Role of protein kinase C and μ-opioid receptor (MOPr) desensitization in tolerance to morphine in rat locus coeruleus neurons

European Journal of Neuroscience

Volumn 29, Issue 2, 2009, Pages 307-318

  Bailey, C P ^a   Llorente, J ^b   Gabra, B H ^c   Smith, F L ^a,d   Dewey, W L ^c   Kelly, E ^b   Henderson, G ^b  

^a HARDING UNIVERSITY   (United States)

^b University of Bath   (United Kingdom)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Desensitization; Morphine; Opiates; Tolerance

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; MORPHINE; OPIATE RECEPTOR; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DESENSITIZATION; IN VITRO STUDY; LOCUS CERULEUS; MALE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT;

ANIMALS; COMPUTER SIMULATION; DRUG TOLERANCE; LOCUS COERULEUS; MALE; MORPHINE; NARCOTICS; NEURONS; ORGAN CULTURE TECHNIQUES; PROTEIN KINASE C; RATS; RATS, WISTAR; RECEPTORS, OPIOID, MU;

EID: 58449100187     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06573.x     Document Type: Article

References (51)

1. Alvarez, V.A., Arttamangkul, S., Dang, V., Salem, A., Whistler, J.L., von Zastrow, M., Grandy, D.K. Williams, J.T. (2002) Mu-Opioid receptors: ligand-dependent activation of potassium conductance, desensitization, and internalization. J. Neurosci., 22, 5769 5776.
2. Bailey, C.P., Couch, D., Johnson, E., Griffiths, K., Kelly, E. Henderson, G. (2003) Mu-opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine. J. Neurosci., 23, 10515 10520.
3. Bailey, C.P., Kelly, E. Henderson, G. (2004) Protein kinase C activation enhances morphine-induced rapid desensitization of mu-opioid receptors in mature rat locus ceruleus neurons. Mol. Pharmacol., 66, 1592 1598.
4. Bailey, C.P., Smith, F.L., Kelly, E., Dewey, W.L. Henderson, G. (2006) How important is protein kinase C in mu-opioid receptor desensitization and morphine tolerance Trends Pharmacol. Sci., 27, 558 565.
5. Black, J.W., Leff, P., Shankley, N.P. Wood, J. (1985) An operational model of pharmacological agonism: the effect of E/[A] curve shape on agonist dissociation constant estimation. Br. J. Pharmacol., 84, 561 571.
6. Bohn, L.M., Lefkowitz, R.J. Caron, M.G. (2002) Differential mechanisms of morphine antinociceptive tolerance revealed in (beta)arrestin-2 knock-out mice. J. Neurosci., 22, 10494 11050.
7. Chen, L., Wright, L.R., Chen, C.H., Oliver, S.F., Wender, P.A. Mochly-Rosen, D. (2001) Molecular transporters for peptides: delivery of a cardioprotective epsilonPKC agonist peptide into cells and intact ischemic heart using a transport system, R(7). Chem. Biol., 8, 1123 1129.
8. 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.
9. Connor, M., Osborne, P.B. Christie, M.J. (2004) Mu-opioid receptor desensitization: is morphine different Br. J. Pharmacol., 143, 685 696.
10. Dang, V.C. Williams, J.T. (2005) Morphine-induced mu-opioid receptor desensitization. Mol. Pharmacol., 68, 1127 1132.
11. Dourish, C.T., O'Neill, M.F., Coughlan, J., Kitchener, S.J., Hawley, D. Iversen, S.D. (1990) The selective CCK-B receptor antagonist L-365,260 enhances morphine analgesia and prevents morphine tolerance in the rat. Eur. J. Pharmacol., 176, 35 44.
12. Finn, A.K. Whistler, J.L. (2001) Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron, 32, 829 839.
13. Gabra, B.H., Bailey, C.P., Kelly, E., Sanders, A.V., Henderson, G., Smith, F.L. Dewey, W.L. (2007) Evidence for an important role of protein phosphatases in the mechanism of morphine tolerance. Brain Res., 1159, 86 93.
14. Gold, S.J., Han, M.H., Herman, A.E., Ni, Y.G., Pudiak, C.M., Aghajanian, G.K., Liu, R.J., Potes, B.W., Mumby, S.M. Nestler, E.J. (2003) Regulation of RGS proteins by chronic morphine in rat locus coeruleus. Eur. J. Neurosci., 17, 971 980.
