Skip to main content Accessibility help

Epigenetic regulation of cognition: A circumscribed review of the field

  • Elena L. Grigorenko (a1) (a2) (a3) (a4), Sergey A. Kornilov (a1) (a2) (a3) and Oksana Yu. Naumova (a2) (a3)

The last decade has been marked by an increased interest in relating epigenetic mechanisms to complex human behaviors, although this interest has not been balanced, accentuating various types of affective and primarily ignoring cognitive functioning. Recent animal model data support the view that epigenetic processes play a role in learning and memory consolidation and help transmit acquired memories even across generations. In this review, we provide an overview of various types of epigenetic mechanisms in the brain (DNA methylation, histone modification, and noncoding RNA action) and discuss their impact proximally on gene transcription, protein synthesis, and synaptic plasticity and distally on learning, memory, and other cognitive functions. Of particular importance are observations that neuronal activation regulates the dynamics of the epigenome's functioning under precise timing, with subsequent alterations in the gene expression profile. In turn, epigenetic regulation impacts neuronal action, closing the circle and substantiating the signaling pathways that underlie, at least partially, learning, memory, and other cognitive processes.

Corresponding author
Address correspondence and reprint requests to: Elena L. Grigorenko, University of Houston, Texas Institute for Measurement, Evaluation, and Statistics/Center for Advanced Computing & Data Systems, 4849 Calhoun Road, Houston, TX 77024; E-mail:
Hide All
Adkins, R. M., Krushkal, J., Tylavsky, F. A., & Thomas, F. (2011). Racial differences in gene-specific DNA methylation levels are present at birth. Birth Defects Research: Part A, Clinical and Molecular Teratology, 91, 728736.
Alarcon, J. M., Malleret, G., Touzani, K., Vronskaya, S., Ishii, S., Kandel, E. R., et al. (2004). Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: A model for the cognitive deficit in Rubinstein–Taybi syndrome and its amelioration. Neuron, 42, 947959.
Allis, C. D., Berger, S. L., Cote, J., Dent, S., Jenuwein, T., Kouzarides, T., et al. (2007). New nomenclature for chromatin-modifying enzymes Cell, 131, 633636.
Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U., & Zoghbi, H. Y. (1999). Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nature Genetics, 23, 185188.
Azevedo, F. A. C., Carvalho, L. R. B., Grinberg, L. T., Farfel, J. M., Ferretti, R. E. L., Leite, R. E. P., et al. (2009). Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. Journal of Comparative Neurology, 51, 532541.
Badeaux, A. I., & Shi, Y. (2013). Emerging roles for chromatin as a signal integration and storage platform. Nature Reviews Molecular Cell Biology, 14, 211224.
Bahari-Javan, S., Maddalena, A., Kerimoglu, C., Wittnam, J., Held, T., Bähr, M., et al. (2012). HDAC1 regulates fear extinction in mice. Journal of Neuroscience, 32, 50625073.
Bannister, A. J., & Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Research, 21, 381395.
Bardai, F. H., Price, V., Zaayman, M., Wang, L., & D'Mello, S. R. (2012). Histone deacetylase-1 (HDAC1) is a molecular switch between neuronal survival and death. Journal of Biological Chemistry, 287, 3544435453.
Barrett, R. M., Malvaez, M., Kramar, E., Matheos, D. P., Arrizon, A., Cabrera, S. M., et al. (2011). Hippocampal focal knockout of CBP affects specific histone modifications, long-term potentiation, and long-term memory. Neuropsychopharmacology, 36, 15451556.
Bartolomei, M. S., Webber, A. L., Brunkow, M. E., & Tilghman, S. M. (1993). Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes and Development, 7, 16631673.
Bates, E. A., Victor, M., Jones, A. K., Shi, Y., & Hart, A. C. (2006). Differential contributions of Caenorhabditis elegans histone deacetylases to huntingtin polyglutamine toxicity. Journal of Neuroscience, 26, 28302838.
Bekinschtein, P., Cammarota, M., Katche, C., Slipczuk, L., Rossato, J. I., Goldin, A., et al. (2008). BDNF is essential to promote persistence of long-term memory storage. Proceedings of the National Academy of Sciences, 105, 27112716.
Bird, A. P. (1980). DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Research, 8, 14991504.
Bird, A. P. (1986). CpG-rich islands and the function of DNA methylation. Nature, 321, 209213.
Bird, A. P. (2002). DNA methylation patterns and epigenetic memory. Genes and Development, 16, 621.
Bird, A. P. (2007). Perceptions of epigenetics. Nature, 447, 396398.
Bird, A. P., & Wolffe, A. P. (1999). Methylation-induced repression: Belts, braces, and chromatin. Cell, 99, 451454.
Bonn, S., Zinzen, R. P., Girardot, C., Gustafson, E. H., Gonzalez, A. P., Delhomme, N., et al. (2012) Tissue specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nature Genetics, 44, 148156.
Bordone, L., & Guarente, L. (2005). Calorie restriction, SIRT1 and metabolism: Understanding longevity. Nature Reviews Molecular Cell Biology, 6, 298305.
Boulle, F., van den Hove, D. L. A., Jakob, S. B., Rutten, B. P., Hamon, M., van Os, J., et al. (2012). Epigenetic regulation of the BDNF gene: Implications for psychiatric disorders. Molecular Psychiatry, 17, 584596.
Boyce, W. T., & Kobor, M. S. (2015). Development and the epigenome: The “synapse” of gene–environment interplay. Developmental Science, 18, 123.
Bradbury, J. (2003). Human epigenome project-up and running. PLOS Biology, 1, E82.
Broide, R. S., Redwine, J. M., Aftahi, N., Young, W., Bloom, F. E., & Winrow, C. J. (2007). Distribution of histone deacetylases 1–11 in the rat brain. Journal of Molecular Neuroscience, 31, 4758.
Brownell, J. E., & Allis, C. D. (1996). Special HATs for special occasions: Linking histoneacetylation to chromatin assembly and gene activation. Current Opinion in Genetics and Development, 6, 176184.
Bruck, I., Philippart, M., Giraldi, D., & Antoniuk, S. (1991). Difference in early development of presumed monozygotic twins with Rett syndrome. American Journal of Medical Genetics, 39, 415417.
