Post-endocytic fates of δ-opioid receptor are regulated by GRK2-mediated receptor phosphorylation and distinct β-arrestin isoforms

Journal of Neurochemistry

Volumn 106, Issue 2, 2008, Pages 781-792

  Zhang, Xiaoqing ^a   Wang, Feifei ^a   Chen, Xiaoqing ^a   Chen, Yuejun ^a   Lan, Ma ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

arrestin; GRK; Internalization; Opioid receptor; Post endocytic fate; Receptor degradation

Indexed keywords

BETA ARRESTIN 1; BETA ARRESTIN 2; DELTA OPIATE RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE 2; MUTANT PROTEIN; RNA; ADRBK1 PROTEIN, HUMAN; BETA ARRESTIN; BIOTIN; DIPRENORPHINE; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; NARCOTIC ANALGESIC AGENT; NARCOTIC ANTAGONIST; RETINA S ANTIGEN; SERINE; SMALL INTERFERING RNA; TRITIUM;

ARTICLE; BINDING ASSAY; BIOTINYLATION; CELL SURFACE; CONTROLLED STUDY; ENDOSOME; ENZYME INHIBITION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIOASSAY; REGULATORY MECHANISM; RNA INTERFERENCE; WILD TYPE; CELL LINE; DRUG EFFECT; ENDOCYTOSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; TIME;

ANALGESICS, OPIOID; ARRESTINS; BIOTIN; CELL LINE, TRANSFORMED; DIPRENORPHINE; ENDOCYTOSIS; ENKEPHALIN, D-PENICILLAMINE (2,5)-; G-PROTEIN-COUPLED RECEPTOR KINASE 2; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HUMANS; MUTATION; NARCOTIC ANTAGONISTS; PHOSPHORYLATION; PROTEIN ISOFORMS; RECEPTORS, OPIOID, DELTA; RNA, SMALL INTERFERING; SERINE; TIME FACTORS; TRITIUM;

EID: 51649112003     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05431.x     Document Type: Article

References (50)