15. Granados-Soto, V., Kalcheva, I., Hua, Y., Newton, A. Yaksh, T.L. (2000) Spinal PKC activity and expression: role in tolerance produced by continuous spinal morphine infusion. Pain, 85, 395 404.
16. Haberstock-Debic, H., Kim, K.A., Yu, Y.J. von Zastrow, M. (2005) Morphine promotes rapid, arrestin-dependent endocytosis of mu-opioid receptors in striatal neurons. J. Neurosci., 25, 7847 7857.
17. Harris, G.C. Williams, J.T. (1991) Transient homologous mu-opioid receptor desensitization in rat locus coeruleus neurons. J. Neurosci., 11, 2574 2581.
18. Hua, X.Y., Moore, A., Malkmus, S., Murray, S.F., Dean, N., Yaksh, T.L. Butler, M. (2002) Inhibition of spinal protein kinase Calpha expression by an antisense oligonucleotide attenuates morphine infusion-induced tolerance. Neuroscience, 113, 99 107.
19. Ingram, S.L., Macey, T.A., Fossum, E.N. Morgan, M.M. (2008) Tolerance to repeated morphine administration is associated with increase potency of opioid agonists. Neuropsychopharm., 33, 2494 2504.
20. Inoue, M. Ueda, H. (2000) Protein kinase C-mediated acute tolerance to peripheral mu-opioid analgesia in the bradykinin-nociception test in mice. J. Pharmacol. Exp. Ther., 293, 662 669.
21. Johnson, J.A., Gray, M.O., Chen, C. Mochly-Rosen, D. (1996) A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J. Biol. Chem., 271, 24962 24966.
22. Johnson, E.A., Oldfield, S., Braksator, E., Gonzalez-Cuello, A., Couch, D., Hall, K.J., Mundell, S.J., Bailey, C.P., Kelly, E. Henderson, G. (2006) Agonist-selective mechanisms of mu-opioid receptor desensitisation in human embryonic kidney 293 cells. Mol. Pharmacol., 70, 676 685.
23. Kelly, E., Bailey, C.P. Henderson, G. (2008) Agonist-selective mechanisms of GPCR desensitisation. Br. J. Pharmacol., 153 (Suppl. 1 S379 S388.
24. Lohse, M.J., Benovic, J.L., Caron, M.G. Lefkowitz, R.J. (1990) Multiple pathways of rapid beta 2-adrenergic receptor desensitisation. Delineation with specific inhibitors. J. Biol. Chem., 265, 3202 3211.
25. Matthes, H.W., Maldonado, R., Simonin, F., Valverde, O., Slowe, S., Kitchen, I., Befort, K., Dierich, A., Le Meur, M., Dolle, P., Tzavara, E., Hanoune, J., Roques, B.P. Kieffer, B.L. (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature, 383, 819 823.
26. Mitchell, J.M., Basbaum, A.I. Fields, H.L. (2000) A locus and mechanism of action for associative morphine tolerance. Nat. Neurosci., 3, 47 53.
27. Newton, P.M., Kim, J.A., McGeehan, A.J., Paredes, J.P., Chu, K., Wallace, M.J., Roberts, A.J., Hodge, C.W. Messing, R.O. (2007) Increased response to morphine in mice lacking protein kinase C epsilon. Genes Brain Behav., 6, 329 338.
28. North, R.A. Williams, J.T. (1985) On the potassium conductance increased by opioids in rat locus coeruleus neurones. J. Physiol., 364, 265 280.
29. Osborne, P.B. Williams, J.T. (1995) Characterisation of acute homologous desensitisation of mu-opioid receptor-induced currents in locus coeruleus neurones. Br. J. Pharmacol., 115, 925 932.
30. Patrick, G.A., Dewey, W.L., Huger, F.P., Daves, E.D. Harris, L.S. (1978) Disposition of morphine in chronically infused rats: relationship to antinociception and tolerance. J. Pharmacol. Exp. Ther., 205, 556 562.
31. Popik, P., Kozela, E. Pilc, A. (2000) Selective agonist of group II glutamate metabotropic receptors, LY354740, inhibits tolerance to analgesic effects of morphine in mice. Br. J. Pharmacol., 130, 1425 1431.
32. Powell, K.J., Ma, W., Sutak, M., Doods, H., Quirion, R. Jhamandas, K. (2000) Blockade and reversal of spinal morphine tolerance by peptide and non-peptide calcitonin gene-related peptide receptor antagonists. Br. J. Pharmacol., 131, 875 884.
33. Powell, K.J., Quirion, R. Jhamandas, K. (2003) Inhibition of neurokinin-1-substance P receptor and prostanoid activity prevents and reverses the development of morphine tolerance in vivo and the morphine-induced increase in CGRP expression in cultured dorsal root. Eur. J. Neurosci., 18, 1572 1583.
34. Pu, L., Bao, G.B., Ma, L. Pei, G. (1999) Acute desensitization of nociceptin/orphanin FQ inhibition of voltage-gated calcium channels in freshly dissociated hippocampal neurons. Eur. J. Neurosci., 11, 3610 3616.
35. Roerig, S.C., Fujimoto, J.M. Lange, D.G. (1987) Development of tolerance to respiratory depression in morphine- and etorphine-pellet-implanted mice. Brain Res., 400, 278 284.
36. Romberg, R., Sarton, E., Teppema, L., Matthes, H.W., Kieffer, B.L. Dahan, A. (2003) Comparison of morphine-6-glucuronide and morphine on respiratory depressant and antinociceptive responses in wild type and mu-opioid receptor deficient mice. Br. J. Anaesth., 91, 862 870.
37. Ron, D., Luo, J. Mochly-Rosen, D. (1995) C2 Region-derived peptides inhibit translocation and function of β protein kinase C in vivo. J. Biol. Chem., 270, 24180 24187.
38. Santamarta, M.T., Ulibarri, I. Pineda, J. (2005) Inhibition of neuronal nitric oxide synthase attenuates the development of morphine tolerance in rats. Synapse, 57, 38 46.
39. Shippenberg, T.S., Emmett-Oglesby, M.E. Herz, A. (1989) Morphine-induced place conditioning is not confounded by drug-induced alterations in locomotor activity. Pharmacol. Biochem. Behav., 32, 129 132.
40. 35S]GTPγS autoradiography in rat brain. J. Neurosci., 16, 2684 2692.
41. Smith, F.L., Lohmann, A.B. Dewey, W.L. (1999) Involvement of phospholipid signal transduction pathways in morphine tolerance in mice. Br. J. Pharmacol., 128, 220 226.
42. Smith, F.L., Javed, R.R., Elzey, M.J. Dewey, W.L. (2003) The expression of a high level of morphine antinociceptive tolerance in mice involves both PKC and PKA. Brain Res., 985, 78 88.
43. Smith, F.L., Gabra, B.H., Smith, P.A., Redwood, M.C. Dewey, W.L. (2007) Determination of the role of conventional, novel and atypical PKC isoforms in the expression of morphine tolerance in mice. Pain, 127, 129 139.
44. Stebbins, E.G. Mochly-Rosen, D. (2001) Binding specificity for RACK1 resides in the V5 region of βII protein kinase C. J. Biol. Chem., 276, 29644 29650.
45. Terman, G.W., Jin, W., Cheong, Y.P., Lowe, J., Caron, M.G., Lefkowitz, R.J. Chavkin, C. (2004) G-protein receptor kinase 3 (GRK3) influences opioid analgesic tolerance but not opioid withdrawal. Br. J. Pharmacol., 141, 55 64.
46. Terwilliger, R.Z., Ortiz, J., Guitart, X. Nestler, E.J. (1994) Chronic morphine administration increases beta-adrenergic receptors kinase (beta ARK) levels in the rat locus coeruleus. J. Neurochem., 63, 1983 1986.
47. Tortorici, V., Nogueira, L., Salas, R. Vanegas, H. (2003) Involvement of local cholecystokinin in the tolerance induced by morphine microinjections into the periaqueductal gray of rats. Pain, 102, 9 16.
48. Virk, M.S. Williams, J.T. (2008) Agonist-specific regulation of μ-opioid receptor desensitization and recovery from desensitization. Mol. Pharmacol., 73, 1301 1308.
49. Watkins, L.R., Kinscheck, I.B. Mayer, D.J. (1984) Potentiation of opiate analgesia and apparent reversal of morphine tolerance by proglumide. Science, 224, 395 396.
50. Way, K.J., Chou, E. King, G.L. (2000) Identification of PKC-isoform-specific biological actions using pharmacological approaches. Trends Pharmacol. Sci., 21, 181 187.
51. Zeitz, K.P., Malmberg, A.B., Gilbert, H. Basbaum, A.I. (2001) Reduced development of tolerance to the analgesic effects of morphine and clonidine in PKC gamma mutant mice. Pain, 102, 245 253.