Buck, M. J., & Lieb, J. D. (2004). ChIP-chip: Considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments. Genomics, 83, 349360.
Castel, S. E., & Martienssen, R. A. (2013). RNA interference in the nucleus: Roles for small RNAs in transcription, epigenetics and beyond. Nature Reviews Genetics, 14, 100112.
Cawley, S., Bekiranov, S., Ng, H. H., Kaparonov, P., Sekinger, E. A., Kampa, D., et al. (2004). Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell, 116, 499509.
Cervoni, N., & Szyf, M. (2001). Demethylase activity is directed by histone acetylation. Journal of Biological Chemistry, 276, 4077840787.
Chahrour, M., Jung, S. Y., Shaw, C., Zhou, X., Wong, S. T. C., Qin, J., et al. (2008). MeCP2, a key contributor to neurological disease, activates and represses transcription. Science, 320, 12241229.
Chahrour, M., & Zoghbi, H. Y. (2007). The story of Rett syndrome: From clinic to neurobiology. Neuron, 56, 422437.
Chan, H. M., & La Thangue, N. B. (2001). p300/CBP proteins: HATs for transcriptional bridges and scaffolds. Journal of Cell Science, 114, 23632373.
Chen, C. M., Chen, H. L., Hsiau, T. H., Shi, H., Brock, G. J., Wei, S. H., et al. (2003). Methylation target array for rapid analysis of CpG island hypermethylation in multiple tissue genomes. American Journal of Pathology, 163, 3745.
Chen, G., Zou, X., Watanabe, H., van Deursen, J. M., & Shen, J. (2010). CREB binding protein is required for both short-term and long-term memory formation. Journal of Neuroscience, 30, 1306613070.
Chen, W. G., Chang, Q., Lin, Y., Meissner, A., West, A. E., Griffith, E. C., et al. (2003). Depression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science, 302, 885889.
Choi, D. C., Maguschak, K. A., Ye, K., Jang, S.-W., Myers, K. M., & Ressler, K. J. (2010). Prelimbic cortical BDNF is required for memory of learned fear but not extinction or innate fear. Proceedings of the National Academy of Sciences, 107, 26752680.
Chuang, J. C., & Jones, P. A. (2007). Epigenetics and microRNAs. Pediatric Research, 61, 24R29R.
Cong, S. Y., Pepers, B. A., Evert, B. O., Rubinsztein, D. C., Roos, R. A., van Ommen, G. J., et al. (2005). Mutant huntingtin represses CBP, but not p300, by binding and protein degradation. Molecular and Cellular Neuroscience, 30, 560571.
Cougot, N., Bhattacharyya, S. N., Tapia-Arancibia, L., Bordonné, R., Filipowicz, W., Bertrand, E., et al. (2008). Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. Journal of Neuroscience, 28, 1379313804.
Cowansage, K. K., LeDoux, J. E., & Monfils, M. H. (2010). Brain-derived neurotrophic factor: A dynamic gatekeeper of neural plasticity. Current Molecular Pharmacology, 3, 1229.
Crick, F. (1984). Memory and molecular turnover. Nature, 312, 101.
Crosio, C., Heitz, E., Allis, C. D., Borrelli, E., & Sassone-Corsi, P. (2003). Chromatin remodeling and neuronal response: Multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. Journal of Cell Science, 116, 49054914.
Czyz, W., Morahan, J. M., Ebers, G. C., & Ramagopalan, S. V. (2012). Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences. BMC Medicine, 10, 93.
Dash, P. K., Moore, A. N., Kobori, N., & Runyan, J. D. (2007). Molecular activity underlying working memory. Learning and Memory, 14, 554563.
Davies, M. N., Volta, M., Pidsley, R., Lunnon, K., Dixit, A., Lovestone, S., et al. (2012). Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biology, 13, R43.
Davis, H. P., & Squire, L. R. (1984). Protein synthesis and memory: A review. Psychological Bulletin, 96, 518559.
Day, J. J., & Sweatt, J. D. (2010). DNA methylation and memory formation. Nature Neuroscience, 13, 13191323.
Day, J. K., Bauer, A. M., desBordes, C., Zhuang, Y., Kim, B.-E., Newton, L. G., et al. (2002). Genistein alters methylation patterns in mice. Journal of Nutrition, 132, 2419S2423S.
Deaton, A. M., & Bird, A. (2011). CpG islands and the regulation of transcription. Genes and Development, 25, 10101022.
de Ruijter, A. J., van Gennip, A. H., Caron, H. N., Kemp, S., & van Kuilenburg, A. B. (2003). Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochemical Journal, 370, 737749.
Duncan, B. K., & Miller, J. H. (1980). Mutagenic deamination of cytosine residues in DNA. Nature, 287, 560561.
Esteller, M. (2008). Epigenetics in evolution and disease. Lancet, 372, S90S96.
Fan, G., Beard, C., Chen, R. Z., Csankovszki, G., Sun, Y., Siniaia, M., et al. (2001). DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. Journal of Neuroscience, 21, 788797.
Fatica, A., & Bozzoni, I. (2013). Long non-coding RNAs: New players in cell differentiation and development. Nature Reviews Genetics, 15, 721.
Fazzari, M. J., & Greally, J. M. (2004). Epigenomics: Beyond CpG islands. Nature Reviews Genetics, 5, 446455.
Federman, N., Fustiñana, M. S., & Romano, A. (2009). Histone acetylation is recruited in consolidation as a molecular feature of stronger memories. Learning and Memory, 16, 600606.
Feinberg, A. P. (2001). Methylation meets genomics. Nature Genetics, 27, 910.
Feinberg, A. P. (2011). Genome-scale approaches to the epigenetics of common human disease. Disease, 456, 1321.
Feng, J., Zhou, Y., Campbell, S. L., Le, T., Li, E., Sweatt, J. D., et al. (2010). Dnmt1 and Dnmt3a are required for the maintenance of DNA methylation and synaptic function in adult forebrain neurons. Nature Neuroscience, 13, 423430.
Fischer, A. (2014). Epigenetic memory: The Lamarckian brain. EMBO Journal, 33, 945967.
Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., & Tsai, L. H. (2007). Recovery of learning and memory after neuronal loss is associated with chromatin remodeling. Nature, 447, 178182.
Flexner, J. B., Flexner, L. B., & Stellar, E. (1963). Memory in mice as affected by intracerebral puromycin. Science, 141, 5759.
