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Epigenetic regulation of cognition: A circumscribed review of the field

Published online by Cambridge University Press:  03 October 2016

Elena L. Grigorenko*
Affiliation:
Baylor College of Medicine St. Petersburg State University University of Houston Yale University
Sergey A. Kornilov
Affiliation:
Baylor College of Medicine St. Petersburg State University University of Houston
Oksana Yu. Naumova
Affiliation:
St. Petersburg State University University of Houston
*
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: [email protected].

Abstract

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.

Type
Special Section Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Badeaux, A. I., & Shi, Y. (2013). Emerging roles for chromatin as a signal integration and storage platform. Nature Reviews Molecular Cell Biology, 14, 211224.CrossRefGoogle ScholarPubMed
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.Google Scholar
Bannister, A. J., & Kouzarides, T. (2011). Regulation of chromatin by histone modifications. Cell Research, 21, 381395.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Bird, A. P. (1980). DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Research, 8, 14991504.Google Scholar
Bird, A. P. (1986). CpG-rich islands and the function of DNA methylation. Nature, 321, 209213.Google Scholar
Bird, A. P. (2002). DNA methylation patterns and epigenetic memory. Genes and Development, 16, 621.Google Scholar
Bird, A. P. (2007). Perceptions of epigenetics. Nature, 447, 396398.Google Scholar
Bird, A. P., & Wolffe, A. P. (1999). Methylation-induced repression: Belts, braces, and chromatin. Cell, 99, 451454.Google Scholar
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.CrossRefGoogle ScholarPubMed
Bordone, L., & Guarente, L. (2005). Calorie restriction, SIRT1 and metabolism: Understanding longevity. Nature Reviews Molecular Cell Biology, 6, 298305.Google Scholar
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.Google Scholar
Boyce, W. T., & Kobor, M. S. (2015). Development and the epigenome: The “synapse” of gene–environment interplay. Developmental Science, 18, 123.Google Scholar
Bradbury, J. (2003). Human epigenome project-up and running. PLOS Biology, 1, E82.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Cervoni, N., & Szyf, M. (2001). Demethylase activity is directed by histone acetylation. Journal of Biological Chemistry, 276, 4077840787.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Chahrour, M., & Zoghbi, H. Y. (2007). The story of Rett syndrome: From clinic to neurobiology. Neuron, 56, 422437.Google Scholar
Chan, H. M., & La Thangue, N. B. (2001). p300/CBP proteins: HATs for transcriptional bridges and scaffolds. Journal of Cell Science, 114, 23632373.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Chuang, J. C., & Jones, P. A. (2007). Epigenetics and microRNAs. Pediatric Research, 61, 24R29R.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Crick, F. (1984). Memory and molecular turnover. Nature, 312, 101.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
Dash, P. K., Moore, A. N., Kobori, N., & Runyan, J. D. (2007). Molecular activity underlying working memory. Learning and Memory, 14, 554563.Google Scholar
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.Google Scholar
Davis, H. P., & Squire, L. R. (1984). Protein synthesis and memory: A review. Psychological Bulletin, 96, 518559.Google Scholar
Day, J. J., & Sweatt, J. D. (2010). DNA methylation and memory formation. Nature Neuroscience, 13, 13191323.Google Scholar
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.Google Scholar
Deaton, A. M., & Bird, A. (2011). CpG islands and the regulation of transcription. Genes and Development, 25, 10101022.CrossRefGoogle ScholarPubMed
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.Google Scholar
Duncan, B. K., & Miller, J. H. (1980). Mutagenic deamination of cytosine residues in DNA. Nature, 287, 560561.CrossRefGoogle ScholarPubMed
Esteller, M. (2008). Epigenetics in evolution and disease. Lancet, 372, S90S96.CrossRefGoogle Scholar
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.Google Scholar
Fatica, A., & Bozzoni, I. (2013). Long non-coding RNAs: New players in cell differentiation and development. Nature Reviews Genetics, 15, 721.Google Scholar
Fazzari, M. J., & Greally, J. M. (2004). Epigenomics: Beyond CpG islands. Nature Reviews Genetics, 5, 446455.Google Scholar
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.Google Scholar
Feinberg, A. P. (2001). Methylation meets genomics. Nature Genetics, 27, 910.Google Scholar
