Ligands regulate cell surface level of the human κ opioid receptor by activation-induced down-regulation and pharmacological chaperone-mediated enhancement: Differential effects of nonpeptide and peptide agonists

Journal of Pharmacology and Experimental Therapeutics

Volumn 319, Issue 2, 2006, Pages 765-775

  Chen, Yong ^a   Chen, Chongguang ^a   Wang, Yulin ^a   Liu Chen, Lee Yuan ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 [1 (3,4 DICHLORO N METHYLPHENYLACETAMIDO) 2 (1 PYRROLIDINYL)ETHYL]PHENOXYACETIC ACID; 3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE METHANESULFONATE; ASIMADOLINE; BREFELDIN A; BREMAZOCINE; CHAPERONE; DYNORPHIN; DYNORPHIN A; DYNORPHIN B; ETHYLKETAZOCINE; ETORPHINE; KAPPA OPIATE RECEPTOR AGONIST; LIGAND; NALFURAFINE; NALOXONE; NORBINALTORPHIMINE; OPIATE; OPIATE RECEPTOR; PENTAZOCINE;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL LEVEL; CELL SURFACE; CHO CELL; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; UPREGULATION; WESTERN BLOTTING;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANIMALS; BREFELDIN A; CELL MEMBRANE PERMEABILITY; CHO CELLS; CRICETINAE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENDOPLASMIC RETICULUM; LIGANDS; NALOXONE; PEPTIDES; RECEPTORS, OPIOID, KAPPA;

EID: 33751185359     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.106.107987     Document Type: Article

References (48)