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., et al. (2005). Epigenetic differences arise during the lifetime of monozygotic twins. Proceeding of the National Academy of Sciences, 102, 1060410609.
Fraser, H. B., Lam, L. L., Neumann, S. M., & Kobor, M. S. (2012). Population-specificity of human DNA methylation. Genome Biology, 13, R8.
Frigola, J., Ribas, M., Risques, R. A., & Peinado, M. A. (2002). Methylome profiling of cancer cells by amplification of intermethylated sites (AIMS). Nucleic Acids Research, 30, e28.
Gao, J., Wang, W. Y., Mao, Y. W., Gräff, J., Guan, J. S., Pan, L., et al. (2010). A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature, 466, 11051109.
Goate, A., & Hardy, J. (2012). Twenty years of Alzheimer's disease-causing mutations. Journal of Neurochemisty, 120, 38.
Gräff, J., Kim, D., Dobbin, M. M., & Tsai, L. H. (2011). Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiological Reviews, 91, 603649.
Gräff, J., & Mansuy, I. M. (2008). Epigenetic codes in cognition and behaviour. Behavioural Brain Research, 192, 7087.
Gräff, J., Rei, D., Guan, J.-S., Wang, W.-Y., Seo, J., Hennig, K. M., et al. (2012). An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature, 483, 222226.
Gräff, J., & Tsai, L. H. (2013). Histone acetylation: Molecular mnemonics on the chromatin. Nature Reviews Neuroscience, 14, 97111.
Gregoretti, I. V., Lee, Y. M., & Goodson, H. V. (2004). Molecular evolution of the histone deacetylase family: Functional implications of phylogenetic analysis. Journal of Molecular Biology, 338, 1731.
Grewal, S. I., & Moazed, D. (2003). Heterochromatin and epigenetic control of gene expression. Science, 301, 798802.
Guan, J.-S., Haggarty, S. J., Giacometti, E., Dannenberg, J.-H., Joseph, N., Gao, J., et al. (2009). HDAC2 negatively regulates memory formation and synaptic plasticity. Nature, 459, 5560.
Guan, J.-S., Xie, H., & Ding, X. (2015). The role of epigenetic regulation in learning and memory. Experimental Neurology, 268, 3036.
Guan, Z., Giustetto, M., Lomvardas, S., Kim, J.-H., Miniaci, M. C., Schwartz, J. H., et al. (2002). Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell, 111, 483493.
Gupta, S., Kim, S. Y., Artis, S., Molfese, D. L., Schumacher, A., Sweatt, J. D., et al. (2010). Histone methylation regulates memory formation. Journal of Neuroscience, 30, 35893599.
Gupta-Agarwal, S., Franklin, A. V., Deramus, T., Wheelock, M., Davis, R. L., McMahon, L. L., et al. (2012). G9a/GLP histone lysine dimethyltransferase complex activity in the hippocampus and the entorhinal cortex is required for gene activation and silencing during memory consolidation. Journal of Neuroscience, 32, 54405453.
Haass, C., & Selkoe, D. J. (2007). Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer's amyloid beta-peptide. Nature Reviews Molecular Cell Biology, 8, 112116.
Haberland, M., Montgomery, R. L., & Olson, E. N. (2009). The many roles of histone deacetylases in development and physiology: Implications for disease and therapy. Nature Reviews Genetics, 10, 3242.
Hagberg, B., Aicardi, J., Dias, K., & Ramos, O. (1983). A progressive syndrome of autism, dementia, ataxia, and loss of purposeful hand use in girls: Rett's syndrome: Report of 35 cases. Annals of Neurology, 14, 471479.
Haigis, M. C., & Sinclair, D. A. (2010). Mammalian sirtuins: Biological insights and disease relevance. Annual Review of Pathology, 5, 253295.
Harshman, S. W., Young, N. L., Parthun, M. R., & Freiras, M. A. (2013). H1 histones: Current perspectives and challenges. Nucleic Acids Research, 41, 95939609.
Hart, A. K., Fioravante, D., Liu, R. Y., Phares, G. A., Cleary, L. J., & Byrne, J. H. (2011). Serotonin-mediated synapsin expression is necessary for long-term facilitation of the Aplysia sensorimotor synapse. Journal of Neuroscience, 31, 1840118411.
Hatchwell, E., & Greally, J. M. (2007). The potential role of epigenomic dysregulation in complex human disease. Trends in Genetics, 23, 588595.
He, L., & Hannon, G. J. (2004). MicroRNAs: Small RNAs with a big role in gene regulation. Nature Reviews Genetics, 5, 522531.
Heyn, H., Moran, S., Hernando-Herraez, I., Sayols, S., Gomez, A., Sandoval, J., et al. (2013). DNA methylation contributes to natural human variation. Genome Research, 23, 13631372.
Heyward, F. D., & Sweatt, J. D. (2015). DNA methylation in memory formation: Emerging insights. Neuroscientist. Advance online publication.
Holliday, R. (1990). DNA methylation and epigenetic inheritance. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences, 326, 329338.
Holliday, R. (1999). Is there an epigenetic component in long-term memory? Journal of Theoretical Biology, 200, 339341.
Holliday, R., & Pugh, J. E. (1975). DNA modification mechanisms and gene activity during development. Science, 187, 226232.
Hong, E. J., West, A. E., & Greenberg, M. E. (2005). Transcriptional control of cognitive development. Current Opinion in Neurobiology, 15, 2128.
Horvath, S., Zhang, , Langfelder, P., Kahn, R. S., Boks, M. P., van Ekijk, K., et al. (2012). Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biology, 13, R97.
Huang, T. H., Perry, M. R., & Laux, D. E. (1999). Methylation profiling of CpG islands in human breast cancer cells. Human Molecular Genetics, 8, 459470.
Im, H. I., Hollander, J. A., Bali, P., & Kenny, P. J. (2010). MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nature Neuroscience, 13, 11201127.
Im, H. I., & Kenny, P. J. (2012). MicroRNAs in neuronal function and dysfunction. Trends in Neuroscience, 35, 325334.
Imhof, A. (2006). Epigenetic regulators and histone modification. Briefings in Functional Genomics and Proteomics, 5, 222227.