1. Ahn S., Wei H., Garrison T. R. and Lefkowitz R. J. (2004) Reciprocal regulation of angiotensin receptor-activated extracellular signal- regulated kinases by beta-arrestins 1 and 2. J. Biol. Chem. 279, 7807-7811.
2. Barnes W. G., Reiter E., Violin J. D., Ren X. R., Milligan G. and Lefkowitz R. J. (2005) Beta-Arrestin 1 and Galphaq/11 coordi- nately activate RhoA and stress fiber formation following receptor stimulation. J. Biol. Chem. 280, 8041-8050.
3. Brasselet S., Guillen S., Vincent J. P. and Mazella J. (2002) Beta-arrestin is involved in the desensitization but not in the internalization of the somatostatin receptor 2A expressed in CHO cells. FEBS Lett. 516, 124-128.
4. Cao T. T., Deacon H. W., Reczek D., Bretscher A. and von Zastrow M. (1999) A kinase-regulated PDZ-domain interaction controls endocytic sorting of the beta2-adrenergic receptor. Nature 401, 286-290.
5. Cen B., Yu Q., Guo J., Wu Y., Ling K., Cheng Z., Ma L. and Pei G. (2001) Direct binding of fS-arrestins to two distinct intracellular domains of the 5 opioid receptor. J. Neurochem. 76, 1887-1894.
6. Chen C. H., Paing M. M. and Trejo J. (2003) Termination of protease- activated receptor-1 signaling by beta-arrestins is independent of receptor phosphorylation. J. Biol. Chem. 279, 10020-10031.
7. Cong M., Perry S. J., Hu L. A., Hanson P. I., Claing A. and Lefkowitz R. J. (2001) Binding of the beta2 adrenergic receptor to N-ethyl- maleimide-sensitive factor regulates receptor recycling. J. Biol. Chem. 276, 45145-45152.
8. Debaigt C., Hirling H., Steiner P., Vincent J. P. and Mazella J. (2004) Crucial role of neuron-enriched endosomal protein of 21 kDa in sorting between degradation and recycling of internalized G-pro- tein-coupled receptors. J. Biol. Chem. 279, 35687-35691.
9. Dhami G. K., Anborgh P. H., Dale L. B., Sterne-Marr R. and Ferguson S. S. (2002) Phosphorylation-independent regulation of metabo- tropic glutamate receptor signaling by G protein-coupled receptor kinase 2. J. Biol. Chem. 277, 25266-25272.
10. Dicker F., Quitterer U., Winstel R., Honold K. and Lohse M. J. (1999) Phosphorylation-independent inhibition of parathyroid hormone receptor signaling by G protein-coupled receptor kinases. Proc. Natl Acad. Sci. USA 96, 5476-5481.
11. Ferguson S. S. (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24.
12. Ferguson S. S., Downey III W. E., Colapietro A. M., Barak L. S., Menard L. and Caron M. G. (1996) Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internali- zation. Science 271, 363-366.
13. Gage R. M., Kim K. A., Cao T. T. and von Zastrow M. (2001) A transplantable sorting signal that is sufficient to mediate rapid recycling of G protein-coupled receptors. J. Biol. Chem. 276, 44712-44720.
14. Gage R. M., Matveeva E. A., Whiteheart S. W. and von Zastrow M. (2005) Type I PDZ ligands are sufficient to promote rapid recycling of G Protein-coupled receptors independent of binding to N- ethylmaleimide-sensitive factor. J. Biol. Chem. 280, 3305-3313.
15. Galet C., Hirakawa T. and Ascoli M. (2004) The postendocytotic trafficking of the human lutropin receptor is mediated by a transferable motif consisting of the C-terminal cysteine and an upstream leucine. Mol. Endocrinol. 18, 434-446.
16. Gardner L. A., Delos Santos N. M., Matta S. G., Whitt M. A. and Bahouth S. W. (2004) Role of the cyclic AMP-dependent protein kinase in homologous resensitization of the beta1-adrenergic receptor. J. Biol. Chem. 279, 21135-21143.
17. Goodman Jr O. B., Krupnick J. G., Santini F., Gurevich V. V., Penn R. B., Gagnon A. W., Keen J. H. and Benovic J. L. (1996) Beta- arrestin acts as a clathrin adaptor in endocytosis of the beta2- adrenergic receptor. Nature 383, 447-450.
18. Guo J., Wu Y., Zhang W., Zhao J., Devi L. A., Pei G. and Ma L. (2000) Identification of G protein-coupled receptor kinase 2 phosphory- lation sites responsible for agonist-stimulated delta-opioid receptor phosphorylation. Mol. Pharmacol. 58, 1050-1056.
19. Hasbi A., Allouche S., Sichel F., Stanasila L., Massotte D., Landemore G., Polastron J. and Jauzac P. (2000) Internalization and recycling of delta-opioid receptor are dependent on a phosphorylation- dephosphorylation mechanism. J. Pharmacol. Exp. Ther. 293, 237-247.
20. Heydorn A., Sondergaard B. P., Ersboll B., Holst B., Nielsen F. C., Haft C. R., Whistler J. and Schwartz T. W. (2004) A library of 7TM receptor C-terminal tails. Interactions with the proposed post- endocytic sorting proteins ERM-binding phosphoprotein 50 (EBP50), N-ethylmaleimide-sensitive factor (NSF), sorting nexin 1 (SNX1), and G protein-coupled receptor-associated sorting protein (GASP). J. Biol. Chem. 279, 54291-54303.
21. Hirakawa T., Galet C., Kishi M. and Ascoli M. (2003) GIPC binds to the human lutropin receptor (hLHR) through an unusual PDZ domain binding motif, and it regulates the sorting ofthe internalized human choriogonadotropin and the density of cell surface hLHR. J. Biol. Chem. 278, 49348-49357.
22. Innamorati G., Sadeghi H. M., Tran N. T. and Birnbaumer M. (1998) A serine cluster prevents recycling of the V2 vasopressin receptor. Proc. Natl Acad. Sci. USA 95, 2222-2226.
23. Kohout T. A., Lin F. S., Perry S. J., Conner D. A. and Lefkowitz R. J. (2001) Beta-Arrestin 1 and 2 differentially regulate heptahelical receptor signaling and trafficking. Proc. Natl Acad. Sci. USA 98, 1601-1606.
24. Krupnick J. G. and Benovic J. L. (1998) The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol. 38, 289-319.
