Recovery from μ-opioid receptor desensitization after chronic treatment with morphine and methadone

Journal of Neuroscience

Volumn 31, Issue 12, 2011, Pages 4434-4443

  Quillinan, Nidia ^a   Lau, Elaine K ^b   Virk, Michael ^a   Von Zastrow, Mark ^b   Williams, John T ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN 2; G PROTEIN RECEPTOR KINASE 2; METENKEPHALIN; METHADONE; MORPHINE; MU OPIATE RECEPTOR; PROTEIN KINASE; UNCLASSIFIED DRUG; BETA ARRESTIN; G PROTEIN COUPLED RECEPTOR KINASE 2; NARCOTIC AGENT; RETINA S ANTIGEN;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; ENZYME ACTIVITY; ENZYME INHIBITION; MALE; NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR DOWN REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN LEVEL; C57BL MOUSE; DRUG EFFECTS; ENDOCYTOSIS; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE;

ANIMALS; ARRESTINS; BRAIN CHEMISTRY; ENDOCYTOSIS; G-PROTEIN-COUPLED RECEPTOR KINASE 2; MALE; METHADONE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MORPHINE; NARCOTICS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU;

EID: 79953003987     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4874-10.2011     Document Type: Article

References (38)

1. 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. (Pubitemid 35386500)
2. Arttamangkul S, Quillinan N, Low MJ, von Zastrow M, Pintar J, Williams JT (2008) Differential activation and trafficking of micro-opioid receptors in brain slices. Mol Pharmacol 74:972-979.
3. Bagley EE, Chieng BC, Christie MJ, Connor M (2005) Opioid tolerance in periaqueductal gray neurons isolated from mice chronically treated with morphine. Br J Pharmacol 146:68-76.
4. Bailey CP, Couch D, Johnson E, Griffiths K, Kelly E, Henderson G (2003) μ-opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine. J Neurosci 23:10515-10520. (Pubitemid 37485264)
5. Bailey CP, Llorente J, Gabra BH, Smith FL, Dewey WL, Kelly E, Henderson G (2009a) Role of protein kinase C and μ-opioid receptor (MOPr) desensitization in tolerance to morphine in rat locus coeruleus neurons. Eur J Neurosci 29:307-318.
6. Bailey CP, Oldfield S, Llorente J, Caunt CJ, Teschemacher AG, Roberts L, McArdle CA, Smith FL, Dewey WL, Kelly E, Henderson G (2009b) 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.
7. Blake AD, Bot G, Li S, Freeman JC, Reisine T (1997) Differential agonist regulation of the human kappa-opioid receptor. J Neurochem 68:1846-1852. (Pubitemid 27176119)
8. Bohn LM, Gainetdinov RR, Lin FT, Lefkowitz RJ, Caron MG (2000) Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 408:720-723. (Pubitemid 32015987)
9. Bohn LM, Dykstra LA, Lefkowitz RJ, Caron MG, Barak LS (2004) Relative opioid efficacy is determined by the complements of the G protein-coupled receptor desensitization machinery. Mol Pharmacol 66:106-112. (Pubitemid 38822092)
10. Borgland SL, Connor M, Osborne PB, Furness JB, Christie MJ (2003) Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors. J Biol Chem 278:18776-18784. (Pubitemid 36799259)
11. Chavkin C, Goldstein A (1984) Opioid receptor reserve in normal and morphine-tolerance guinea pig ileum myenteric plexus. Proc Natl Acad Sci U S A 81:7253-7257. (Pubitemid 15216736)
12. Christie MJ (2008) Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addition. Br J Phamacol 154:384-396.
13. Christie MJ, Williams JT, North RA (1987) Cellular mechanisms of opioid tolerance: studies in single brain neurons. Mol Pharmacol 32:633-638. (Pubitemid 18004177)
14. Dang VC, Williams JT (2004) Chronic morphine treatment reduces recovery from opioid desensitization. J Neurosci 24:7699-7706. (Pubitemid 39186825)
15. Dang VC, Napier IA, Christie MJ (2009) Two distinct mechanisms mediate acute mu-opioid receptor desensitization in native neurons. J Neurosci 29:3322-3327.
16. Finn AK, Whistler JL (2001) Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32:829-839. (Pubitemid 34024844)
