Quantitative evaluation of human δ opioid receptor desensitization using the operational model of drug action

Molecular Pharmacology

Volumn 71, Issue 5, 2007, Pages 1416-1426

  Navratilova, Edita ^a   Waite, Sue ^a   Stropova, Dagmar ^a   Eaton, Miriam C ^a   Alves, Isabel D ^a   Hruby, Victor J ^a,b,c   Roeske, William R ^a,c,d   Yamamura, Henry I ^a,c,d   Varga, Eva V ^a,d,e  

^a UNIVERSITY OF ARIZONA   (United States)

^b The University of Arizona   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

^e UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BETA ARRESTIN 2; CYCLIC AMP; DELTA OPIATE RECEPTOR; DELTORPHIN; DELTORPHIN II; FORSKOLIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG ACTIVITY; ENDOCYTOSIS; GENE MUTATION; INTERNALIZATION; KINETICS; MATHEMATICAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; RECEPTOR BINDING; RECEPTOR DOWN REGULATION; RECEPTOR SENSITIVITY;

ALANINE; ANIMALS; ARRESTINS; CHO CELLS; CRICETINAE; CRICETULUS; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; KINETICS; MODELS, BIOLOGICAL; MUTATION; OLIGOPEPTIDES; PHOSPHORYLATION; RECEPTORS, OPIOID, DELTA; SERINE; TIME FACTORS;

EID: 34247466007     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.106.030023     Document Type: Article

References (36)

