Cocaine-induced alterations in nucleus accumbens ionotropic glutamate receptor subunits in human and non-human primates

Journal of Neurochemistry

Volumn 95, Issue 6, 2005, Pages 1785-1793

  Hemby, Scott E ^a   Tang, Wenxue ^b   Muly, Emil C ^b,c   Kuhar, Michael J ^b,c   Howell, Leonard ^b,c   Mash, Deborah C ^d  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Cocaine; Glutamate; Nucleus accumbens; Protein expression; Putamen

Indexed keywords

AMPA RECEPTOR; COCAINE; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 5; IONOTROPIC RECEPTOR; KAINIC ACID RECEPTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; RECEPTOR SUBUNIT;

ADULT; ARTICLE; CLINICAL ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; DRUG OVERDOSE; DRUG WITHDRAWAL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RHESUS MONKEY; STATISTICAL SIGNIFICANCE; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ADULT; ANIMALS; BLOTTING, WESTERN; COCAINE; COCAINE-RELATED DISORDERS; FEMALE; HUMANS; MACACA MULATTA; MALE; MIDDLE AGED; NEURAL PATHWAYS; NUCLEUS ACCUMBENS; OVERDOSE; PHOSPHORYLATION; PUTAMEN; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SELF ADMINISTRATION; SERINE; UP-REGULATION; VENTRAL TEGMENTAL AREA;

MACACA MULATTA; PRIMATES; RODENTIA;

EID: 29144498033     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03517.x     Document Type: Article

References (60)

1. Borges K. and Dingledine R. (2002) Molecular pharmacology and physiology of glutamate receptors, in Glutamate and Addiction (Herman B. H., Frankenheim J., Litten R. Z., Sheridan P. H., Weight F. F. and Zukin S. R., eds), pp. 3-22. Humana Press, Totawa, NJ.
2. Breese C. R., Freedman R. and Leonard S. S. (1995) Glutamate receptor subtype expression in human post-mortem brain tissue from schizophrenics and alcohol abusers. Brain Res. 674, 82-90.
3. Burkhalter A. and Bernardo K. L. (1989) Organization of corticocortical connections in human visual cortex. Proc. Natl Acad. Sci. USA 86, 1071-1075.
4. Byrd L. D. (1979) The behavioral effects of cocaine: rate dependency or rate constancy. Eur. J. Pharmacol. 56, 355-362.
5. Carlezon W. A. Jr, Thome J., Olson V. G., Lane-Ladd S. B., Brodkin E. S., Hiroi N., Duman R. S., Neve R. L. and Nestler E. J. (1998) Regulation of cocaine reward by CREB. Science 282, 2272-2275.
6. Chung H. J., Xia J., Scannevin R. H., Zhang X. and Huganir R. L. (2000) Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20, 7258-7267.
7. Churchill L., Swanson C. J., Urbina M. and Kalivas P. W. (1999) Repeated cocaine alters glutamate receptor subunit levels in the nucleus accumbens and ventral tegmental area of rats that develop behavioral sensitization. J. Neurochem. 72, 2397-2403.
8. Cornish J. L. and Kalivas P. W. (2000) Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction. J. Neurosci. 20, RC89.
9. Cornish J. L. and Kalivas P. W. (2001) Cocaine sensitization and craving: differing roles for dopamine and glutamate in the nucleus accumbens. J. Addictive Dis. 20, 43-54.
10. Cornish J. L., Duffy P. and Kalivas P. W. (1999) A role for nucleus accumbens glutamate transmission in the relapse to cocaine-seeking behavior. Neuroscience 93, 1359-1367.
11. Crespo J. A., Oliva J. M., Ghasemzadeh M. B., Kalivas P. W. and Ambrosio E. (2002) Neuroadaptive changes in NMDAR1 gene expression after extinction of cocaine self-administration. Ann. NY Acad. Sci. 965, 78-91.
12. Di Ciano P. and Everitt B. J. (2002) Reinstatement and spontaneous recovery of cocaine-seeking following extinction and different durations of withdrawal. Behav. Pharmacol. 13, 397-405.
13. Dingledine R., Borges K., Bowie D. and Traynelis S. F. (1999) The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
14. DSM-IV. (1994) Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association, Washington, DC.
15. Fitzgerald L. W., Ortiz J., Hamedani A. G. and Nestler E. J. (1996) Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents. J. Neurosci. 16, 274-282.
16. Ghasemzadeh M. B., Nelson L. C., Lu X. Y. and Kalivas P. W. (1999) Neuroadaptations in ionotropic and metabotropic glutamate receptor mRNA produced by cocaine treatment. J. Neurochem. 11, 157-165.
17. Guerguerian A. M., Brambrink A. M., Traystman R. J., Huganir R. L. and Martin L. J. (2002) Altered expression and phosphorylation of N-methyl-D-aspartate receptors in piglet striatum after hypoxia-ischemia. Brain Res. Mol Brain Res. 104, 66-80.
18. Haile C. N., Hiroi N., Nestler E. J. and Kosten T. A. (2001) Differential behavioral responses to cocaine are associated with dynamics of mesolimbic dopamine proteins in Lewis and Fischer 344 rats. Synapse 41, 179-190.
19. Herd J. A., Morse W. H., Kelleher R. T. and Jones L. G. (1969) Arterial hypertension in the squirrel monkey during behavioral experiments. Am. J. Physiol. 217, 24-29.
20. Hernandez A., Andollo W. and Hearn W. L. (1994) Analysis of cocaine and metabolites in brain using solid phase extraction and full-scanning gas chromatography/ion trap mass spectrometry. Forensic Sci Int. 65, 149-156.
21. Hiroi N., Brown J. R., Haile C. N., Ye H., Greenberg M. E. and Nestler E. J. (1997) FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaine's psychomotor and rewarding effects. Proc. Natl Acad. Sci. USA 94, 10397-10402.
22. Hope B., Kosofsky B., Hyman S. E. and Nestler E. J. (1992) Regulation of immediate early gene expression and AP-1 binding in the rat nucleus accumbens by chronic cocaine. Proc. Natl Acad. Sci. USA 89, 5764-5768.
23. Howell L. L. and Wilcox K. M. (2001) Intravenous drug self-administration in non-human primates, in Methods of Behavior Analysis in Neuroscience (Buccafusco J. J., ed.), pp. 91-110. CRC Press, Boca Raton, FL.
24. Kalivas P. W., McFarland K., Bowers S., Szumlinski K., Xi Z. X. and Baker D. (2003) Glutamate transmission and addiction to cocaine. Ann. NY Acad. Sci. 1003, 169-175.
25. Kalivas P. W., Volkow N. and Seamans J. (2005) Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 45, 647-650.
26. Kelz M. B., Chen J., Carlezon W. A. Jr et al. (1999) Expression of the transcription factor δFosB in the brain controls sensitivity to cocaine. Nature 401, 272-276.
27. Kosinski C. M., Standaert D. G., Counihan T. J., Scherzer C. R., Kerner J. A., Daggett L. P., Velicelebi G., Penney J. B., Young A. B. and Landwehrmeyer G. B. (1998) Expression of N-methyl-D-aspartate receptor subunit mRNAs in the human brain: striatum and globus pallidus. J. Comp. Neurol. 390, 63-74.
28. Krebs M. O., Trovero F., Desban M., Gauchy C., Glowinski J. and Kernel M. L. (1991) Distinct presynaptic regulation of dopamine release through NMDA receptors in striosome- and matrix-enriched areas of the rat striatum. J. Neurosci. 11, 1256-1262.
29. Lindsey K. P., Wilcox K. M., Votaw J. R., Goodman M. M., Plisson C., Carroll F. I., Rice K. C. and Howell L. L. (2004) Effects of dopamine transporter inhibitors on cocaine self-administration in rhesus monkeys: relationship to transporter occupancy determined by positron emission tomography neuroimaging. J. Pharmacol. Exp. Ther. 309, 959-969.
30. Lu L., Grimm J. W., Shaham Y. and Hope B. T. (2003) Molecular neuroadaptations in the accumbens and ventral tegmental area during the first 90 days of forced abstinence from cocaine self-administration in rats. J. Neurochem. 85, 1604-1613.
31. Lu W., Monteggia L. M. and Wolf M. E. (2002) Repeated administration of amphetamine or cocaine does not alter AMPA receptor subunit expression in the rat midbrain. Neuropsychopharmacology 26, 1-13.
32. Lynd-Balta E. and Haber S. N. (1994) The organization of midbrain projections to the ventral striatum in the primate. Neuroscience 59, 609-623.
33. Martin L. J., Blackstone C. D., Huganir R. L. and Price D. L. (1993) The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits. J. Neurosci. 13, 782-792.
34. Matsuda S., Mikawa S. and Hirai H. (1999) Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J. Neurochem. 73, 1765-1768.
35. McFarland K., Lapish C. C. and Kalivas P. W. (2003) Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci. 23, 3531-3537.
36. McFarland K., Davidge S. B., Lapish C. C. and Kalivas P. W. (2004) Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J. Neurosci. 24, 1551-1560.
37. Meredith G. E. (1999) The synaptic framework for chemical signaling in nucleus accumbens. Ann. NY Acad. Sci. 877, 140-156.
38. Miserendino M. J. and Nestler E. J. (1995) Behavioral sensitization to cocaine: modulation by the cyclic AMP system in the nucleus accumbens. Brain Res. 674, 299-306.
39. Nestler E. J., Terwilliger R. Z., Walker J. R., Sevarino K. A. and Duman R. S. (1990) Chronic cocaine treatment decreases levels of the G protein subunits Giot and Goot in discrete regions of rat brain. J. Neurochem. 55, 1079-1082.
40. Nye H. E., Hope B. T, Kelz M. B., Iadarola M. and Nestler E. J. (1995) Pharmacological studies of the regulation of chronic FOS-related antigen induction by cocaine in the striatum and nucleus accumbens. J. Pharmacol. Exp. Therapeutics 275, 1671-1680.
41. Ouagazzal A., Nieoullon A. and Amalric M. (1994) Locomotor activation induced by MK-801 in the rat: postsynaptic interactions with dopamine receptors in the ventral striatum. Eur. J. Pharmacol. 251, 229-236.
42. Park W. K., Bari A. A., Jey A. R., Anderson S. M., Spealman R. D., Rowlett J. K. and Pierce R. C. (2002) Cocaine administered into the medial prefrontal cortex reinstates cocaine-seeking behavior by increasing AMPA receptor-mediated glutamate transmission in the nucleus accumbens. J. Neurosci. 22, 2916-2925.
43. Pich E. M., Pagliusi S. R., Tessari M., Talabot-Ayer D., Hooft van Huijsduijnen R. and Chiamulera C. (1997) Common neural substrates for the addictive properties of nicotine and cocaine. Science 275, 83-86.
44. Pliakas A. M., Carlson R. R., Neve R. L., Konradi C., Nestler E. J. and Carlezon W. A. Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J. Neurosci. 21, 7397-7403.
45. Preuss T. M. (1995) Do rats have prefrontal cortex? The Rose-Woolsey-Akert Program reconsidered. J. Cog. Neurosci. 7, 1-24.
46. Ruttenber A. J., Lawler-Heavner J., Yin M., Wetli C. V., Hearn W. L. and Mash D. C. (1997) Fatal excited delirium following cocaine use: epidemiologic findings provide new evidence for mechanisms of cocaine toxicity. J. Forensic Sci. 42, 25-31.
47. Seidenman K. J., Steinberg J. P., Huganir R. and Malinow R. (2003) Glutamate receptor subunit 2 serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J. Neurosci. 23, 9220-9228.
48. Self D. W., Genova L. M., Hope B. T., Barnhart W. J., Spencer J. J. and Nestler E. J. (1998) Involvement of cAMP-dependent protein kinase in the nucleus accumbens in cocaine self-administration and relapse of cocaine-seeking behavior. J. Neurosci. 18, 1848-1859.
49. Smart T. G. (1997) Regulation of excitatory and inhibitory neurotransmitter-gated ion channels by protein phosphorylation. Curr. Opin. Neurobiol. 7, 358-367.
50. Striplin C. D. and Kalivas P. W. (1992) Correlation between behavioral sensitization to cocaine and G protein ADP-ribosylation in the ventral tegmental area. Brain Res. 579, 181-186.
51. Sutton M. A., Schmidt E. F., Choi K. H., Schad C. A., Whisler K., Simmons D., Karanian D. A., Monteggia L. M., Neve R. L. and Self D. W. (2003) Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature 421, 70-75.
52. Tang W.-X., Fasulo W. H., Mash D. C. and Hemby S. E. (2003) Molecular profiling of midbrain dopamine regions in cocaine overdose victims. J. Neurochem. 85, 911-924.
53. Tarazi F. I., Campbell A., Yeghiayan S. K. and Baldessarini R. J. (1998) Localization of ionotropic glutamate receptors in caudate-putamen and nucleus accumbens septi of rat brain: comparison of NMDA, AMPA, and kainate receptors. Synapse 30, 227-235.
54. Terwilliger R. Z., Beitner-Johnson D., Sevarino K. A., Crain S. M. and Nestler E. J. (1991) 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 Res. 548, 100-110.
55. Toda S., McGinty J. F. and Kalivas P. W. (2002) Repeated cocaine administration alters the expression of genes in corticolimbic circuitry after a 3-week withdrawal: a DNA macroarray study. J. Neurochem. 82, 1290-1299.
56. Ungless M. A., Whistler J. L., Malenka R. C. and Bonci A. (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411, 583-587.
57. White F. J. and Kalivas P. W. (1998) Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Dependence 51, 141-153.
58. White F. J., Hu X. T., Zhang X. F. and Wolf M. E. (1995) Repeated administration of cocaine or amphetamine alters neuronal responses to glutamate in the mesoaccumbens dopamine system. J. Pharmacol. Exp. Therapeutics 273, 445-454.
59. Williams S. M. and Goldman-Rakic P. S. (1998) Widespread origin of the primate mesofrontal dopamine system. Cerebral Cortex 8, 321-345.
60. Zhang X. F., Hu X. T., White F. J. and Wolf M. E. (1997) Increased responsiveness of ventral tegmental area dopamine neurons to glutamate after repeated administration of cocaine or amphetamine is transient and selectively involves AMPA receptors. J. Pharmacol. Exp. Therapeutics 281, 699-706.