Formation of μ-/κ-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 46, 2010, Pages 20115-20119

  Chakrabarti, Sumita ^a   Liu, Nai Jiang ^a   Gintzler, Alan R ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Estrous cycle; Sex steroids; Sexual dimorphism; Signaling complexes estrogen and progesterone

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; DYNORPHIN A; HETERODIMER; KAPPA OPIATE RECEPTOR; MORPHINE; MU OPIATE RECEPTOR; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; NORBINALTORPHIMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; CONFERENCE PAPER; CONTROLLED STUDY; DIESTRUS; DIMERIZATION; FEMALE; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SPINAL ANESTHESIA; SPINAL CORD; TRANSDUCER;

EID: 78650551486     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1009923107     Document Type: Article

References (41)

1. Rollman GB, Lautenbacher S (2001) Sex differences in musculoskeletal pain. Clin J Pain 17:20-24.
2. Yunus MB (2001) The role of gender in fibromyalgia syndrome. Curr Rheumatol Rep 3:128-134.
3. Mayer EA, Naliboff B, Lee O, Munakata J, Chang L (1999) Review article: Gender- related differences in functional gastrointestinal disorders. Aliment Pharmacol Ther 13 (Suppl 2):65-69.
4. Larijani GE, Goldberg ME, Gratz I, Warshal DP (2004) Analgesic and hemodynamic effects of a single 7.5-mg intravenous dose of morphine in patients with moderate-to-severe postoperative pain. Pharmacotherapy 24:1675-1680.
5. Mogil JS, Sternberg WF, Kest B, Marek P, Liebeskind JC (1993) Sex differences in the antagonism of swim stress-induced analgesia: Effects of gonadectomy and estrogen replacement. Pain 53:17-25.
6. Kayser V, Berkley KJ, Keita H, Gautron M, Guilbaud G (1996) Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat. Brain Res 742:352-354.
7. Coyle DE, Sehlhorst CS, Mascari C (1995) Female rats are more susceptible to the development of neuropathic pain using the partial sciatic nerve ligation (PSNL) model. Neurosci Lett 186:135-138.
8. Cicero TJ, Nock B, Meyer ER (1997) Sex-related differences in morphine's antinociceptive activity: Relationship to serum and brain morphine concentrations. J Pharmacol Exp Ther 282:939-944.
9. Barrett AC, Smith ES, Picker MJ (2002) Sex-related differences in mechanical nociception and antinociception produced by mu-and kappa-opioid receptor agonists in rats. Eur J Pharmacol 452:163-173.
10. Unruh AM (1996) Gender variations in clinical pain experience. Pain 65:123-167.
11. Gear RW, et al. (1996) Kappa-opioids produce significantly greater analgesia in women than in men. Nat Med 2:1248-1250.
12. Gear RW, et al. (2003) Sexual dimorphism in very low dose nalbuphine postoperative analgesia. Neurosci Lett 339:1-4.
13. Gear RW, et al. (1999) The kappa opioid nalbuphine produces gender-and dose-dependent analgesia and antianalgesia in patients with postoperative pain. Pain 83: 339-345.
14. Gear RW, et al. (1996) Gender difference in analgesic response to the kappa-opioid pentazocine. Neurosci Lett 205:207-209.
15. Mogil JS, et al. (2003) The melanocortin-1 receptor gene mediates female-specific mechanisms of analgesia in mice and humans. Proc Natl Acad Sci USA 100:4867-4872.
16. Sternberg WF, et al. (1995) Neonatal testosterone exposure influences neuro-chemistry of non-opioid swim stress-induced analgesia in adultmice. Pain 63:321-326.
17. Liu NJ, von Gizycki H, Gintzler AR (2007) Sexually dimorphic recruitment of spinal opioid analgesic pathways by the spinal application of morphine. J Pharmacol Exp Ther 322:654-660.
18. Zadina JE, Hackler L, Ge LJ, Kastin AJ (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386:499-502.
19. Stevens CW, Yaksh TL (1986) Dynorphin A and related peptides administered intrathecally in the rat: A search for putative kappa opiate receptor activity. J Pharmacol Exp Ther 238:833-838.
20. Przewtocka B, Dziedzicka M, Lasoh W, Przewtocki R (1992) Differential effects of opioid receptor agonists on nociception and cAMP level in the spinal cord of monoarthritic rats. Life Sci 50:45-54.
21. Piercey MF, Einspahr FJ (1989) Spinal analgesic actions of kappa receptor agonists, U-50488H and spiradoline (U-62066). J Pharmacol Exp Ther 251:267-271.
22. Schmauss C (1987) Spinal kappa-opioid receptor-mediated antinociception is stimulus-specific. Eur J Pharmacol 137:197-205.
23. Angers S, Salahpour A, Bouvier M (2002) Dimerization: An emerging concept for G protein-coupled receptor ontogeny and function. Annu Rev Pharmacol Toxicol 42: 409-435.
24. George SR, O'Dowd BF, Lee SP (2002) G-protein-coupled receptor oligomerization and its potential for drug discovery. Nat Rev Drug Discov 1:808-820.
25. Maggio R, Scarselli M, Novi F, Millan MJ, Corsini GU (2003) Potent activation of dopamine D3/D2 heterodimers by the antiparkinsonian agents, 532504, pramipexole and ropinirole. J Neurochem 87:631-641.
26. Jordan BA, Devi LA (1999) G-protein-coupled receptor heterodimerization modulates receptor function. Nature 399:697-700.
27. Franco R, et al. (2000) Evidence for adenosine/dopamine receptor interactions: Indications for heteromerization. Neuropsychopharmacology 23 (4 Suppl):S50-S59.
28. Galvez T, et al. (2001) Allosteric interactions between GB1 and GB2 subunits are required for optimal GABA(B) receptor function. EMBO J 20:2152-2159.
29. Terrillon S, Barberis C, Bouvier M (2004) Heterodimerization of V1a and V2 vasopressin receptors determines the interaction with beta-arrestin and their trafficking patterns. Proc Natl Acad Sci USA 101:1548-1553.
30. Lee SP, et al. (2004) Dopamine D1 and D2 receptor Co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 279:35671-35678.
31. Mellado M, et al. (2001) Chemokine receptor homo-or heterodimerization activates distinct signaling pathways. EMBO J 20:2497-2507.
32. Holtman JR, Jr, Wala EP (2006) Characterization of the antinociceptive effect of oxycodone in male and female rats. Pharmacol Biochem Behav 83:100-108.
33. Garzón J, Sánchez-Blázquez P, Höllt V, Lee NM, Loh HH (1983) Endogenous opioid peptides: Comparative evaluation of their receptor affinities in the mouse brain. Life Sci 33 (Suppl 1):291-294.
34. George SR, et al. (2000) Oligomerization of mu-and delta-opioid receptors. Generation of novel functional properties. J Biol Chem 275:26128-26135.
35. Rashid AJ, et al. (2007) D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci USA 104:654-659.
36. Kearn CS, Blake-Palmer K, Daniel E, Mackie K, Glass M (2005) Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors enhances heterodimer formation: A mechanism for receptor cross-talk? Mol Pharmacol 67:1697-1704.
37. Ellis J, Pediani JD, Canals M, Milasta S, Milligan G (2006) Orexin-1 receptor-cannabinoid CB1 receptor heterodimerization results in both ligand-dependent and-independent coordinated alterations of receptor localization and function. J Biol Chem 281:38812-38824.
38. Park PS, Sum CS, Pawagi AB, Wells JW (2002) Cooperativity and oligomeric status of cardiac muscarinic cholinergic receptors. Biochemistry 41:5588-5604.
39. Lai J, Ossipov MH, Vanderah TW, Malan TP, Jr, Porreca F (2001) Neuropathic pain: The paradox of dynorphin. Mol Interv 1:160-167.
40. Chalecka-Franaszek E, Weems HB, Crowder AT, Cox BM, Cote TE (2000) Immunoprecipitation of high-affinity, guanine nucleotide-sensitive, solubilized mu-opioid receptors from rat brain: Coimmunoprecipitation of the G proteins G(alpha o), G(alpha i1), and G(alpha i3). J Neurochem 74:1068-1078.
41. Chakrabarti S, Chang A, Gintzler AR (2010) Subcellular localization of mu-opioid receptor G(s) signaling. J Pharmacol Exp Ther 333:193-200.