DNA methylation in the medial prefrontal cortex regulates alcohol-induced behavior and plasticity

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 6153-6164

  Barbier, Estelle ^a   Tapocik, Jenica D ^b   Juergens, Nathan ^b   Pitcairn, Caleb ^b   Borich, Abbey ^b   Schank, Jesse R ^b   Sun, Hui ^b   Schuebel, Kornel ^b   Zhou, Zhifeng ^b   Yuan, Qiaoping ^b   Vendruscolo, Leandro F ^c   Goldman, David ^b   Heilig, Markus ^a,b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Alcoholism; DNA methylation; DNMT; Epigenetics; Neurotransmitter release; Plasticity

Indexed keywords

LENTIVIRUS VECTOR; NEUROTRANSMITTER; SYNAPTOTAGMIN II; TRANSCRIPTOME; ALCOHOL; ENZYME INHIBITOR; METHYLTRANSFERASE; N PHTHALOYLTRYPTOPHAN; NERVE PROTEIN; PHTHALIMIDE DERIVATIVE; SYT2 PROTEIN, RAT; TRYPTOPHAN;

ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA ISOLATION; DNA METHYLATION; DOWN REGULATION; GAS CHROMATOGRAPHY; GENE EXPRESSION; GENE SEQUENCE; IMMUNOHISTOCHEMISTRY; MALE; MEDIAL PREFRONTAL CORTEX; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; DECISION MAKING; DISEASE MODEL; DRUG EFFECTS; DRUG SELF ADMINISTRATION; GENE EXPRESSION PROFILING; GENETIC TRANSDUCTION; GENETICS; INSTRUMENTAL CONDITIONING; METABOLISM; NONPARAMETRIC TEST; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; WISTAR RAT;

ALCOHOLISM; ANIMALS; CHOICE BEHAVIOR; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; DNA METHYLATION; ENZYME INHIBITORS; ETHANOL; GENE EXPRESSION PROFILING; MALE; METHYLTRANSFERASES; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; PHTHALIMIDES; PREFRONTAL CORTEX; RATS; RATS, WISTAR; SELF ADMINISTRATION; STATISTICS, NONPARAMETRIC; SYNAPTOTAGMIN II; TRANSDUCTION, GENETIC; TRYPTOPHAN;

EID: 84929251128     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4571-14.2015     Document Type: Article

References (40)

