Opioid receptor internalization contributes to dermorphin-mediated antinociception

Neuroscience

Volumn 168, Issue 2, 2010, Pages 543-550

  Macey, T A ^a   Ingram, S L ^a   Bobeck, E N ^a   Hegarty, D M ^b   Aicher, S A ^b   Arttamangkul, S ^b   Morgan, M M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Analgesia; Endocytosis; Opiate; Pain modulation; Periaqueductal gray

Indexed keywords

BICUCULLINE; CHLORNALTREXAMINE; CONCANAVALIN A; DERM A 594; DERMORPHIN DERIVATIVE; DYNAMIN; DYNAMIN DOMINANT NEGATIVE INHIBITORY PEPTIDE; G PROTEIN COUPLED RECEPTOR; MU OPIATE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; HOT PLATE TEST; INTERNALIZATION; LATENT PERIOD; MALE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; WAKEFULNESS;

ANALGESICS, OPIOID; ANIMALS; BICUCULLINE; CONCANAVALIN A; DYNAMINS; FLUORESCENT DYES; MALE; MICROINJECTIONS; NALTREXONE; NEURONS; OPIOID PEPTIDES; PAIN; PAIN MEASUREMENT; PEPTIDES; PERIAQUEDUCTAL GRAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, OPIOID, MU;

EID: 77952878395     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.04.003     Document Type: Article

References (62)

1. Alvarez V.A., Arttamangkul S., Dang V., Salem A., Whistler J.L., Von Zastrow M., Grandy D.K., Williams J.T. mu-Opioid receptors: ligand-dependent activation of potassium conductance, desensitization, and internalization. J Neurosci 2002, 22:5769-5776.
2. Amiche M., Sagan S., Mor A., Pelaprat D., Rostene W., Delfour A., Nicolas P. Characterisation and visualisation of [3H] dermorphin binding to mu opioid receptors in the rat brain. Combined high selectivity and affinity in a natural peptide agonist for the morphine (mu) receptor. Eur J Biochem 1990, 189:625-635.
3. Arttamangkul S., Alvarez-Maubecin V., Thomas G., Williams J.T., Grandy D.K. Binding and internalization of fluorescent opioid peptide conjugates in living cells. Mol Pharmacol 2000, 58:1570-1580.
4. Arttamangkul S., Quillinan N., Low M.J., von Zastrow M., Pintar J., Williams J.T. Differential activation and trafficking of micro-opioid receptors in brain slices. Mol Pharmacol 2008, 74:972-979.
5. Arttamangkul S., Torrecilla M., Kobayashi K., Okano H., Williams J.T. Separation of mu-opioid receptor desensitization and internalization: endogenous receptors in primary neuronal cultures. J Neurosci 2006, 26:4118-4125.
6. Bailey C.P., Couch D., Johnson E., Griffiths K., Kelly E., Henderson G. Mu-opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine. J Neurosci 2003, 23:10515-10520.
7. Bobeck E.N., McNeal A.L., Morgan M.M. Drug dependent sex-differences in periaqueducatal gray mediated antinociception in the rat. Pain 2009, 147:210-216.
8. Bodnar R., Paul D., Pasternak G.W. Synergistic analgesic interactions between the periaqueductal gray and the locus coeruleus. Brain Res 1991, 558:224-230.
9. Bodnar R.J., Williams C.L., Lee S.J., Pasternak G.W. Role of mu 1-opiate receptors in supraspinal opiate analgesia: a microinjection study. Brain Res 1988, 447:25-34.
10. Bohn L.M., Dykstra L.A., Lefkowitz R.J., Caron M.G., Barak L.S. Relative opioid efficacy is determined by the complements of the G protein-coupled receptor desensitization machinery. Mol Pharmacol 2004, 66:106-112.
11. Bohn L.M., Lefkowitz R.J., Gainetdinov R.R., Peppel K., Caron M.G., Lin F.T. Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 1999, 286:2495-2498.
12. Borgland S.L., Connor M., Osborne P.B., Furness J.B., Christie M.J. Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors. J Biol Chem 2003, 278:18776-18784.
13. Chen W., Song B., Lao L., Perez O.A., Kim W., Marvizon J.C. Comparing analgesia and mu-opioid receptor internalization produced by intrathecal enkephalin: requirement for peptidase inhibition. Neuropharmacology 2007, 53:664-676.
14. Chen W., Song B., Zhang G., Marvizon J.C. Effects of veratridine and high potassium on micro-opioid receptor internalization in the rat spinal cord: stimulation of opioid release versus inhibition of internalization. J Neurosci Methods 2008, 170:285-293.
15. Commons K.G. Translocation of presynaptic delta opioid receptors in the ventrolateral periaqueductal gray after swim stress. J Comp Neurol 2003, 464:197-207.
16. Dang V.C., Williams J.T. Chronic morphine treatment reduces recovery from opioid desensitization. J Neurosci 2004, 24:7699-7706.
17. Dang V.C., Williams J.T. Morphine-induced mu-opioid receptor desensitization. Mol Pharmacol 2005, 68:1127-1132.
18. Duchardt F., Fotin-Mleczek M., Schwarz H., Fischer R., Brock R. A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 2007, 8:848-866.
19. Fang F.G., Haws C.M., Drasner K., Williamson A., Fields H.L. Opioid peptides (DAGO-enkephalin, dynorphin A(1-13), BAM 22P) microinjected into the rat brainstem: comparison of their antinociceptive effect and their effect on neuronal firing in the rostral ventromedial medulla. Brain Res 1989, 501:116-128.
20. Finn A.K., Whistler J.L. Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 2001, 32:829-839.
21. Hack S.P., Bagley E.E., Chieng B.C., Christie M.J. Induction of delta-opioid receptor function in the midbrain after chronic morphine treatment. J Neurosci 2005, 25:3192-3198.
22. He L., Fong J., von Zastrow M., Whistler J.L. Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell 2002, 108:271-282.
23. Ignatova E.G., Belcheva M.M., Bohn L.M., Neuman M.C., Coscia C.J. Requirement of receptor internalization for opioid stimulation of mitogen-activated protein kinase: biochemical and immunofluorescence confocal microscopic evidence. J Neurosci 1999, 19:56-63.
24. Ingram S.L., Traynor J.R. Role of PKC in functional selectivity at the mu-opioid receptor: from pharmacological curiosity to therapeutic potential. Br J Pharmacol 2009, 158:154-156.
25. Jacquet Y.F., Lajtha A. The periaqueductal gray: site of morphine analgesia and tolerance as shown by 2-way cross tolerance between systemic and intracerebral injections. Brain Res 1976, 103:501-513.
26. Keith D.E., Murray S.R., Zaki P.A., Chu P.C., Lissin D.V., Kang L., Evans C.J., von Zastrow M. Morphine activates opioid receptors without causing their rapid internalization. J Biol Chem 1996, 271:19021-19024.
27. Kelly E., Bailey C.P., Henderson G. Agonist-selective mechanisms of GPCR desensitization. Br J Pharmacol 2008, 153(Suppl 1):S379-S388.
28. Kim J.A., Bartlett S., He L., Nielsen C.K., Chang A.M., Kharazia V., Waldhoer M., Ou C.J., Taylor S., Ferwerda M., Cado D., Whistler J.L. Morphine-induced receptor endocytosis in a novel knockin mouse reduces tolerance and dependence. Curr Biol 2008, 18:129-135.
29. Kim S.J., Kim M.Y., Lee E.J., Ahn Y.S., Baik J.H. Distinct regulation of internalization and mitogen-activated protein kinase activation by two isoforms of the dopamine D2 receptor. Mol Endocrinol 2004, 18:640-652.
30. Koch T., Hollt V. Role of receptor internalization in opioid tolerance and dependence. Pharmacol Ther 2008, 117:199-206.
31. Koch T., Widera A., Bartzsch K., Schulz S., Brandenburg L.O., Wundrack N., Beyer A., Grecksch G., Hollt V. Receptor endocytosis counteracts the development of opioid tolerance. Mol Pharmacol 2005, 67:280-287.
32. Kramer H.K., Simon E.J. mu and delta-opioid receptor agonists induce mitogen-activated protein kinase (MAPK) activation in the absence of receptor internalization. Neuropharmacology 2000, 39:1707-1719.
33. Lane D.A., Morgan M.M. Antinociceptive tolerance to morphine from repeated nociceptive testing in the rat. Brain Res 2005, 1047:65-71.
34. Lane D.A., Patel P.A., Morgan M.M. Evidence for an intrinsic mechanism of antinociceptive tolerance within the ventrolateral periaqueductal gray of rats. Neuroscience 2005, 135:227-234.
35. Lao L., Song B., Chen W., Marvizon J.C. Noxious mechanical stimulation evokes the segmental release of opioid peptides that induce mu-opioid receptor internalization in the presence of peptidase inhibitors. Brain Res 2008, 1197:85-93.
36. Liao D., Grigoriants O.O., Wang W., Wiens K., Loh H.H., Law P.Y. Distinct effects of individual opioids on the morphology of spines depend upon the internalization of mu opioid receptors. Mol Cell Neurosci 2007, 35:456-469.
37. Luttrell L.M., Daaka Y., Della Rocca G.J., Lefkowitz R.J. G protein-coupled receptors mediate two functionally distinct pathways of tyrosine phosphorylation in rat 1a fibroblasts. Shc phosphorylation and receptor endocytosis correlate with activation of Erk kinases. J Biol Chem 1997, 272:31648-31656.
38. Macey T.A., Bobeck E.N., Hegarty D.M., Aicher S.A., Ingram S.L., Morgan M.M. ERK1/2 activation counteracts morphine tolerance in the periaqueductal gray of the rat. J Pharmacol Exp Ther 2009, 331:412-418.
39. Macey T.A., Lowe J.D., Chavkin C. Mu opioid receptor activation of ERK1/2 is GRK3 and arrestin dependent in striatal neurons. J Biol Chem 2006, 281:34515-34524.
40. Morgan M.M., Ashley M.D., Ingram S.L., Christie M.J. Behavioral consequences of delta-opioid receptor activation in the periaqueductal gray of morphine tolerant rats. Neural Plast 2009, 2009:516328.
41. Morgan M.M., Clayton C.C. Defensive behaviors evoked from the ventrolateral periaqueductal gray of the rat: comparison of opioid and GABA disinhibition. Behav Brain Res 2005, 164:61-66.
42. Morgan M.M., Fossum E.N., Levine C.S., Ingram S.L. Antinociceptive tolerance revealed by cumulative intracranial microinjections of morphine into the periaqueductal gray in the rat. Pharmacol Biochem Behav 2006, 85:214-219.
43. Morgan M.M., Whitney P.K., Gold M.S. Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res 1998, 804:159-166.
44. Murphy J.E., Padilla B.E., Hasdemir B., Cottrell G.S., Bunnett N.W. Endosomes: a legitimate platform for the signaling train. Proc Natl Acad Sci U S A 2009, 106:17615-17622.
45. Ossipov M.H., Kovelowski C.J., Nichols M.L., Hruby V.J., Porreca F. Characterization of supraspinal antinociceptive actions of opioid delta agonists in the rat. Pain 1995, 62:287-293.
46. Paxinos G., Watson S.J. The rat brain in stereotaxic coordinates 2005, Academic Press, Sydney.
47. Pippig S., Andexinger S., Lohse M.J. Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization. Mol Pharmacol 1995, 47:666-676.
48. Pradhan A.A., Becker J.A., Scherrer G., Tryoen-Toth P., Filliol D., Matifas A., Massotte D., Gaveriaux-Ruff C., Kieffer B.L. In vivo delta opioid receptor internalization controls behavioral effects of agonists. PLoS One 2009, 4:e5425.
49. Randich A., Thurston C.L., Ludwig P.S., Robertson J.D., Rasmussen C. Intravenous morphine-induced activation of vagal afferents: peripheral, spinal, and CNS substrates mediating inhibition of spinal nociception and cardiovascular responses. J Neurophysiol 1992, 68:1027-1045.
50. Rossi G.C., Pasternak G.W., Bodnar R.J. Mu and delta opioid synergy between the periaqueductal gray and the rostro-ventral medulla. Brain Res 1994, 665:85-93.
51. Sorkin A., von Zastrow M. Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 2009, 10:609-622.
52. Tallarida R.J. Drug synergism: its detection and applications. J Pharmacol Exp Ther 2001, 298:865-872.
53. Tanowitz M., von Zastrow M. A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J Biol Chem 2003, 278:45978-45986.
54. Trafton J.A., Basbaum A.I. The contribution of spinal cord neurokinin-1 receptor signaling to pain. J Pain 2000, 1:57-65.
55. Trafton J.A., Basbaum A.I. [d-Ala2, N-MePhe4, Gly-ol5] enkephalin-induced internalization of the micro opioid receptor in the spinal cord of morphine tolerant rats. Neuroscience 2004, 125:541-543.
56. Virk M.S., Williams J.T. Agonist-specific regulation of mu-opioid receptor desensitization and recovery from desensitization. Mol Pharmacol 2008, 73:1301-1308.
57. von Zastrow M., Svingos A., Haberstock-Debic H., Evans C. Regulated endocytosis of opioid receptors: cellular mechanisms and proposed roles in physiological adaptation to opiate drugs. Curr Opin Neurobiol 2003, 13:348-353.
58. Wang H.Y., Berrios M., Malbon C.C. Localization of beta-adrenergic receptors in A431 cells in situ. Effect of chronic exposure to agonist. Biochem J 1989, 263:533-538.
59. Wolfe B.L., Trejo J. Clathrin-dependent mechanisms of G protein-coupled receptor endocytosis. Traffic 2007, 8:462-470.
60. Xiang Y., Devic E., Kobilka B. The PDZ binding motif of the beta 1 adrenergic receptor modulates receptor trafficking and signaling in cardiac myocytes. J Biol Chem 2002, 277:33783-33790.
61. Zambotti F., Zonta N., Parenti M., Tommasi R., Vicentini L., Conci F., Mantegazza P. Periaqueductal gray matter involvement in the muscimol-induced decrease of morphine antinociception. Naunyn Schmiedebergs Arch Pharmacol 1982, 318:368-369.
62. Zheng H., Loh H.H., Law P.Y. Beta-arrestin-dependent mu-opioid receptor-activated extracellular signal-regulated kinases (ERKs) translocate to nucleus in contrast to G protein-dependent ERK activation. Mol Pharmacol 2008, 73:178-190.