Region-dependent attenuation of μ opioid receptor-mediated G-protein activation in mouse CNS as a function of morphine tolerance

British Journal of Pharmacology

Volumn 151, Issue 8, 2007, Pages 1324-1333

  Sim Selley, L J ^a   Scoggins, K L ^a   Cassidy, M P ^a   Smith, L A ^a   Dewey, W L ^a   Smith, F L ^a   Selley, D E ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

35S GTP S autoradiography; Brainstem; Desensitization; Downregulation; Opiate; Spinal cord

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); MORPHINE; MU OPIATE RECEPTOR; PLACEBO; SULFUR 35;

ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; ATTENUATION; BEHAVIOR; CAUDATE NUCLEUS; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DESENSITIZATION; DRUG DOSE INCREASE; DRUG EFFECT; DRUG EXPOSURE; DRUG IMPLANTATION; HYPOTHERMIA; MALE; MORPHINE TOLERANCE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN FUNCTION; PUTAMEN; RECEPTOR BINDING; SOLITARY TRACT NUCLEUS; SPINAL CORD; SPINAL CORD DORSAL HORN; TISSUE SECTION;

ANALGESICS, OPIOID; ANIMALS; BINDING SITES; CENTRAL NERVOUS SYSTEM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; GTP-BINDING PROTEINS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HYPOTHERMIA; MALE; MICE; MORPHINE; PAIN MEASUREMENT; POSTERIOR HORN CELLS; RECEPTORS, OPIOID, MU; SOLITARY NUCLEUS; TAIL;

EID: 34547856184     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0707328     Document Type: Article

References (51)

1. Bailey CP, Couch D, Johnson E, Griffiths K, Kelley E, Henderson G (2003). Opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine. J Neurosci 23: 10515-10520.
2. Bergman J, France CP, Holtzman SG, Katz JL, Koek W, Stephens DN (2000). Agonist efficacy, drug dependence, and medications development: preclinical evaluation of opioid, dopaminergic, and GABAA-ergic ligands. Psychopharmacology (Berl) 153: 67-84.
3. Bliss CI (1967). Statistics in Biology. McGraw-Hill: New York.
4. Bohn LM, Gainetdinov RR, Lin FT, Lefkowitz RJ, Caron MG (2000). Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 408: 720-723.
5. Bohn LM, Lefkowitz RJ, Caron MG (2002). Differential mechanisms of morphine antinociceptive tolerance revealed in barrestin-2 knock-out mice. J Neurosci 22: 10494-10500.
6. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, Lin FT (1999). Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 286: 2495-2498.
7. Bradford MM (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
8. Breivogel CS, Selley DE, Childers SR (1997). Acute and chronic effects of opioids on delta and mu receptor activation of G-proteins in NG108-15 and SK-N-SH cell membranes. J Neurochem 68: 1462-1472.
9. Childers SR (1991). Opioid receptor-coupled second messengers. Life Sci 48: 1991-2003.
10. Christie MJ, Williams JT, North RA (1987). Cellular mechanisms of opioid tolerance: studies in single brain neurons. Mol Pharmacol 32: 633-638.
11. Colquhoun D (1971). Lectures on Biostatistics: An Introduction to Statistics with Applications in Biology and Medicine. Clarendon Press: Oxford.
12. Deng HB, Yu Y, Wang H, Guang W, Wang JB (2001). Agonist-induced μ opioid receptor phosphorylation and functional desensitization in rat thalamus. Brain Research 898: 204-214.
13. De Vry J, Donselaar I, Van Ree JM (1989). Intraventricular self-administration of heroin in the rat: reward seems dissociated from analgesia and physical dependence. Eur J Pharmacol 161: 19-25.
14. Fan X, Zhang J, Zhang X, Yue W, Ma L (2002). Acute and chronic morphine treatments and morphine withdrawal differentially regulate GRK2 and GRK5 gene expression in rat brain. Neuropharmacology 43: 809-816.
15. Fields HL, Basbaum AI (1978). Brainstem control of spinal pain-transmission neurons. Annu Rev Physiol 40: 217-248.
16. Gintzler AR, Adapa ID, Toll L, Medina VM, Wang L (1997). Modulation of enkephalin release by nociceptin (orphanin FQ). Eur J Pharmacol 325: 29-34.
17. Harris LS, Pierson AK (1964). Some narcotic antagonists in the benzomorphan series. J Pharmacol Exp Ther 143: 141-148.
18. 3H]flunitrazapam are elevated in discrete brain regions of butorphanol-withdrawal rats. Neurochem Res 27: 939-946.
19. Kameyama T, Nabeshima T, Ukai M, Yamaguchi K (1978). Morphine-induced Straub tail reaction and spinal catecholamine metabolite content: antagonism of naloxone to morphine-induced effects in mice. Chem Pharm Bull (Tokyo) 26: 2615-2618.
20. 35S]thio]-triphosphate autoradiography in rat brain. Eur J Pharmacol 446: 43-51.
21. Kolesnikov YA, Jain S, Wilson R, Pasternak GW (1996). Peripheral morphine analgesia: synergy with central sites and a target of morphine tolerance. J Pharmacol Exp Ther 279: 502-506.
22. 35S]GTPγS binding. Synapse 47: 243-249.
23. Law PY, Wong YH, Loh HH (2000). Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40: 389-430.
24. Loh HH, Liu HC, Cavalli A, Yang W, Chen YF, Wei LN (1998). Mu opioid receptor knockout in mice: effects on ligand-induced analgesia and morphine lethality. Mol Brain Res 54: 321-326.
25. Maher CE, Eisenach JC, Pan H-L, Xiao R, Childers SR (2001). Chronic intrathecal morphine administration produces homologous mu receptor/G-protein desensitization specifically in spinal cord. Brain Res 895: 1-8.
26. Matthes HWD, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I et al. (1996). Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the μ-opioid receptor gene. Nature 383: 819-823.
27. McDaid J, Dallimore JE, Mackie AR, Napier TC (2006). Changes in accumbal and pallidal pCREB and deltaFosB in morphine-sensitized rats: correlations with receptor-evoked electrophysiological measures in the ventral pallidum. Neuropsychopharmacology 31: 1212-1226.
28. Nestler EJ, Alreja M, Aghajanian GK (1994). Molecular and cellular mechanisms of opiate action: studies in the locus coeruleus. Brain Res Bull 35: 521-528.
29. Noble F, Cox BM (1996). Differential desensitization of mu- and delta-opioid receptors in selected neural pathways following chronic morphine treatment. Br J Pharmacol 117: 161-169.
30. Nozaki-Taguchi N, Yaksh TL (1999). Characterization of the anti-hyperalgesic action of a novel peripheral mu-opioid receptor agonist - loperamide. Anesthesiology 90: 225-234.
31. O'Callaghan JP, Holtzman SG (1975). Quantification of the analgesic activity of narcotic antagonists by a modified hot-plate procedure. J Pharmacol Exp Ther. 192: 497-505.
32. Ossipov MH, Lai J, King T, Vanderah TW, Malan Jr TP, Hruby VJ et al. (2004). Antinociceptive and nociceptive actions of opioids. J Neurobiol 61: 126-148.
33. Ozaita A, Escriba PV, Ventayol P, Murga C, Mayor JF, Garcia-Sevilla JA (1998). Regulation of G protein-coupled receptor kinase 2 in brains of opiate-treated rats and human opiate addicts. J Neurochem 70: 1249-1257.
34. Patel MB, Patel CN, Rajashekara V, Yoburn BC (2002). Opioid agonists differentially regulate μ-opioid receptors and trafficking proteins in vivo. Mol Pharmacol 62: 1464-1470.
35. Patrick GA, Dewey WL, Spaulding TC, Harris LS (1975). Relationship of brain morphine levels to analgesic activity in acutely treated mice and rats and in pellet implanted mice. J Pharmacol Exp Ther 193: 876-883.
36. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates. Academic Press: San Diego, CA.
37. Powell KR, Holtzman SG (2001). Parametric evaluation of the development of sensitization to the effects of morphine on locomotor activity. Drug Alcohol Depend 62: 83-90.
38. Puttfarcken PS, Cox BM (1989). Morphine-induced desensitization and downregulation at mu-receptors in 7315C pituitary tumor cells. Life Sci 45: 1937-1942.
39. Roerig SC, O'Brien SM, Fujimoto JM, Wilcox GL (1984). Tolerance to morphine analgesia: decreased multiplicative interaction between spinal and supraspinal sites. Brain Res 308: 360-363.
40. 35S]thio]-triphosphate binding. Proc Natl Acad Sci USA 92: 7242-7246.
41. 35S] GTPγS autoradiography in rat brain. J Neurosci 16: 2684-2692.
42. Sim-Selley LJ, Selley DE, Vogt LJ, Childers SR, Martin TJ (2000). Chronic heroin self-administration desensitizes mu opioid receptor-activated G-proteins in specific regions of rat brain. J Neurosci 20: 4555-4562.
43. Smith FL, Javed RR, Elzey MJ, Dewey WL (2003). The expression of a high level of morphine antinociceptive tolerance in mice involves both PKC and PKA. Brain Res 985: 78-88.
44. Stafford K, Gomes AB, Shen J, Yoburn BC (2001). Opioid receptor downregulation contributes to opioid tolerance in vivo. Pharmacol Biochem Behav 69: 233-237.
45. Tao P-L, Law P-Y, Loh HH (1987). Decrease in delta and mu opioid receptor binding capacity in rat brain after chronic etorphine treatment. J Pharmacol Exp Ther 240: 809-816.
46. Tao P-L, Lee C-R, Law P-Y, Loh HH (1993). The interaction of the mu-opioid receptor and G protein is altered after chronic morphine treatment in rats. Nauyn-Schmiedeberg's Arch Pharmacol 348: 504-508.
47. Tian M, Broxmeyer HE, Fan Y, Lai Z, Zhang S, Aronica S et al. (1997). Altered hematopoiesis, behavior, and sexual function in μ opioid receptor-deficient mice. J Exp Med 185: 1517-1522.
48. Vigano D, Rubino T, Di Chiara G, Ascari I, Massi P, Parolaro D (2003). Mu opioid receptor signaling in morphine sensitization. Neuroscience 117: 921-929.
49. Way EL, Loh HH, Shen FH (1969). Simultaneous quantitative assessment of morphine tolerance and physical dependence. J Pharmacol Exp Ther 167: 1-8.
50. Zhang G, Lagrange AH, Ronnekleiv OK, Kelly MJ (1996). Tolerance of hypothalamic β-endorphin neurons to μ-opioid receptor activation after chronic morphine. J Pharmacol Exp Ther 277: 551-558.
51. Zhang J, Ferguson SSG, Barak LS, Bodduluri SR, Laporte SA, Law P-Y et al. (1998). Role for G protein-coupled receptor kinase in agonist-specific regulation of μ-opioid receptor responsiveness. Proc Natl Acad Sci USA 95: 7157-7162.