17. Gainetdinov RR, Premont RT, Bohn LM, Lefkowitz RJ, Caron MG (2004) Desensitization of G protein-coupled receptors and neuronal functions. Annu Rev Neurosci 27:107-144. (Pubitemid 39050399)
18. Gintzler AR, Chakrabarti S (2008) The ambiguities of opioid tolerance mechanisms: barriers to pain therapeutics or new pain therapeutic possibilities. J Pharmacol Exp Ther 325:709-713. (Pubitemid 351724306)
19. Grecksch G, Bartzsch K, Widera A, Becker A, Höllt V, Koch T (2006) Development of tolerance and sensitization to different opioid agonists in rats. Psychopharmacology 186:177-184. (Pubitemid 43727334)
20. Harris GC, Williams JT (1991) Transient homologous mu-opioid receptor desensitization in rat locus coeruleus neurons. J Neurosci 11:2574-2581.
21. Jaber M, Koch WJ, Rockman H, Smith B, Bond RA, Sulik KK, Ross J Jr, Lefkowitz RJ, Caron MG, Giros B (1996) Essential role of beta-adrenergic receptor kinase 1 in cardiac development and function. Proc Natl Acad Sci U S A 93:12974-12979. (Pubitemid 26382754)
22. Johnson EA, Oldfield S, Braksator E, Gonzalez-Cuello A, Couch D, Hall KJ, Mundell SJ, Bailey CP, Kelly E, Henderson G (2006) Agonist-selective mechanisms of mu-opioid receptor desensitization in human embryonic kidney 293 cells. Mol Pharmacol 70:676-685. (Pubitemid 44092328)
23. Kenski DM, Zhang C, von Zastrow M, Shokat KM (2005) Chemical genetic engineering of G protein-coupled receptor kinase 2. J Biol Chem 280:35051-35061. (Pubitemid 41504640)
24. Kieffer BL, Evans CJ (2002) Opioid tolerance: in search of the holy grail. Cell 108:587-590. (Pubitemid 34241419)
25. Koch T, Höllt V (2008) Role of receptor internalization in opioid tolerance and dependence. Pharmacol Ther 117:199-206.
26. Koch T, Widera A, Bartzsch K, Schulz S, Brandenburg LO, Wundrack N, Beyer A, Grecksch G, Höllt V (2005) Receptor endocytosis counteracts the development of opioid tolerance. Mol Pharmacol 67:280-287. (Pubitemid 40069989)
27. Martini L, Whistler JL (2007) The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Curr Opin Neurobiol 17:556-564.
28. Osborne PB, Williams JT (1995) Characterization of acute homologous desensitization of μ-opioid receptor-induced current in locus coeruleus neurones. Br J Pharmacol 115:925-932.
29. Rodriguez-Martin I, Braksator E, Bailey CP, Goodchild S, Marrion NV, Kelly E, Henderson G (2008) Methadone: does it really have low efficacy at μ-opioid receptors? Neuroreport 19:589-593.
30. Ross GR, Gabra BH, Dewey WL, Akbarali HI (2008) Morphine tolerance in the mouse ileum and colon. J Pharmacol Exp Ther 327:561-572.
31. Schulz S, Mayer D, Pfeiffer M, Stumm R, Koch T, Höllt V (2004) Morphine induces terminal micro-opioid receptor desensitization by sustained phosphorylation of serine-375. EMBO J 23:3282-3289. (Pubitemid 39209152)
32. Stafford K, Gomes AB, Shen J, Yoburn BC (2001) mu-Opioid receptor downregulation contributes to opioid tolerance in vivo. Pharmacol Biochem Behav 69:233-237. (Pubitemid 32566268)
33. Torrecilla M, Quillinan N, Williams JT, Wickman K (2008) Pre- and post-synaptic regulation of locus coeruleus neurons after chronic morphine treatment: a study of GIRK-knockout mice. Eur J Neurosci 28:618-624. (Pubitemid 352040411)
34. Walker EA, Young AM (2001) Differential tolerance to antinociceptive effects of mu opioids during repeated treatment with etonitazene, morphine, or buprenorphine in rats. Psychopharmacology 154:131-142. (Pubitemid 32186498)
35. Walwyn W, Evans CJ, Hales TG (2007) Beta-arrestin2 and c-Src regulate the constitutive activity and recycling of μ opioid receptors in dorsal root ganglion neurons. J Neurosci 27:5092-5104. (Pubitemid 46741772)
36. Whistler JL, Chuang HH, Chu P, Jan LY, von Zastrow M (1999) Functional dissociation of mu opioid receptor signaling and endocytosis: implications for the biology of opiate tolerance and addiction. Neuron 23:737-746. (Pubitemid 29411563)
37. Williams JT, Christie MJ, Manzoni O (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81:299-343. (Pubitemid 32096178)
38. 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. (Pubitemid 27498167)