Jablonka, E., & Lamb, M. J. (2002). The changing concept of epigenetics. Annals of the New York Academy of Sciences, 981, 8296.
Jaenisch, R., & Bird, A. (2003). Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nature Genetics, 33, 245254.
Jiang, H., Poirier, M. A., Liang, Y., Pei, Z., Weiskittel, C. E., Smith, W. W., et al. (2006). Depletion of CBP is directly linked with cellular toxicity caused by mutant huntingtin. Neurobiology of Disease, 23, 543551.
Jiang, Y., Langley, B., Lubin, F. D., Renthal, W., Wood, M. A., Yasui, D. H., et al. (2008). Epigenetics in the nervous system. Journal of Neuroscience, 28, 1175311759.
Jones, P. A., & Liang, G. (2009). Rethinking how DNA methylation patterns are maintained. Nature Reviews Genetics, 10, 805811.
Josselyn, S. A. (2005). What's right with my mouse model? New insights into the molecular and cellular basis of cognition from mouse models of Rubinstein–Taybi Syndrome. Learning and Memory, 12, 8083.
Kaas, G. A., Zhong, C., Eason, D. E., Ross, D. L., Vachhani, R. V., Ming, G. L., et al. (2013). TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron, 79, 10861093.
Kaminsky, Z. A., Tang, T., Wang, S.-C., Ptak, C., Oh, G. H. T., Wong, A. H. C., et al. (2009). DNA methylation profiles in monozygotic and dizygotic twins. Nature Genetics, 41, 240245.
Kandel, E. R. (2001). The molecular biology of memory storage: A dialogue between genes and synapses. Science, 294, 10301038.
Kandel, E. R. (2012). The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Molecular Brain, 5, 14.
Karr, J., Vagin, V., Chen, K., Ganesan, S., Olenkina, O., Gvozdev, V., et al. (2009). Regulation of glutamate receptor subunit availability by microRNAs. Journal of Cell Biology, 185, 685697.
Kaur, P., Tan, J. R., Karolina, D. S., Sepramaniam, S., Armugam, A., Wong, P. T. H., et al. (2016). A long non-coding RNA, BC048612 and a microRNA, miR-203 coordinate the gene expression of neuronal growth regulator 1 (NEGR1) adhesion protein. Biochimica et Biophysica Acta, 1863, 533543.
Kerimoglu, C., Agis-Balboa, R. C., Kranz, A., Stilling, R., Bahari-Javan, S., Benito-Garagorri, E., et al. (2013). Histone-methyltransferase mll2 (kmt2b) is required for memory formation in mice. Journal of Neuroscience, 33, 34523464.
Kim, J., Kollhoff, A., Bergmann, A., & Stubbs, L. (2003). Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3. Human Molecular Genetics, 12, 233245.
Kim, M. S., Akhtar, M. W., Adachi, M., Mahgoub, M., Bassel-Duby, R., Kavalali, E. T., et al. (2012). An essential role for histone deacetylase 4 in synaptic plasticity and memory formation. Journal of Neuroscience, 32, 1087910886.
Kinde, B., Gabel, H. W., Gilbert, C. S., Griffith, E. C., & Greenberg, M. E. (2015). Reading the unique DNA methylation landscape of the brain: Non-CpG methylation, hydroxymethylation, and MeCP2. Proceedings of the National Academy of Sciences, 112, 68006806.
Kiser, D. P., Rivero, O., & Lesch, K.-P. (2015). Annual Research Review: The (epi)genetics of neurodevelopmental disorders in the era of whole-genome sequencing—Unveiling the dark matter. Journal of Child Psychology and Psychiatry, 56, 278295.
Klose, R. J., & Bird, A. P. (2003). Molecular biology: MeCP2 repression goes nonglobal. Science, 302, 793795.
Klose, R. J., & Bird, A. P. (2006). Genomic DNA methylation: The mark and its mediators. Trends in Biochemical Sciences, 31, 8997.
Korzus, E., Rosenfeld, M. G., & Mayford, M. (2004). CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron, 42, 961972.
Koseki, T., Mouri, A., Mamiya, T., Aoyama, Y., Toriumi, K., Suzuki, S., et al. (2012). Exposure to enriched environments during adolescence prevents abnormal behaviours associated with histone deacetylation in phencyclidine-treated mice. International Journal of Neuropsychopharmacology, 15, 14891501.
Kouzarides, T. (2007). Chromatin modifications and their function. Cell, 128, 693705.
Kozlenkov, A., Wang, M., Roussos, P., Rudchenko, S., Barbu, M., Bibikova, M., et al. (2016). Substantial DNA methylation differences between two major neuronal subtypes in human brain. Nucleic Acids Research, 44, 25932612.
Kriaucionis, S., & Heintz, N. (2009). The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science, 324, 929930.
Kurihara, M., Shiraishi, A., Satake, H., & Kimura, A. P. (2014). A conserved noncoding sequence can function as a spermatocyte-specific enhancer and a bidirectional promoter for a ubiquitously expressed gene and a testis-specific long noncoding RNA. Journal of Molecular Biology, 426, 30693093.
Laird, P. W. (2010). Principles and challenges of genomewide DNA methylation analysis. Nature Reviews Genetics, 11, 191203.
Latham, J. A., & Dent, S. Y. (2007). Cross-regulation of histone modifications. Nature Structural and Molecular Biology, 14, 10171024.
Leader, J. E., Wang, C., Popov, V. M., Fu, M., & Pestell, R. G. (2006). Epigenetics and the estrogen receptor. Annals of New York Academy of Sciences, 1089, 7387.
Lee, K., Kim, J. H., Kwon, O. B., An, K., Ryu, J., Cho, K., et al. (2012). An activity-regulated microRNA, miR-188, controls dendritic plasticity and synaptic transmission by downregulating neuropilin-2. Journal of Neuroscience, 32, 56785687.
Lee, K. K., & Workman, J. L. (2007). Histone acetyltransferase complexes: One size doesn't fit all. Nature Reviews Molecular Cell Biology, 8, 285295.
Leibrock, J., Lottspeich, F., Hohn, A., Hofer, M., Hengerer, B., Masiakowski, P., et al. (1989). Molecular cloning and expression of brain-derived neurotrophic factor. Nature, 341, 149152.
Levenson, J. M., O'Riordan, K. J., Brown, K. D., Trinh, M. A., Molfese, D. L., & Sweatt, J. D. (2004). Regulation of histone acetylation during memory formation in the hippocampus. Journal of Biological Chemistry, 279, 4054540559.
Levine, A., Worrell, T. R., Zimnisky, R., & Schmauss, C. (2012). Early life stress triggers sustained changes in histone deacetylase expression and histone H4 modifications that alter responsiveness to adolescent antidepressant treatment. Neurobiology of Disease, 45, 488498.
Li, B., Carey, M., & Workman, J. L. (2007). The role of chromatin during transcription. Cell, 128, 707719.
Li, E., Beard, C., & Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature, 366, 362365.
Li, X., Wei, W., Zhao, Q.-Y., Widagdo, J., Baker-Andresen, D., Flavell, C. R., et al. (2014). Neocortical Tet3-mediated accumulation of 5-hydroxymethylcytosine promotes rapid behavioral adaptation. Proceedings of the National Academy of Sciences, 111, 71207125.
Li, Z., Van Calcar, S., Qu, C., Cavenee, W. K., Zhang, M. Q., & Ren, B. (2003). A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proceedings of the National Academy of Sciences, 100, 81648169.
Lipsky, R. H. (2013). Epigenetic mechanisms regulating learning and long-term memory. International Journal of Developmental Neuroscience, 31, 353358.
Lipsky, R. H., Xu, K., Zhu, D., Kelly, C., Terhakopian, A., Novelli, A., et al. (2001). Nuclear factor kappaB is a critical determinant in N-methyl-d-aspartate receptormediated neuroprotection. Journal of Neurochemistry, 24, 254264.
Lisman, J. E. (1985). A mechanism for memory storage insensitive to molecular turnover: A bistable autophosphorylating kinase. Proceedings of the National Academy of Sciences, 82, 30553057.
Lister, R., Mukamel, E. A., Nery, J. R., Urich, M., Puddifoot, C. A., Johnson, N. D., et al. (2013). Global epigenomic reconfiguration during mammalian brain development. Science, 341, 629.
Lopez-Atalaya, J. P., Ciccarelli, A., Viosca, J., Valor, L. M., Jimenez-Minchan, M., Canals, S., et al. (2011). CBP is required for environmental enrichment-induced neurogenesis and cognitive enhancement. EMBO Journal, 30, 42874298.
Lubin, F. D., Roth, T. L., & Sweatt, J. D. (2008). Epigenetic regulation of bdnf gene transcription in the consolidation of fear memory. Journal of Neuroscience, 28, 1057610586.
Lubin, F. D., & Sweatt, J. D. (2007). The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron, 55, 942957.
Ma, D. K., Jang, M.-H., Guo, J. U., Kitabatake, Y., Chang, M.-L., Pow-anpongkul, N., et al. (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science, 323, 10741077.
Maharana, C., Sharma, K. P., & Sharma, S. K. (2010). Depolarization induces acetylation of histone H2B in the hippocampus. Neuroscience, 167, 354360.
Malvaez, M., McQuown, S. C., Rogge, G. A., Astarabadi, M., Jacques, V., Carreiro, S., et al. (2013). HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proceedings of the National Academy of Sciences, 110, 26472651.
Margueron, R., Trojer, P., & Reinberg, D. (2005). The key to development: Interpreting the histone code? Current Opinion in Genetics and Development, 15, 163176.
Martinowich, K., Hattori, D., Wu, H., Fouse, S. D., He, F., Hu, Y., et al. (2003). DNA methylation-related chromatin remodeling in activity-dependent Bdnf gene regulation. Science, 302, 890893.
Martone, R., Euskirchen, G., Bertrone, P., Hartman, S., Royce, T. E., Luscombe, N. M., et al. (2003). Distribution of NF-kappaB-binding sites across human chromosome 22. Proceedings of the National Academy of Sciences, 100, 1224712252.
Maurice, T., Duclot, F., Meunier, J., Naert, G., Givalois, L., Meffre, J., et al. (2008). Altered memory capacities and response to stress in p300/CBP-associated factor (PCAF) histone acetylase knockout mice. Neuropsychopharmacology, 33, 15841602.
Maze, I., Covington, H. E. I., Dietz, D. M., LaPlant, Q., Renthal, W., Russo, S. J., et al. (2010). Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science, 327, 213216.
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C. T., Hallett, M., Meaney, M. J., et al. (2011). Broad epigenetic signature of maternal care in the brain of adult rats. PLOS ONE, 6, e14739.
McQuown, S. C., Barrett, R. M., Matheos, D. P., Post, R. J., Rogge, G. A., Alenghat, T., et al. (2011). HDAC3 is a critical negative regulator of long-term memory formation. Journal of Neuroscience, 31, 764774.
McQuown, S. C., & Wood, M. A. (2011). HDAC3 and the molecular brake pad hypothesis. Neurobiology of Learning and Memory, 96, 2734.
Mercer, T. R., & Mattick, J. S. (2013). Structure and function of long noncoding RNAs in epigenetic regulation. Nature Structural and Molecular Biology, 20, 300307.
Miller, C. A., Campbell, S. L., & Sweatt, J. D. (2008). DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiology of Learning and Memory, 89, 599603.
Miller, C. A., & Sweatt, J. D. (2007). Covalent modification of DNA regulates memory formation. Neuron, 53, 857869.
Moen, E. L., Zhang, X., Mu, W., Delaney, S. M., & Wing, C., McQuade, J., et al. (2013). Genome-wide variation of cytosine modifications between European and African populations and the implications for complex traits. Genetics, 194, 987996.
Motil, K. J., Schultz, R., Brown, B., Glaze, D. G., & Percy, A. K. (1994). Altered energy balance may account for growth failure in Rett syndrome. Journal of Child Neurology, 9, 315319.
Murphy, S. E., Norbury, R., Godlewska, B. R., Cowen, P. J., Mannie, Z. M., Harmer, C. J., et al. (2013). The effect of the serotonin transporter polymorphism (5-HTTLPR) on amygdala function: A meta-analysis. Molecular Psychiatry, 18, 512520.
Neelamegam, R., Ricq, E. L., Malvaez, M., Patnaik, D., Norton, S., Carlin, S. M., et al. (2012). Brain-penetrant LSD1 inhibitors can block memory consolidation. ACS Chemical Neuroscience, 3, 120128.
Nelson, E. D., Bal, M., Kavalali, E. T., & Monteggia, L. M. (2011). Selective impact of MeCP2 and associated histone deacetylases on the dynamics of evoked excitatory neurotransmission. Journal of Neurophysiology, 106, 193201.
Ng, S. B., Bigham, A. W., Buckingham, K. J., Hannibal, M. C., McMillin, M. J., Gildersleeve, H. I., et al. (2010). Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nature Genetics, 42, 790793.
Nikolova, Y. S., & Hariri, A. R. (2015). Can we observe epigenetic effects on human brain function? Trends in Cognitive Sciences, 19, 366373.
Nikolova, Y. S., Koenen, K. C., Galea, S., Wang, C. M., Seney, M. L., Sibillie, E., et al. (2014). Beyond genotype: Serotonin transporter epigenetic modification predicts human brain function. Nature Neuroscience, 17, 11531155.
Niikawa, N., Kuroki, Y., Kajii, T., Matsuura, N., Ishikiriyama, S., Tonoki, H., et al. (1988). Kabuki make-up (Niikawa–Kuroki) syndrome: A study of 62 patients. American Journal of Medical Genetics, 31, 565589.
Nott, A., Watson, P. M., Robinson, J. D., Crepaldi, L., & Riccio, A. (2008). S-nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature, 455, 411415.
Novik, K. L., Nimmrich, I., Genc, B., Maier, S., Piepenbrock, C., Olek, A., et al. (2002). Epigenomics: Genome-wide study of methylation phenomena. Current Issues in Molecular Biology, 4, 111128.
Oike, Y., Hata, A., Mamiya, T., Kaname, T., Noda, Y., Suzuki, M., et al. (1999). Truncated CBP protein leads to classical Rubinstein–Taybi syndrome phenotypes in mice: Implications for a dominant-negative mechanism. Human Molecular Genetics, 8, 387396.
Oliveira, A. M., Hemstedt, T. J., & Bading, H. (2012). Rescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities. Nature Neuroscience, 15, 11111113.
Oliveira, A. M., Wood, M. A., McDonough, C. B., & Abel, T. (2007). Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits. Learning and Memory, 14, 564572.
Oztan, O., Aydin, C., & Isgor, C. (2011). Stressful environmental and social stimulation in adolescence causes antidepressant-like effects associated with epigenetic induction of the hippocampal BDNF and mossy fibre sprouting in the novelty-seeking phenotype. Neuroscience Letters, 501, 107111.
Park, C. S., Rehrauer, H., & Mansuy, I. M. (2013). Genome-wide analysis of H4K5 acetylation associated with fear memory in mice. BMC Genomics, 8, 539545.
Park, H., & Poo, M. M. (2012). Neurotrophin regulation of neural circuit development and function. Nature Reviews Neuroscience, 14, 723.
Pastor, W. A., Aravind, L., & Rao, A. (2013). TETonic shift: Biological roles of TET proteins in DNA demethylation and transcription. Nature Reviews Molecular Cell Biology, 14, 341356.
Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Java, S., Agis-Balboa, R. C., et al. (2010). Altered histone acetylation is associated with age-dependent memory impairment in mice. Science, 328, 753756.
Penn, N. W., Suwalski, R., O'Riley, C., Bojanowski, K., & Yura, R. (1972). The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid. Biochemical Journal, 126, 781790.
Petrif, F., Giles, R. H., Dauwerse, H. G., Saris, J. J., Hennekam, R. C. M., Masuno, M., et al. (1995). Rubinstein–Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature, 376, 348351.
Pfeifer, G. P., Steigerwald, S. D., Hansen, R. S., Gartler, S. M., & Riggs, A. D. (1990). Polymerase chain reaction-aided genomic sequencing of an X chromosome-linked CpG island: Methylation patterns suggest clonal inheritance, CpG site autonomy, and an explanation of activity state stability. Proceedings of the National Academy of Sciences, 87, 82528256.
Plass, C., Shibata, H., Kalcheva, I., Mullins, L., Kotelevtseva, N., Mullins, J., et al. (1996). Identification of Grf1 on mouse chromosome 9 as an imprinted gene by RLGS-M. Nature Genetics, 14, 106109.
Polderman, T. J. C., Benyamin, B., de Leeuw, C. A., Sullivan, P. F., van Bochoven, A., Visscher, P. M., et al. (2015). Meta-analysis of the heritability of human traits based on fifty years of twin studies. Nature Genetics, 47, 702709.
Portela, A., & Esteller, M. (2010). Epigenetic modifications and human disease. Nature Biotechnology, 28, 10571068.
Psotta, L., Lessmann, V., & Endres, T. (2013). Impaired fear extinction learning in adult heterozygous BDNF knock-out mice. Neurobiology of Learning and Memory, 103, 3438.
Ptashne, M. (2007). On the use of the word “epigenetic.” Current Biology, 17, R233R236.
Puckett, R. E., & Lubin, F. D. (2011). Epigenetic mechanisms in experience-driven memory formation and behavior. Epigenomics, 3, 649664.
Qureshi, I. A., & Mehler, M. F. (2012). Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nature Reviews Neuroscience, 13, 528541.
Rajasethupathy, P., Antonov, I., Sheridan, R., Frey, S., Sander, C., Tuschl, T., et al. (2012). A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell, 149, 693707.
Rett, A. (1966). On an unusual brain atrophy syndrome in hyperammonemia in childhood. Wiener Medizinische Wochenschrift, 116, 723726.
Rideout, W. M. III, Eggan, K., & Jaenisch, R. (2001). Nuclear cloning and epigenetic reprogramming of the genome. Science, 293, 10931098.
Ridley, R. M., Frith, C. D., Crow, T. J., & Conneally, P. M. (1988). Anticipation in Huntington's disease is inherited through the male line but may originate in the female. Journal of Medical Genetics, 28, 589595.
Riggs, A. D. (1975). X inactivation, differentiation, and DNA methylation. Cytogenetics and Genome Research, 14, 925.
Ringrose, L., & Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annual Review of Genetics, 38, 413443.
Roadmap Epigenomics. (2015). Integrative analysis of 111 reference human epigenomes. Nature, 518, 317330.
