Persistent alterations in mesolimbic gene expression with abstinence from cocaine self-administration

Neuropsychopharmacology

Volumn 33, Issue 8, 2008, Pages 1807-1817

  Freeman, Willard M ^a   Patel, Kruti M ^a   Brucklacher, Robert M ^a   Lull, Malinda E ^a   Erwin, Mandi ^a   Morgan, Drake ^b   Roberts, David C S ^c   Vrana, Kent E ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; Behavior; Functional genomics; Incubation; Medial prefrontal cortex; Nucleus accumbens

Indexed keywords

COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; EARLY GROWTH RESPONSE FACTOR 1; HISTONE H3; NEUROPEPTIDE Y; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COCAINE DEPENDENCE; CONTROLLED STUDY; DRUG WITHDRAWAL; GENE EXPRESSION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ANIMALS; BEHAVIOR, ANIMAL; CHROMATIN; COCAINE-RELATED DISORDERS; EXTINCTION, PSYCHOLOGICAL; GENE EXPRESSION; IMMEDIATE-EARLY PROTEINS; IMMUNOPRECIPITATION; LIMBIC SYSTEM; MALE; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SELF ADMINISTRATION; SUBSTANCE WITHDRAWAL SYNDROME; TRANSCRIPTION, GENETIC;

EID: 45149114766     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301577     Document Type: Article

References (79)