Feinberg, A. P. (2011). Genome-scale approaches to the epigenetics of common human disease. Disease, 456, 1321.Google Scholar
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.Google Scholar
Fischer, A. (2014). Epigenetic memory: The Lamarckian brain. EMBO Journal, 33, 945967.CrossRefGoogle ScholarPubMed
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.Google Scholar
Flexner, J. B., Flexner, L. B., & Stellar, E. (1963). Memory in mice as affected by intracerebral puromycin. Science, 141, 5759.Google Scholar
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.Google Scholar
Fraser, H. B., Lam, L. L., Neumann, S. M., & Kobor, M. S. (2012). Population-specificity of human DNA methylation. Genome Biology, 13, R8.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Goate, A., & Hardy, J. (2012). Twenty years of Alzheimer's disease-causing mutations. Journal of Neurochemisty, 120, 38.Google Scholar
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.Google Scholar
Gräff, J., & Mansuy, I. M. (2008). Epigenetic codes in cognition and behaviour. Behavioural Brain Research, 192, 7087.Google Scholar
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.Google Scholar
Gräff, J., & Tsai, L. H. (2013). Histone acetylation: Molecular mnemonics on the chromatin. Nature Reviews Neuroscience, 14, 97111.Google Scholar
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.Google Scholar
Grewal, S. I., & Moazed, D. (2003). Heterochromatin and epigenetic control of gene expression. Science, 301, 798802.Google Scholar
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.Google Scholar
Guan, J.-S., Xie, H., & Ding, X. (2015). The role of epigenetic regulation in learning and memory. Experimental Neurology, 268, 3036.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Haigis, M. C., & Sinclair, D. A. (2010). Mammalian sirtuins: Biological insights and disease relevance. Annual Review of Pathology, 5, 253295.CrossRefGoogle ScholarPubMed
Harshman, S. W., Young, N. L., Parthun, M. R., & Freiras, M. A. (2013). H1 histones: Current perspectives and challenges. Nucleic Acids Research, 41, 95939609.Google Scholar
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.Google Scholar
Hatchwell, E., & Greally, J. M. (2007). The potential role of epigenomic dysregulation in complex human disease. Trends in Genetics, 23, 588595.Google Scholar
He, L., & Hannon, G. J. (2004). MicroRNAs: Small RNAs with a big role in gene regulation. Nature Reviews Genetics, 5, 522531.Google Scholar
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.CrossRefGoogle ScholarPubMed
Heyward, F. D., & Sweatt, J. D. (2015). DNA methylation in memory formation: Emerging insights. Neuroscientist. Advance online publication.Google Scholar
Holliday, R. (1990). DNA methylation and epigenetic inheritance. Philosophical Transactions of the Royal Society of London: Series B, Biological Sciences, 326, 329338.Google Scholar
Holliday, R. (1999). Is there an epigenetic component in long-term memory? Journal of Theoretical Biology, 200, 339341.Google Scholar
Holliday, R., & Pugh, J. E. (1975). DNA modification mechanisms and gene activity during development. Science, 187, 226232.Google Scholar
Hong, E. J., West, A. E., & Greenberg, M. E. (2005). Transcriptional control of cognitive development. Current Opinion in Neurobiology, 15, 2128.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Im, H. I., & Kenny, P. J. (2012). MicroRNAs in neuronal function and dysfunction. Trends in Neuroscience, 35, 325334.Google Scholar
Imhof, A. (2006). Epigenetic regulators and histone modification. Briefings in Functional Genomics and Proteomics, 5, 222227.Google Scholar
Jablonka, E., & Lamb, M. J. (2002). The changing concept of epigenetics. Annals of the New York Academy of Sciences, 981, 8296.Google Scholar
Jaenisch, R., & Bird, A. (2003). Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals. Nature Genetics, 33, 245254.Google Scholar
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.Google Scholar
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.Google Scholar
Jones, P. A., & Liang, G. (2009). Rethinking how DNA methylation patterns are maintained. Nature Reviews Genetics, 10, 805811.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Kandel, E. R. (2001). The molecular biology of memory storage: A dialogue between genes and synapses. Science, 294, 10301038.Google Scholar
Kandel, E. R. (2012). The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Molecular Brain, 5, 14.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Klose, R. J., & Bird, A. P. (2003). Molecular biology: MeCP2 repression goes nonglobal. Science, 302, 793795.CrossRefGoogle ScholarPubMed
