Agonists at the δ-opioid receptor modify the binding of μ-receptor agonists to the μ-δ receptor hetero-oligomer

British Journal of Pharmacology

Volumn 161, Issue 5, 2010, Pages 1122-1136

  Kabli, N ^a,b   Martin, N ^a,b   Fan, T ^a   Nguyen, T ^a   Hasbi, A ^a,b   Balboni, G ^c   O'dowd, B F ^a,b   George, S R ^a,b  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

opioid receptor; opioid receptor; Binding pocket; Chronic morphine exposure; Clathrin; Heteromer; Internalization

Indexed keywords

CLATHRIN; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLORNITHYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; DYNAMIN; G PROTEIN ALPHA Z SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MEMBRANE PROTEIN; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; OLIGOMER; PERTUSSIS TOXIN; RADIOLIGAND; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CELL STRAIN HEK293; CHEMICAL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG EXPOSURE; DRUG RECEPTOR BINDING; EMBRYO; ENDOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIGAND BINDING; LONG TERM EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS;

ANALGESICS, OPIOID; BINDING, COMPETITIVE; CELL LINE; GTP-BINDING PROTEIN ALPHA SUBUNITS; HUMANS; LIGANDS; MICROSCOPY, CONFOCAL; MORPHINE; PROTEIN BINDING; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU;

EID: 77958588956     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00944.x     Document Type: Article

References (45)

