Decreased μ-opioid receptor signalling and a reduction in calcium current density in sensory neurons from chronically morphine-treated mice

British Journal of Pharmacology

Volumn 148, Issue 7, 2006, Pages 947-955

  Johnson, Emma E ^a   Chieng, Billy ^a   Napier, Ian ^a   Connor, Mark ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Analgesia; Chronic opioids; Morphine tolerance; Neuroadaptation; Trigeminal ganglion

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; BACLOFEN; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MESSENGER RNA; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; GUANINE NUCLEOTIDE BINDING PROTEIN; ION CHANNEL; NARCOTIC ANALGESIC AGENT; PROSTAGLANDIN E RECEPTOR; PROSTAGLANDIN EP3 RECEPTOR;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CALCIUM CURRENT; CELL FUNCTION; CONTROLLED STUDY; DRUG SELECTIVITY; EMULSION; INHIBITION KINETICS; LONG TERM CARE; MALE; MORPHINE TOLERANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR AFFINITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SLOW RELEASE FORMULATION; TRIGEMINUS GANGLION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL SEPARATION; CYTOLOGY; DRUG EFFECT; ELECTROPHYSIOLOGY; METABOLISM; NOCICEPTIVE RECEPTOR; PAIN ASSESSMENT; PHYSIOLOGY;

ANALGESICS, OPIOID; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CELL SEPARATION; ELECTROPHYSIOLOGY; GTP-BINDING PROTEINS; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MORPHINE; NEURONS, AFFERENT; NOCICEPTORS; PAIN MEASUREMENT; RECEPTORS, OPIOID, MU; RECEPTORS, PROSTAGLANDIN E; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRIGEMINAL GANGLION;

EID: 33749358049     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/sj.bjp.0706820     Document Type: Article

References (45)