1. Barber A, Bartoszyk GD, Bender HM, Gottschlich R, Greiner HE, Harting J, Mauler F, Minck KO, Murray RD, and Simon M (1994) A pharmacological profile of the novel, peripherally-selective κ-opioid receptor agonist, EMD 61753. Br J Pharmacol 113:1317-1327.
2. Belcheva MM, Barg J, Gloeckner C, Gao XM, Chuang DM, and Coscia CJ (1992) Antagonist-induced transient down-regulation of δ-opioid receptors in NG108-15 cells. Mol Pharmacol 42:445-452.
3. Belcheva MM, Barg J, McHale RJ, Dawn S, Ho MT, Ignatova E, and Coscia CJ (1993) Differential down- and up-regulation of rat brain opioid receptor types and subtypes by buprenorphine. Mol Pharmacol 44:173-179.
4. Bernier V, Bichet DG, and Bouvier M (2004) Pharmacological chaperone action on G-protein-coupled receptors. Curr Opin Pharmacol 4:528-533.
5. Chaipatikul V, Erickson-Herbrandson LJ, Loh HH, and Law PY (2003) Rescuing the traffic-deficient mutants of rat μ-opioid receptors with hydrophobic ligands. Mol Pharmacol 64:32-41.
6. Chen C, Li JG, Chen Y, Huang P, Wang Y, and Liu-Chen LY (2006) GEC1 interacts with the κ opioid receptor and enhances expression of the receptor. J Biol Chem 281:7983-7993.
7. Ellgaard L and Helenius A (2003) Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4:181-191.
8. Fortin JP, Dziadulewicz EK, Gera L, and Marceau F (2006) A nonpeptide antagonist reveals a highly glycosylated state of the rabbit kinin B1 receptor. Mol Pharmacol 69:1146-1157.
9. Gelman MS and Kopito RR (2002) Rescuing protein conformation: prospects for pharmacological therapy in cystic fibrosis. J Clin Investig 110:1591-1597.
10. Henry DJ, Grandy DK, Lester HA, Davidson N, and Chavkin C (1995) κ-Opioid receptors couple to inwardly rectifying potassium channels when coexpressed by Xenopus oocytes. Mol Pharmacol 47:551-557.
11. o proteins. J Biol Chem 279:25002-25009.
12. Janovick JA, Maya-Nunez G, and Conn PM (2002) Rescue of hypogonadotropic hypogonadism-causing and manufactured GnRH receptor mutants by a specific protein-folding template: misrouted proteins as a novel disease etiology and therapeutic target. J Clin Endocrinol Metab 87:3255-3262.
13. Kleizen B and Braakman I (2004) Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 16:343-349.
14. Law P-Y, Erickson LJ, El Kouhen R, Dicker L, Solberg J, Wang W, Miller E, Burd AL, and Loh HH (2000a) Receptor density and recycling affect the rate of agonist-induced desensitization of μ-opioid receptor. Mol Pharmacol 58:388-398.
15. Law P-Y, Wong YH, and Loh HH (2000b) Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40:389-430.
16. Lesscher HM, Bailey A, Burbach JP, van Ree JM, Kitchen I, and Gerrits MA (2003) Receptor-selective changes in μ-, δ- and κ-opioid receptors after chronic naltrexone treatment in mice. Eur J Neurosci 17:1006-1012.
17. Li J, Chen C, Huang P, and Liu-Chen L-Y (2001a) Inverse agonist up-regulates the constitutively active D3.49(164)Q mutant of the rat μ opioid receptor by stabilizing the structure and blocking constitutive internalization and down-regulation. Mol Pharmacol 60:1064-1075.
18. Li J, Huang P, Chen C, de Riel JK, Weinstein H, and Liu-Chen L-Y (2001b) Constitutive activation of the μ opioid receptor by mutation of D3.49(164), but not D3.32(147): D3.49(164) is critical for stabilization of the inactive form of the receptor and for its expression. Biochem 40:12039-12050.
19. Li J, Li J-G, Chen C, Zhang F, and Liu-Chen L-Y (2002) Molecular basis of differences in (-)(trans)-3,4-dichloro-N-methyl-N-[2-(1-pyrrolidiny)- cyclohexyl]benzeneacetamide-induced desensitization and phosphorylation between human and rat κ-opioid receptors expressed in Chinese hamster ovary cells. Mol Pharmacol 61:73-84.
20. Li J-G, Benovic JL, and Liu-Chen L-Y (2000) Mechanisms of agonist-induced down-regulation of the human κ-opioid receptor: internalization is required for down-regulation. Mol Pharmacol 58:795-801.
21. Li J-G, Luo LY, Krupnick JG, Benovic JL, and Liu-Chen L-Y (1999) U50,488H-induced internalization of the human κ opioid receptor involves a β-arrestin- and dynamin-dependent mechanism: κ receptor internalization is not required for mitogen-activated protein kinase activation. J Biol Chem 274:12087-12094.
22. Li J-G, Zhang F, Jin XL, and Liu-Chen L-Y (2003) Differential regulation of the human κ opioid receptor by agonists: etorphine and levorphanol reduced dynorphin A- and U50,488H-induced internalization and phosphorylation. J Pharmacol Exp Ther 305:531-540.
23. Liu-Chen L-Y (2004) Agonist-induced regulation and trafficking of κ opioid receptors. Life Sci 75:511-536.
24. Magzoub M and Graslund A (2004) Cell-penetrating peptides: [corrected] from inception to application. Q Rev Biophys 37:147-195.
25. Marie N, Lecoq I, Jauzac P, and Allouche S (2003) Differential sorting of human δ-opioid receptors after internalization by peptide and alkaloid agonists. J Biol Chem 278:22795-22804.