1. Alexander SPH, Mathie A, Peters JA (2009). Guide to Receptors and Channels (GRAC), 4th edn. Br J Pharmacol 158 (Suppl. 1): S1-S254.
2. Avidor-Reiss T, Bayewitch M, Levy R, Matus-Leibovitch N, Nevo I, Vogel Z (1995). Adenylylcyclase supersensitization in mu-opioid receptor-transfected Chinese hamster ovary cells following chronic opioid treatment. J Biol Chem 270: 29732-29738.
3. Balboni G, Salvadori S, Guerrini R, Negri L, Giannini E, Jinsmaa Y et al. (2002). Potent delta-opioid receptor agonists containing the dmt-Tic pharmacophore. J Med Chem 45: 5556-5563.
4. Blake Ad, Bot G, Freeman JC, Reisine T (1997). differential opioid agonist regulation of the mouse mu opioid receptor. J Biol Chem 272: 782-790.
5. Bradbury FA, Zelnik JC, Traynor JR (2009). G protein independent phosphorylation and internalization of the delta-opioid receptor. J Neurochem 109: 1526-1535.
6. Chen Y, Mestek A, Liu J, Hurley JA, Yu L (1993). Molecular cloning and functional expression of a mu-opioid receptor from rat brain. Mol Pharmacol 44: 8-12.
7. Chidiac P, Green MA, Pawagi AB, Wells JW (1997). Cardiac muscarinic receptors. Cooperativity as the basis for multiple states of affinity. Biochemistry 36: 7361-7379.
8. Christie MJ (2008). Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. Br J Pharmacol 154: 384-396.
9. Connor M, Osborne PB, Christie MJ (2004). Mu-opioid receptor desensitization: is morphine different? Br J Pharmacol 143: 685-696.
10. deLean A, Lefkowitz RJ (1980). dihydroergocryptine binding and alpha-adrenoreceptors in smooth muscle. Nature 283: 109-110.
11. Eisinger dA, Ammer H, Schulz R (2002). Chronic morphine treatment inhibits opioid receptor desensitization and internalization. J Neurosci 22: 10192-10200.
12. Fan T, Varghese G, Nguyen T, Tse R, O'dowd BF, George SR (2005). A role for the distal carboxyl tails in generating the novel pharmacology and G protein activation profile of mu and delta opioid receptor hetero-oligomers. J Biol Chem 280: 38478-38488.
13. Ferguson SS, Zhang J, Barak LS, Caron MG (1998). Molecular mechanisms of G protein-coupled receptor desensitization and resensitization. Life Sci 62: 1561-1565.
14. Finn AK, Whistler JL (2001). Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32: 829-839.
15. Fong HK, Yoshimoto KK, Eversole-Cire P, Simon MI (1988). Identification of a GTP-binding protein alpha subunit that lacks an apparent AdP-ribosylation site for pertussis toxin. Proc Natl Acad Sci U S A 85: 3066-3070.
16. George SR, Fan T, Xie Z, Tse R, Tam V, Varghese G et al. (2000). Oligomerization of mu- and delta-opioid receptors. Generation of novel functional properties. J Biol Chem 275: 26128-26135.
17. Gomes I, Jordan BA, Gupta A, Trapaidze N, Nagy V, devi LA (2000). Heterodimerization of mu and delta opioid receptors: a role in opiate synergy. J Neurosci 20: RC110.
18. Gomes I, Gupta A, Filipovska J, Szeto HH, Pintar JE, devi LA (2004). A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia. Proc Natl Acad Sci U S A 101: 5135-5139.
19. Green MA, Chidiac P, Wells JW (1997). Cardiac muscarinic receptors. Relationship between the G protein and multiple states of affinity. Biochemistry 36: 7380-7394.
20. Gulya K, Krivan M, Nyolczas N, Sarnyai Z, Kovacs GL (1988). Central effects of the potent and highly selective mu opioid antagonist d-Phe-Cys-Tyr-d-Trp-Orn-Thr-Pen-Thr-NH2 (CTOP) in mice. Eur J Pharmacol 150: 355-360.
21. Hasbi A, Nguyen T, Fan T, Cheng R, Rashid A, Alijaniaram M et al. (2007). Trafficking of preassembled opioid mu-delta heterooligomer-Gz signaling complexes to the plasma membrane: coregulation by agonists. Biochemistry 46: 12997-13009.
22. Holz GG, Kream RM, Spiegel A, dunlap K (1989). G proteins couple alpha-adrenergic and GABAb receptors to inhibition of peptide secretion from peripheral sensory neurons. J Neurosci 9: 657-666.
23. Kara E, Lin H, Strange PG (2010). Co-operativity in agonist binding at the d2 dopamine receptor: evidence from agonist dissociation kinetics. J Neurochem 112: 1442-1453.
24. Kieffer BL, Befort K, Gaveriaux-Ruff C, Hirth CG (1992). The delta-opioid receptor: isolation of a cdNA by expression cloning and pharmacological characterization. Proc Natl Acad Sci U S A 89: 12048-12052.
25. Koch T, Schulz S, Schroder H, Wolf R, Raulf E, Hollt V (1998). Carboxyl-terminal splicing of the rat mu opioid receptor modulates agonist-mediated internalization and receptor resensitization. J Biol Chem 273: 13652-13657.
26. Law PY, Erickson-Herbrandson LJ, Zha QQ, Solberg J, Chu J, Sarre A et al. (2005). Heterodimerization of mu- and delta-opioid receptors occurs at the cell surface only and requires receptor-G protein interactions. J Biol Chem 280: 11152-11164.
27. Levac BA, O'dowd BF, George SR (2002). Oligomerization of opioid receptors: generation of novel signaling units. Curr Opin Pharmacol 2: 76-81.
28. Li S, Zhu J, Chen C, Chen YW, deriel JK, Ashby B et al. (1993). Molecular cloning and expression of a rat kappa opioid receptor. Biochem J 295 (Pt 3): 629-633.
29. Pak Y, O'dowd BF, Wang JB, George SR (1999). Agonist-induced, G protein-dependent and -independent down-regulation of the mu opioid receptor. The receptor is a direct substrate for protein-tyrosine kinase. J Biol Chem 274: 27610-27616.
30. Portoghese PS, Sultana M, Takemori AE (1988). Naltrindole, a highly selective and potent non-peptide delta opioid receptor antagonist. Eur J Pharmacol 146: 185-186.
31. Premont RT, Buku A, Iyengar R (1989). The G alpha z gene product in human erythrocytes. Identification as a 41-kilodalton protein. J Biol Chem 264: 14960-14964.
32. Remmers AE, Clark MJ, Liu XY, Medzihradsky F (1998). delta opioid receptor down-regulation is independent of functional G protein yet is dependent on agonist efficacy. J Pharmacol Exp Ther 287: 625-632.
33. Rothman RB, Westfall TC (1982). Allosteric coupling between morphine and enkephalin receptors in vitro. Mol Pharmacol 21: 548-557.
34. Rozenfeld R, devi LA (2007). Receptor heterodimerization leads to a switch in signaling: beta-arrestin2-mediated ERK activation by mu-delta opioid receptor heterodimers. Faseb J 21: 2455-2465.
35. Rutherford JM, Wang J, Xu H, dersch CM, Partilla JS, Rice KC et al. (2008). Evidence for a mu-delta opioid receptor complex in CHO cells co-expressing mu and delta opioid peptide receptors. Peptides 29: 1424-1431.
36. Segredo V, Burford NT, Lameh J, Sadee W (1997). A constitutively internalizing and recycling mutant of the mu-opioid receptor. J Neurochem 68: 2395-2404.
37. Sharma SK, Klee WA, Nirenberg M (1975). dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance. Proc Natl Acad Sci U S A 72: 3092-3096.
38. Snook LA, Milligan G, Kieffer BL, Massotte d (2008). Co-expression of mu and delta opioid receptors as receptor-G protein fusions enhances both mu and delta signalling via distinct mechanisms. J Neurochem 105: 865-873.
39. Szeto HH, Lovelace JL, Fridland G, Soong Y, Fasolo J, Wu d et al. (2001). In vivo pharmacokinetics of selective mu-opioid peptide agonists. J Pharmacol Exp Ther 298: 57-61.
40. Toews ML (2000). Radioligand binding assays for G-protein coupled receptor internalization. In: Benovic JL (ed.). Regulation of G-protein Coupled Receptor Function and Expression. Wiley-Liss: Toronto, ON, Canada, pp. 199-230.
41. Traynor JR, Elliott J (1993). delta-opioid receptor subtypes and cross-talk with mu-receptors. Trends Pharmacol Sci 14: 84-86.
42. Waldhoer M, Bartlett SE, Whistler JL (2004). Opioid receptors. Annu Rev Biochem 73: 953-990.
43. Yan F, Mosier Pd, Westkaemper RB, Roth BL (2008). Galpha-subunits differentially alter the conformation and agonist affinity of kappa-opioid receptors. Biochemistry 47: 1567-1578.
44. Zaki PA, Keith dE, Jr, Brine GA, Carroll FI, Evans CJ (2000). Ligand-induced changes in surface mu-opioid receptor number: relationship to G protein activation? J Pharmacol Exp Ther 292: 1127-1134.
45. Zhang J, Ferguson SS, Barak LS, Menard L, Caron MG (1996). dynamin and beta-arrestin reveal distinct mechanisms for G protein-coupled receptor internalization. J Biol Chem 271: 18302-18305.