Klose, R. J., & Bird, A. P. (2006). Genomic DNA methylation: The mark and its mediators. Trends in Biochemical Sciences, 31, 8997.Google Scholar
Korzus, E., Rosenfeld, M. G., & Mayford, M. (2004). CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron, 42, 961972.Google Scholar
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.Google Scholar
Kouzarides, T. (2007). Chromatin modifications and their function. Cell, 128, 693705.Google Scholar
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.Google Scholar
Kriaucionis, S., & Heintz, N. (2009). The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science, 324, 929930.Google Scholar
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.Google Scholar
Laird, P. W. (2010). Principles and challenges of genomewide DNA methylation analysis. Nature Reviews Genetics, 11, 191203.Google Scholar
Latham, J. A., & Dent, S. Y. (2007). Cross-regulation of histone modifications. Nature Structural and Molecular Biology, 14, 10171024.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
Lee, K. K., & Workman, J. L. (2007). Histone acetyltransferase complexes: One size doesn't fit all. Nature Reviews Molecular Cell Biology, 8, 285295.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Li, B., Carey, M., & Workman, J. L. (2007). The role of chromatin during transcription. Cell, 128, 707719.Google Scholar
Li, E., Beard, C., & Jaenisch, R. (1993). Role for DNA methylation in genomic imprinting. Nature, 366, 362365.Google Scholar
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.Google Scholar
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.Google Scholar
Lipsky, R. H. (2013). Epigenetic mechanisms regulating learning and long-term memory. International Journal of Developmental Neuroscience, 31, 353358.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Lubin, F. D., & Sweatt, J. D. (2007). The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron, 55, 942957.Google Scholar
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.Google Scholar
Maharana, C., Sharma, K. P., & Sharma, S. K. (2010). Depolarization induces acetylation of histone H2B in the hippocampus. Neuroscience, 167, 354360.Google Scholar
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.Google Scholar
Margueron, R., Trojer, P., & Reinberg, D. (2005). The key to development: Interpreting the histone code? Current Opinion in Genetics and Development, 15, 163176.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
McQuown, S. C., & Wood, M. A. (2011). HDAC3 and the molecular brake pad hypothesis. Neurobiology of Learning and Memory, 96, 2734.Google Scholar
Mercer, T. R., & Mattick, J. S. (2013). Structure and function of long noncoding RNAs in epigenetic regulation. Nature Structural and Molecular Biology, 20, 300307.Google Scholar
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.Google Scholar
Miller, C. A., & Sweatt, J. D. (2007). Covalent modification of DNA regulates memory formation. Neuron, 53, 857869.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Nikolova, Y. S., & Hariri, A. R. (2015). Can we observe epigenetic effects on human brain function? Trends in Cognitive Sciences, 19, 366373.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Oliveira, A. M., Hemstedt, T. J., & Bading, H. (2012). Rescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities. Nature Neuroscience, 15, 11111113.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Park, H., & Poo, M. M. (2012). Neurotrophin regulation of neural circuit development and function. Nature Reviews Neuroscience, 14, 723.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Portela, A., & Esteller, M. (2010). Epigenetic modifications and human disease. Nature Biotechnology, 28, 10571068.Google Scholar
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.CrossRefGoogle ScholarPubMed
Ptashne, M. (2007). On the use of the word “epigenetic.” Current Biology, 17, R233R236.Google Scholar
Puckett, R. E., & Lubin, F. D. (2011). Epigenetic mechanisms in experience-driven memory formation and behavior. Epigenomics, 3, 649664.Google Scholar
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.Google Scholar
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.Google Scholar
Rett, A. (1966). On an unusual brain atrophy syndrome in hyperammonemia in childhood. Wiener Medizinische Wochenschrift, 116, 723726.Google Scholar
Rideout, W. M. III, Eggan, K., & Jaenisch, R. (2001). Nuclear cloning and epigenetic reprogramming of the genome. Science, 293, 10931098.Google Scholar
