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The Scientific World Journal
Volume 2012, Article ID 940613, 9 pages
http://dx.doi.org/10.1100/2012/940613
Review Article

An Emerging New Paradigm in Opioid Withdrawal: A Critical Role for Glia-Neuron Signaling in the Periaqueductal Gray

1Department of Neurology, University of Michigan Medical School, Ann Arbor, MI 48109, USA
2Department of Anesthesiology, University of Miami Miller School of Medicine, Miami, FL 33136, USA
3Department of Anesthesiology, State Key Laboratory of Oncology on Southern China, Cancer Center, Sun Yat-Sen University, Guangzhou 510060, China

Received 21 May 2012; Accepted 6 June 2012

Academic Editors: W. Ma and E. J. Thompson

Copyright © 2012 Handong Ouyang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. F. Chu, D. Y. Liang, X. Li et al., “From mouse to man: the 5-HT3 receptor modulates physical dependence on opioid narcotics,” Pharmacogenetics and Genomics, vol. 19, no. 3, pp. 193–205, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. G. F. Koob and M. Le Moal, “Drug abuse: Hedonic homeostatic dysregulation,” Science, vol. 278, no. 5335, pp. 52–58, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Cami and M. Farre, “Drug addiction,” The New England Journal of Medicine, vol. 349, pp. 975–986, 2003. View at Publisher · View at Google Scholar
  4. A. Kvist, P. Fagergren, J. Whittard et al., “Dysregulated postsynaptic density and endocytic zone in the amygdala of human heroin and cocaine abusers,” Biological Psychiatry, vol. 69, no. 3, pp. 245–252, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. S. L. Ingram, C. W. Vaughan, E. E. Bagley, M. Connor, and M. J. Christie, “Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway,” Journal of Neuroscience, vol. 18, no. 24, pp. 10269–10276, 1998. View at Google Scholar · View at Scopus
  6. S. Hao, S. Liu, X. Zheng et al., “The role of TNFα in the periaqueductal gray during naloxone-precipitated morphine withdrawal in rats,” Neuropsychopharmacology, vol. 36, no. 3, pp. 664–676, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Cushman and V. P. Dole, “Detoxification of rehabilitated methadone maintained patients,” Journal of the American Medical Association, vol. 226, no. 7, pp. 747–752, 1973. View at Publisher · View at Google Scholar · View at Scopus
  8. M. M. Morgan and M. J. Christie, “Analysis of opioid efficacy, tolerance, addiction and dependence from cell culture to human,” British Journal of Pharmacology, vol. 164, pp. 1322–1334, 2011. View at Publisher · View at Google Scholar
  9. K. C. Kirby, M. L. Stitzer, and S. J. Heishman, “Acute opioid physical dependence in humans: effect of varying the morphine-naloxone interval II,” Journal of Pharmacology and Experimental Therapeutics, vol. 255, no. 2, pp. 730–737, 1990. View at Google Scholar · View at Scopus
  10. K. L. Preston, G. E. Bigelow, and I. A. Liebson, “Effects of sublingually given naloxone in opioid-dependent human volunteers,” Drug and Alcohol Dependence, vol. 25, no. 1, pp. 27–34, 1990. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Laschka, Teschemacher Hj., P. Mehraein, and A. Herz, “Sites of action of morphine involved in the development of physical dependence in rats. II. Morphine withdrawal precipitated by application of morphine antagonists into restricted parts of the ventricular system and by microinjection into various brain areas,” Psychopharmacologia, vol. 46, no. 2, pp. 141–147, 1976. View at Google Scholar · View at Scopus
  12. G. F. Koob, R. Maldonado, and L. Stinus, “Neural substrates of opiate withdrawal,” Trends in Neurosciences, vol. 15, no. 5, pp. 186–191, 1992. View at Publisher · View at Google Scholar · View at Scopus
  13. A. A. McPhie and G. A. Barr, “Regional Fos expression induced by morphine withdrawal in the 7-day-old rat,” Developmental Psychobiology, vol. 51, no. 7, pp. 544–552, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. K. A. Keay and R. Bandler, “Periaqueductal Gray,” in The Rat Nervous System, G. Paxinos, Ed., pp. 243–257, Elsevier Academic Press, New York, NY, USA, 3rd edition, 2004. View at Google Scholar
  15. N. S. Floyd, K. A. Keay, and R. Bandler, “A calbindin immunoreactive 'deep pain' recipient thalamic nucleus in the rat,” NeuroReport, vol. 7, no. 2, pp. 622–626, 1996. View at Google Scholar · View at Scopus
  16. K. E. Krout and A. D. Loewy, “Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat,” The Journal of Comparative Neurology, vol. 424, pp. 111–141, 2000. View at Publisher · View at Google Scholar
  17. R. Bandler and M. T. Shipley, “Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?” Trends in Neurosciences, vol. 17, no. 9, pp. 379–389, 1994. View at Publisher · View at Google Scholar · View at Scopus
  18. C. W. Vaughan and M. J. Christie, “Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductalgrey in vitro,” Journal of Physiology, vol. 498, no. 2, pp. 463–472, 1997. View at Google Scholar · View at Scopus
  19. R. Maldonado, L. Stinus, L. H. Gold, and G. F. Koob, “Role of different brain structures in the expression of the physical morphine withdrawal syndrome,” Journal of Pharmacology and Experimental Therapeutics, vol. 261, no. 2, pp. 669–677, 1992. View at Google Scholar · View at Scopus
  20. M. A. Bozarth, “Physical dependence produced by central morphine infusions: an anatomical mapping study,” Neuroscience and Biobehavioral Reviews, vol. 18, no. 3, pp. 373–383, 1994. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Wei and H. Loh, “Physical dependence on opiate like peptides,” Science, vol. 193, no. 4259, pp. 1262–1263, 1976. View at Google Scholar · View at Scopus
  22. R. L. Stornetta, F. E. Norton, and P. G. Guyenet, “Autonomic areas of rat brain exhibit increased Fos-like immunoreactivity during opiate withdrawal in rats,” Brain Research, vol. 624, no. 1-2, pp. 19–28, 1993. View at Google Scholar · View at Scopus
  23. B. Chieng, K. A. Keay, and M. J. Christie, “Increased fos-like immunoreactivity in the periaqueductal gray of anaesthetised rats during opiate withdrawal,” Neuroscience Letters, vol. 183, no. 1-2, pp. 79–82, 1995. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Couceyro and J. Douglass, “Precipitated morphine withdrawal stimulates multiple activator protein-1 signaling pathways in rat brain,” Molecular Pharmacology, vol. 47, no. 1, pp. 29–39, 1995. View at Google Scholar · View at Scopus
  25. B. Chieng and M. J. Christie, “Local opioid withdrawal in rat single periaqueductal gray neurons in vitro,” Journal of Neuroscience, vol. 16, no. 22, pp. 7128–7136, 1996. View at Google Scholar · View at Scopus
  26. Y. Fukunaga and S. Kishioka, “Enkephalinergic neurons in the periaqueductal gray and morphine withdrawal,” Japanese Journal of Pharmacology, vol. 82, no. 3, pp. 175–180, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. J. L. Sonnenberg, F. J. Rauscher III, J. I. Morgan, and T. Curran, “Regulation of proenkephalin by Fos and Jun,” Science, vol. 246, no. 4937, pp. 1622–1625, 1989. View at Google Scholar · View at Scopus
  28. Y. Fukunaga, S. Nishida, N. Inoue, M. Miyamoto, S. Kishioka, and H. Yamamoto, “Time course of morphine withdrawal and preproenkephalin gene expression in the periaqueductal gray of rats,” Molecular Brain Research, vol. 55, no. 2, pp. 221–231, 1998. View at Publisher · View at Google Scholar · View at Scopus
  29. P. G. Haydon, J. Blendy, S. J. Moss, and F. Rob Jackson, “Astrocytic control of synaptic transmission and plasticity: a target for drugs of abuse?” Neuropharmacology, vol. 56, supplement 1, pp. 83–90, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Guo, R. M. Pascual, S. Wang et al., “Cytokines regulate β-2-adrenergic receptor responsiveness in airway smooth muscle via multiple PKA- and EP2 receptor-dependent mechanisms,” Biochemistry, vol. 44, no. 42, pp. 13771–13782, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. S. A. Shore, J. Laporte, I. P. Hall, E. Hardy, and R. A. Panettieri, “Effect of IL-1β on responses of cultured human airway smooth muscle cells to bronchodilator agonists,” American Journal of Respiratory Cell and Molecular Biology, vol. 16, no. 6, pp. 702–712, 1997. View at Google Scholar · View at Scopus