Roberson, E. D., & Sweatt, J. D. (2001). Memory-forming chemical reactions. Reviews in the Neurosciences, 12, 4150.
Roelfsema, J. H., White, S. J., Ariyürek, Y., Bartholdi, D., Niedrist, D., Papadia, F., et al. (2005). Genetic heterogeneity in Rubinstein–Taybi syndrome: Mutations in both the CBP and EP300 genes cause disease. American Journal of Human Genetics, 76, 572580.
Roth, T. L., & Sweatt, J. D. (2010). Epigenetic marking of the BDNF gene by early-life adverse experiences. Hormones and Behavior, 59, 315320.
Rubinstein, J. H., & Taybi, H. (1963). Broad thumbs and toes and facial abnormalities: Possible mental retardation syndrome. American Journal of Diseases of Children, 105, 588608.
Rudenko, A., Dawlaty, M. M., Seo, J., Cheng, A. W., Meng, J., Le, T., et al. (2013). Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron, 79, 11091122.
Rudenko, A., & Tsai, L.-H. (2014). Epigenetic modifications in the nervous system and their impact upon cognitive impairments. Neuropharmacology, 80, 7082.
Rujirabanjerd, S., Nelson, J., Tarpey, P. S., Hackett, A., Edkins, S., Raymond, F. L., et al. (2012). Identification and characterization of two novel JARID1C mutations: Suggestion of an emerging genotype–phenotype correlation. European Journal of Human Genetics, 18, 330335.
Russo, V. E. A., Martienssen, R. A., & Riggs, A. D. (Eds.) (1996). Epigenetic mechanisms of gene regulation. Woodbury, NY: Cold Spring Harbor Laboratory Press.
Saba, R., Störchel, P. H., Aksoy-Aksel, A., Kepura, F., Lippi, G., Plant, T. D., et al. (2012). Dopamine-regulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons. Journal of Molecular Cell Biology, 32, 619632.
Sananbenesi, F., & Fischer, A. (2009). The epigenetic bottleneck of neurodegenerative and psychiatric diseases. Biological Chemistry, 390, 11451153.
Sando, R. I., Gounko, N., Pieraut, S., Liao, L., Yates, J. I., & Maximov, A. (2012). HDAC4 governs a transcriptional program essential for synaptic plasticity and memory. Cell, 151, 821834.
Schaefer, A., Sampath, S. C., Intrator, A., Min, A., Gertler, T. S., Surmeier, D. J., et al. (2009). Control of cognition and adaptive behavior by the GLP/G9a epigenetic suppressor complex. Neuron, 64, 678691.
Schmitt, M., & Matthies, H. (1979). Biochemical studies on histones of the central nervous system: III. Incorporation of [14C]-acetate into the histones of different rat brain regions during a learning experiment. Acta Biologica et Medica Germanica, 38, 683689.
Schratt, G. M. (2009). microRNAs at the synapse. Nature Reviews Neuroscience, 10, 842849.
Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., et al. (2006). A brain-specific microRNA regulates dendritic spine development. Nature, 439, 283289.
Schultz, W. (2002). Getting formal with dopamine and reward. Neuron, 36, 241263.
Schwartz, Y. B., & Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nature Reviews Genetics, 8, 922.
Sennvik, K., Fastbom, J., Blomberg, M., Wahlund, L.-O., Winblad, B., & Benedikz, E. (2000). Levels of alpha- and beta-secretase cleaved amyloid precursor protein in the cerebrospinal fluid of Alzheimer's disease patients. Neuroscience Letters, 278, 169172.
Shahbazian, M. D., & Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annual Review of Biochemistry, 76, 75100.
Shibata, H., Hirotsune, S., Okazaki, Y., Komatsubara, H., Muramatsu, M., Takagi, N., et al. (1994). Genetic mapping and systematic screening of mouse endogenously imprinted loci detected with restriction landmark genome scanning method (RLGS). Mammalian Genome, 5, 797800.
Shirayama, Y., Chen, A. C., Nakagawa, S., Russell, D. S., & Duman, R. S. (2002). Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. Journal of Neuroscience, 22, 32513261.
Shukla, A., Sehgal, M., & Singh, T. R. (2015). Hydroxymethylation and its potential implication in DNA repair system: A review and future perspectives. Gene, 564, 109118.
Simensen, R. J., Rogers, R. C., Collins, J. S., Abidi, F., Schwartz, C. E., & Stevenson, R. E. (2012). Short-term memory deficits in carrier females with KDM5C mutations. Journal of Genetic Counseling, 23, 3140.
Singer, J., Roberts-Ems, J., & Riggs, A. D. (1979). Methylation of mouse liver DNA studied by means of the restriction enzymes MspI and HpaII. Science, 203, 10191021.
Smith, A. K., Kilaru, V., Klengel, T., Mercer, K. B., Bradley, B., Conneely, K. N., et al. (2015). DNA extracted from saliva for methylation studies of psychiatric traits: Evidence tissue specificity and relatedness to brain. American Journal of Medical Genetics, 168B, 3644.
Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A., et al. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature, 484, 339344.
Smith, Z. D., & Meissner, A. (2013). DNA methylation: Roles in mammalian development. Nature Reviews Genetics, 14, 204220.
Spruijt, C. G., Gnerlich, F., Smits, A. H., Pfaffeneder, T., Jansen, P. W., Bauer, C., et al. (2013). Dynamic readers for 5-(hydroxy) methylcytosine and its oxidized derivatives. Cell, 152, 11461159.
Stadler, F., Kolb, G., Rubusch, L., Baker, S. P., Jones, E. G., & Akbarian, S. (2005). Histone methylation at gene promoters is associated with developmental regulation and region-specific expression of ionotropic and metabotropic glutamate receptors in human brain. Journal of Neurochemistry, 94, 324336.
Strahl, B. D., & Allis, C. D. (2000). The language of covalent histone modifications. Nature, 403, 4145.
Sui, L., Wang, Y., Ju, L. H., & Chen, M. (2012). Epigenetic regulation of reelin and brain-derived neurotrophic factor genes in long-term potentiation in rat medial prefrontal cortex. Neurobiology of Learning and Memory, 97, 425440.
Swank, M. W., & Sweatt, J. D. (2001). Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. Journal of Neuroscience, 21, 33833391.
Sweatt, J. D. (2001). The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. Journal of Neurochemistry, 76, 110.