1. AKINS, P.T. & MCCLESKEY, E.W. (1993). Characterization of potassium currents in adult rat sensory neurons and modulation by opioids and cyclic AMP. Neuroscience, 56, 759-769.
2. BAGLEY, E.E., CHIENG, B., CHRISTIE, M.J. & CONNOR, M. (2005a). Opioid tolerance in periaqueductal grey neurons isolated from mice chronically treated with morphine. Br. J. Pharmacol., 146, 68-76.
3. BAGLEY, E.E., GERKE, M.B., VAUGHAN, C.W., HACK, S.P. & CHRISTIE, M.J. (2005b). GABA transporter currents activated by protein kinase A excite midbrain neurons during opioid withdrawal. Neuron, 45, 433-445.
4. BAILEY, C.P. & CONNOR, M. (2005). Opioids: cellular mechanisms of tolerance and physical dependence. Curr. Opin. Pharmacol., 5, 60-68.
5. 2+ current in the action potentials of nociceptive sensory neurons. J. Neurosci., 22, 10277-10290.
6. BORGLAND, S.L., CONNOR, M. & CHRISTIE, M.J. (2001). Nociceptin inhibits calcium channel currents in a subpopulation of small nociceptive trigeminal ganglion neurons in mouse. J. Physiol. (London), 536, 35-47.
7. 2 inhibits calcium current in two subpopulations of acutely isolated mouse trigeminal sensory neurons. J. Physiol. (London), 539, 433-444.
8. BUSTIN, S.A., BENES, V., NOLAN, T. & PFAFFL, M.W. (2005). Quantitative real time RT-PCR - a perspective. J. Mol. Endocrinol., 34, 597-601.
9. BUNTIN-MUSHOCK, C., PHILLIP, L., MORIYAMA, K. & PALMER, P.P. (2005). Age-dependent opioid escalation in chronic pain patients. Anesth. Analg., 100, 1740-1745.
10. CHRISTIE, M.J., WILLIAMS, J.T. & NORTH, R.A. (1987). Cellular mechanisms of opioid tolerance: studies in single brain neurons. Mol Pharmacol, 32, 633-638.
11. CONNOR, M., BORGLAND, S.L. & CHRISTIE, M.J. (1999a). Continued morphine modulation of calcium channel currents in acutely isolated locus coeruleus neurons from morphine-dependent rats. Br. J. Pharmacol., 128, 1561-1569.
12. CONNOR, M., SCHULLER, A., PINTAR, J.E. & CHRISTIE, M.J. (1999b). Opioid receptor modulation of calcium channel current in periaqueductal grey neurons form C57B16/J mice and mutant mice lacking MOR-1. Br. J. Pharmacol., 126, 1553-1558.
13. 1A agonist (3-chloro-4-fluoro-phenyl)-[4-fluoro-4-{[(5-methyl-pyridin-2-ylmethyl)-amino] -methyl}piperidin-1-yl]-methadone (F 13640) attenuates allodynia-like behavior in a rat model of trigeminal neuropathic pain. J. Pharmacol. Exp. Ther., 306, 505-514.
14. 2+ channel function? Trends Pharmacol. Sci., 26, 427-436.
15. DIONNE, R.A., LEPINSKI, A.M., GORDON, S.M., JABER, L., BRAHIM, J.S. & HARGREAVES, K.M. (2001). Analgesic effects of peripherally administered opioids in clinical models of acute and chronic inflammation. Clin. Pharmacol. Ther., 70, 66-73.
16. EISENBERG, E., VOS, B.P. & STRASSMAN, A.M. (1996). The peripheral antinociceptive effect of morphine in a rat model of facial pain. Neuroscience, 72, 519-525.
17. GARDELL, L.R., WANG, R., BURGESS, S.E., OSSIPOV, M.H., VANDERAH, T.W., MALAN, T.P., LAI, J. & PORRECA, F. (2002). Sustained morphine exposure induces a spinal dynorphin-dependent enhancement of excitatory transmitter release from primary afferent fibers. J. Neurosci., 22, 6747-6755.
18. GARZON, J., RODRIGUEZ-MUNOZ, M., DE LA TORRE-MADRID, E. & SANCHEZ-BLASQUEZ, P. (2005). Effector antagonism by the regulators of G protein signalling (RGS) proteins causes desensitization of mu-opioid receptors in the CNS. Psychopharmacology, 180, 1-11.
19. GENDRON, L., LUCIDO, A.L., MENNICKEN, F., O'DONNELL, D., VINCENT, J.-P., STROH, T. & BEAUDET, A. (2006). Morphine and pain-related stimuli enhance cellular availability of somatic d-opioid receptors in rat dorsal root ganglia. J. Neurosci., 26, 953-962.
20. GU, G., KONDO, I., HUA, X.-Y. & YAKSH, T.L. (2005). Resting and evoked spinal substance P release during chronic intrathecal morphine infusion: parallels with tolerance and dependence. J. Pharmacol. Exp. Ther., 314, 1362-1369.
21. HAMILL, O.P., MARTY, A., NEHER, E., SAKMANN, B. & SIGWORTH, F.J. (1981). Improved patch-clamp techniques for high resolution current recording from cells and cell free membrane patches. Pflugers Archiv., 391, 85-100.
22. HONORE, P., CATHELINE, G., LE GUEN, S. & BESSON, J.-M. (1997). Chronic treatment with systemic morphine induced tolerance to the systemic and peripheral antinociceptive effects of morphine on both carrageenan induced mechanical hyperalgesia and spinal c-Fos expression. Pain, 71, 99-108.
23. INGRAM, S.L., VAUGHAN, C.W., BAGLEY, E.E., CONNOR, M. & CHRISTIE, MJ. (1998). Enhanced opioid efficacy in opioid dependence is due to an additional signal transduction pathway. J. Neurosci., 18, 10269-10276.
24. JOHNSON, E.E., CHRISTIE, M.J. & CONNOR, M. (2005). The role of opioid receptor phosphorylation and trafficking in adaptations to persistent opioid treatment. Neurosignals, 14, 290-302.
25. KENNEDY, C. & HENDERSON, G. (1991). Opioid receptor inhibition of calcium current: development of homologous tolerance in single SH-SY5Y cells after chronic exposure to morphine in vitro. Mol. Pharmacol., 49, 937-944.
26. KENNEDY, C. & HENDERSON, G. (1992). Chronic exposure to morphine does not induce dependence at the level of the calcium channel current in human SH-SY5Y cells. Neuroscience, 49, 937-944.
27. KING, T., GARDELL, L.R., WANG, R., VARDANYAN, A., OSSIPOV, M.H., MALAN, T.P., VANDERAH, T.W., HUNT, S.P., HRUBY, V.J., LAI, J. & PORRECA, F. (2005). Role of NK-1 neurotransmission in opioid-induced hyperalgesia. Pain, 116, 276-288.
28. LIKAR, R., SITTL, R., GRAGGER, K., PIPAM, W., BLATNIG, H., BRESCHOU, C., SCHALK, H.V., STEIN, C. & SCHAFER, M. (1998). Peripheral morphine analgesia in dental surgery. Pain, 75, 145-150.
29. MA, W., ZHENG, W.-H., POWELL, K., JHAMANDAS, K. & 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.
30. MCQUAY, H. (1999). Opioids in pain management. The Lancet, 353, 2229-2232.
31. MENARD, D.P., VAN ROSSUM, D., KAR, S., ST. PIERRE, S., SUTAK, M., JHAMANDAS, K. & QUIRION, R. (1996). A calcitonin gene-related peptide receptor antagonist prevents the development of tolerance to spinal morphine analgesia. J. Neurosci., 16, 2342-2351.
32. MEUSER, T., GIESECKE, T., GABRIEL, A., HORSCH, M., SABATOWSKI, R., HESCHLER, J., GROND, S. & PALMER, P.P. (2003). Mu-opioid receptor mRNA regulation during morphine tolerance in the rat peripheral nervous system. Anesth. Analg., 97, 1458-1463.
33. NOMURA, K., REUVENY, E. & NARAHASHI, T. (1994). Opioid inhibition and desensitization of calcium channel currents in rat dorsal root ganglion neurons. J. Pharmacol. Exp. Ther., 270, 466-474.
34. OSSIPOV, M.H., LAI, J., KING, T., VANDERAH, T.W., MALAN, T.P., HRUBY, V.J. & PORECCA, F. (2004). Antinociceptive and nociceptive actions of opioids. J. Neurobiol., 61, 125-148.
35. PATEL, M.B., PATERL, C.N., RAJASHEKARA, V. & YOBURN, B.C. (2002). Opioid agonists differentially regulate m-opioid receptor trafficking proteins in vivo. Mol. Pharmacol., 62, 1464-1470.
36. PELISSIER, T., PAJOT, J. & DALLEL, R. (2002). The orofacial capsaicin test in rats: effects of different capsaicin concentrations and morphine. Pain, 96, 81-87.
37. POLASTRON, J., MEUNIER, J.-C. & JAUZAC, P. (1994). Chronic morphine induces tolerance and desensitization of m-opioid receptor but not down-regulation in rabbit. Eur. J. Pharmacol., 266, 139-146.
38. ROBERTS, L.A., CHRISTIE, M.J. & CONNOR, M. (2002). Anandamide is a partial agonist at native vanilloid receptors in acutely isolated mouse trigeminal sensory neurons. Br. J. Pharmacol., 137, 421-428.
39. SAMORISKI, G.M. & GROSS, R.A. (2000). Functional compartmentalization of opioid desensitization in primary sensory neurons. J. Pharmacol. Exp. Ther., 294, 500-509.
40. SCHULLER, A.G.P., KING, M.A., ZHANG, J., BOLAN, E., PAN, Y.-X., MORGAN, D.J., CHANG, A., CZICK, M.E., UNTERWALD, E.M., PASTERNAK, G.W. & PINTAR, J.E. (1999). Retention of heroin and morphine-6b-glucuronide analgesia in anew strain of mice lacking exon 1 one MOR-1. Nat. Neurosci., 2, 151-156.
41. SCHULZ, S., MAYER, D., PFEIFFER, M., STUMM, R., KOCH, T. & HOLLT, V. (2004). Morphine induces terminal μ-opioid receptor desensitization by sustained phosphorylation of serine-375. EMBO J., 23, 3282-3289.
42. STAROWICZ, K., OBARA, I., PRZEWLOCKI, R. & PRZEWLOCKA, B. (2005). Inhibition of morphine tolerance by spinal melanocortin receptor blockade. Pain, 117, 401-411.
43. TERWILLIGER, R.Z., ORTIZ, J., GUITART, X. & NESTLER, E.J. (1994). Chronic morphine administration increases b-adrenergic kinase (BARK) levels in the rat locus coeruleus. J. Neurochem., 63, 1983-1986.
44. WILLIAMS, J.T., CHRISTIE, M.J. & MANZONI, O. (2001). Cellular and synaptic adaptations mediating opioid dependence. Physiol. Rev., 81, 299-343.
45. XIE, G.-X. & PALMER, P.P. (2005). RGS proteins: new players in the field of opioid signaling and tolerance mechanisms. Anesth. Analg., 100, 1034-1042.