Endogenous regulator of G protein signaling proteins reduce μ-opioid receptor desensitization and down-regulation and adenylyl cyclase tolerance in C6 cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 312, Issue 2, 2005, Pages 809-815

  Clark, Mary J ^a   Traynor, John R ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; DIPRENORPHINE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; FORSKOLIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETAGAMMA SUBUNIT; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); MORPHINE; MU OPIATE RECEPTOR; PERTUSSIS TOXIN; RGS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DESENSITIZATION; DRUG TOLERANCE; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSFECTION; GLIOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR DOWN REGULATION; RECEPTOR SENSITIVITY;

ADENYLATE CYCLASE; ANALGESICS, OPIOID; CELL LINE, TUMOR; CELLS, CULTURED; CYCLIC AMP; DOWN-REGULATION; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GLIOMA; GTP PHOSPHOHYDROLASES; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; PERTUSSIS TOXIN; RECEPTORS, OPIOID, MU; RGS PROTEINS;

EID: 13244283093     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.104.074641     Document Type: Article

References (36)

1. Bishop GB, Cullinan WE, Curran E, and Gutstein HB (2002) Abused drugs modulate RGS4 mRNA levels in rat brain: comparison between acute drug treatment and a drug challenge after chronic treatment. Neurobiol Dis 10:334-343.
2. Bohn LM, Gainetdinov RR, Lin F-T, Lefkowitz RJ, and Caron MG (2000) μ-Opioid receptor desensitization by β-arrestin-2 determines morphine tolerance but not dependence. Nature (Lond) 408:720-723.
3. Bohn LM, Lefkowitz RJ, and Caron MG (2002) Differential mechanisms of morphine antinociceptive tolerance revealed in β-arrestin-2 knockout mice. J Neurosci 22:10494-10500.
4. Borgland SL (2001) Acute opioid receptor desensitization and tolerance: is there a link? Clin Exp Pharmacol Physiol 28:147-154.
5. Chakrabarti S, Yang W, Law P-Y, and Loh HH (1997) The μ-opioid receptor down-regulates differently from the δ-opioid receptor: requirement of a high affinity receptor/G protein complex formation. Mol Pharmacol 52:105-113.
6. Chao J and Nestler EJ (2004) Molecular neurobiology of drug addiction. Annu Rev Med 55:113-132.
7. + channels. Proc Natl Acad Sci USA 95:11727-11732.
8. o. J Biol Chem 278:9418-9425.
9. Clark MJ, Neubig RR, and Traynor JR (2004) Endogenous regulator of G protein signaling proteins suppress Gαo-dependent, μ-opioid agonist-mediated adenylyl cyclase supersensitization. J Pharmacol Exp Ther 310:215-222.
10. Eitan S, Bryant CD, Saliminejad N, Yang YC, Vojdani E, Keith D Jr, Polakiewicz R, and Evans CJ (2003) Brain region-specific mechanisms for acute morphine-induced mitogen-activated protein kinase modulation and distinct patterns of activation during analgesic tolerance and locomotor sensitization. J Neurosci 23:8360-8369.
11. Garzón J, López-Fando A, and Sánchez-Blázquez P (2003) The R7 subfamily of RGS proteins assists tachyphylaxis and acute tolerance at μ-opioid receptors. Neuropsychopharmacology 28:1983-1990.
12. Garzón J, Rodríguez-Díaz M, López-Fando A, and Sánchez-Blázquez P (2001) RGS9 proteins facilitate acute tolerance to mu-opioid effects. Eur J Neurosci 13:801-811.
13. Gold SJ, Han M-H, Herman AE, Ni YG, Pudiak CM, Aghajanian GK, Liu R-J, Potts BW, Mumby SM, and Nestler EJ (2003) Regulation of RGS proteins by chronic morphine in rat locus coeruleus. Eur J Neurosci 17:971-980.
14. Gomes BA, Shen J, Stafford K, Patel M, and Yoburn BC (2002) μ-Opioid receptor down-regulation and tolerance are not equally dependent upon G-protein signaling. Pharmacol Biochem Behav 72:273-278.
15. 2A receptor desensitization and resensitization reveal an arrestin-, GRK2- and GRK5-independent mode of regulation in human embryonic kidney 293 cells. Mol Pharmacol 60:1020-1030.