1. Agudelo M, Gandhi N, Saiyed Z, Pichili V, Thangavel S, Khatavkar P, Yndart-Arias A, Nair M (2011) Effects of alcohol on histone deacetylase 2 (HDAC2) and the neuroprotective role of trichostatin A (TSA). Alcohol Clin Exp Res 35:1550-1556. CrossRef Medline
2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. CrossRef Medline
3. Björk K, Saarikoski ST, Arlinde C, Kovanen L, Osei-Hyiaman D, Ubaldi M, Reimers M, Hyytiä P, Heilig M, Sommer WH (2006) Glutathione-S-transferase expression in the brain: possible role in ethanol preference and longevity. FASEB J 20:1826-1835. CrossRef Medline
4. Brenet F, Moh M, Funk P, Feierstein E, Viale AJ, Socci ND, Scandura JM (2011) DNA methylation of the first exon is tightly linked to transcriptional silencing. PLoS One 6:el4524. CrossRef Medline
5. Brueckner B, Garcia Boy R, Siedlecki P, Musch T, Kliem HC, Zielenkiewicz P, Suhai S, Wiessler M, Lyko F (2005) Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases. Cancer Res 65:6305-6311. CrossRef Medline
6. Chapman ER (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77:615-641. CrossRef Medline
7. Cippitelli A, Karlsson C, Shaw JL, Thorsell A, Gehlert DR, Heilig M (2010) Suppression of alcohol self-administration and reinstatement of alcohol seeking by melanin-concentrating hormone receptor 1 (MCH1-R) antagonism in Wistar rats. Psychopharmacology (Berl) 211:367-375. CrossRef Medline
8. Dayas CV, Liu X, Simms JA, Weiss F (2007) Distinct patterns of neural activation associated with ethanol seeking: effects of naltrexone. Biol Psychiatry 61:979-989. CrossRef Medline
9. Fandy TE (2009) Development of DNA methyltransferase inhibitors for the treatment of neoplastic diseases. Curr Med Chem 16:2075-2085. CrossRef Medline
10. Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, Silva AJ, Fan G (2010) Dnmtl and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 13:423-430. CrossRef Medline
11. Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, Gil L, Gordon L, Hendrix M, Hourlier T, Johnson N, Kähäri AK, Keefe D, Keenan S, Kinsella R, Komorowska M, et al. (2012) Ensembl 2012. Nucleic Acids Res 40: D84-D90. CrossRef Medline
12. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80. CrossRef Medline
13. Heilig M, Egli M, Crabbe JC, Becker HC (2010) Acute withdrawal, protracted abstinence and negative affect in alcoholism: are they linked? Addict Biol 15:169-184. CrossRef Medline
14. Iwamoto K, Bundo M, Ueda J, Oldham MC, Ukai W, Hashimoto E, Saito T, Geschwind DH, Kato T (2011) Neurons show distinctive DNA methylation profile and higher interindividual variations compared with nonneurons. Genome Res 21:688-696. CrossRef Medline
15. Kalivas PW (2008) Addiction as a pathology in prefirontal cortical regulation of corticostriatal habit circuitry. NeurotoxRes 14:185-189. CrossRef Medline
16. Koros E, Kostowski W, Bienkowski P (1999) Operant responding for ethanol in rats with a long-term history of free-choice ethanol drinking. Alcohol Alcohol 34:685-689. CrossRef Medline
17. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. CrossRef Medline
18. LaPlant Q, Vialou V, Covington HE 3rd, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iñiguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolaños CA, Kabbaj M, et al. (2010) Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13:1137—1143. CrossRef Medline
19. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmühl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OF, Spengler D (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12:1559-1566. CrossRef Medline
20. Pandey SC, Ugale R, Zhang H, Tang L, Prakash A (2008) Brain chromatin remodeling: a novel mechanism of alcoholism. J Neurosci 28:3729-3737. CrossRef Medline
21. Rimondini R, Arlinde C, Sommer W, Heilig M (2002) Long-lasting increase in voluntary ethanol consumption and transcriptional regulation in the rat brain after intermittent exposure to alcohol. FASEB J 16:27-35. CrossRef Medline
22. Sakharkar AJ, Zhang H, Tang L, Shi G, Pandey SC (2012) Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol. Alcohol Clin Exp Res 36:61-71. CrossRef Medline
23. Sakharkar AJ, Zhang H, Tang L, Baxstrom K, Shi G, Moonat S, Pandey SC (2012) Effects of histone deacetylase inhibitors on amygdaloid histone acetylation and neuropeptide Y expression: a role in anxiety-like and alcohol-drinking behaviours. Int J Neuropsychopharmacol 17:1207-1220. CrossRef Medline
24. Smyth GK (2005) Limma: linear models for microarray data. In: Bioinformatics and computational biology solutions using R and bioconductor. Springer: New York.
25. Tabakoff B, Cornell N, Hoffman PL (1986) Alcohol tolerance. Ann Emerg Med 15:1005-1012. CrossRef Medline
26. Tapocik JD, Solomon M, Flanigan M, Meinhardt M, Barbier E, Schank JR, Schwandt M, Sommer WH, Heilig M (2012) Coordinated dysregulation of mRNAs and microRNAs in the rat medial prefrontal cortex following a history of alcohol dependence. Pharmacogenomics J 13: 286-296. CrossRef Medline
27. Tapocik JD, Barbier E, Flanigan M, Solomon M, Pincus A, Pilling A, Sun H, Schank JR, King C, Heilig M (2014) microRNA-206 in rat medial prefrontal cortex regulates BDNF expression and alcohol drinking. J Neurosci 34:4581-4588. CrossRef Medline
28. Tian W, Zhao M, Li M, Song T, Zhang M, Quan L, Li S, Sun ZS (2012) Reversal of cocaine-conditioned place preference through methyl supplementation in mice: altering global DNA methylation in the prefrontal cortex. PLoS One 7:e33435. CrossRef Medline
29. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111. CrossRef Medline
30. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562-578. CrossRef Medline
31. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121. CrossRef Medline
32. Tzschentke TM (2000) The medial prefrontal cortex as a part of the brain reward system. Amino Acids 19:211-219. CrossRef Medline
33. Umylny BWSJ (2012) Beyond the pipelines: Clous computing facilitates management, distribution, security and analysis of high speed sequencer data. In: Tag-based next generation sequencing (Harbers M, Kahl G, eds). Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany.
34. Varodayan FP, Pignataro L, Harrison NL (2011) Alcohol induces synaptotagmin 1 expression in neurons via activation of heat shock factor 1. Neuroscience 193:63-71. CrossRef Medline
35. Vendruscolo LF, Barbier E, Schlosburg JE, Misra KK, Whitfield TW Jr, Logrip ML, Rivier C, Repunte-Canonigo V, Zorrilla EP, Sanna PP, Heilig M, Koob GF (2012) Corticosteroid-dependent plasticity mediates compulsive alcohol drinking in rats. J Neurosci 32:7563-7571. CrossRef Medline
36. Warnault V, Darcq E, Levine A, Barak S, Ron D (2013) Chromatin remodeling: a novel strategy to control excessive alcohol drinking. Transl Psychiatry 3:e231. CrossRef Medline
37. Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854. CrossRef Medline
38. Wong CC, Mill J, Fernandes C (2011) Drugs and addiction: an introduction to epigenetics. Addiction 106:480-489. CrossRef Medline
39. Worst TJ, Tan JC, Robertson DJ, Freeman WM, Hyytia P, Kiianmaa K, Vrana KE (2005) Transcrip tome analysis of frontal cortex in alcoholpreferring and nonpreferring rats. J Neurosci Res 80:529-538. CrossRef Medline
40. Wu H, Zhang Y (2014) Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156:45-68. CrossRef Medline