1. Allouche S, Roussel M, Marie N, and Jauzac P (1999) Differential desensitization of human [delta]-opioid receptors by peptide and alkaloid agonists. Eur J Pharmacol 371:235-240.
2. Barak LS, Gilchrist J, Becker JM, and Kim K-M (2006) Relationship between the G protein signaling and homologous desensitization of G protein-coupled receptors. Biochem Biophys Res Commun 339:695-700.
3. Black JW, Leff P, Shankley NP, and Wood J (1985) An operational model of pharmacological agonism: the effect of E/[A] curve shape on agonist dissociation constant estimation. Br J Pharmacol 84:561-571.
4. Borgland SL, Connor M, Osborne PB, Furness JB, and Christie MJ (2003) Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of μ-opioid receptors. J Biol Chem 278:18776-18784.
5. Burns ME, Mendez A, Chen CK, Almuete A, Quillinan N, Simon MI, Baylor DA, and Chen J (2006) Deactivation of phosphorylated and nonphosphorylated rhodopsin by arrestin splice variants. J Neurosci 26:1036-1044.
6. Connor M, Osborne PB, and Christie MJ (2004) Mu-opioid receptor desensitization: is morphine different? Br J Pharmacol 143:685-696.
7. Daaka Y, Luttrell LM, and Lefkowitz RJ (1997) Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature (Lond) 390:88-91.
8. Dang VC and Christie MJ (2006) Beta-arrestin-2 independent regulation of mu opioid receptor in locus coeruleus neurones (http://www.inrcworld.org/ 2006meeting/INRC%202006%20Poster%20Abstracts.pdf), p. 48, in Posters of the International Narcotics Research Conference; July 9-14, 2006; St. Paul, Minnesota. International Narcotics Research Conference; Tulsa, Oklahoma.
9. Dicker F, Quitterer U, Winstel R, Honold K, and Lohse MJ (1999) Phosphorylation-independent inhibition of parathyroid hormone receptor signaling by G protein-coupled receptor kinases. Proc Natl Acad Sci USA 96:5476-5481.
10. Eisinger DA, Ammer H, and Schulz R (2002) Chronic morphine treatment inhibits opioid receptor desensitization and internalization. J Neurosci 22:10192-10200.
11. Freedman NJ, Ament AS, Oppermann M, Stoffel RH, Exum ST, and Lefkowitz RJ (1997) Phosphorylation and desensitization of human endothelin A and B receptors. Evidence for G protein-coupled receptor kinase specificity. J Biol Chem 272:17734-17743.
12. Gilman AG (1970) A protein binding assay for adenosine 3′:5′-cyclic monophosphate. Proc Natl Acad Sci USA 67:305-312.
13. Gurevich VV and Gurevich EV (2004) The molecular acrobatics of arrestin activation. Trends Pharmacol Sci 25:105-111.
14. Hall RA and Lefkowitz RJ (2002) Regulation of G protein-coupled receptor signaling by scaffold proteins. Circ Res 91:672-680.
15. Hasbi A, Allouche S, Sichel F, Stanasila L, Massotte D, Landemore G, Polastron J, and Jauzac P (2000) Internalization and recycling of μ-opioid receptor are dependent on a phosphorylation-dephosphorylation mechanism. J Pharmacol Exp Ther 293:237-247.
16. Hasbi A, Polastron J, Allouche S, Stanasila L, Massotte D, and Jauzac P (1998) Desensitization of the delta-opioid receptor correlates with its phosphorylation in SK-N-BE cells: involvement of a G protein-coupled receptor kinase. J Neurochem 70:2129-2138.
17. Kouhen OM, Wang G, Solberg J, Erickson LJ, Law PY, and Loh HH (2000) Hierarchical phosphorylation of delta-opioid receptor regulates agonist-induced receptor desensitization and internalization. J Biol Chem 275:36659-36664.
18. Krasel C, Vilardaga JP, Bunemann M, and Lohse MJ (2004) Kinetics of G-protein-coupled receptor signalling and desensitization. Biochem Soc Trans 32:1029-1031.
19. Law PY, Kouhen OM, Solberg J, Wang W, Erickson LJ, and Loh HH (2000) Deltorphin II-induced rapid desensitization of δ-opioid receptor requires both phosphorylation and internalization of the receptor. J Biol Chem 275:32057-32065.
20. Li 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)-Gβγ complex on membrane is required for GRK2 function in vivo. J Biol Chem 278:30219-30226.
21. 2-adrenergic receptor desensitization. Delineation with specific inhibitors. J Biol Chem 265:3202-3211.
22. Lowe JD, Celver JP, Gurevich VV, and Chavkin C (2002) μ-Opioid receptors desensitize less rapidly than δ-opioid receptors due to less efficient activation of arrestin. J Biol Chem 277:15729-15735.
23. Malatynska E, Wang Y, Knapp RJ, Waite S, Calderon S, Rice K, Hruby VJ, Yamamura HI, and Roeske WR (1996) Human δ opioid receptor: functional studies on stably transfected Chinese hamster ovary cells after acute and chronic treatment with the selective nonpeptidic agonist SNC-80. J Pharmacol Exp Ther 278:1083-1089.
24. Marion S, Oakley RH, Kim K-M, Caron MG, and Barak LS (2006) A β-arrestin binding determinant common to the second intracellular loops of rhodopsin family G protein-coupled receptors. J Biol Chem 281:2932-2938.
25. Navratilova E, Eaton MC, Stropova D, Varga EV, Vanderah TW, Roeske WR, and Yamamura HI (2005) Morphine promotes phosphorylation of the human delta-opioid receptor at serine 363. Eur J Pharmacol 519:212-214.
26. Navratilova E, Varga EV, Stropova D, Jambrosic JC, Roeske WR, and Yamamura HI (2004) Mutation S363A in the human delta-opioid receptor selectively reduces down-regulation by a peptide agonist. Eur J Pharmacol 485:341-343.
27. 5]enkephalin. Eur J Pharmacol 387:R11-R13.
28. Osborne PB and Williams JT (1995) Characterization of acute homologous desensitization of mu-opioid receptor-induced currents in locus coeruleus neurones. Br J Pharmacol 115:925-932.
29. Quock RM, Burkey TH, Varga E, Hosohata Y, Hosohata K, Cowell SM, Slate CA, Ehlert FJ, Roeske WR, and Yamamura HI (1999) The δ-opioid receptor: molecular pharmacology, signal transduction, and the determination of drug efficacy. Pharmacol Rev 51:503-532.
30. Quock RM, Hosohata Y, Knapp RJ, Burkey TH, Hosohata K, Zhang X, Rice KC, Nagase H, Hruby VJ, Porreca F, et al. (1997) Relative efficacies of δ-opioid receptor agonists at the cloned human δ-opioid receptor. Eur J Pharmacol 326:101-104.
31. Trzeciakowski JP (1999) Stimulus amplification, efficacy, and the operational model. Part I - binary complex occupancy mechanisms. J Theor Biol 198:329-346.
32. Varga EV, Rubenzik MK, Stropova D, Sugiyama M, Grife V, Hruby VJ, Rice KC, Roeske WR, and Yamamura HI (2003) Converging protein kinase pathways mediate adenylyl cyclase superactivation upon chronic δ-opioid agonist treatment. J Pharmacol Exp Ther 306:109-115.
33. Whaley BS, Yuan N, Birnbaumer L, Clark RB, and Barber R (1994) Differential expression of the β-adrenergic receptor modifies agonist stimulation of adenylyl cyclase: a quantitative evaluation. Mol Pharmacol 45:481-489.
34. Willets J and Kelly E (2001) Desensitization of endogenously expressed [delta]-opioid receptors: no evidence for involvement of G protein-coupled receptor kinase 2. Eur J Pharmacol 431:133-141.
35. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, and Chen J (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature (Lond) 389:505-509.
36. Zhang X, Wang F, Chen X, Li J, Xiang B, Zhang YQ, Li BM, 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.