  32. R. Z. Terwilliger, D. Beitner-Johnson, K. A. Sevarino, S. M. Crain, and E. J. Nestler, “A general role for adaptations in G-proteins and the cyclic AMP system in mediating the chronic actions of morphine and cocaine on neuronal function,” Brain Research, vol. 548, no. 1-2, pp. 100–110, 1991. View at Google Scholar · View at Scopus
  33. J. P. Fedynyshyn and N. M. Lee, “μ type opioid receptors in rat periaqueductal gray-enriched P2 membrane are coupled to G-protein-mediated inhibition of adenylyl cyclase,” FEBS Letters, vol. 253, no. 1-2, pp. 23–27, 1989. View at Publisher · View at Google Scholar · View at Scopus
  34. E. E. Bagley, M. B. Gerke, C. W. Vaughan, S. P. Hack, and M. J. Christie, “GABA transporter currents activated by protein kinase A excite midbrain neurons during opioid withdrawal,” Neuron, vol. 45, no. 3, pp. 433–445, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. S. B. Lane-Ladd, J. Pineda, V. A. Boundy et al., “CREB (cAMP response element-binding protein) in the locus coeruleus: biochemical, physiological, and behavioral evidence for a role in opiate dependence,” Journal of Neuroscience, vol. 17, no. 20, pp. 7890–7901, 1997. View at Google Scholar · View at Scopus
  36. L. J. Punch, D. W. Self, E. J. Nestler, and J. R. Taylor, “Opposite modulation of opiate withdrawal behaviors on microinfusion of a protein kinase A inhibitor versus activator into the locus coeruleus or periaqueductal gray,” Journal of Neuroscience, vol. 17, no. 21, pp. 8520–8527, 1997. View at Google Scholar · View at Scopus
  37. R. Maldonado, O. Valverde, C. Garbay, and B. P. Roques, “Protein kinases in the locus coeruleus and periaqueductal gray matter are involved in the expression of opiate withdrawal,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 352, no. 5, pp. 565–575, 1995. View at Google Scholar · View at Scopus
  38. T. Jolas and G. K. Aghajanian, “Opioids suppress spontaneous and NMDA-induced inhibitory postsynaptic currents in the dorsal raphe nucleus of the rat in vitro,” Brain Research, vol. 755, no. 2, pp. 229–245, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Hacker, N. P. Pedersen, B. C. H. Chieng, K. A. Keay, and M. J. Christie, “Enhanced Fos expression in glutamic acid decarboxylase immunoreactive neurons of the mouse periaqueductal grey during opioid withdrawal,” Neuroscience, vol. 137, no. 4, pp. 1389–1396, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. J. T. Williams, M. J. Christie, and O. Manzoni, “Cellular and synaptic adaptations mediating opioid dependence,” Physiological Reviews, vol. 81, no. 1, pp. 299–343, 2001. View at Google Scholar · View at Scopus
  41. S. P. Hack, C. W. Vaughan, and M. J. Christie, “Modulation of GABA release during morphine withdrawal in midbrain neurons in vitro,” Neuropharmacology, vol. 45, no. 5, pp. 575–584, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. E. E. Bagley, J. Hacker, V. I. Chefer et al., “Drug-induced GABA transporter currents enhance GABA release to induce opioid withdrawal behaviors,” Nature Neuroscience, vol. 14, no. 12, pp. 1548–1554, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Stern, “Glia. Glee for glia. Introduction,” Science, vol. 330, no. 6005, p. 773, 2010. View at Google Scholar · View at Scopus
  44. D. B. Tower and O. M. Young, “The activities of butyrylcholinesterase and carbonic anhydrase, the rate of anaerobic glycolysis, and the question of a constant density of glial cells in cerebral cortices of various mammalian species from mouse to whale,” Journal of Neurochemistry, vol. 20, pp. 269–278, 1973. View at Google Scholar · View at Scopus
  45. D. Rossi and A. Volterra, “Astrocytic dysfunction: insights on the role in neurodegeneration,” Brain Research Bulletin, vol. 80, no. 4-5, pp. 224–232, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. M. M. Halassa, T. Fellin, and P. G. Haydon, “The tripartite synapse: roles for gliotransmission in health and disease,” Trends in Molecular Medicine, vol. 13, no. 2, pp. 54–63, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. J. S. Bains and S. H. R. Oliet, “Glia: they make your memories stick!,” Trends in Neurosciences, vol. 30, no. 8, pp. 417–424, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. M. R. Hutchinson, S. T. Bland, K. W. Johnson, K. C. Rice, S. F. Maier, and L. R. Watkins, “Opioid-induced glial activation: mechanisms of activation and implications for opioid analgesia, dependence, and reward,” TheScientificWorldJOURNAL, vol. 7, no. 2, pp. 98–111, 2007. View at Google Scholar · View at Scopus
  49. A. Ledeboer, M. R. Hutchinson, L. R. Watkins, and K. W. Johnson, “Ibudilast (AV-411): a new class therapeutic candidate for neuropathic pain and opioid withdrawal syndromes,” Expert Opinion on Investigational Drugs, vol. 16, no. 7, pp. 935–950, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. M. R. Hutchinson, S. S. Lewis, B. D. Coats et al., “Reduction of opioid withdrawal and potentiation of acute opioid analgesia by systemic AV411 (ibudilast),” Brain, Behavior, and Immunity, vol. 23, no. 2, pp. 240–250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Song and Z. Q. Zhao, “The involvement of glial cells in the development of morphine tolerance,” Neuroscience Research, vol. 39, no. 3, pp. 281–286, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. V. Raghavendra, M. D. Rutkowski, and J. A. Deleo, “The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats,” Journal of Neuroscience, vol. 22, no. 22, pp. 9980–9989, 2002. View at Google Scholar · View at Scopus
  53. I. N. Johnston, E. D. Milligan, J. Wieseler-Frank et al., “A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine,” Journal of Neuroscience, vol. 24, no. 33, pp. 7353–7365, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. V. Raghavendra, F. Y. Tanga, and J. A. DeLeo, “Attenuation of morphine tolerance, withdrawal-induced hyperalgesia, and associated spinal inflammatory immune responses by propentofylline in rats,” Neuropsychopharmacology, vol. 29, no. 2, pp. 327–334, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. S. S. Lewis, M. R. Hutchinson, B. D. Coats et al., “AV411, a blood brain barrier permeable glial activation inhibitor, reduces morphine withdrawal behaviors in rats,” Proceedings of the Society for Neuroscience, pp. 765–762, 2006. View at Google Scholar
  56. M. R. Hutchinson, S. S. Lewis, B. D. Coats et al., “Possible involvement of toll-like receptor 4/myeloid differentiation factor-2 activity of opioid inactive isomers causes spinal proinflammation and related behavioral consequences,” Neuroscience, vol. 167, no. 3, pp. 880–893, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. M. R. Hutchinson, L. C. Loram, Y. Zhang et al., “Evidence that tricyclic small molecules may possess toll-like receptor and myeloid differentiation protein 2 activity,” Neuroscience, vol. 168, no. 2, pp. 551–563, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. X. Wang, L. C. Loram, K. Ramos et al., “Morphine activates neuroinflammation in a manner parallel to endotoxin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 16, pp. 6325–6330, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. O. Saito, C. I. Svensson, M. W. Buczynski et al., “Spinal glial TLR4-mediated nociception and production of prostaglandin E2 and TNF,” British Journal of Pharmacology, vol. 160, no. 7, pp. 1754–1764, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. I. Bettoni, F. Comelli, C. Rossini et al., “Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice,” GLIA, vol. 56, no. 12, pp. 1312–1319, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Volterra and J. Meldolesi, “Astrocytes, from brain glue to communication elements: the revolution continues,” Nature Reviews Neuroscience, vol. 6, no. 8, pp. 626–640, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. M. R. Hutchinson, Y. Zhang, M. Shridhar et al., “Evidence that opioids may have toll-like receptor 4 and MD-2 effects,” Brain, Behavior, and Immunity, vol. 24, no. 1, pp. 83–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Pickering, D. Cumiskey, and J. J. O'Connor, “Actions of TNF-α on glutamatergic synaptic transmission in the central nervous system,” Experimental Physiology, vol. 90, no. 5, pp. 663–670, 2005. View at Publisher · View at Google Scholar · View at Scopus
  64. L. M. Garcia-Segura, B. Lorenz, and L. L. DonCarlos, “The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output,” Reproduction, vol. 135, no. 4, pp. 419–429, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. E. A. Bushong, M. E. Martone, Y. Z. Jones, and M. H. Ellisman, “Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains,” Journal of Neuroscience, vol. 22, no. 1, pp. 183–192, 2002. View at Google Scholar · View at Scopus
  66. M. M. Halassa, T. Fellin, H. Takano, J. H. Dong, and P. G. Haydon, “Synaptic islands defined by the territory of a single astrocyte,” Journal of Neuroscience, vol. 27, no. 24, pp. 6473–6477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. A. Araque, V. Parpura, R. P. Sanzgiri, and P. G. Haydon, “Tripartite synapses: Glia, the unacknowledged partner,” Trends in Neurosciences, vol. 22, no. 5, pp. 208–215, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. M. M. Halassa and P. G. Haydon, “Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior,” Annual Review of Physiology, vol. 72, pp. 335–355, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. Q. S. Liu, Q. Xu, G. Arcuino, J. Kang, and M. Nedergaard, “Astrocyte-mediated activation of neuronal kainate receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 3172–3177, 2004. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Narita, M. Suzuki, N. Kuzumaki, M. Miyatake, and T. Suzuki, “Implication of activated astrocytes in the development of drug dependence: differences between methamphetamine and morphine,” Annals of the New York Academy of Sciences, vol. 1141, pp. 96–104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. L. R. Watkins, M. R. Hutchinson, E. D. Milligan, and S. F. Maier, “'Listening' and 'talking' to neurons: implications of immune activation for pain control and increasing the efficacy of opioids,” Brain Research Reviews, vol. 56, no. 1, pp. 148–169, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. R. X. Zhang, A. Li, B. Liu et al., “IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats,” Pain, vol. 135, no. 3, pp. 232–239, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. T. Nakagawa and M. Satoh, “Involvement of glial glutamate transporters in morphine dependence,” Annals of the New York Academy of Sciences, vol. 1025, pp. 383–388, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Srinivasan, J. H. Yen, D. J. Joseph, and W. Friedman, “Cell type-specific interleukin-1β signaling in the CNS,” Journal of Neuroscience, vol. 24, no. 29, pp. 6482–6488, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. W. Guo, H. Wang, M. Watanabe et al., “Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain,” Journal of Neuroscience, vol. 27, no. 22, pp. 6006–6018, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. A. De, J. M. Krueger, and S. M. Simasko, “Tumor necrosis factor α increases cytosolic calcium responses to AMPA and KCl in primary cultures of rat hippocampal neurons,” Brain Research, vol. 981, no. 1-2, pp. 133–142, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. X. Jin and R. W. Gereau, “Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-α,” Journal of Neuroscience, vol. 26, no. 1, pp. 246–255, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. F. Grassi, A. M. Mileo, L. Monaco, A. Punturieri, A. Santoni, and F. Eusebi, “TNF-α increases the frequency of spontaneous miniature synaptic currents in cultured rat hippocampal neurons,” Brain Research, vol. 659, no. 1-2, pp. 226–230, 1994. View at Google Scholar · View at Scopus
  79. L. Zhang, T. Berta, Z. Z. Xu, T. Liu, J. Y. Park, and R. R. Ji, “TNF-alpha contributes to spinal cord synaptic plasticity and inflammatory pain: distinct role of TNF receptor subtypes 1 and 2,” Pain, vol. 152, no. 2, pp. 419–427, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. D. Stellwagen, E. C. Beattie, J. Y. Seo, and R. C. Malenka, “Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-α,” Journal of Neuroscience, vol. 25, no. 12, pp. 3219–3228, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. J. G. Liu and K. J. S. Anand, “Protein kinases modulate the cellular adaptations associated with opioid tolerance and dependence,” Brain Research Reviews, vol. 38, no. 1-2, pp. 1–19, 2001. View at Publisher · View at Google Scholar · View at Scopus
  82. X. Ren, Y. Noda, T. Mamiya, T. Nagai, and T. Nabeshima, “A neuroactive steroid, dehydroepiandrosterone sulfate, prevents the development of morphine dependence and tolerance via c-fos expression linked to the extracellular signal-regulated protein kinase,” Behavioural Brain Research, vol. 152, no. 2, pp. 243–250, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. J. L. Cao, J. H. He, H. L. Ding, and Y. M. Zeng, “Activation of the spinal ERK signaling pathway contributes naloxone-precipitated withdrawal in morphine-dependent rats,” Pain, vol. 118, no. 3, pp. 336–349, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. D. L. Muller and E. M. Unterwald, “In vivo regulation of extracellular signal-regulated protein kinase (ERK) and protein kinase B (Akt) phosphorylation by acute and chronic morphine,” Journal of Pharmacology and Experimental Therapeutics, vol. 310, no. 2, pp. 774–782, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. C. Núñez, M. T. Castells, M. L. Laorden, and M. V. Milanés, “Regulation of extracellular signal-regulated kinases (ERKs) by naloxone-induced morphine withdrawal in the brain stress system,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 378, no. 4, pp. 407–420, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. E. J. Nestler, “Molecular neurobiology of addiction,” American Journal on Addictions, vol. 10, no. 3, pp. 201–217, 2001. View at Publisher · View at Google Scholar · View at Scopus
  87. R. Maldonado, J. A. Blendy, E. Tzavara et al., “Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB,” Science, vol. 273, no. 5275, pp. 657–659, 1996. View at Google Scholar · View at Scopus
  88. K. L. Widnell, D. S. Russell, and E. J. Nestler, “Regulation of expression of cAMP response element-binding protein in the locus coeruleus in vivo and in a locus coeruleus-like cell line in vitro,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 23, pp. 10947–10951, 1994. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Z. Shaw-Lutchman, M. Barrot, T. Wallace et al., “Regional and cellular mapping of camp response element-mediated transcription during naltrexone-precipitated morphine withdrawal,” Journal of Neuroscience, vol. 22, no. 9, pp. 3663–3672, 2002. View at Google Scholar · View at Scopus
  90. J. A. Blendy and R. Maldonado, “Genetic analysis of drug addiction: the role of cAMP response element binding protein,” Journal of Molecular Medicine, vol. 76, no. 2, pp. 104–110, 1998. View at Publisher · View at Google Scholar · View at Scopus
  91. E. J. Nestler, “Is there a common molecular pathway for addiction?” Nature Neuroscience, vol. 8, no. 11, pp. 1445–1449, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. I. C. Anthony, J. C. Arango, B. Stephens, P. Simmonds, and J. E. Bell, “The effects of illicit drugs on the HIV infected brain,” Frontiers in Bioscience, vol. 13, no. 4, pp. 1294–1307, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. S. M. Ferguson, S. Fasano, P. Yang, R. Brambilla, and T. E. Robinson, “Knockout of ERK1 enhances cocaine-evoked immediate early gene expression and behavioral plasticity,” Neuropsychopharmacology, vol. 31, no. 12, pp. 2660–2668, 2006. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Johannessen, M. P. Delghandi, and U. Moens, “What turns CREB on?” Cellular Signalling, vol. 16, no. 11, pp. 1211–1227, 2004. View at Publisher · View at Google Scholar · View at Scopus