26. Marinova Z, Vukojevic V, Surcheva S, Yakovleva T, Cebers G, Pasikova N, Usynin I, Hugonin L, Fang W, Hallberg M, et al. (2005) Translocation of dynorphin neuropeptides across the plasma membrane: a putative mechanism of signal transmission. J Biol Chem 280:26360-26370.
27. Millan MJ, Morris BJ, and Herz A (1988) Antagonist-induced opioid receptor upregulation. I. Characterization of supersensitivity to selective mu and kappa agonists. J Pharmacol Exp Ther 247:721-728.
28. Morello JP, Salahpour A, Laperriere A, Bernier V, Arthus MF, Lonergan M, Petaja-Repo U, Angers S, Morin D, Bichet DG, et al. (2000) Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants. J Clin Investig 105:887-895.
29. Morris BJ, Millan MJ, and Herz A (1988) Antagonist-induced opioid receptor upregulation. II. Regionally specific modulation of mu, delta and kappa binding sites in rat brain revealed by quantitative autoradiography. J Pharmacol Exp Ther 247:729-736.
30. Petaja-Repo UE, Hogue M, Bhalla S, Laperriere A, Morello JP, and Bouvier M (2002) Ligands act as pharmacological chaperones and increase the efficiency of δ opioid receptor maturation. EMBO (Eur Mol Biol Organ) 21:1628-1637.
31. Portoghese PS, Lipkowski AW, and Takemori AE (1987) Binaltorphimine and norbinaltorphimine, potent and selectivity κ-opioid receptor antagonists. Life Sci 4:1287-1292.
32. Rajashekara V, Patel CN, Patel K, Purohit V, and Yoburn BC (2003) Chronic opioid antagonist treatment dose-dependently regulates μ-opioid receptors and trafficking proteins in vivo. Pharmacol Biochem Behav 75:909-913.
33. Rios RM, Tassin AM, Celati C, Antony C, Boissier MC, Homberg JC, and Bornens M (1994) A peripheral protein associated with the cis-Golgi network redistributes in the intermediate compartment upon brefeldin A treatment. J Cell Biol 125:997-1013.
34. Roth BL, Baner K, Westkaemper R, Siebert D, Rice KC, Steinberg S, Ernsberger P, and Rothman RB (2002) Salvinorin A: a potent naturally occurring nonnitrogenous κ opioid selective agonist. Proc Natl Acad Sci USA 99:11934-11939.
35. Roth BL, Kroeze WK, Patel S, and Lopez E (2000) The multiplicity of serotonin receptors: uselessly diverse molecules or an embarrassment of riches? Neuroscientist 6:252-262.
36. Samama P, Bond RA, Rockman HA, Milano CA, and Lefkowitz RJ (1997) Ligand-induced overexpression of a constitutively active 2-adrenergic receptor: pharmacological creation of a phenotype in transgenic mice. Proc Natl Acad Sci USA 94:137-141.
37. Seki T, Awamura S, Kimura C, Ide S, Sakano K, Minami M, Nagase H, and Satoh M (1999) Pharmacological properties of TRK-820 on cloned μ-, δ- and κ-opioid receptors and nociceptin receptor. Eur J Pharmacol 376:159-167.
38. Shaw JS, Carroll JA, Alcock P, and Main BG (1989) ICI 204448: a kappa-opioid agonist with limited access to the CNS. Br J Pharmacol 96:986-992.
39. Szmuszkovicz J (1999) U-50,488 and the kappa receptor. Part II: 1991-1998. Prog Drug Res 53:1-51.
40. Tallarida RJ and Murray RB (1987) Pharmacokinetics IV: plasma concentration-time data, in Manual of Pharmacologic Calculations with Computer Programs (Tallarida RJ and Murray RB eds) pp 93-98, Springer-Verlag, New York.
41. +-ATPase and the Golgi apparatus in the recycling of PTH/PTHrP receptor. Am J Physiol 286:E704-E710.
42. Ulloa-Aguirre A, Janovick JA, Brothers SP, and Conn PM (2004) Pharmacologic rescue of conformationally-defective proteins: implications for the treatment of human disease. Traffic 5:821-837.
43. Van Craenenbroeck K, Clark SD, Cox MJ, Oak JN, Liu F, and Van Tol HH (2005) Folding efficiency is rate-limiting in dopamine D4 receptor biogenesis. J Biol Chem 280:19350-19357.
44. von Voigtlander PF, Lahti RA, and Ludens JH (1983) U-50,488: a selective and structurally novel non-mu (kappa) opioid agonist. J Pharmacol Exp Ther 224:7-12.
45. Wang Y, Tang K, Inan S, Siebert D, Holzgrabe U, Lee DY, Huang P, Li JG, Cowan A, and Liu-Chen L-Y (2005) Comparison of pharmacological activities of three distinct κ ligands (salvinorin A, TRK-820 and 3FLB) on κ opioid receptors in vitro and their antipruritic and antinociceptive activities in vivo. J Pharmacol Exp Ther 312:220-230.
46. Xu W, Campillo M, Pardo L, Kim DR, and Liu-Chen LY (2005) The seventh transmembrane domains of the δ and κ opioid receptors have different accessibility patterns and interhelical interactions. Biochemistry 44:16014-16025.
47. Zhang F, Li J, Li J-G, and Liu-Chen L-Y (2002) (-)U50,488H [(trans)-3,4-dichloro-N-methyl-N-[2-(1-pyrrolidinyl)-cyclohexyl] benzeneacetamide] induces internalization and down-regulation of the human, but not the rat, κ-opioid receptor: structural basis for the differential regulation. J Pharmacol Exp Ther 302:1184-1192.
48. 35S]GTPγS binding to membranes: determination of potencies and efficacies of ligands. J Pharmacol Exp Ther 282:676-684.