Chronic cocaine-regulated epigenomic changes in mouse nucleus accumbens

Genome Biology

Volumn 15, Issue 4, 2014, Pages

  Feng, Jian ^a   Wilkinson, Matthew ^a   Liu, Xiaochuan ^a   Purushothaman, Immanuel ^a   Ferguson, Deveroux ^a   Vialou, Vincent ^a   Maze, Ian ^a   Shao, Ningyi ^a   Kennedy, Pamela ^a   Koo, JaWook ^a   Dias, Caroline ^a   Laitman, Benjamin ^a   Stockman, Victoria ^a   LaPlant, Quincey ^a   Cahill, Michael E ^a   Nestler, Eric J ^a   Shen, Li ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; GROWTH FACTOR; HISTONE H3; HISTONE H3K27ME3; HISTONE H3K36ME3; HISTONE H3K4ME1; HISTONE H3K4ME3; HISTONE H3K9ME2; HISTONE H3K9ME3; RNA POLYMERASE II; TRANSCRIPTOME; UNCLASSIFIED DRUG; HISTONE; MESSENGER RNA; RBFOX1 PROTEIN, MOUSE; RNA BINDING PROTEIN;

A2BP1 GENE; ACTIN FILAMENT; ADULT; ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CHROMATIN; COCAINE DEPENDENCE; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION REGULATION; HISTONE METHYLATION; HISTONE MODIFICATION; INTRACELLULAR SIGNALING; LONG TERM EXPOSURE; LONG TERM POTENTIATION; MALE; MOLECULAR PATHOLOGY; MOUSE; NERVE CELL PLASTICITY; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEUS ACCUMBENS; PROTEIN PROCESSING; REGULATOR GENE; RNA SEQUENCE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; WNT SIGNALING PATHWAY; ANIMAL; C57BL MOUSE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; METABOLISM;

ALTERNATIVE SPLICING; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; COCAINE; COCAINE-RELATED DISORDERS; EPIGENESIS, GENETIC; HISTONES; MALE; MICE; MICE, INBRED C57BL; NUCLEUS ACCUMBENS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84908499387     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-4-r65     Document Type: Article

References (79)

1. Nestler EJ: Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2001, 2:119-128. 10.1038/35053570.
2. Robison AJ, Nestler EJ: Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 2011, 12:623-637. 10.1038/nrn3111.
3. Day JJ, Sweatt JD: DNA methylation and memory formation. Nat Neurosci 2010, 13:1319-1323. 10.1038/nn.2666.
4. Peixoto L, Abel T: The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 2013, 38:62-76. 10.1038/npp.2012.86.
5. Jonkman S, Kenny PJ: Molecular, Cellular, and Structural Mechanisms of Cocaine Addiction: A Key Role for MicroRNAs. Neuropsychopharmacology 2013, 38:198-211. 10.1038/npp.2012.120.
6. Feng J, Nestler EJ: Epigenetic mechanisms of drug addiction. Curr Opin Neurobiol 2013, 23:521-528. 10.1016/j.conb.2013.01.001.
7. Renthal W, Maze I, Krishnan V, Covington HE, Xiao G, Kumar A, Russo SJ, Graham A, Tsankova N, Kippin TE, Kerstetter KA, Neve RL, Haggarty SJ, McKinsey TA, Bassel-Duby R, Olson EN, Nestler EJ: Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007, 56:517-529. 10.1016/j.neuron.2007.09.032.
8. LaPlant Q, Vialou V, Covington HE, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iniguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolanos CA, Kabbaj M, Xiao G, Neve RL, Hurd YL, Oosting RS, Fan G, Morrison JH, Nestler EJ: Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 2010, 13:1137-1143. 10.1038/nn.2619.
9. Maze I, Covington HE, Dietz DM, LaPlant Q, Renthal W, Russo SJ, Mechanic M, Mouzon E, Neve RL, Haggarty SJ, Ren Y, Sampath SC, Hurd YL, Greengard P, Tarakhovsky A, Schaefer A, Nestler EJ: Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 2010, 327:213-216. 10.1126/science.1179438.
10. Malvaez M, Sanchis-Segura C, Vo D, Lattal KM, Wood MA: Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference. Biol Psychiatry 2010, 67:36-43. 10.1016/j.biopsych.2009.07.032.
11. Kumar A, Choi K-H, Renthal W, Tsankova NM, Theobald DEH, Truong H-T, Russo SJ, LaPlant Q, Sasaki TS, Whistler KN, Neve RL, Self DW, Nestler EJ: Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 2005, 48:303-314. 10.1016/j.neuron.2005.09.023.
12. Kennedy PJ, Feng J, Robison AJ, Maze I, Badimon A, Mouzon E, Chaudhury D, Damez-Werno DM, Haggarty SJ, Han MH, Bassel-Duby R, Olson EN, Nestler EJ: Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 2013, 16:434-440. 10.1038/nn.3354.
13. Renthal W, Kumar A, Xiao G, Wilkinson M, Covington HE, Maze I, Sikder D, Robison AJ, LaPlant Q, Dietz DM, Russo SJ, Vialou V, Chakravarty S, Kodadek TJ, Stack A, Kabbaj M, Nestler EJ: Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 2009, 62:335-348. 10.1016/j.neuron.2009.03.026.
14. Jenuwein T, Allis CD: Translating the histone code. Science 2001, 293:1074-1080. 10.1126/science.1063127.
15. Zhou VW, Goren A, Bernstein BE: Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 2011, 12:7-18.
16. Wang Z, Gerstein M, Snyder M: RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009, 10:57-63. 10.1038/nrg2484.
17. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T: Epigenetics in alternative pre-mRNA splicing. Cell 2011, 144:16-26. 10.1016/j.cell.2010.11.056.
18. Li Q, Lee JA, Black DL: Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 2007, 8:819-831. 10.1038/nrn2237.
19. Park PJ: ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet 2009, 10:669-680.
20. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M: An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. 10.1038/nature11247.
21. Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K: High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837. 10.1016/j.cell.2007.05.009.
22. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111. 10.1093/bioinformatics/btp120.
23. DeLuca DS, Levin JZ, Sivachenko A, Fennell T, Nazaire M-D, Williams C, Reich M, Winckler W, Getz G: RNA-SeQC: RNA-seq metrics for quality control and process optimization. Bioinformatics 2012, 28:1530-1532. 10.1093/bioinformatics/bts196.
24. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-515. 10.1038/nbt.1621.
25. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L: Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7:562-578. 10.1038/nprot.2012.016.
26. Merico D, Isserlin R, Stueker O, Emili A, Bader GD: Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 2010, 5:e13984. 10.1371/journal.pone.0013984.
27. Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
28. Huang DW, Sherman BT, Lempicki RA: Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13. 10.1093/nar/gkn923.
29. Maze I, Nestler EJ: The epigenetic landscape of addiction. Ann N Y Acad Sci 2011, 1216:99-113. 10.1111/j.1749-6632.2010.05893.x.
30. Shen L, Shao N, Liu X, Nestler E: ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 2014, 15:284. 10.1186/1471-2164-15-284.
31. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE: Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560. 10.1038/nature06008.