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.CrossRefGoogle Scholar
Riggs, A. D. (1975). X inactivation, differentiation, and DNA methylation. Cytogenetics and Genome Research, 14, 925.Google Scholar
Ringrose, L., & Paro, R. (2004). Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annual Review of Genetics, 38, 413443.Google Scholar
Roadmap Epigenomics. (2015). Integrative analysis of 111 reference human epigenomes. Nature, 518, 317330.Google Scholar
Roberson, E. D., & Sweatt, J. D. (2001). Memory-forming chemical reactions. Reviews in the Neurosciences, 12, 4150.Google Scholar
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.Google Scholar
Roth, T. L., & Sweatt, J. D. (2010). Epigenetic marking of the BDNF gene by early-life adverse experiences. Hormones and Behavior, 59, 315320.Google Scholar
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.Google Scholar
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.Google Scholar
Rudenko, A., & Tsai, L.-H. (2014). Epigenetic modifications in the nervous system and their impact upon cognitive impairments. Neuropharmacology, 80, 7082.Google Scholar
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.Google Scholar
Russo, V. E. A., Martienssen, R. A., & Riggs, A. D. (Eds.) (1996). Epigenetic mechanisms of gene regulation. Woodbury, NY: Cold Spring Harbor Laboratory Press.Google Scholar
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.Google Scholar
Sananbenesi, F., & Fischer, A. (2009). The epigenetic bottleneck of neurodegenerative and psychiatric diseases. Biological Chemistry, 390, 11451153.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Schratt, G. M. (2009). microRNAs at the synapse. Nature Reviews Neuroscience, 10, 842849.Google Scholar
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.Google Scholar
Schultz, W. (2002). Getting formal with dopamine and reward. Neuron, 36, 241263.Google Scholar
Schwartz, Y. B., & Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nature Reviews Genetics, 8, 922.Google Scholar
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.Google Scholar
Shahbazian, M. D., & Grunstein, M. (2007). Functions of site-specific histone acetylation and deacetylation. Annual Review of Biochemistry, 76, 75100.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Smith, Z. D., & Meissner, A. (2013). DNA methylation: Roles in mammalian development. Nature Reviews Genetics, 14, 204220.Google Scholar
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.Google Scholar
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.Google Scholar
Strahl, B. D., & Allis, C. D. (2000). The language of covalent histone modifications. Nature, 403, 4145.Google Scholar
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.Google Scholar
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.Google Scholar
Sweatt, J. D. (2001). The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. Journal of Neurochemistry, 76, 110.Google Scholar
Sweatt, J. D. (2009). Experience-dependent epigenetic modifications in the central nervous system. Biological Psychiatry, 65, 191197.Google Scholar
Sweatt, J. D. (2013). The emerging field of neuroepigenetics. Neuron, 80, 624632.Google Scholar
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.Google Scholar
Szyf, M. (2009). Epigenetics DNA methylation, and chromatin modifying drugs. Annual Review of Pharmacology and Toxicology, 49, 243263.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Tsankova, N., Renthal, W., Kumar, A., & Nestler, E. J. (2007). Epigenetic regulation in psychiatric disorders. Nature Reviews Neuroscience, 8, 355367.Google Scholar
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.Google Scholar
Van Speybroeck, L. (2002). From epigenesis to epigenetics: The case of C. H. Waddington. Annals of New York Academy of Sciences, 981, 6181.Google Scholar
Waddington, C. H. (1942). The epigenotype. Endeavour, 1, 1820.Google Scholar
Waddington, C. H. (1957). The strategy of the genes. London: Allen & Unwin.Google Scholar
Walker, F. O. (2007). Huntington's disease. Lancet, 369, 218228.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Wu, C.-T., & Morris, J. R. (2001). Genes, genetics, and epigenetics: A correspondence. Science, 293, 11031105.Google Scholar
Wu, H., & Zhang, Y. (2014). Reversing DNA methylation: Mechanisms, genomics, and biological functions. Cell, 156, 4568.Google Scholar
Wu, S. C., & Zhang, Y. (2010). Active DNA demethylation: Many roads lead to Rome. Nature Reviews Molecular Cell Biology, 11, 607620.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar