Glycogen synthase kinase 3β in the nucleus accumbens core is critical for methamphetamine-induced behavioral sensitization

Journal of Neurochemistry

Volumn 118, Issue 1, 2011, Pages 126-139

  Xu, Chun Mei ^a   Wang, Jun ^a   Wu, Ping ^a   Xue, Yan Xue ^a   Zhu, Wei Li ^a   Li, Qian Qian ^a   Zhai, Hai Feng ^a   Shi, Jie ^a   Lu, Lin ^a  

^a PEKING UNIVERSITY   (China)

Author keywords

glycogen synthase kinase 3 ; locomotor activity; methamphetamine; nucleus accumbens; sensitization

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE; METHAMPHETAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN REGION; CONTROLLED STUDY; EXPERIMENTAL DESIGN; LOCOMOTION; LONG TERM EXPOSURE; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SENSITIZATION; TISSUE SECTION; WESTERN BLOTTING;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; BEHAVIOR, ADDICTIVE; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM STIMULANTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOGEN SYNTHASE KINASE 3; LITHIUM CHLORIDE; MALE; METHAMPHETAMINE; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

RATTUS;

EID: 79958778339     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07281.x     Document Type: Article

References (77)

1. Abrahamson J. R., (1983) Use of lithium to control drug abuse. Am. J. Psychiatry 140, 1256.
2. Anderton B. H., (1999) Alzheimer's disease: clues from flies and worms. Curr. Biol. 9, R106-R109. (Pubitemid 29087538)
3. Bauer M., Alda M., Priller J., and, Young L. T., (2003) Implications of the neuroprotective effects of lithium for the treatment of bipolar and neurodegenerative disorders. Pharmacopsychiatry 36 (Suppl. 3), S250-S254. (Pubitemid 38085143)
4. Beasley C., Cotter D., Khan N., Pollard C., Sheppard P., Varndell I., Lovestone S., Anderton B., and, Everall I., (2001) Glycogen synthase kinase-3beta immunoreactivity is reduced in the prefrontal cortex in schizophrenia. Neurosci. Lett. 302, 117-120. (Pubitemid 32274223)
5. Beaulieu J. M., Sotnikova T. D., Yao W. D., Kockeritz L., Woodgett J. R., Gainetdinov R. R., and, Caron M. G., (2004) Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc. Natl. Acad. Sci. U S A 101, 5099-5104. (Pubitemid 38469209)
6. Beaulieu J. M., Sotnikova T. D., Marion S., Lefkowitz R. J., Gainetdinov R. R., and, Caron M. G., (2005) An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122, 261-273. (Pubitemid 41032989)
7. Beaulieu J. M., Gainetdinov R. R., and, Caron M. G., (2007a) The Akt-GSK-3 signaling cascade in the actions of dopamine. Trends Pharmacol. Sci. 28, 166-172. (Pubitemid 46483722)
8. Beaulieu J. M., Tirotta E., Sotnikova T. D., Masri B., Salahpour A., Gainetdinov R. R., Borrelli E., and, Caron M. G., (2007b) Regulation of Akt signaling by D2 and D3 dopamine receptors in vivo. J. Neurosci. 27, 881-885. (Pubitemid 46174508)
9. Bhat R. V., Shanley J., Correll M. P., Fieles W. E., Keith R. A., Scott C. W., and, Lee C. M., (2000) Regulation and localization of tyrosine216 phosphorylation of glycogen synthase kinase-3beta in cellular and animal models of neuronal degeneration. Proc. Natl. Acad. Sci. U S A 97, 11074-11079.
10. Bhat R., Xue Y., Berg S., et al. (2003) Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem. 278, 45937-45945. (Pubitemid 37432740)
11. Bossert J. M., Poles G. C., Wihbey K. A., Koya E., and, Shaham Y., (2007) Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. J. Neurosci. 27, 12655-12663. (Pubitemid 350127821)
12. Bradberry C. W., (2007) Cocaine sensitization and dopamine mediation of cue effects in rodents, monkeys, and humans: areas of agreement, disagreement, and implications for addiction. Psychopharmacology (Berl) 191, 705-717. (Pubitemid 46355892)
13. Bradberry C. W., and, Roth R. H., (1989) Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis. Neurosci. Lett. 103, 97-102. (Pubitemid 19207489)
14. Cadoni C., and, Di Chiara G., (1999) Reciprocal changes in dopamine responsiveness in the nucleus accumbens shell and core and in the dorsal caudate-putamen in rats sensitized to morphine. Neuroscience 90, 447-455. (Pubitemid 29161395)
15. Cadoni C., and, Di Chiara G., (2000) Differential changes in accumbens shell and core dopamine in behavioral sensitization to nicotine. Eur. J. Pharmacol. 387, R23-R25. (Pubitemid 30067840)
16. Cadoni C., Solinas M., and, Di Chiara G., (2000) Psychostimulant sensitization: differential changes in accumbal shell and core dopamine. Eur. J. Pharmacol. 388, 69-76. (Pubitemid 30066438)
17. Carlezon W. A., Jr, and, Nestler E. J., (2002) Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci. 25, 610-615. (Pubitemid 35356507)
18. Di Chiara G., (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res. 137, 75-114. (Pubitemid 35346430)
19. Di Chiara G., Bassareo V., Fenu S., et al. (2004) Dopamine and drug addiction: the nucleus accumbens shell connection. Neuropharmacology 47 (Suppl. 1), 227-241. (Pubitemid 39298267)
20. Edwards S., Graham D. L., Bachtell R. K., and, Self D. W., (2007) Region-specific tolerance to cocaine-regulated cAMP-dependent protein phosphorylation following chronic self-administration. Eur. J. Neurosci. 25, 2201-2213. (Pubitemid 46581745)
21. Emamian E. S., Hall D., Birnbaum M. J., Karayiorgou M., and, Gogos J. A., (2004) Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat. Genet. 36, 131-137. (Pubitemid 38174370)
22. Flemenbaum A., Cronson A. J., and, Weddige R. L., (1979) Lithium in opiate abuse: a theoretical approach. Compr. Psychiatry 20, 91-99. (Pubitemid 9124735)
23. Gould T. D., and, Manji H. K., (2005) Glycogen synthase kinase-3: a putative molecular target for lithium mimetic drugs. Neuropsychopharmacology 30, 1223-1237. (Pubitemid 40848077)
24. Hernandez F., Borrell J., Guaza C., Avila J., and, Lucas J. J., (2002) Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem. 83, 1529-1533. (Pubitemid 35477491)
25. Hooper C., Markevich V., Plattner F., et al. (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur. J. Neurosci. 25, 81-86. (Pubitemid 46096224)
26. Hughes K., Nikolakaki E., Plyte S. E., Totty N. F., and, Woodgett J. R., (1993) Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J. 12, 803-808. (Pubitemid 23073729)
27. Hyman S. E., (2005) Addiction: a disease of learning and memory. Am. J. Psychiatry 162, 1414-1422. (Pubitemid 41105555)
28. Hyman S. E., Malenka R. C., and, Nestler E. J., (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29, 565-598. (Pubitemid 44476856)
29. Ikemoto S., and, Wise R. A., (2004) Mapping of chemical trigger zones for reward. Neuropharmacology 47 (Suppl. 1), 190-201. (Pubitemid 39298264)
30. Ito R., Robbins T. W., and, Everitt B. J., (2004) Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat. Neurosci. 7, 389-397. (Pubitemid 38429179)
31. Jongen-Relo A. L., Voorn P., and, Groenewegen H. J., (1994) Immunohistochemical characterization of the shell and core territories of the nucleus accumbens in the rat. Eur. J. Neurosci. 6, 1255-1264. (Pubitemid 24243630)
32. Jope R. S., and, Johnson G. V., (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95-102. (Pubitemid 38186580)
33. Kalivas P. W., (2004) Recent understanding in the mechanisms of addiction. Curr. Psychiatry Rep. 6, 347-351. (Pubitemid 39591815)
34. Kalivas P. W., and, Duffy P., (1990) Effect of acute and daily cocaine treatment on extracellular dopamine in the nucleus accumbens. Synapse 5, 48-58. (Pubitemid 20110621)
35. Kalivas P. W., and, Stewart J., (1991) Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res. Brain Res. Rev. 16, 223-244.
36. Kimura T., Yamashita S., Nakao S., Park J. M., Murayama M., Mizoroki T., Yoshiike Y., Sahara N., and, Takashima A., (2008) GSK-3beta is required for memory reconsolidation in adult brain. PLoS ONE 3, e3540.
37. Kleindienst N., and, Greil W., (2003) Lithium in the long-term treatment of bipolar disorders. Eur. Arch. Psychiatry Clin. Neurosci. 253, 120-125. (Pubitemid 37205470)
38. Koob G. F., and, Le Moal M., (2008) Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos. Trans. R Soc. Lond. B Biol. Sci. 363, 3113-3123.
39. Koros E., and, Dorner-Ciossek C., (2007) The role of glycogen synthase kinase-3beta in schizophrenia. Drug News Perspect. 20, 437-445. (Pubitemid 350232812)
40. Kozlovsky N., Belmaker R. H., and, Agam G., (2002) GSK-3 and the neurodevelopmental hypothesis of schizophrenia. Eur. Neuropsychopharmacol. 12, 13-25. (Pubitemid 34098826)
41. Kozlovsky N., Regenold W. T., Levine J., Rapoport A., Belmaker R. H., and, Agam G., (2004) GSK-3beta in cerebrospinal fluid of schizophrenia patients. J. Neural Transm. 111, 1093-1098. (Pubitemid 39037129)
42. Lei G., Xia Y., and, Johnson K. M., (2008) The role of Akt-GSK-3beta signaling and synaptic strength in phencyclidine-induced neurodegeneration. Neuropsychopharmacology 33, 1343-1353. (Pubitemid 351521719)
43. Leroy K., and, Brion J. P., (1999) Developmental expression and localization of glycogen synthase kinase-3beta in rat brain. J. Chem. Neuroanat. 16, 279-293. (Pubitemid 29296952)
44. Li Y. Q., Li F. Q., Wang X. Y., Wu P., Zhao M., Xu C. M., Shaham Y., and, Lu L., (2008) Central amygdala extracellular signal-regulated kinase signaling pathway is critical to incubation of opiate craving. J. Neurosci. 28, 13248-13257.
45. Lu L., Hope B. T., Dempsey J., Liu S. Y., Bossert J. M., and, Shaham Y., (2005) Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat. Neurosci. 8, 212-219. (Pubitemid 40194052)
46. Masri B., Salahpour A., Didriksen M., Ghisi V., Beaulieu J. M., Gainetdinov R. R., and, Caron M. G., (2008) Antagonism of dopamine D2 receptor/beta-arrestin 2 interaction is a common property of clinically effective antipsychotics. Proc. Natl. Acad. Sci. U S A 105, 13656-13661.
47. Miller J. S., Tallarida R. J., and, Unterwald E. M., (2009) Cocaine-induced hyperactivity and sensitization are dependent on GSK3. Neuropharmacology 56, 1116-1123.
48. O'Brien W. T., and, Klein P. S., (2007) Regulation of glycogen synthase kinase-3 in patients with affective disorders. Biol. Psychiatry 61, 139-141. (Pubitemid 46072792)
49. Parkitna J. R., Obara I., Wawrzczak-Bargiela A., Makuch W., Przewlocka B., and, Przewlocki R., (2006) Effects of glycogen synthase kinase 3beta and cyclin-dependent kinase 5 inhibitors on morphine-induced analgesia and tolerance in rats. J. Pharmacol. Exp. Ther. 319, 832-839.
50. Paulson P. E., and, Robinson T. E., (1995) Amphetamine-induced time-dependent sensitization of dopamine neurotransmission in the dorsal and ventral striatum: a microdialysis study in behaving rats. Synapse 19, 56-65.
51. Peineau S., Taghibiglou C., Bradley C., et al. (2007) LTP inhibits LTD in the hippocampus via regulation of GSK3beta. Neuron 53, 703-717. (Pubitemid 46283369)
52. Peineau S., Bradley C., Taghibiglou C., Doherty A., Bortolotto Z. A., Wang Y. T., and, Collingridge G. L., (2008) The role of GSK-3 in synaptic plasticity. Br. J. Pharmacol. 153 (Suppl. 1), S428-S437. (Pubitemid 351341021)
53. Perrine S. A., Miller J. S., and, Unterwald E. M., (2008) Cocaine regulates protein kinase B and glycogen synthase kinase-3 activity in selective regions of rat brain. J. Neurochem. 107, 570-577.
54. Pontieri F. E., Tanda G., and, Di Chiara G., (1995) Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens. Proc. Natl. Acad. Sci. U S A 92, 12304-12308.
55. Prickaerts J., Moechars D., Cryns K., Lenaerts I., van Craenendonck H., Goris I., Daneels G., Bouwknecht J. A., and, Steckler T., (2006) Transgenic mice overexpressing glycogen synthase kinase 3beta: a putative model of hyperactivity and mania. J. Neurosci. 26, 9022-9029. (Pubitemid 44319393)
56. Robinson T. E., (1984) Behavioral sensitization: characterization of enduring changes in rotational behavior produced by intermittent injections of amphetamine in male and female rats. Psychopharmacology (Berl) 84, 466-475. (Pubitemid 15179663)
57. Robinson T. E., and, Becker J. B., (1986) Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res. 396, 157-198. (Pubitemid 16100809)
58. Robinson T. E., and, Berridge K. C., (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 18, 247-291. (Pubitemid 23219500)
59. Robinson T. E., and, Berridge K. C., (2003) Addiction. Annu. Rev. Psychol. 54, 25-53. (Pubitemid 37417487)
60. Robinson T. E., and, Berridge K. C., (2008) Review. The incentive sensitization theory of addiction: some current issues. Philos. Trans. R Soc. Lond. B Biol. Sci. 363, 3137-3146.
61. Robinson T. E., and, Kolb B., (1999) Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur. J. Neurosci. 11, 1598-1604. (Pubitemid 29192234)
62. Robinson T. E., Jurson P. A., Bennett J. A., and, Bentgen K. M., (1988) Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with (+)-amphetamine: a microdialysis study in freely moving rats. Brain Res. 462, 211-222.
63. Robinson T. E., Gorny G., Mitton E., and, Kolb B., (2001) Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39, 257-266. (Pubitemid 32099681)
64. Sachs G. S., (1996) Treatment-resistant bipolar depression. Psychiatr. Clin. North Am. 19, 215-236. (Pubitemid 26184100)
65. Stewart J., and, Badiani A., (1993) Tolerance and sensitization to the behavioral effects of drugs. Behav. Pharmacol. 4, 289-312. (Pubitemid 23258353)
66. Takashima A., (2006) GSK-3 is essential in the pathogenesis of Alzheimer's disease. J. Alzheimers Dis. 9, 309-317. (Pubitemid 44253325)
67. Thomas M. J., Kalivas P. W., and, Shaham Y., (2008) Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br. J. Pharmacol. 154, 327-342. (Pubitemid 351670603)
68. Vezina P., (2004) Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs. Neurosci. Biobehav. Rev. 27, 827-839. (Pubitemid 38199613)
69. Voorn P., Jorritsma-Byham B., Van Dijk C., and, Buijs R. M., (1986) The dopaminergic innervation of the ventral striatum in the rat: a light- and electron-microscopical study with antibodies against dopamine. J. Comp. Neurol. 251, 84-99. (Pubitemid 16012190)
70. Wada A., (2009) Lithium and neuropsychiatric therapeutics: neuroplasticity via glycogen synthase kinase-3beta, beta-catenin, and neurotrophin cascades. J. Pharmacol. Sci. 110, 14-28.
71. Wang Q. M., Fiol C. J., DePaoli-Roach A. A., and, Roach P. J., (1994) Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269, 14566-14574.
72. 2+/calmodulin-dependent kinase II-dependent mechanism. Mol. Pharmacol. 71, 835-842. (Pubitemid 46294095)
73. White F. J., and, Kalivas P. W., (1998) Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Depend. 51, 141-153. (Pubitemid 28353762)
74. 2 receptors in the ventral striatum: multiple effects or receptor subtypes? Nihon Shinkei Seishin Yakurigaku Zasshi 17, 91-95. (Pubitemid 27274094)
75. Xu C. M., Wang J., Wu P., Zhu W. L., Li Q. Q., Xue Y. X., Zhai H. F., Shi J., and, Lu L., (2009) Glycogen synthase kinase 3beta in the nucleus accumbens core mediates cocaine-induced behavioral sensitization. J. Neurochem. 111, 1357-1368.
76. Zangen A., Solinas M., Ikemoto S., Goldberg S. R., and, Wise R. A., (2006) Two brain sites for cannabinoid reward. J. Neurosci. 26, 4901-4907. (Pubitemid 44315331)
77. Zhu L. Q., Wang S. H., Liu D., Yin Y. Y., Tian Q., Wang X. C., Wang Q., Chen J. G., and, Wang J. Z., (2007) Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments. J. Neurosci. 27, 12211-12220. (Pubitemid 350085482)