32. Shen L, Shao N-Y, Liu X, Maze I, Feng J, Nestler EJ: diffReps: detecting differential chromatin modification sites from ChIP-seq data with biological replicates. PLoS One 2013, 8:e65598. 10.1371/journal.pone.0065598.
33. Ingenuity Pathway Analysis [ http://www.ingenuity.com/ ].
34. Andersson R, Enroth S, Rada-Iglesias A, Wadelius C, Komorowski J: Nucleosomes are well positioned in exons and carry characteristic histone modifications. Genome Res 2009, 19:1732-1741. 10.1101/gr.092353.109.
35. Spies N, Nielsen CB, Padgett RA, Burge CB: Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 2009, 36:245-254. 10.1016/j.molcel.2009.10.008.
36. Sims RJ, Millhouse S, Chen CF, Lewis BA, Erdjument-Bromage H, Tempst P, Manley JL, Reinberg D: Recognition of trimethylated histone h3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 2007, 28:665-676. 10.1016/j.molcel.2007.11.010.
37. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T: Regulation of alternative splicing by histone modifications. Science 2010, 327:996-1000. 10.1126/science.1184208.
38. Saint-André V, Batsché E, Rachez C, Muchardt C: Histone H3 lysine 9 trimethylation and HP1γ favor inclusion of alternative exons. Nat Struct Mol Biol 2011, 18:337-344. 10.1038/nsmb.1995.
39. Katz Y, Wang ET, Airoldi EM, Burge CB: Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat Methods 2010, 7:1009-1015. 10.1038/nmeth.1528.
40. Anders S, Reyes A, Huber W: Detecting differential usage of exons from RNA-seq data. Genome Res 2012, 22:2008-2017. 10.1101/gr.133744.111.
41. Chasin LA: Searching for splicing motifs. Adv Exp Med Biol 2007, 623:85-106. 10.1007/978-0-387-77374-2_6.
42. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Noble WS: MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208. 10.1093/nar/gkp335.
43. Zhu H, Hasman RA, Barron VA, Luo G, Lou H: A nuclear function of Hu proteins as neuron-specific alternative RNA processing regulators. Mol Biol Cell 2006, 17:5105-5114. 10.1091/mbc.E06-02-0099.
44. Yano M, Okano HJ, Okano H: Involvement of Hu and heterogeneous nuclear ribonucleoprotein K in neuronal differentiation through p21 mRNA post-transcriptional regulation. J Biol Chem 2005, 280:12690-12699. 10.1074/jbc.M411119200.
45. Merzdorf CS: Emerging roles for zic genes in early development. Dev Dyn 2007, 236:922-940. 10.1002/dvdy.21098.
46. Kuroyanagi H: Fox-1 family of RNA-binding proteins. Cell Mol Life Sci 2009, 66:3895-3907. 10.1007/s00018-009-0120-5.
47. Fujii R, Takumi T: TLS facilitates transport of mRNA encoding an actin-stabilizing protein to dendritic spines. J Cell Sci 2005, 118:5755-5765. 10.1242/jcs.02692.
48. Fujii R, Okabe S, Urushido T, Inoue K, Yoshimura A, Tachibana T, Nishikawa T, Hicks GG, Takumi T: The RNA binding protein TLS is translocated to dendritic spines by mGluR5 activation and regulates spine morphology. Curr Biol 2005, 15:587-593. 10.1016/j.cub.2005.01.058.
49. McClellan KA, Ruzhynsky VA, Douda DN, Vanderluit JL, Ferguson KL, Chen D, Bremner R, Park DS, Leone G, Slack RS: Unique requirement for Rb/E2F3 in neuronal migration: evidence for cell cycle-independent functions. Mol Cell Biol 2007, 27:4825-4843. 10.1128/MCB.02100-06.
50. Chen D, Pacal M, Wenzel P, Knoepfler PS, Leone G, Bremner R: Division and apoptosis of E2f-deficient retinal progenitors. Nature 2009, 462:925-929. 10.1038/nature08544.
51. Ferguson D, Koo JW, Feng J, Heller E, Rabkin J, Heshmati M, Renthal W, Neve R, Liu X, Shao N, Sartorelli V, Shen L, Nestler EJ: Essential role of SIRT1 signaling in the nucleus accumbens in cocaine and morphine action. J Neurosci 2013, 33:16088-16098. 10.1523/JNEUROSCI.1284-13.2013.
52. Davis S, Bozon B, Laroche S: How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav Brain Res 2003, 142:17-30. 10.1016/S0166-4328(02)00421-7.
53. Shibata H, Huynh DP, Pulst SM: A novel protein with RNA-binding motifs interacts with ataxin-2. Hum Mol Genet 2000, 9:1303-1313. 10.1093/hmg/9.9.1303.
54. Bhalla K, Phillips HA, Crawford J, McKenzie OL, Mulley JC, Eyre H, Gardner AE, Kremmidiotis G, Callen DF: The de novo chromosome 16 translocations of two patients with abnormal phenotypes (mental retardation and epilepsy) disrupt the A2BP1 gene. J Hum Genet 2004, 49:308-311.
55. Barnby G, Abbott A, Sykes N, Morris A, Weeks DE, Mott R, Lamb J, Bailey AJ, Monaco AP: Candidate-gene screening and association analysis at the autism-susceptibility locus on chromosome 16p: evidence of association at GRIN2A and ABAT. Am J Hum Genet 2005, 76:950-966. 10.1086/430454.
56. Martin CL, Duvall JA, Ilkin Y, Simon JS, Arreaza MG, Wilkes K, Alvarez-Retuerto A, Whichello A, Powell CM, Rao K: Cytogenetic and molecular characterization of A2BP1/FOX1 as a candidate gene for autism. Am J Med Genet B Neuropsychiatr Genet 2007, 144:869-876.