25. Lefkowitz R. J. (1998) G protein-coupled receptors. III. New roles for receptor kinases and beta-arrestins in receptor signaling and desensitization. J. Biol. Chem. 273, 18677-18680.
26. J. G., Chen C. and Liu-Chen L. Y. (2002) Ezrin-radixin-moesin- binding phosphoprotein-50/Na+/H+ exchanger regulatory factor (EBP50/NHERF) blocks U50,488H-induced down-regulation of the human kappa opioid receptor by enhancing its recycling rate. J. Biol. Chem. 277, 27545-27552.
27. J., Xiang B., Su W., Zhang X., Huang Y. and Ma L. (2003) Agonist-induced formation of opioid receptor-G protein-coupled receptor kinase (GRK)-G beta gamma complex on membrane is required for GRK2 function in vivo. J. Biol. Chem. 278, 30219-30226.
28. Murray S. R., Evans C. J. and von Zastrow M. (1998) Phosphorylation is not required for dynamin-dependent endocytosis of a truncated mutant opioid receptor. J. Biol. Chem. 273, 24987-24991.
29. Navratilova E., Waite S., Stropova D., Eaton M. C., Alves I. D., Hruby V. J., Roeske W. R., Yamamura H. I. and Varga E. V. (2007) Quantitative evaluation of human delta opioid receptor desensiti- zation using the operational model of drug action. Mol. Pharmacol. 71, 1416-1426.
30. Oakley R. H., Laporte S. A., Holt J. A., Caron M. G. and Barak L. S. (2000) Differential affinities of visual arrestin, β-arrestin1, and β- arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem. 275, 17-201.
31. Oakley R. H., Laporte S. A., Holt J. A., Barak L. S. and Caron M. G. (2001) Molecular determinants underlying the formation of stable intracellular G protein-coupled receptor-beta-arrestin complexes after receptor endocytosis. J. Biol. Chem. 276, 19452-19460.
32. 1A angiotensin receptor. J. Biol. Chem. 276, 37761-37768.
33. Paasche J. D., Attramadal T., Sandberg C., Johansen H. K. and Attra- madal H. (2001) Mechanisms of endothelin receptor subtype- specific targeting to distinct intracellular trafficking pathways. J. Biol. Chem. 276, 34041-34050.
34. Paasche J. D., Attramadal T., Kristiansen K., Oksvold M. P., Johansen H. K., Huitfeldt H. S., Dahl S. G. and Attramadal H. (2005) Subtype-specific sorting of the ETA endothelin receptor by a novel endocytic recycling signal for G protein-coupled receptors. Mol. Pharmacol. 67, 1581-1590.
35. Pei G., Kieffer B. L., Lefkowitz R. J. and Freedman N. J. (1995) Agonist-dependent phosphorylation of the mouse delta-opioid receptor: involvement of G protein-coupled receptor kinases but not protein kinase C. Mol. Pharmacol. 48, 173-177.
36. Pierce K. L., Premont R. T. and Lefkowitz R. J. (2002) Seven-trans- membrane receptors. Nat. Rev. Mol. Cell. Biol. 3, 639-650.
37. Qiu Y., Law P. Y. and Loh H. H. (2003) Mu-opioid receptor desensiti- zation: role of receptor phosphorylation, internalization, and representation. J. Biol. Chem. 278, 36733-36739.
38. Qiu Y., Loh H. H. and Law P. Y. (2007) Phosphorylation of the delta-opioid receptor regulates its beta-arrestins selectivity and subsequent receptor internalization and adenylyl cyclase desensitization. J. Biol. Chem. 282, 22315-22323.
39. Richardson M. D., Balius A. M., Yamaguchi K., Freilich E. R., Barak L. S. and Kwatra M. M. (2003) Human substance P receptor lacking the C-terminal domain remains competent to desensitize and internalize. J. Neurochem. 84, 854-863.
40. Seck T., Baron R. and Horne W. C. (2003) Binding of filamin to the C- terminal tail of the calcitonin receptor controls recycling. J. Biol. Chem. 278, 10408-10416.
41. Trejo J. and Coughlin S. R. (1999) The cytoplasmic tails of protease- activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J. Biol. Chem. 274, 2216-2224.
42. Tsao P. I. and von Zastrow M. (2000) Type-specific sorting of G protein- coupled receptors after endocytosis. J. Biol. Chem. 275, 11130-11140.
43. Tsao P., Cao T. and von Zastrow M. (2001) Role of endocytosis in mediating downregulation of G-protein-coupled receptors. Trends Pharmacol. Sci. 22, 91-96.
44. Vargas G. A. and Von Zastrow M. (2004) Identification of a novel endocytic recycling signal in the D1 dopamine receptor. J. Biol. Chem. 279, 37461-37469.
45. Vogler O., Nolte B., Voss M., Schmidt M., Jakobs K. H. and van Koppen C. J. (1999) Regulation of muscarinic acetylcholine receptor sequestration and function by beta-arrestin. J. Biol. Chem. 274, 12333-12338.
46. Wang Y., Zhou Y., Szabo K., Haft C. R. and Trejo J. (2002) Down- regulation of protease-activated receptor-1 is regulated by sorting nexin 1. Mol. Biol. Cell 13, 1965-1976.
47. Whistler J. L., Tsao P. and von Zastrow M. (2001) A phosphorylation- regulated brake mechanism controls the initial endocytosis of opioid receptors but is not required for post-endocytic sorting to lysosomes. J. Biol. Chem. 276, 34331-34338.
48. Whistler J. L., Enquist J., Marley A., Fong J., Gladher F., Tsuruda P., Murray S. R. and Von Zastrow M. (2002) Modulation of pos- tendocytic sorting of G protein-coupled receptors. Science 297, 615-620.
49. Xiang Y. and Kobilka B. (2003) The PDZ-binding motif of the beta2-adrenoceptor is essential for physiologic signaling and trafficking in cardiac myocytes. Proc. Natl. Acad. Sci. USA 100, 10776-10781.
50. Zhang X. Q., Wang F. F., Chen X. Q., Li J. L., Xiang B., Li B. M., Zhang Y. Q. and Ma L. (2005) Beta-arrestin1 and beta-arrestin2 are differentially required for phosphorylation-dependent and -independent internalization of delta-opioid receptors. J. Neurochem. 95, 169-178.