Mu opioid receptor-effector coupling and trafficking in dorsal root ganglia neurons

Neuroscience

Volumn 142, Issue 2, 2006, Pages 493-503

  Walwyn, W M ^a   Wei, W ^a   Xie, C W ^a   Chiu, K ^a   Kieffer, B L ^b   Evans, C J ^a   Maidment, N T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

desensitization; dorsal root ganglia neurons; internalization; mu opioid receptor; synthesis; trafficking

Indexed keywords

CALCIUM; DELTA OPIATE RECEPTOR; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MORPHINE; MU OPIATE RECEPTOR; RAB PROTEIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CELL TRANSPORT; CHIMERA; CONTROLLED STUDY; ENDOSOME; IN VIVO STUDY; INCUBATION TIME; KNOCKOUT MOUSE; LYSOSOME; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SPINAL GANGLION; WHOLE CELL;

ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BACLOFEN; CELLS, CULTURED; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; ENKEPHALINS; FLOW CYTOMETRY; GABA AGONISTS; GANGLIA, SPINAL; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MORPHINE; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN TRANSPORT; RECEPTORS, OPIOID, MU; TIME FACTORS; TRANSFECTION;

EID: 33748765783     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.06.021     Document Type: Article

References (44)

1. Afify E.A., Law P.Y., Riedl M., Elde R., and Loh H.H. Role of carboxyl terminus of mu- and delta-opioid receptor in agonist-induced down-regulation. Brain Res Mol Brain Res 54 1 (1998) 24-34
2. Alvarez V.A., Arttamangkul S., Dang V., Salem A., Whistler J.L., Von Zastrow M., Grandy D.K., and Williams J.T. mu-Opioid receptors: Ligand-dependent activation of potassium conductance, desensitization, and internalization. J Neurosci 22 13 (2002) 5769-5776
3. Arttamangkul S., Torrecilla M., Kobayashi K., Okano H., and Williams J.T. Separation of mu-opioid receptor desensitization and internalization: endogenous receptors in primary neuronal cultures. J Neurosci 26 15 (2006) 4118-4125
4. Borgland S.L., Connor M., Osborne P.B., Furness J.B., and Christie M.J. Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors. J Biol Chem 278 21 (2003) 18776-18784
5. Celver J., Xu M., Jin W., Lowe J., and Chavkin C. Distinct domains of the mu-opioid receptor control uncoupling and internalization. Mol Pharmacol 65 3 (2004) 528-537
6. Cen B., Xiong Y., Ma L., and Pei G. Direct and differential interaction of beta-arrestins with the intracellular domains of different opioid receptors. Mol Pharmacol 59 4 (2001) 758-764
7. Connor M., Osborne P.B., and Christie M.J. Mu-opioid receptor desensitization: is morphine different?. Br J Pharmacol 143 6 (2004) 685-696
8. Cox B.M. Agonists at mu-opioid receptors spin the wheels to keep the action going. Mol Pharmacol 67 1 (2005) 12-14
9. Dang V.C., and Williams J.T. Chronic morphine treatment reduces recovery from opioid desensitization. J Neurosci 24 (2004) 7699-7706
10. Duttaroy A., and Yoburn B.C. The effect of intrinsic efficacy on opioid tolerance. Anesthesiology 82 5 (1995) 1226-1236
11. Edwardson J.M., and Szekeres P.G. Endocytosis and recycling of muscarinic receptors. Life Sci 64 (1999) 487-494
12. Finn A.K., and Whistler J.L. Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32 5 (2001) 829-839
13. Fiorillo C.D., and Williams J.T. Opioid desensitization: interactions with G-protein-coupled receptors in the locus coeruleus. J Neurosci 16 4 (1996) 1479-1485
14. Haberstock-Debic H., Kim K.A., Yu Y.J., and von Zastrow M. Morphine promotes rapid, arrestin-dependent endocytosis of mu-opioid receptors in striatal neurons. J Neurosci 25 34 (2005) 7847-7857
15. Haberstock-Debic H., Wein M., Barrot M., Colago E.E., Rahman Z., Neve R.L., Pickel V.M., Nestler E.J., von Zastrow M., and Svingos A.L. Morphine acutely regulates opioid receptor trafficking selectively in dendrites of nucleus accumbens neurons. J Neurosci 23 10 (2003) 4324-4332
16. Harris G.C., and Williams J.T. Transient homologous mu-opioid receptor desensitization in rat locus coeruleus neurons. J Neurosci 11 8 (1991) 2574-2581
17. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., and Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95 5 (1998) 2509-2514
18. Keith D.E., Anton B., Murray S.R., Zaki P.A., Chu P.C., Lissin D.V., Monteillet-Agius G., Stewart P.L., Evans C.J., and von Zastrow M. mu-Opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in the mammalian brain. Mol Pharmacol 53 3 (1998) 377-384
19. Keith D.E., Murray S.R., Zaki P.A., Chu P.C., Lissin D.V., Kang L., Evans C.J., and von Zastrow M. Morphine activates opioid receptors without causing their rapid internalization. J Biol Chem 271 32 (1996) 19021-19024
20. Kieffer B.L., and Evans C.J. Opioid tolerance: in search of the holy grail. Cell 108 5 (2002) 587-590
21. Koch T., Schulz S., Pfeiffer M., Klutzny M., Schroder H., Kahl E., and Hollt V. C-terminal splice variants of the mouse mu-opioid receptor differ in morphine-induced internalization and receptor resensitization. J Biol Chem 276 33 (2001) 31408-31414
22. Koch T., Schulz S., Schroder H., Wolf R., Raulf E., and Hollt V. Carboxyl-terminal splicing of the rat mu opioid receptor modulates agonist-mediated internalization and receptor resensitization. J Biol Chem 273 (1998) 13652-13657
23. Koch T., Widera A., Bartzsch K., Schulz S., Brandenburg L.O., Wundrack N., Beyer A., Grecksch G., and Hollt V. Receptor endocytosis counteracts the development of opioid tolerance. Mol Pharmacol 67 1 (2005) 280-287
24. Law P.Y., Erickson L.J., El-Kouhen R., Dicker L., Solberg J., Wang W., Miller E., Burd A.L., and Loh H.H. Receptor density and recycling affect the rate of agonist-induced desensitization of mu-opioid receptor. Mol Pharmacol 58 2 (2000) 388-398
25. Li G., and Stahl P.D. Post-translational processing and membrane association of the two early endosome-associated rab GTP-binding proteins (rab4 and rab5). Arch Biochem Biophys 304 2 (1993) 471-478
26. Matthes H.W., Maldonado R., Simonin F., Valverde O., Slowe S., Kitchen I., Befort K., Dierich A., Le Meur M., Dolle P., Tzavara E., Hanoune J., Roques B.P., and Kieffer B.L. Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383 6603 (1996) 819-823
27. Mitchell H., Choudhury A., Pagano R.E., and Leof E.B. Ligand-dependent and -independent transforming growth factor-beta receptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol Biol Cell 15 9 (2004) 4166-4178
28. Mollenhauer H.H., Morre D.J., and Rowe L.D. Alteration of intracellular traffic by monensin: mechanism, specificity and relationship to toxicity. Biochim Biophys Acta 1031 2 (1990) 225-246
29. Mueller A., and Strange P.G. Mechanisms of internalization and recycling of the chemokine receptor, CCR5. Eur J Biochem 271 2 (2004) 243-252
30. Nomura K., Reuveny E., and Narahashi T. Opioid inhibition and desensitization of calcium channel currents in rat dorsal root ganglion neurons. J Pharmacol Exp Ther 270 2 (1994) 466-474
31. Oakley R.H., Laporte S.A., Holt J.A., Barak L.S., and Caron M.G. Association of beta-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J Biol Chem 274 45 (1999) 32248-32257
32. Odley A., Hahn H.S., Lynch R.A., Marreez Y., Osinska H., Robbins J., and Dorn II G.W. Regulation of cardiac contractility by Rab4-modulated beta2-adrenergic receptor recycling. Proc Natl Acad Sci U S A 101 18 (2004) 7082-7087
33. Pippig S., Andexinger S., and Lohse M.J. Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization. Mol Pharmacol 47 4 (1995) 666-676
34. Polakiewicz R.D., Schieferl S.M., Dorner L.F., Kansra V., and Comb M.J. A mitogen-activated protein kinase pathway is required for μ-opioid receptor desensitization. J Biol Chem 273 20 (1998) 12402-12406
35. Prather P.L., Song L., Piros E.T., Law P.Y., and Hales T.G. delta-Opioid receptors are more efficiently coupled to adenylyl cyclase than to L-type Ca(2+) channels in transfected rat pituitary cells. J Pharmacol Exp Ther 295 2 (2000) 552-562
36. Ren M., Xu G., Zeng J., De Lemos-Chiarandini C., Adesnik M., and Sabatini D.D. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci U S A 95 11 (1998) 6187-6192
37. Roosterman D., Cottrell G.S., Schmidlin F., Steinhoff M., and Bunnett N.W. Recycling and resensitization of the neurokinin 1 receptor. Influence of agonist concentration and Rab GTPases. J Biol Chem 279 29 (2004) 30670-30679
38. Samoriski G.M., and Gross R.A. Functional compartmentalization of opioid desensitization in primary sensory neurons. J Pharmacol Exp Ther 294 2 (2000) 500-509
39. Schulz R., Wehmeyer A., and Schulz K. Opioid receptor types selectively cointernalize with G protein-coupled receptor kinases 2 and 3. J Pharmacol Exp Ther 300 2 (2002) 376-384
40. Sheff D.R., Daro E.A., Hull M., and Mellman I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 145 1 (1999) 123-139
41. Tan M., Groszer M., Tan A.M., Pandya A., Liu X., and Xie C.W. Phosphoinositide 3-kinase cascade facilitates mu-opioid desensitization in sensory neurons by altering G-protein-effector interactions. J Neurosci 23 32 (2003) 10292-10301
42. Walwyn W.M., Keith Jr. D.E., Wei W., Tan A.M., Xie C.W., Evans C.J., Kieffer B.L., and Maidment N.T. Functional coupling, desensitization and internalization of virally expressed mu opioid receptors in cultured dorsal root ganglion neurons from mu opioid receptor knockout mice. Neuroscience 123 1 (2004) 111-121
43. Whistler J.L., Chuang H.H., Chu P., Jan L.Y., and von Zastrow M. Functional dissociation of mu opioid receptor signaling and endocytosis: implications for the biology of opiate tolerance and addiction. Neuron 23 4 (1999) 737-746
44. Woolf P.J., and Linderman J.J. Untangling ligand induced activation and desensitization of G-protein-coupled receptors. Biophys J 84 1 (2003) 3-13