57. Sebat J, Lakshmi B, Malhotra D, Troge J, Lese-Martin C, Walsh T, Yamrom B, Yoon S, Krasnitz A, Kendall J, Leotta A, Pai D, Zhang R, Lee Y-H, Hicks J, Spence SJ, Lee AT, Puura K, Lehtimäki T, Ledbetter D, Gregersen PK, Bregman J, Sutcliffe JS, Jobanputra V, Chung W, Warburton D, King M-C, Skuse D, Geschwind DH, Gilliam TC, et al.: Strong association of de novo copy number mutations with autism. Science 2007, 316:445-449. 10.1126/science.1138659.
58. Gehman LT, Stoilov P, Maguire J, Damianov A, Lin CH, Shiue L, Ares M Jr, Mody I, Black DL: The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet 2011, 43:706-711. 10.1038/ng.841.
59. Amir-Zilberstein L, Blechman J, Sztainberg Y, Norton WH, Reuveny A, Borodovsky N, Tahor M, Bonkowsky JL, Bally-Cuif L, Chen A, Levkowitz G: Homeodomain protein otp and activity-dependent splicing modulate neuronal adaptation to stress. Neuron 2012, 73:279-291. 10.1016/j.neuron.2011.11.019.
60. Lee JA, Tang ZZ, Black DL: An inducible change in Fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons. Genes Dev 2009, 23:2284-2293. 10.1101/gad.1837009.
61. Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, Mill J, Cantor RM, Blencowe BJ, Geschwind DH: Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 2011, 474:380-384. 10.1038/nature10110.
62. Grant CE, Bailey TL, Noble WS: FIMO: scanning for occurrences of a given motif. Bioinformatics 2011, 27:1017-1018. 10.1093/bioinformatics/btr064.
63. Licatalosi DD, Darnell RB: Splicing regulation in neurologic disease. Neuron 2006, 52:93-101. 10.1016/j.neuron.2006.09.017.
64. Ranum LP, Cooper TA: RNA-mediated neuromuscular disorders. Annu Rev Neurosci 2006, 29:259-277. 10.1146/annurev.neuro.29.051605.113014.
65. Hishimoto A, Liu QR, Drgon T, Pletnikova O, Walther D, Zhu XG, Troncoso JC, Uhl GR: Neurexin 3 polymorphisms are associated with alcohol dependence and altered expression of specific isoforms. Hum Mol Genet 2007, 16:2880-2891. 10.1093/hmg/ddm247.
66. Mains RE, Kiraly DD, Eipper-Mains JE, Ma XM, Eipper BA: Kalrn promoter usage and isoform expression respond to chronic cocaine exposure. BMC Neurosci 2011, 12:20. 10.1186/1471-2202-12-20.
67. Moyer RA, Wang D, Papp AC, Smith RM, Duque L, Mash DC, Sadee W: Intronic polymorphisms affecting alternative splicing of human dopamine D2 receptor are associated with cocaine abuse. Neuropsychopharmacology 2011, 36:753-762. 10.1038/npp.2010.208.
68. Schor IE, Rascovan N, Pelisch F, Allo M, Kornblihtt AR: Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing. Proc Natl Acad Sci U S A 2009, 106:4325-4330. 10.1073/pnas.0810666106.
69. Fogel BL, Wexler E, Wahnich A, Friedrich T, Vijayendran C, Gao FY, Parikshak N, Konopka G, Geschwind DH: RBFOX1 regulates both splicing and transcriptional networks in human neuronal development. Hum Mol Genet 2012, 21:4171-4186. 10.1093/hmg/dds240.
70. Lee AY, Chen W, Stippec S, Self J, Yang F, Ding XJ, Chen S, Juang YC, Cobb MH: Protein kinase WNK3 regulates the neuronal splicing factor Fox-1. Proc Natl Acad Sci U S A 2012, 109:16841-16846. 10.1073/pnas.1215406109.
71. Marques F, Sousa J, Coppola G, Gao F, Puga R, Brentani H, Geschwind D, Sousa N, Correia-Neves M, Palha J: Transcriptome signature of the adult mouse choroid plexus. Fluids Barriers CNS 2011, 8:10. 10.1186/2045-8118-8-10.
72. Li X, Buxbaum J: Transthyretin and the brain re-visited: Is neuronal synthesis of transthyretin protective in Alzheimer's disease? Mol Neurodegener 2011, 6:79. 10.1186/1750-1326-6-79.
73. Hovatta I, Zapala M, Broide R, Schadt E, Libiger O, Schork N, Lockhart D, Barlow C: DNA variation and brain region-specific expression profiles exhibit different relationships between inbred mouse strains: implications for eQTL mapping studies. Genome Biol 2007, 8:R25. 10.1186/gb-2007-8-2-r25.
74. Bowyer J, Patterson T, Saini U, Hanig J, Thomas M, Camacho L, George N, Chen J: Comparison of the global gene expression of choroid plexus and meninges and associated vasculature under control conditions and after pronounced hyperthermia or amphetamine toxicity. BMC Genomics 2013, 14:147. 10.1186/1471-2164-14-147.
75. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, Li W, Liu XS: Model-based Analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:9.
76. Ohnishi YN, Ohnishi YH, Hokama M, Nomaru H, Yamazaki K, Tominaga Y, Sakumi K, Nestler EJ, Nakabeppu Y: FosB is essential for the enhancement of stress tolerance and antagonizes locomotor sensitization by DeltaFosB. Biol Psychiatry 2011, 70:487-495. 10.1016/j.biopsych.2011.04.021.
77. Vialou V, Robison AJ, LaPlant QC, Covington HE III, Dietz DM, Ohnishi YN, Mouzon E, Rush AJ III, Watts EL, Wallace DL: [Delta] FosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nat Neurosci 2010, 13:745-752. 10.1038/nn.2551.
78. Benjamini Y, Hochberg Y: Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B-Method 1995, 57:289-300.
79. Jensen ST, Liu JS: Bayesian clustering of transcription factor binding motifs. J Am Stat Assoc 2008, 103:188-200. 10.1198/016214507000000365.