Regulation of chromatin structure in memory formation

This brief review focuses on the role of epigenetic mechanisms in plasticity and memory formation, and their identification as targets of activity-dependent regulation in neurons. Epigenetic modifications of chromatin, namely post-translational modifications of nuclear proteins and covalent modification of DNA, result in potent regulation of gene readout. Recent data have demonstrated that epigenetic mechanisms play a significant role in regulating synaptic plasticity and memory. In this review, we focus on this theme, describing some basic background concerning epigenetic molecular mechanisms, and describing recent results concerning plasticity and memory formation. As an understanding of these novel mechanisms of transcriptional regulation promises to invigorate many areas of investigation, we end by speculating upon some of the open questions ripe for discovery.

[1]  Stephen T. C. Wong,et al.  MeCP2, a Key Contributor to Neurological Disease, Activates and Represses Transcription , 2008, Science.

[2]  M. Greenberg,et al.  Activating a Repressor , 2008, Science.

[3]  Christopher M. Gallo,et al.  Diversity in the Sir2 family of protein deacetylases , 2004, Journal of leukocyte biology.

[4]  J. David Sweatt,et al.  The MAPK cascade is required for mammalian associative learning , 1998, Nature Neuroscience.

[5]  J. Sweatt,et al.  Epigenetic Regulation of bdnf Gene Transcription in the Consolidation of Fear Memory , 2008, The Journal of Neuroscience.

[6]  David R. Liu,et al.  Conversion of 5-Methylcytosine to 5- Hydroxymethylcytosine in Mammalian DNA by the MLL Partner TET1 , 2009 .

[7]  Vladimir Benes,et al.  Transient cyclical methylation of promoter DNA , 2008, Nature.

[8]  J. Sweatt,et al.  Covalent Modification of DNA Regulates Memory Formation , 2007, Neuron.

[9]  T. Bredy,et al.  Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. , 2007, Learning & memory.

[10]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[11]  Yang Shi,et al.  Dynamic regulation of histone lysine methylation by demethylases. , 2007, Molecular cell.

[12]  G. Ming,et al.  Neuronal Activity–Induced Gadd45b Promotes Epigenetic DNA Demethylation and Adult Neurogenesis , 2009, Science.

[13]  E. Kavalali,et al.  Activity-Dependent Suppression of Miniature Neurotransmission through the Regulation of DNA Methylation , 2008, The Journal of Neuroscience.

[14]  James P. Curley,et al.  Epigenetic mechanisms mediating the long-term effects of maternal care on development , 2009, Neuroscience & Biobehavioral Reviews.

[15]  D. Molfese,et al.  Regulation of Histone Acetylation during Memory Formation in the Hippocampus* , 2004, Journal of Biological Chemistry.

[16]  Shaomin Li,et al.  Transgenerational Rescue of a Genetic Defect in Long-Term Potentiation and Memory Formation by Juvenile Enrichment , 2009, The Journal of Neuroscience.

[17]  Michael J Meaney,et al.  Epigenetic programming by maternal behavior , 2004, Nature Neuroscience.

[18]  I. Weaver,et al.  Regional-specific global cytosine methylation and DNA methyltransferase expression in the adult rat hippocampus , 2008, Neuroscience Letters.

[19]  T. Abel,et al.  Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits. , 2007, Learning & memory.

[20]  Peter A. Jones,et al.  DNA methylation: The nuts and bolts of repression , 2007, Journal of cellular physiology.

[21]  E. Kandel,et al.  Chromatin Acetylation, Memory, and LTP Are Impaired in CBP+/− Mice A Model for the Cognitive Deficit in Rubinstein-Taybi Syndrome and Its Amelioration , 2004, Neuron.

[22]  A. Célérier,et al.  Altered Memory Capacities and Response to Stress in p300/CBP-Associated Factor (PCAF) Histone Acetylase Knockout Mice , 2008, Neuropsychopharmacology.

[23]  Joel M Stein,et al.  Histone Deacetylase Inhibitors Enhance Memory and Synaptic Plasticity via CREB: CBP-Dependent Transcriptional Activation , 2007, The Journal of Neuroscience.

[24]  L. Thompson,et al.  Therapeutic application of histone deacetylase inhibitors for central nervous system disorders , 2008, Nature Reviews Drug Discovery.

[25]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[26]  T. Bale,et al.  Sex-Specific Programming of Offspring Emotionality after Stress Early in Pregnancy , 2008, The Journal of Neuroscience.

[27]  A. Mortazavi,et al.  Genome-Wide Mapping of in Vivo Protein-DNA Interactions , 2007, Science.

[28]  Raja Jothi,et al.  Genome-wide identification of in vivo protein–DNA binding sites from ChIP-Seq data , 2008, Nucleic acids research.

[29]  A. Bird DNA methylation patterns and epigenetic memory. , 2002, Genes & development.

[30]  T. Abel,et al.  Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. , 2008, Current opinion in pharmacology.

[31]  T. Abel,et al.  Combinatorial chromatin modifications and memory storage: a code for memory? , 2006, Learning & memory.

[32]  N. Heintz,et al.  The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain , 2009, Science.

[33]  R. Marmorstein,et al.  Structure and function of histone acetyltransferases , 2001, Cellular and Molecular Life Sciences CMLS.

[34]  C. Allis,et al.  The language of covalent histone modifications , 2000, Nature.

[35]  S. Akbarian,et al.  Epigenetic Regulation in Human Brain—Focus on Histone Lysine Methylation , 2009, Biological Psychiatry.

[36]  Li-Huei Tsai,et al.  Recovery of learning and memory is associated with chromatin remodelling , 2007, Nature.

[37]  J. David Sweatt,et al.  Evidence That DNA (Cytosine-5) Methyltransferase Regulates Synaptic Plasticity in the Hippocampus* , 2006, Journal of Biological Chemistry.

[38]  I. Mansuy,et al.  Epigenetic codes in cognition and behaviour , 2008, Behavioural Brain Research.

[39]  C. Disteche,et al.  Sex-Specific Expression of the X-Linked Histone Demethylase Gene Jarid1c in Brain , 2008, PloS one.

[40]  M. Szyf Epigenetics, DNA methylation, and chromatin modifying drugs. , 2009, Annual review of pharmacology and toxicology.

[41]  J. David Sweatt,et al.  Experience-Dependent Epigenetic Modifications in the Central Nervous System , 2009, Biological Psychiatry.

[42]  E. Olson,et al.  The many roles of histone deacetylases in development and physiology: implications for disease and therapy , 2009, Nature Reviews Genetics.

[43]  K. Martin,et al.  To Learn Better, Keep the HAT on , 2004, Neuron.

[44]  T. Bredy,et al.  The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. , 2008, Learning & memory.

[45]  J. Sweatt,et al.  DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity , 2008, Neurobiology of Learning and Memory.

[46]  J. Sweatt,et al.  Lasting Epigenetic Influence of Early-Life Adversity on the BDNF Gene , 2009, Biological Psychiatry.

[47]  E. Nestler,et al.  Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action , 2006, Nature Neuroscience.

[48]  M. Mayford,et al.  CBP Histone Acetyltransferase Activity Is a Critical Component of Memory Consolidation , 2004, Neuron.

[49]  Albert Jeltsch,et al.  Cyclical DNA methylation of a transcriptionally active promoter , 2008, Nature.

[50]  Paolo Sassone-Corsi,et al.  Decoding the Epigenetic Language of Neuronal Plasticity , 2008, Neuron.