16. Hollinger S and Hepler JR (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54:527-559.
17. Jeong S-W and Ikeda SR (2000) Endogenous regulator of G-protein signaling proteins modify N-type calcium channel modulation in rat sympathetic neurons. J Neurosci 20:4489-4496.
18. Kupnick JG and Benovic JL (1998) The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu Rev Pharmacol Toxicol 38:289-319.
19. Lan K-L, Sarvazyan NA, Taussig R, Mackenzie RG, DiBello PR, Dohlman HG, and Neubig RR (1998) A point mutation in Galphao and Galpha1 blocks interaction with regulator of G protein signaling proteins. J Biol Chem 273:12794-12797.
20. Lee KO, Akil H, Woods JH, and Traynor JR (1999) Differential binding properties of oripavines at cloned mu- and delta-opioid receptors. Eur J Pharmacol 378:323-330.
21. Ma W, Zheng WH, Powell K, Jhamandas K and Quirion R (2001) Chronic morphine exposure increases the phosphorylation of MAP kinases and the transcription factor CREB in dorsal root ganglion neurons: an in vitro and in vivo study. Eur J Neurosci 14:1091-1104.
22. Milligan G (1988) Techniques used in the identification and analysis of functional pertussis toxin-sensitive guanine nucleotide binding proteins. Biochem J 255:1-13.
23. Neubig RR and Siderovski DP (2002) Regulators of G-protein signaling as new central nervous system drug targets. Nat Rev Drug Discov 1:187-197.
24. Ni YG, Gold SJ, Iredale PA, Terwilliger RZ, Duman RS, and Nestler EJ (1999) Region-specific regulation of RGS4 (regulator of G-protein-signaling protein type 4) in brain by stress and glucocorticoids: in vivo and in vitro studies. J Neurosci 19:3674-3680.
25. Pak P, O'Dowd BF, Wang JBN, and George SR (1999) Agonist-induced G protein dependent and independent down-regulation of the μ-opioid receptor. J Biol Chem 274:27610-27616.
26. Patel MB, Patel CN, Rajashekara V, and Yoburn BC (2002) Opioid agonists differ-entklly regulate μ-opioid receptors and trafficking proteins in vivo. Mol Pharmacol 62:1464-1470.
27. Polakiewicz RD, Schieferl SM, Dorner LF, Kansra V, and Comb MJ (1998) A mitogen-activated protein kinase pathway is required for μ-opioid receptor desen-sitization. J Biol Chem 273:12402-12406.
28. Potenza MN, Gold SJ, Roby-Shemkowitz A, Lerner MR, and Nestler EJ (1999) Effects of regulators of G protein-signaling proteins on the functional response of the mu-opioid receptor in a melanophore-based assay. J Pharmacol Exp Ther 291:482-491.
29. Sánchez-Blázquez P, Rodríguez-Díaz M, López-Fando A, Rodríguez-Muñoz M, and Garzón J (2003) The GBeta5 subunit that associates with the R7 subfamily of RGS proteins regulates mu-opioid effects. Neuropharmacology 45:82-95.
30. Schmidt H, Schultz S, Klutzny M, Koch T, Handel M, and Hollt V (2000) Involvement of mitogen-activated protein kinase in agonist-induced phosphorylation of the μ-opioid receptor in HEK 293 cells. J Neurochem 74:414-422.
31. Snow BE, Brothers GM, and Siderovski DP (2002) Molecular cloning of regulators of G-protein signaling family members and characterization of binding specificity of RGS12 PDZ domain. Methods Enzymol 344:740-761.
32. Traynor JR and Nahorski SR (1995) Modulation of mu-opioid agonists of guanosine 5′-O-(3-[35S]thio)triphosphate binding to membranes from human neuroblastoma SH-SY5Y cells. Mol Pharmacol 47:848-854.
33. Watts VJ (2002) Molecular mechanisms for heterologous sensitization of adenylate cyclase. J Pharmacol Exp Ther 302:1-7.
34. Yabaluri N and Medzihradsky F (1997) Down-regulation of μ-opioid receptor by full but not partial agonists is independent of G protein coupling. Mol Pharmacol 52:896-902.
35. iα2-protein in opioid tolerance and μ-opioid receptor down-regulation in vivo. Synapse 47:109-116.
36. Zachariou V, Georgescu D, Sanchez N, Rahman Z, DiLeone R, Berton O, Neve RL, Sim-Selley LJ, Selley DE, Gold SJ, et al. (2003) Essential role for RGS9 in opiate action. Proc Natl Acad Sci USA 100:13656-13661.