Sweatt, J. D. (2009). Experience-dependent epigenetic modifications in the central nervous system. Biological Psychiatry, 65, 191197.
Sweatt, J. D. (2013). The emerging field of neuroepigenetics. Neuron, 80, 624632.
Szulwach, K. E., Li, X., Li, Y., Song, C.-X., Wu, H., Dai, Q., et al. (2011). 5-hmC–mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nature Neuroscience, 14, 16071616.
Szyf, M. (2009). Epigenetics DNA methylation, and chromatin modifying drugs. Annual Review of Pharmacology and Toxicology, 49, 243263.
Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., et al. (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 324, 930935.
Takai, D., & Jones, P. A. (2002). Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proceedings of the National Academy of Sciences, 99, 37403745.
Tao, X., West, A. E., Chen, W. G., Corfas, G., & Greenberg, M. E. (2002). A calcium-responsive transcription factor, CaRF, that regulates neuronal activity-dependent expression of BDNF. Neuron, 33, 383395.
Teh, A. L., Pan, H., Chen, L., Ong, M. L., & Dogra, S., Wong, J., et al. (2014). The effect of genotype and in utero environment on inter-individual variation in neonate DNA methylomes. Genome Research, 24, 10641074.
Thompson, T. M., Sharfi, D., Lee, M., Yrigollen, C. M., Naumova, O. Y., & Grigorenko, E. L. (2013). Comparison of whole-genome DNA methylation patterns in whole blood, saliva, and lymphoblastoid cell lines. Behavior Genetics, 43, 168176.
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007). Epigenetic regulation in psychiatric disorders. Nature Reviews Neuroscience, 8, 355367.
Tylee, D. S., Kawaguchi, D. M., & Glatt, S. J. (2013). On the outside, looking in: A review and evaluation of the comparability of blood and brain “-omes.” American Journal of Medical Genetics, 162B, 595603.
Van Speybroeck, L. (2002). From epigenesis to epigenetics: The case of C. H. Waddington. Annals of New York Academy of Sciences, 981, 6181.
Waddington, C. H. (1942). The epigenotype. Endeavour, 1, 1820.
Waddington, C. H. (1957). The strategy of the genes. London: Allen & Unwin.
Walker, F. O. (2007). Huntington's disease. Lancet, 369, 218228.
Walker, M. P., LaFerla, F. M., Oddo, S. S., & Brewer, G. J. (2013). Reversible epigenetic histone modifications and Bdnf expression in neurons with aging and from a mouse model of Alzheimer's disease. Age, 35, 519531.
Wang, D., Szyf, M., Benkelfat, C., Provençal, N., Turecki, G., Caramaschi, D., et al. (2012). Peripheral SLC6A4 DNA methylation is associated with in vivo measures of human brain serotonin synthesis and childhood physical aggression. PLOS ONE, 7, e39501.
Wang, W. H., Cheng, L. C., Pan, F. Y., Xue, B., Wang, D. Y., Chen, Z., et al. (2011). Intracellular trafficking of histone deacetylase 4 regulates long-term memory formation. Anatomical Record, 294, 10251034.
Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., et al. (2008). Combinatorial patterns of histone acetylations and methylations in the human genome. Nature Genetics, 40, 897903.
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847854.
Weinberg, M. S., Villeneuve, L. M., Ehsani, A., Amarzguioui, M., Aagaard, L., Chen, Z. X., et al. (2006). The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA, 12, 256262.
Weinmann, A. S., Yan, P. S., Oberley, M. J., Huang, T. H., & Farnham, P. J. (2002). Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. Genes and Development, 16, 235244.
Wells, J., Yan, P. S., Cechvala, M., Huang, T., & Farnham, P. J. (2003). Identification of novel pRb binding sites using CpG microarrays suggests that E2F recruits pRb to specific genomic sites during S phase. Oncogene, 22, 14451460.
Williams, S. R., Aldred, M. A., Der Kaloustian, V. M., Halal, F., Gowans, G., McLeod, D. R., et al. (2010). Haploinsufficiency of HDAC4 causes brachydactyly mental retardation syndrome, with brachydactyly type E, developmental delays, and behavioral problems. American Journal of Human Genetics, 87, 219228.
Wood, M. A., Attner, M. A., Oliveira, A. M., Brindle, P. K., & Abel, T. (2006). A transcription factor-binding domain of the coactivator CBP is essential for long-term memory and the expression of specific target genes. Learning and Memory, 13, 609617.
Wood, M. A., Kaplan, M. P., Park, A., Blanchard, E. J., Oliveira, A. M., Lombardi, T. L., et al. (2005). Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learning and Memory, 12, 111119.
Wu, C.-T., & Morris, J. R. (2001). Genes, genetics, and epigenetics: A correspondence. Science, 293, 11031105.
Wu, H., & Zhang, Y. (2014). Reversing DNA methylation: Mechanisms, genomics, and biological functions. Cell, 156, 4568.
Wu, S. C., & Zhang, Y. (2010). Active DNA demethylation: Many roads lead to Rome. Nature Reviews Molecular Cell Biology, 11, 607620.
Xie, H., Liu, Y., Zhu, Y., Ding, X., Yang, Y., & Guan, J.-S. (2014). In vivo imaging of immediate early gene expression reveals layer-specific memory traces in the mammalian brain. Proceedings of the National Academy of Sciences, 111, 27882793.
Yan, P. S., Chen, C. M., Sji, H., Rahmatpanah, F., Wei, S. H., & Huang, T. H. (2002). Applications of CpG island microarrays for high-throughput analysis of DNA methylation. Journal of Nutrition, 132, S2430S2434.
Yan, P. S., Perry, M. R., Laux, D. E., Asare, A. L., Caldwell, C. W., & Huang, T. H. (2000). CpG island arrays: An application toward deciphering epigenetic signatures of breast cancer. Clinical Cancer Research, 6, 14321438.
Yang, J., Lee, T., Kim, J., Cho, M.-C., Han, B.-G., Lee, J.-Y., et al. (2013). Ubiquitous polygenicity of human complex traits: Genome-wide analysis of 49 traits in Koreans. PLOS Genetics, 9, e1003355.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Development and Psychopathology
  • ISSN: 0954-5794
  • EISSN: 1469-2198
  • URL: /core/journals/development-and-psychopathology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed