Involvement of the K+-Cl- co-transporter KCC2 in the sensitization to morphine-induced hyperlocomotion under chronic treatment with zolpidem in the mesolimbic system

Journal of Neurochemistry

Volumn 125, Issue 5, 2013, Pages 747-755

  Shibasaki, Masahiro ^a   Masukawa, Daiki ^a   Ishii, Kazunori ^a   Yamagishi, Yui ^a   Mori, Tomohisa ^a   Suzuki, Tsutomu ^a  

^a HOSHI UNIVERSITY   (Japan)

Author keywords

benzodiazepine; drug dependence; KCC2; morphine; nucleus accumbens; zolpidem

Indexed keywords

FUROSEMIDE; MORPHINE; PHOSPHOPROTEIN PHOSPHATASE 1; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 2; PROTEIN KINASE C GAMMA; UNCLASSIFIED DRUG; ZOLPIDEM TARTRATE;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DOWN REGULATION; ENZYME REGULATION; FOREBRAIN; HOT PLATE TEST; HYPERACTIVITY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; LIMBIC SYSTEM; LOCOMOTION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SENSITIZATION; SIGNAL TRANSDUCTION; TAIL FLICK TEST; THERMAL STIMULATION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; DRUG SYNERGISM; LIMBIC SYSTEM; MALE; MICE; MICE, INBRED ICR; MORPHINE; PSYCHOMOTOR AGITATION; PYRIDINES; SYMPORTERS; TREATMENT OUTCOME; UP-REGULATION;

EID: 84877942190     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12258     Document Type: Article

References (48)

1. Ballantyne J. C., and, LaForge K. S., (2007) Opioid dependence and addiction during opioid treatment of chronic pain. Pain 129, 235-255.
2. Ben-Ari Y., (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739.
3. Browne R., Sloan D., Fahy S., Keating S., Moran C., and, O'Connor J., (1998) Detection of benzodiazepine abuse in opiate addicts. Ir. Med. J. 91, 18-19.
4. Darke S. G., Ross J. E., and, Hall W. D., (1995) Benzodiazepine use among injecting heroin users. Med. J. Aust. 162, 645-647.
5. Eto M., Kitazawa T., and, Brautigan D. L., (2004) Phosphoprotein inhibitor CPI-17 specificity depends on allosteric regulation of protein phosphatase-1 by regulatory subunits. Proc. Natl Acad. Sci. USA 101, 8888-8893.
6. Fukakusa A., Nagai T., Mizoguchi H., et al,. (2008) Role of tissue plasminogen activator in the sensitization of methamphetamine-induced dopamine release in the nucleus accumbens. J. Neurochem. 105, 436-444.
7. Funada M., Suzuki T., Narita M., Misawa M., and, Nagase H., (1993) Modification of morphine-induced locomotor activity by pertussis toxin: biochemical and behavioral studies in mice. Brain Res. 619, 163-172.
8. Gauvain G., Chamma I., Chevy Q., Cabezas C., Irinopoulou T., Bodrug N., Carnaud M., Levi S., and, Poncer J. C., (2011) The neuronal K-Cl cotransporter KCC2 influences postsynaptic AMPA receptor content and lateral diffusion in dendritic spines. Proc. Natl Acad. Sci. USA 108, 15474-15479.
9. Giorgetti M., Javaid J. I., Davis J. M., Costa E., Guidotti A., Appel S. B., and, Brodie M. S., (1998) Imidazenil, a positive allosteric GABAA receptor modulator, inhibits the effects of cocaine on locomotor activity and extracellular dopamine in the nucleus accumbens shell without tolerance liability. J. Pharmacol. Exp. Ther. 287, 58-66.
10. Heikkinen A. E., Moykkynen T. P., and, Korpi E. R., (2009) Long-lasting modulation of glutamatergic transmission in VTA dopamine neurons after a single dose of benzodiazepine agonists. Neuropsychopharmacology 34, 290-298.
11. Hojsted J., and, Sjogren P., (2007) Addiction to opioids in chronic pain patients: a literature review. Eur. J. Pain 11, 490-518.
12. Iguchi M. Y., Handelsman L., Bickel W. K., and, Griffiths R. R., (1993) Benzodiazepine and sedative use/abuse by methadone maintenance clients. Drug Alcohol Depend. 32, 257-266.
13. Invernizzi R., Pozzi L., and, Samanin R., (1991) Release of dopamine is reduced by diazepam more in the nucleus accumbens than in the caudate nucleus of conscious rats. Neuropharmacology 30, 575-578.
14. Johnson S. W., and, North R. A., (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12, 483-488.
15. Laviolette S. R., Gallegos R. A., Henriksen S. J., and, van der Kooy D., (2004) Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat. Neurosci. 7, 160-169.
16. Lee H. H., Walker J. A., Williams J. R., Goodier R. J., Payne J. A., and, Moss S. J., (2007) Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J. Biol. Chem. 282, 29777-29784.
17. Lee H. H., Deeb T. Z., Walker J. A., Davies P. A., and, Moss S. J., (2011) NMDA receptor activity downregulates KCC2 resulting in depolarizing GABAA receptor-mediated currents. Nat. Neurosci. 14, 736-743.
18. Lee A. Y., Chen W., Stippec S., Self J., Yang F., Ding X., Chen S., Juang Y. C., and, Cobb M. H., (2012) Protein kinase WNK3 regulates the neuronal splicing factor Fox-1. Proc. Natl Acad. Sci. USA 109, 16841-16846.
19. Leri F., and, Franklin K. B., (2000) Diazepam in the ventral striatum dissociates dopamine-dependent and dopamine-independent place conditioning. NeuroReport 11, 2553-2557.
20. Liu Y., Chen J., Song T., Hu C., Tang Y., Zhang X., and, Zhao J., (2009) Contribution of K+-Cl- cotransporter 2 in MK-801-induced impairment of long term potentiation. Behav. Brain Res. 201, 300-304.
21. Malmberg A. B., and, Basbaum A. I., (1998) Partial sciatic nerve injury in the mouse as a model of neuropathic pain: behavioral and neuroanatomical correlates. Pain 76, 215-222.
22. Morgan E. T., Sewer M. B., Iber H., et al,. (1998) Physiological and pathophysiological regulation of cytochrome P450. Drug Metab. Dispos. 26, 1232-1240.
23. Mori T., Ito S., Narita M., Suzuki T., and, Sawaguchi T., (2004) Combined effects of psychostimulants and morphine on locomotor activity in mice. J. Pharmacol. Sci. 96, 450-458.
24. Narita M., Takahashi Y., Takamori K., Funada M., Suzuki T., Misawa M., and, Nagase H., (1993) Effects of kappa-agonist on the antinociception and locomotor enhancing action induced by morphine in mice. Jpn. J. Pharmacol. 62, 15-24.
25. Narita M., Aoki T., Ozaki S., Yajima Y., and, Suzuki T., (2001) Involvement of protein kinase Cgamma isoform in morphine-induced reinforcing effects. Neuroscience 103, 309-314.
26. Narita M., Mizuo K., Shibasaki M., and, Suzuki T., (2002) Up-regulation of the G(q/11alpha) protein and protein kinase C during the development of sensitization to morphine-induced hyperlocomotion. Neuroscience 111, 127-132.
27. Narita M., Shibasaki M., Mizuo K., and, Suzuki T., (2003) Changes in G-protein activity mediated through the stimulation of dopamine and GABA(B) receptors in the mesolimbic dopaminergic system of morphine-sensitized mice. Addict. Biol. 8, 319-325.
28. Narita M., Akai H., Nagumo Y., Sunagawa N., Hasebe K., Nagase H., Kita T., Hara C., and, Suzuki T., (2004) Implications of protein kinase C in the nucleus accumbens in the development of sensitization to methamphetamine in rats. Neuroscience 127, 941-948.
29. Narita M., Nagumo Y., Hashimoto S., et al,. (2006) Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J. Neurosci. 26, 398-405.
30. Panhelainen A. E., Vekovischeva O. Y., Aitta-Aho T., Rasanen I., Ojanpera I., and, Korpi E. R., (2011) Diazepam-induced neuronal plasticity attenuates locomotor responses to morphine and amphetamine challenges in mice. Neuroscience 192, 312-321.
31. Pitchot W., and, Ansseau M., (2009) Zolpidem dependence and withdrawal seizure. Rev. Med. Liege 64, 407-408.
32. Price T. J., Cervero F., Gold M. S., Hammond D. L., and, Prescott S. A., (2009) Chloride regulation in the pain pathway. Brain Res. Rev. 60, 149-170.
33. Rivera C., Voipio J., Thomas-Crusells J., et al,. (2004) Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24, 4683-4691.
34. Rooney S., Kelly G., Bamford L., Sloan D., and, O'Connor J. J., (1999) Co-abuse of opiates and benzodiazepines. Ir. J. Med. Sci. 168, 36-41.
35. Rowlett J. K., Platt D. M., Lelas S., Atack J. R., and, Dawson G. R., (2005) Different GABAA receptor subtypes mediate the anxiolytic, abuse-related, and motor effects of benzodiazepine-like drugs in primates. Proc. Natl Acad. Sci. USA 102, 915-920.
36. Rudolph U., and, Mohler H., (2006) GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr. Opin. Pharmacol. 6, 18-23.
37. Rudolph U., Crestani F., Benke D., Brunig I., Benson J. A., Fritschy J. M., Martin J. R., Bluethmann H., and, Mohler H., (1999) Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 401, 796-800.
38. Segura M., Barbosa J., Torrens M., Farre M., Castillo C., Segura J., and, de la Torre R., (2001) Analytical methodology for the detection of benzodiazepine consumption in opioid-dependent subjects. J. Anal. Toxicol. 25, 130-136.
39. Seltzer Z., Dubner R., and, Shir Y., (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43, 205-218.
40. Shibasaki M., Watanabe K., Takeda K., Itoh T., Tsuyuki T., Narita M., Mori T., and, Suzuki T., (2013) Effect of chronic ethanol treatment on mu-opioid receptor function, interacting proteins and morphine-induced place preference. Psychopharmacology (in press).
41. Tan K. R., Brown M., Labouebe G., Yvon C., Creton C., Fritschy J. M., Rudolph U., and, Luscher C., (2010) Neural bases for addictive properties of benzodiazepines. Nature 463, 769-774.
42. Tsuda M., Chiba Y., Suzuki T., and, Misawa M., (1998a) Upregulation of NMDA receptor subunit proteins in the cerebral cortex during diazepam withdrawal. Eur. J. Pharmacol. 341, R1-R2.
43. Tsuda M., Shimizu N., Yajima Y., Suzuki T., and, Misawa M., (1998b) Hypersusceptibility to DMCM-induced seizures during diazepam withdrawal in mice: evidence for upregulation of NMDA receptors. Naunyn Schmiedebergs Arch. Pharmacol. 357, 309-315.
44. Vinkers C. H., Olivier B., Hanania T., Min W., Schreiber R., Hopkins S. C., Campbell U., and, Paterson N., (2011) Discriminative stimulus properties of GABAA receptor positive allosteric modulators TPA023, ocinaplon and NG2-73 in rats trained to discriminate chlordiazepoxide or zolpidem. Eur. J. Pharmacol. 668, 190-193.
45. Walker B. M., and, Ettenberg A., (2005) Intra-ventral tegmental area heroin-induced place preferences in rats are potentiated by peripherally administered alprazolam. Pharmacol. Biochem. Behav. 82, 470-477.
46. Xiang K., Earl D. E., Davis K. M., Giovannucci D. R., Greenfield L. J. Jr, and, Tietz E. I., (2008) Chronic benzodiazepine administration potentiates high voltage-activated calcium currents in hippocampal CA1 neurons. J. Pharmacol. Exp. Ther. 327, 872-883.
47. Yang H., Huang L. Y., Zeng D. Y., et al,. (2012) Decrease of intracellular chloride concentration promotes endothelial cell inflammation by activating nuclear factor-kappaB pathway. Hypertension 60, 1287-1293.
48. Zarrindast M. R., Heidari-Darvishani A., Rezayof A., Fathi-Azarbaijani F., Jafari-Sabet M., and, Hajizadeh-Moghaddam A., (2007) Morphine-induced sensitization in mice: changes in locomotor activity by prior scheduled exposure to GABAA receptor agents. Behav. Pharmacol. 18, 303-310.