PAIN
Volume 114, Issue 1 , Pages 81-92 , March 2005

Evidence for a long-term influence on morphie tolerance after previous morphine exposure: role of neuronal glucocorticoid receptors

Received 18 August 2004 ,Revised 13 October 2004 ,Accepted 22 November 2004.

References 

  1. Aley KO, Levine JD. Different mechanisms mediate development and expression of tolerance and dependence for peripheral μ-opioid antinociception in rat. J Neurosci. 1997;17:8018–8023
  2. Bailey CP, Couch D, Johnson E, Griffiths K, Kelly E, Henderson G. μ-Opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine. J Neurosci. 2003;23:10515–10520
  3. Ballantyne J, Mao J. Opioid therapy for chronic pain. N Engl J Med. 2003;349:1943–1953
  4. Bohn LM, Gainestdinov RR, Lin FT, Lefkowitz RJ, Caron MG. Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature. 2000;408:720–723
  5. Cameron SA, Dutia MB. Lesion-induced plasticity in rat vestibular nucleus neurons is dependent on glucocorticod receptor activation. J Physiol. 1999;518:151–158
  6. Capasso A, Di Giannuario A, Loizzo A, Pieretti S, Sorrentino L. Central interaction of dexamethasone and RU-38486 on morphine antinociception in mice. Life Sci. 1992;51:PL139–PL143
  7. Castonguay TW, Beaulieu S, Eskay RL, Barden N, Kamara K, Khozin S, et al. The effects of adrenalectomy and aldosterone replacement in trasgenic mice expressing antisense RNA to the type 2 glucocorticoid receptor. Physiol Behav. 2002;77:417–423
  8. Cho K, Little HJ. Effects of corticosterone on excitatory amino acid responses in dopamine-sensitive neurons in the ventral tegmental area. Neuroscience. 1999;88:837–845
  9. Cintra A, Molander C, Fuxe K. Colocalization of Fos- and glucocorticod receptor-immunoreactivities is present only in a very restricted population of dorsal horn neurons of the rat spinal cord after nociceptive stimulation. Brain Res. 1993;632:334–338
  10. Collingridge GL, Singer W. Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci. 1990;11:290–296
  11. Coussens CM, Kerr DS, Abraham WC. Glucoocrticoid receptor activation lowers the threshold for NMDA-receptor-dependent homosynaptic long-term depression in the hippocampus through activation of voltage-dependent calcium channels. J Neurophysiol. 1997;78:1–9
  12. De Nicola AF, Moses DF, Gonzalez S, Orti E. Adrenocorticoid action in the spinal cord: some unique molecular properties of glucocorticoid receptors. Cell Mol Neurobiol. 1989;9:179–192
  13. Deroche-Gamonet V, Sillaber I, Aouizerate B, Izawa R, Jaber M, Ghozlan S, et al. The glucocorticord receptor as a potential target to reduce cocaine abuse. J Neurosci. 2003;23:4785–4790
  14. Drouin J, Sun YL, Tremblay S, Lavender P, Schmidt TJ, de Lean A, et al. Homodimer formation is rate-limiting for high affinity DNA binding by glucocorticoid receptor. Mol Endocrinol. 1992;6:1299–1309
  15. Gartner H, Graul MC, Oesterreicher TJ, Finegold MJ, Henning S. Development of the fetal intestine in mice lacking the glucocorticoid receptor (GR). J Cell Physiol. 2002;194:80–87
  16. Gintzler AR, Chakrabarti S. Opioid tolerance and the emergence of new opioid receptro-coupled signaling. Mol Neurobiol. 2001;21:21–33
  17. Grisel JE, Watkins LR, Maier SF. Associative and non-associative mechanisms of morphine analgesic tolerance are neurochemically distinct in the rat spinal cord. Psychopharmacology (Berl). 1996;128:248–255
  18. He L, Fong J, von Zastrow M, Whistler JL. Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell. 2002;108:271–282
  19. Jolas T, Nestler EJ, Aghajanian GK. Chronic morphine increases GABA tone on serotonergic neurons of the dorsal raphe nucleus: association with an up-regulation of the cyclic AMP pathway. Neuroscience. 2000;95:433–443
  20. Kuwahara S, Arima H, Banno R, Sato I, Kondo N, Oiso Y. Regulation of vasopressin gene expression by cAMP and glucocorticoids in parvocellular neurons of the paraventricular nucleus in rat hypothalamic organotypic cultures. J Neurosci. 2003;23:10231–10237
  21. Madison DV, Malenka RC, Nicoll RA. Mechanisms underlying long-term potentiation of synaptic transmission. Annu Rev Neurosci. 1991;14:379–397
  22. Mao J. Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. Pain. 2002;100:213–217
  23. Mao J, Regelson W, Kalimi M. Molecular mechanisms of RU 486 action: a review. Mol Cell Biol. 1992;109:1–8
  24. Mao J, Price DD, Mayer DJ. Mechanisms of hyperalgesia and opiate tolerance: a current view of their possible interactions. Pain. 1995;62:259–274
  25. Mao J, Price DD, Mayer DJ. Experimental mononeuropathy reduces the antinociceptive effects of morphine: implications for common intracellular mechanisms involved in morphine tolerance and neuropathic pain. Pain. 1995;61:353–364