1. Bennett SA, Arnold JM, Chen J, Stenger J, Paul DL, Roberts DC (1999). Long-term changes in connexin32 gap junction protein and mRNA expression following cocaine self-administration in rats. Eur J Neurosci 11: 3329-3338.
2. Bisaga A, Aharonovich E, Garawi F, Levin FR, Rubin E, Raby WN et al (2006). A randomized placebo-controlled trial of gabapentin for cocaine dependence. Drug Alcohol Depend 81: 267-274.
3. Boudreau AC, Wolf ME (2005). Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens. J Neurosci 25: 9144-9151.
4. Bowyer JF, Pogge AR, Delongchamp RR, O'callaghan JP, Patel KM, Vrana KE et al (2007). A threshold neurotoxic amphetamine exposure inhibits parietal cortex expression of synaptic plasticity-related genes. Neuroscience 144: 66-76.
5. Brenz Verca MS, Widmer DA, Wagner GC, Dreyer J (2001). Cocaine-induced expression of the tetraspanin CD81 and its relation to hypothalamic function. Mol Cell Neurosci 17: 303-316.
6. Carlezon Jr WA, Nestler EJ (2002). Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci 25: 610-615.
7. Childress AR, Mozley PD, McElgin W, Fitzgerald J, Reivich M, O'Brien CP (1999). Limbic activation during cue-induced cocaine craving. Am J Psychiatry 156: 11-18.
8. Chomczynski P, Mackey K (1995). Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. Biotechniques 19: 942-945.
9. Dackis CA, Kampman KM, Lynch KG, Pettinati HM, O'Brien CP (2005). A double-blind, placebo-controlled trial of modafinil for cocaine dependence. Neuropsychopharmacology 30: 205-211.
10. Daunais JB, McGinty JF (1995). Cocaine binges differentially alter striatal preprodynorphin and zif/268 mRNAs. Brain Res Mol Brain Res 29: 201-210.
11. Douglass J, McKinzie AA, Couceyro P (1995). PCR differential display identifies a rat brain mRNA that is transcriptionally regulated by cocaine and amphetamine. J Neurosci 15: 2471-2481.
12. Fagergren P, Hurd YL (1999). Mesolimbic gender differences in peptide CART mRNA expression: effects of cocaine. Neuroreport 10: 3449-3452.
13. Fosnaugh JS, Bhat RV, Yamagata K, Worley PF, Baraban JM (1995). Activation of arc, a putative 'effector' immediate early gene, by cocaine in rat brain. J Neurochem 64: 2377-2380.
14. Freeman WM, Brebner K, Lynch WJ, Patel KM, Robertson DJ, Roberts DC et al (2002a). Changes in rat frontal cortex gene expression following chronic cocaine. Brain Res Mol Brain Res 104: 11-20.
15. Freeman WM, Brebner K, Lynch WJ, Robertson DJ, Roberts DC, Vrana KE (2001a). Cocaine-responsive gene expression changes in rat hippocampus. Neuroscience 108: 371-380.
16. Freeman WM, Brebner K, Patel KM, Lynch WJ, Roberts DC, Vrana KE (2002b). Repeated cocaine self-administration causes multiple changes in rat frontal cortex gene expression. Neurochem Res 27: 1181-1192.
17. Freeman WM, Nader MA, Nader SH, Robertson DJ, Gioia L, Mitchell SM et al (2001b). Chronic cocaine-mediated changes in non-human primate nucleus accumbens gene expression. J Neurochem 77: 542-549.
18. Fumagalli F, Bedogni F, Frasca A, Di PL, Racagni G, Riva MA (2006). Corticostriatal up-regulation of activity-regulated cytoskeletal-associated protein expression after repeated exposure to cocaine. Mol Pharmacol 70: 1726-1734.
19. Gawin FH, Kleber HD (1986). Abstinence symptomatology and psychiatric diagnosis in cocaine abusers. Clinical observations Arch Gen Psychiatry 43: 107-113.
20. Ghasemzadeh MB, Nelson LC, Lu XY, Kalivas PW (1999). Neuroadaptations in ionotropic and metabotropic glutamate receptor mRNA produced by cocaine treatment. J Neurochem 72: 157-165.
21. Gossop M, Marsden J, Stewart D, Kidd T (2003). The National Treatment Outcome Research Study (NTORS): 4-5 year follow-up results. Addiction 98: 291-303.
22. Graybiel AM, Moratalla R, Robertson HA (1990). Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc Natl Acad Sci USA 87: 6912-6916.
23. Grimm JW, Hope BT, Wise RA, Shaham Y (2001). Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412: 141-142.
24. Helton TE, Daunais JB, McGinty JF (1993). Convulsant doses of cocaine alter immediate early gene and opioid peptide expression in rat limbic forebrain. Brain Res Mol Brain Res 20: 285-288.
25. Hunter RG, Vicentic A, Rogge G, Kuhar MJ (2005). The effects of cocaine on CART expression in the rat nucleus accumbens: a possible role for corticosterone. Eur J Pharmacol 517: 45-50.
26. Hurd YL, Fagergren P (2000). Human cocaine- and amphetamine-regulated transcript (CART) mRNA is highly expressed in limbic- and sensory-related brain regions. J Comp Neurol 425: 583-598.
27. Jaworski JN, Jones DC (2006). The role of CART in the reward/reinforcing properties of psychostimulants. Peptides 27: 1993-2004.
28. Kalivas PW, McFarland K (2003). Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berl) 168: 44-56.
29. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT et al (2005). Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48: 303-314.
30. Lee JL, Di CP, Thomas KL, Everitt BJ (2005). Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47: 795-801.
31. Lee JL, Milton AL, Everitt BJ (2006). Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J Neurosci 26: 5881-5887.
32. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
33. Lu L, Dempsey J, Shaham Y, Hope BT (2005a). Differential long-term neuroadaptations of glutamate receptors in the basolateral and central amygdala after withdrawal from cocaine self-administration in rats. J Neurochem 94: 161-168.
34. Lu L, Grimm JW, Hope BT, Shaham Y (2004). Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47(Suppl 1): 214-226.
35. Lu L, Grimm JW, Shaham Y, Hope BT (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.
36. Lu L, Hope BT, Dempsey J, Liu SY, Bossert JM, Shaham Y (2005b). Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat Neurosci 8: 212-219.
37. Lu L, Uejima JL, Gray SM, Bossert JM, Shaham Y (2007). Systemic and central amygdala injections of the mGluR(2/3) agonist LY379268 attenuate the expression of incubation of cocaine craving. Biol Psychiatry 61: 591-598.
38. Maley D, Mei J, Lu H, Johnson DL, Ilyin SE (2004). Multiplexed RT-PCR for high throughput screening applications. Comb Chem High Throughput Screen 7: 727-732.
39. Marcellino D, Roberts DC, Navarro G, Filip M, Agnati L, Lluis C et al (2007). Increase in A2A receptors in the nucleus accumbens after extended cocaine self-administration and its disappearance after cocaine withdrawal. Brain Res 1143: 208-220.
40. Marie-Claire C, Laurendeau I, Canestrelli C, Courtin C, Vidaud M, Roques B et al (2003). Fos but not Cart (cocaine and amphetamine regulated transcript) is overexpressed by several drugs of abuse: a comparative study using real-time quantitative polymerase chain reaction in rat brain. Neurosci Lett 345: 77-80.
41. Mateo Y, Lack CM, Morgan D, Roberts DC, Jones SR (2005). Reduced dopamine terminal function and insensitivity to cocaine following cocaine binge self-administration and deprivation. Neuropsychopharmacology 30: 1455-1463.
42. McClung CA, Nestler EJ (2003). Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6: 1208-1215.
43. McCracken CB, Hamby SM, Patel KM, Morgan D, Vrana KE, Roberts DC (2005). Extended cocaine self-administration and deprivation produces region-specific and time-dependent changes in connexin36 expression in rat brain. Synapse 58: 141-150.
44. Moratalla R, Robertson HA, Graybiel AM (1992). Dynamic regulation of NGFI-A (zif268, egr1) gene expression in the striatum. J Neurosci 12: 2609-2622.
45. Morgan D, Brebner K, Lynch WJ, Roberts DC (2002). Increases in the reinforcing efficacy of cocaine after particular histories of reinforcement. Behav Pharmacol 13: 389-396.
46. Morgan D, Liu Y, Roberts DC (2006). Rapid and persistent sensitization to the reinforcing effects of cocaine. Neuropsychopharmacology 31: 121-128.
47. Morgan D, Roberts DC (2004). Sensitization to the reinforcing effects of cocaine following binge-abstinent self-administration. Neurosci Biobehav Rev 27: 803-812.
48. Morgan D, Smith MA, Roberts DC (2005). Binge self-administration and deprivation produces sensitization to the reinforcing effects of cocaine in rats. Psychopharmacology (Berl) 178: 309-316.
49. Mutschler NH, Miczek KA, Hammer Jr RP (2000). Reduction of zif268 messenger RNA expression during prolonged withdrawal following 'binge' cocaine self-administration in rats. Neuroscience 100: 531-538.
50. Nestler EJ (2004). Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol Sci 25: 210-218.
51. O'Brien CP (2005). Anticraving medications for relapse prevention: a possible new class of psychoactive medications. Am J Psychiatry 162: 1423-1431.
52. O'Brien CP (1996). Recent developments in the pharmacotherapy of substance abuse. J Consult Clin Psychol 64: 677-686.
53. O'Brien CP, Childress AR, Ehrman R, Robbins SJ (1998). Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12: 15-22.
54. Paxinos G, Watson C (2004). The Rat Brain in Stereotaxic Coordinates. Elsevier: New York.
55. Rebec GV, Sun W (2005). Neuronal substrates of relapse to cocaine-seeking behavior: role of prefrontal cortex. J Exp Anal Behav 84: 653-666.
56. Risinger RC, Salmeron BJ, Ross TJ, Amen SL, Sanfilipo M, Hoffmann RG et al (2005). Neural correlates of high and craving during cocaine self-administration using BOLD fMRI. Neuroimage 26: 1097-1108.
57. Roberts DC, Brebner K, Vincler M, Lynch WJ (2002). Patterns of cocaine self-administration in rats produced by various access conditions under a discrete trials procedure. Drug Alcohol Depend 67: 291-299.
58. Roberts DC, Goeders NE (1989). Drug self-administration: experimental methods and determinants. In: Boulton AA, Baker GB, Greenshaw AJ (eds). Neuromethods: Psychopharmacology. Clifton, NJ, USA, Humana, pp 349-398.
59. Roh TY, Cuddapah S, Zhao K (2005). Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19: 542-552.
60. Rohsenow DJ, Monti PM, Martin RA, Michalec E, Abrams DB (2000). Brief coping skills treatment for cocaine abuse: 12-month substance use outcomes. J Consult Clin Psychol 68: 515-520.
61. Samaha AN, Mallet N, Ferguson SM, Gonon F, Robinson TE (2004). The rate of cocaine administration alters gene regulation and behavioral plasticity: implications for addiction. J Neurosci 24: 6362-6370.
62. Shaham Y, Hope BT (2005). The role of neuroadaptations in relapse to drug seeking. Nat Neurosci 8: 1437-1439.
63. Sinha R (2001). How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 158: 343-359.
64. Sutton MA, Schmidt EF, Choi KH, Schad CA, Whisler K, Simmons D et al (2003). Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature 421: 70-75.
65. Szumlinski KK, Abernathy KE, Oleson EB, Klugmann M, Lominac KD, He DY et al (2006). Homer isoforms differentially regulate cocaine-induced neuroplasticity. Neuropsychopharmacology 31: 768-777.
66. Taepavarapruk P, Phillips AG (2003). Neurochemical correlates of relapse to d-amphetamine self-administration by rats induced by stimulation of the ventral subiculum. Psychopharmacology (Berl) 168: 99-108.
67. Thiele TE, Badia-Elder NE (2003). A role for neuropeptide Y in alcohol intake control: evidence from human and animal research. Physiol Behav 79: 95-101.
68. Todtenkopf MS, Mihalakopoulos A, Stellar JR (2002). Withdrawal duration differentially affects c-fos expression in the medial prefrontal cortex and discrete subregions of the nucleus accumbens in cocaine-sensitized rats. Neuroscience 114: 1061-1069.
69. Tsankova NM, Kumar A, Nestler EJ (2004). Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci 24: 5603-5610.
70. Valjent E, Aubier B, Corbille AG, Brami-Cherrier K, Caboche J, Topilko P et al (2006). Plasticity-associated gene Krox24/Zif268 is required for long-lasting behavioral effects of cocaine. J Neurosci 26: 4956-4960.
71. Volkow ND, Wang GJ, Ma Y, Fowler JS, Wong C, Ding YS et al (2005). Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J Neurosci 25: 3932-3939.
72. Vorel SR, Liu X, Hayes RJ, Spector JA, Gardner EL (2001). Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292: 1175-1178.
73. Wahlestedt C, Karoum F, Jaskiw G, Wyatt RJ, Larhammar D, Ekman R et al (1991). Cocaine-induced reduction of brain neuropeptide Y synthesis dependent on medial prefrontal cortex. Proc Natl Acad Sci USA 88: 2078-2082.
74. Wallace BC (1989). Psychological and environmental determinants of relapse in crack cocaine smokers. J Subst Abuse Treat 6: 95-106.
75. Ward SJ, Lack C, Morgan D, Roberts DC (2006). Discrete-trials heroin self-administration produces sensitization to the reinforcing effects of cocaine in rats. Psychopharmacology (Berl) 185: 150-159.
76. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al (2004). Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
77. Werme M, Olson L, Brene S (2000). NGFI-B and nor1 mRNAs are upregulated in brain reward pathways by drugs of abuse: different effects in Fischer and Lewis rats. Brain Res Mol Brain Res 76: 18-24.
78. Westwood SC, Hanson GR (1999). Effects of stimulants of abuse on extrapyramidal and limbic neuropeptide Y systems. J Pharmacol Exp Ther 288: 1160-1166.
79. Zetterstrom RH, Williams R, Perlmann T, Olson L (1996). Cellular expression of the immediate early transcription factors Nurr1 and NGFI-B suggests a gene regulatory role in several brain regions including the nigrostriatal dopamine system. Brain Res Mol Brain Res 41: 111-120.