Can changes in histone acetylation contribute to memory formation?

Trends in Genetics

Volumn 30, Issue 12, 2014, Pages 529-539

  Lopez Atalaya, Jose P ^a   Barco, Angel ^a  

^a CSIC   (Spain)

Author keywords

Activity driven transcription; Epigenetics; HDACi; Histone acetylation; Histone code; Learning and memory; Transcriptional regulation

Indexed keywords

ACYLTRANSFERASE; ADAPTOR PROTEIN; DNA HELICASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; HISTONE METHYLTRANSFERASE; LYSINE ACYLTRANSFERASE; NEURONAL NITRIC OXIDE SYNTHASE; PROTEIN KINASE; RIBOSOME PROTEIN; RNA HELICASE; UNCLASSIFIED DRUG; HISTONES; TRANSCRIPTION FACTORS;

AMYOTROPHIC LATERAL SCLEROSIS; COGNITION; EPIGENETICS; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HISTONE ACETYLATION; HUMAN; MEMORY; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; NUCLEOSOME; REVIEW; RNA EDITING; ACETYLATION; GENETICS; HUMANS; METABOLISM; MODELS, GENETIC; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS; PHYSIOLOGY; TRANSCRIPTIONAL ACTIVATION;

ACETYLATION; HISTONES; HUMANS; MEMORY; MODELS, GENETIC; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEURONS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84916237122     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2014.09.003     Document Type: Review

References (124)

1. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
2. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294:1030-1038.
3. Fischer A. Epigenetic memory: the Lamarckian brain. EMBO J. 2014, 33:945-967.
4. Zovkic I.B., et al. Epigenetic regulation of memory formation and maintenance. Learn. Mem. 2013, 20:61-74.
5. Sweatt J.D. The emerging field of neuroepigenetics. Neuron 2013, 80:624-632.
6. Day J.J., Sweatt J.D. Epigenetic mechanisms in cognition. Neuron 2011, 70:813-829.
7. Maze I., et al. Histone regulation in the CNS: basic principles of epigenetic plasticity. Neuropsychopharmacology 2013, 38:3-22.
8. Graff J., Tsai L.H. Histone acetylation: molecular mnemonics on the chromatin. Nat. Rev. Neurosci. 2013, 14:97-111.
9. Peixoto L., Abel T. The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 2013, 38:62-76.
10. Graff J., Tsai L.H. The potential of HDAC inhibitors as cognitive enhancers. Annu. Rev. Pharmacol. Toxicol. 2013, 53:311-330.
11. Fischer A., et al. Targeting the correct HDAC(s) to treat cognitive disorders. Trends Pharmacol. Sci. 2010, 31:605-617.
12. Choudhary C., et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
13. Bedford D.C., Brindle P.K. Is histone acetylation the most important physiological function for CBP and p300?. Aging 2012, 4:247-255.
14. Sterner D.E., et al. The SANT domain of Ada2 is required for normal acetylation of histones by the yeast SAGA complex. J. Biol. Chem. 2002, 277:8178-8186.
15. Sun Z., et al. Deacetylase-independent function of HDAC3 in transcription and metabolism requires nuclear receptor corepressor. Mol. Cell 2013, 52:769-782.
16. Fischle W., et al. Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol. Cell 2002, 9:45-57.
17. Lahm A., et al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:17335-17340.
18. Korzus E., et al. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
19. Chueh A.C., et al. Mechanisms of histone deacetylase inhibitor-regulated gene expression in cancer cells. Antioxid. Redox Signal. 2014, 10.1089/ars.2014.5863.
20. Vecsey C.G., et al. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 2007, 27:6128-6140.
21. Johnstone R.W., Licht J.D. Histone deacetylase inhibitors in cancer therapy: is transcription the primary target?. Cancer Cell 2003, 4:13-18.
22. Gaub P., et al. HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ. 2010, 17:1392-1408.
23. Brochier C., et al. Specific acetylation of p53 by HDAC inhibition prevents DNA damage-induced apoptosis in neurons. J. Neurosci. 2013, 33:8621-8632.
24. Dompierre J.P., et al. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 2007, 27:3571-3583.
25. 14C-acetate into the histones of different rat brain regions during a learning experiment. Acta Biol. Med. Ger. 1979, 38:683-689. (in German).
26. Castellano J.F., et al. Reassessing the effects of histone deacetylase inhibitors on hippocampal memory and cognitive aging. Hippocampus 2014, 24:1006-1016.
27. Allfrey V.G., et al. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. U.S.A. 1964, 51:786-794.
28. Kurdistani S.K., Grunstein M. Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell Biol. 2003, 4:276-284.
29. Turner B.M. The adjustable nucleosome: an epigenetic signaling module. Trends Genet. 2012, 28:436-444.
30. Mutskov V., et al. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol. Cell. Biol. 1998, 18:6293-6304.
31. Neumann H., et al. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 2009, 36:153-163.
32. Shogren-Knaak M., et al. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
33. Huang H., et al. HistoneHits: a database for histone mutations and their phenotypes. Genome Res. 2009, 19:674-681.
34. Martin A.M., et al. Redundant roles for histone H3 N-terminal lysine residues in subtelomeric gene repression in Saccharomyces cerevisiae. Genetics 2004, 167:1123-1132.
35. Dion M.F., et al. Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5501-5506.
36. Ling X., et al. Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. Genes Dev. 1996, 10:686-699.
37. Clapier C.R., et al. A critical epitope for substrate recognition by the nucleosome remodeling ATPase ISWI. Nucleic Acids Res. 2002, 30:649-655.
38. Schubeler D., et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004, 18:1263-1271.
39. Wang Z., et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 2008, 40:897-903.
40. Hall S.E., et al. A cellular memory of developmental history generates phenotypic diversity in C. elegans. Curr. Biol. 2010, 20:149-155.
41. Kharchenko P.V., et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 2011, 471:480-485.
42. Hodl M., Basler K. Transcription in the absence of histone H3.3. Curr. Biol. 2009, 19:1221-1226.
43. Anamika K., et al. Lessons from genome-wide studies: an integrated definition of the coactivator function of histone acetyl transferases. Epigenetics Chromatin 2010, 3:18.
44. Zhang H., et al. Uncoupling transcription from covalent histone modification. PLoS Genet. 2014, 10:e1004202.
45. Lopez-Atalaya J.P., et al. Genomic targets, and histone acetylation and gene expression profiling of neural HDAC inhibition. Nucleic Acids Res. 2013, 41:8072-8084.
46. Kaneda R., et al. Genome-wide screening for target regions of histone deacetylases in cardiomyocytes. Circ. Res. 2005, 97:210-218.
47. Valor L.M., et al. Genomic landscape of transcriptional and epigenetic dysregulation in early onset polyglutamine disease. J. Neurosci. 2013, 33:10471-10482.
48. Shin J.H., et al. Genome-wide ChIP-seq mapping and analysis reveal butyrate-induced acetylation of H3K9 and H3K27 correlated with transcription activity in bovine cells. Funct. Integr. Genomics 2012, 12:119-130.
49. Osorio F.G., et al. Nuclear envelope alterations generate an aging-like epigenetic pattern in mice deficient in Zmpste24 metalloprotease. Aging Cell 2010, 9:947-957.
50. Dudakovic A., et al. Histone deacetylase inhibition promotes osteoblast maturation by altering the histone H4 epigenome and reduces Akt phosphorylation. J. Biol. Chem. 2013, 288:28783-28791.
51. Wang Z., et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009, 138:1019-1031.
52. Yamagoe S., et al. Interaction of histone acetylases and deacetylases in vivo. Mol. Cell. Biol. 2003, 23:1025-1033.
53. Silva A.J., et al. Molecular and cellular approaches to memory allocation in neural circuits. Science 2009, 326:391-395.
54. Garner A.R., et al. Generation of a synthetic memory trace. Science 2012, 335:1513-1516.
55. Ramirez S., et al. Creating a false memory in the hippocampus. Science 2013, 341:387-391.
56. Deng W., et al. Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. Elife 2013, 2:e00312.
57. Guzowski J.F., et al. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr. Opin. Neurobiol. 2005, 15:599-606.
58. Dagnas M., Mons N. Region- and age-specific patterns of histone acetylation related to spatial and cued learning in the water maze. Hippocampus 2013, 23:581-591.
59. Graff J., et al. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 2014, 156:261-276.
60. Bilang-Bleuel A., et al. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioural response. Eur. J. Neurosci. 2005, 22:1691-1700.
61. Crepaldi L., et al. Binding of TFIIIC to sine elements controls the relocation of activity-dependent neuronal genes to transcription factories. PLoS Genet. 2013, 9:e1003699.
62. Park C.S., et al. Genome-wide analysis of H4K5 acetylation associated with fear memory in mice. BMC Genomics 2013, 14:539.
63. Graff J., et al. Dynamic histone marks in the hippocampus and cortex facilitate memory consolidation. Nat. Commun. 2012, 3:991.
64. Barrett R.M., Wood M.A. Beyond transcription factors: the role of chromatin modifying enzymes in regulating transcription required for memory. Learn. Mem. 2008, 15:460-467.
65. Zentner G.E., Henikoff S. Regulation of nucleosome dynamics by histone modifications. Nat. Struct. Mol. Biol. 2013, 20:259-266.
66. van Attikum H., Gasser S.M. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 2009, 19:207-217.
67. Taverna S.D., et al. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 2007, 14:1025-1040.
68. Sanchez R., et al. The bromodomain: from epigenome reader to druggable target. Biochim. Biophys. Acta 2014, 1839:676-685.
69. Waddington C.H. The Strategy of the Genes: A Discussion of Some Aspects of Theoretical Biology 1957, Allen & Unwin.
70. Henikoff S., Shilatifard A. Histone modification: cause or cog?. Trends Genet. 2011, 27:389-396.
71. Guertin M.J., Lis J.T. Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet. 2010, 6:e1001114.
72. Raj A., et al. Stochastic mRNA synthesis in mammalian cells. PLoS Biol. 2006, 4:e309.
73. Bonn S., et al. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat. Genet. 2012, 44:148-156.
74. Xie W., et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 2013, 153:1134-1148.
75. Gifford C.A., et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 2013, 153:1149-1163.
76. Zhu J., et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 2013, 152:642-654.
77. Kasper L.H., et al. CBP/p300 double null cells reveal effect of coactivator level and diversity on CREB transactivation. EMBO J. 2010, 29:3660-3672.
78. Valor L.M., et al. Ablation of CBP in forebrain principal neurons causes modest memory and transcriptional defects and a dramatic reduction of histone acetylation, but does not affect cell viability. J. Neurosci. 2011, 31:1652-1663.
79. Jin Q., et al. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J. 2011, 30:249-262.
80. Bolden J.E., et al. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 2006, 5:769-784.
81. Allis C.D., et al. New nomenclature for chromatin-modifying enzymes. Cell 2007, 131:633-636.
82. Dudai Y. Memory from A to Z: Keywords, Concepts, and Beyond 2002, Oxford University Press.
83. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
84. Tan M., et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011, 146:1016-1028.
85. Sims R.J., Reinberg D. Is there a code embedded in proteins that is based on post-translational modifications?. Nat. Rev. Mol. Cell Biol. 2008, 9:815-820.
86. Rando O.J. Combinatorial complexity in chromatin structure and function: revisiting the histone code. Curr. Opin. Genet. Dev. 2012, 22:148-155.
87. Gardner K.E., et al. Operating on chromatin, a colorful language where context matters. J. Mol. Biol. 2011, 409:36-46.
88. Lee J.S., et al. The language of histone crosstalk. Cell 2010, 142:682-685.
89. Zhao S., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327:1000-1004.
90. Lundby A., et al. Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep. 2012, 2:419-431.
91. Yang X.J., Seto E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell 2008, 31:449-461.
92. Liu Z., et al. CPLM: a database of protein lysine modifications. Nucleic Acids Res. 2014, 42:D531-D536.
93. Tang Y., et al. Acetylation is indispensable for p53 activation. Cell 2008, 133:612-626.
94. Hirayama J., et al. CLOCK-mediated acetylation of BMAL1 controls circadian function. Nature 2007, 450:1086-1090.
95. Chen L., et al. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 2001, 293:1653-1657.
96. Schroder S., et al. Acetylation of RNA polymerase II regulates growth-factor-induced gene transcription in mammalian cells. Mol. Cell 2013, 52:314-324.
97. Chen S., et al. Repression of RNA polymerase I upon stress is caused by inhibition of RNA-dependent deacetylation of PAF53 by SIRT7. Mol. Cell 2013, 52:303-313.
98. Liu D., et al. Proteomic analysis reveals differentially regulated protein acetylation in human amyotrophic lateral sclerosis spinal cord. PLoS ONE 2013, 8:e80779.
99. Jeong H., et al. Acetylation targets mutant huntingtin to autophagosomes for degradation. Cell 2009, 137:60-72.
100. Zocchi L., Sassone-Corsi P. SIRT1-mediated deacetylation of MeCP2 contributes to BDNF expression. Epigenetics 2012, 7:695-700.
101. Shalizi A., et al. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 2006, 311:1012-1017.
102. Yeh S.H., et al. Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory. Mol. Pharmacol. 2004, 65:1286-1292.
103. Federman N., et al. Nuclear factor κB-dependent histone acetylation is specifically involved in persistent forms of memory. J. Neurosci. 2013, 33:7603-7614.
104. Lanzillotta A., et al. The acetylation of RelA in Lys310 dictates the NF-κB-dependent response in post-ischemic injury. Cell Death Dis. 2010, 1:e96.
105. Chen J., et al. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling. J. Biol. Chem. 2005, 280:40364-40374.
106. Cuccurazzu B., et al. Upregulation of mGlu2 receptors via NF-κB p65 acetylation is involved in the proneurogenic and antidepressant effects of acetyl-L-carnitine. Neuropsychopharmacology 2013, 38:2220-2230.
107. Lanzillotta A., et al. Targeted acetylation of NF-kappaB/RelA and histones by epigenetic drugs reduces post-ischemic brain injury in mice with an extended therapeutic window. Neurobiol. Dis. 2012, 49C:177-189.
108. Li Y., et al. Role of p300 in regulating neuronal nitric oxide synthase gene expression through nuclear factor-κB-mediated way in neuronal cells. Neuroscience 2013, 248:681-689.
109. Di Giovanni S., et al. The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J. 2006, 25:4084-4096.
110. Ichi S., et al. Role of Pax3 acetylation in the regulation of Hes1 and Neurog2. Mol. Biol. Cell 2011, 22:503-512.
111. Cohen T.J., et al. The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat. Commun. 2011, 2:252.
112. Noack M., et al. HDAC6 inhibition results in tau acetylation and modulates tau phosphorylation and degradation in oligodendrocytes. Glia 2014, 62:535-547.
113. Kim G.W., et al. Mice lacking α-tubulin acetyltransferase 1 are viable but display α-tubulin acetylation deficiency and dentate gyrus distortion. J. Biol. Chem. 2013, 288:20334-20350.
114. Li L., et al. MEC-17 deficiency leads to reduced α-tubulin acetylation and impaired migration of cortical neurons. J. Neurosci. 2012, 32:12673-12683.
115. Beurel E. HDAC6 regulates LPS-tolerance in astrocytes. PLoS ONE 2011, 6:e25804.
116. d'Ydewalle C., et al. HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease. Nat. Med. 2011, 17:968-974.
117. Xu X., et al. A selective histone deacetylase-6 inhibitor improves BDNF trafficking in hippocampal neurons from Mecp2 knockout mice: implications for Rett syndrome. Front. Cell. Neurosci. 2014, 8:68.
118. de Groote M.L., et al. Epigenetic editing: targeted rewriting of epigenetic marks to modulate expression of selected target genes. Nucleic Acids Res. 2012, 40:10596-10613.
119. Pick H., et al. Engineering chromatin states: chemical and synthetic biology approaches to investigate histone modification function. Biochim. Biophys. Acta 2014, 1839:644-656.
120. Hathaway N.A., et al. Dynamics and memory of heterochromatin in living cells. Cell 2012, 149:1447-1460.
121. Konermann S., et al. Optical control of mammalian endogenous transcription and epigenetic states. Nature 2013, 500:472-476.
122. Gilbert L.A., et al. CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 2013, 154:442-451.
123. Chrivia J.C., et al. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 1993, 365:855-859.
124. Nott A., et al. S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 2008, 455:411-415.