  26. Mao J, Price DD, Phillips LL, Lu J, Mayer DJ. Increases in protein kinase C gamma immunoreactivity in the spinal cord of rats associated with tolerance to the analgesic effects of morphine. Brain Res. 1995;677:257–267
  27. Mao J, Sung B, Ji RR, Lim G. Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci. 2002;22:8312–8323
  28. Marinelli M, Aouizerate B, Barrot M, Le Moal M, Piazza P. Dopamine-dependent responses to morphine depend on glucocorticoid receptors. Proc Natl Acad Sci USA. 1998;95:7742–7747
  29. Nair SM, Werkman TR, Craig J, Finnell R, Joels M, Eberwine JH. Corticosterone regulation of ion channel conductance and mRNA levels in individual hippocampal CA1 neurons. J Neurosci. 1998;18:2685–2696
  30. Neeck G, Renkawitz R, Eggert M. Molecular aspects of glucocorticoid hormone action in rheumatoid arthritis. Cytokines Cell Mol Ther. 2002;7:61–69
  31. Nestler EJ, Aghajanian GK. Molecular and cellular basis of addiction. Science. 1997;278:58–63
  32. Oitzl MS, Fluttert M, Sutanto W, de Kloet ER. Continuous blockade of brain glucocorticoid receptors facilitate spatial learning and memory in rats. Eur J Neurosci. 1998;10:3759–3766
  33. Olds JL, Anderson ML, McPhie DL, Ataten LD, Alkon DL. Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science. 1989;245:866–869
  34. Pieretti S, Capasso A, Di Giannuario A, Loizzo A, Sorrentino L. The interaction of peripherally and centrally administered dexamethasone and RU38486 on morphine analgesia in mice. Gen Pharmacol. 1991;22:929–933
  35. Quirarte GL, Roozendaal B, McGaugh JL. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdale. Proc Natl Acad Sci USA. 1997;94:14048–14053
  36. Refojo D, Liberman AC, Holsboer F, Arzt E. Transcription factor-mediated molecular mechanisms involved in the functional cross-talk between cytokines and glucocorticoids. Immunol Cell Biol. 2001;79:385–394
  37. Roosendaal B, Williams GL, McGaugh JL. Glucocorticoid receptor activation in the rat nucleus of the solitary tract facilitates memory consolidation: involvement of the basolateral amygdale. Eur J Neurosci. 1999;11:1317–1323
  38. Roosendaal B, Mcreynolds JJ, McGaugh JL. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci. 2003;24:1385–1392
  39. Schoffelmeer AN, Voorn P, Jonker AJ, Wardeh G, Nestby P, Vanderschuren LJ, et al. Morphine-induced increase in D-1 receptor regulated signal transduction in rat striatal neurons and its facilitation by glucocorticoid receptor activation: possible role in behavioral sensitization. Neurochem Res. 1996;21:1417–1423
  40. Sim-Selley LJ, Selley DE, Vogt LJ, Childers SR, Martin TJ. Chronic heroin self-administration desensitizes mu opioid receptor-activated G-proteins in specific regions of rat brain. J Neurosci. 2000;20:4555–4562
  41. Smith GD, Seckl JR, Scheward WJ, Bennie JG, Carroll SM, Dick H, et al. Effect of adrenalectomy and dexamethasone on neuropeptide content of dorsal root ganglia in the rat. Brain Res. 1991;564:27–30
  42. Spanagel B, Stohr T, Barden N, Holsboer F. Morphine-induced locomotor and neurochemical stimulation is enhanced in transgenic mice with impaired glucocorticod receptor function. J Neuroendocrinol. 1996;8:93–97
  43. St-Hilaire M, Tremblay PO, Levesque D, Barden N, Rouillard C. Effects of cocaine on c-Fos and NGFI-B mRNA expression in transgenic mice underexpressing glucocorticoid receptors. Neuropsychopharmacology. 2003;28:478–489
  44. Takahashi T, Sugimachi K, Kaneto H. Role of adrenal glucocorticoids in the blockade of the development of analgesic tolerance to morphine by footshock stress exposure in mice. Jpn J Pharmacol. 1989;51:329–336
  45. Takahashi T, Kimoto T, Tanabe N, Hattori TA, Yasumatsu N, Kawata T. Corticosterone acutely prolonged N-methyl-d-aspartate receptor mediated Ca2+ elevation in cultured rat hippocampal neurons. J Neurochem. 2002;83:1441–1451
  46. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet. 1999;23:99–103
  47. Trujillo KA, Akil H. Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science. 1991;251:85–87
  48. Xu NJ, Bao L, Fan HP, Bao GB, Pu L, Lu YJ, et al. Morphine withdrawal increases glutamate uptake and surface expression of glutamate transporter GLT-1 at hippocampal synapses. J Neurosci. 2003;23:4775–4784
  49. Yaksh TL, Rudy TA. Chronic catheterization of the spinal subarachnoid space. Physiol Behav. 1976;17:1031–1036
  50. Zeitz KP, Malmberg AB, Gilbert H, Basbaum AI. Reduced development of tolerance to the analgesic effects of morphine and clonidine in PKCgamma mutant mice. Pain. 2002;94:245–253

PII: S0304-3959(04)00565-2

doi: 10.1016/j.pain.2004.11.019

PAIN
Volume 114, Issue 1 , Pages 81-92 , March 2005