmstad GO, Fields HL, (2006). The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol 577: 907-924.
37. Marker CL, Stoffel M, Wickman K, (2004). Spinal G-protein-gated K + channels formed by GIRK1 and GIRK2 subunits modulate thermal nociception and contribute to morphine analgesia. J Neurosci 24: 2806-2812.
38. Matsui A, Williams JT, (2011). Opioid-sensitive GABA inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons. J Neurosci 31: 17729-17735.
39. McPherson J, Rivero G, Baptist M, Llorente J, Al-Sabah S, Krasel C, et al. (2010). μ-opioid receptors: correlation of agonist efficacy for signalling with ability to activate internalization. Mol Pharmacol 78: 756-766.
40. Melief EJ, Miyatake M, Bruchas MR, Chavkin C, (2010). Ligand-directed c-Jun N-terminal kinase activation disrupts opioid receptor signaling. Proc Natl Acad Sci U S A 107: 11608-11613.
41. Miller RJ, (1998). Presynaptic receptors. Annu Rev Pharmacol Toxicol 38: 201-207.
42. Mitrovic I, Margeta-Mitrovic M, Bader S, Stoffel M, Jan LY, Basbaum AI, (2003). Contribution of GIRK2-mediated postsynaptic signaling to opiate and alpha 2-adrenergic analgesia and analgesic sex differences. Proc Natl Acad Sci U S A 100: 271-276.
43. Nakamura A, Fujita M, Ono H, Hongo Y, Kanbara T2, Ogawa K, et al. (2013). G protein-gated inwardly rectifying potassium (GIRK) channels play a primary role in the antinociceptive effect of oxycodone, but not morphine, at supraspinal sites. Br J Pharmacol 171: 253-264.
44. Patierno S, Anselmi L, Jaramillo I, Scott D, Garcia R, Sternini C, (2011). Morphine induces μ opioid receptor endocytosis in guinea pig enteric neurons following prolonged receptor activation. Gastroenterology 140: 618-626.
45. Pennock RL, Dicken MS, Hentges ST, (2012). Multiple inhibitory G-protein-coupled receptors resist acute desensitization in the presynaptic but not postsynaptic compartments of neurons. J Neurosci 32: 10192-10200.
46. Pennock RL, Hentges ST, (2011). Differential expression and sensitivity of presynaptic and postsynaptic opioid receptors regulating hypothalamic proopiomelanocortin neurons. J Neurosci 31: 281-288.
47. Ramirez DM, Kavalali ET, (2011). Differential regulation of spontaneous and evoked neurotransmitter release at central synapses. Curr Opin Neurobiol 21: 275-282.
48. Sesack SR, Pickel VM, (1995). Ultrastructural relationships between terminals immunoreactive for enkephalin, GABA, or both transmitters in the rat ventral tegmental area. Brain Res 672: 261-275.
49. Vaughan CW, Ingram SL, Connor MA, Christie MJ, (1997). How opioids inhibit GABA-mediated neurotransmission. Nature 390: 611-614.
50. Wetherington JP, Lambert NA, (2002a). Differential desensitization of responses mediated by presynaptic and postsynaptic A1 adenosine receptors. J Neurosci 22: 1248-1255.
51. Wetherington JP, Lambert NA, (2002b). GABA(B) receptor activation desensitizes postsynaptic GABA(B) and A(1) adenosine responses in rat hippocampal neurones. J Physiol 544: 459-467.
52. Whistler JL, von Zastrow M, (1998). Morphine-activated opioid receptors elude desensitization by beta-arrestin. Proc Natl Acad Sci U S A 95: 9914-9919.
53. Williams JT, Ingram SL, Henderson G, Chavkin C, von Zastrow M, Schulz S, et al. (2013). Regulation of μ-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol Rev 65: 223-254.
54. Xia Y, Driscoll JR, Wilbrecht L, Margolis EB, Fields HL, Hjelmstad GO, (2011). Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J Neurosci 31: 7811-7816.
55. Zheng H, Chu J, Zhang Y, Loh HH, Law PY, (2011). Modulating micro-opioid receptor phosphorylation switches agonist-dependent signaling as reflected in PKCepsilon activation and dendritic spine stability. J Biol Chem 286: 12724-12733.