Brain function and chromatin plasticity

Nature

Volumn 465, Issue 7299, 2010, Pages 728-735

  Dulac, Catherine ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIOR; BRAIN; CHROMOSOME; DISEASE; GENE EXPRESSION; HERITABILITY; NEUROLOGY; SIGNAL;

BRAIN FUNCTION; CHROMATIN; CHROMATIN STRUCTURE; DNA METHYLATION; ELECTROENCEPHALOGRAM; EPIGENETICS; GENE EXPRESSION; HUMAN; MITOSIS; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; GENOMIC IMPRINTING; HISTONES; HUMANS; INHERITANCE PATTERNS; NEURONAL PLASTICITY;

EID: 77953429462     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09231     Document Type: Review

References (102)

1. Squire, L. R. Memory and Brain (Oxford Univ. Press, 1987).
2. Berger, S. L., Kouzarides, T., Shiekhattar, R. & Shilatifard, A. An operational definition of epigenetics. Genes Dev. 23, 781-783 (2009).
3. Ptashne, M. On the use of the word 'epigenetic'. Curr. Biol. 1 7, R233-R236 (2007)
4. References 2 and 3 are interesting reviews on the meaning and potential mechanisms of epigenetic regulation.
5. Kramer, J. M. & van Bokhoven, H. Genetic and epigenetic defects in mental retardation. Int. J. Biochem. Cell Biol. 41, 96-107 (2009).
6. Ramocki, M. B. & Zoghbi, H. Y. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 455, 912-918 (2008).
7. Guan, Z. et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111, 483-493 (2002).
8. Amir, R. E. et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nature Genet. 23, 185-188 (1999).
9. Chen, R. Z., Akbarian, S., Tudor, M. & Jaenisch, R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nature Genet. 27, 327-331 (2001).
10. Guy, J., Hendrich, B., Holmes, M., Martin, J. E. & Bird, A. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nature Genet. 27, 322-326 (2001).
11. Luikenhuis, S., Giacometti, E., Beard, C. F. & Jaenisch, R. Expression of MeCP2 in postmitotic neurons rescues Rett syndrome in mice. Proc. Natl Acad. Sci. USA 101, 6033-6038 (2004).
12. Chen, W. G. et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302, 885-889 (2003).
13. Martinowich, K. et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302, 890-893 (2003).
14. Chahrour, M. et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320, 1224-1229 (2008).
15. Zhao, X. et al. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl Acad. Sci. USA 100, 6777-6782 (2003).
16. Martin Caballero, I., Hansen, J., Leaford, D., Pollard, S. & Hendrich, B. D. The methyl-CpG binding proteins Mecp2, Mbd2 and Kaiso are dispensable for mouse embryogenesis, but play a redundant function in neural differentiation. PLoS ONE 4, e4315 (2009).
17. Feng, J. & Fan, G. The role of DNA methylation in the central nervous system and neuropsychiatric disorders. Int. Rev. Neurobiol. 89, 67-84 (2009).
18. Ma, D. K. et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077 (2009).
19. Barreto, G. et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671-675 (2007).
20. Jin, Y. H. et al. Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet. 4, e1000053 (2008).
21. Okada, Y., Yamagata, K., Hong, K., Wakayama, T. & Zhang, Y. A role for the elongator complex in zygotic paternal genome demethylation. Nature 463, 554-558 (2010).
22. Rai, K. et al. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135, 1201-1212 (2008).
23. Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930 (2009).
24. Flavell, S. W. & Greenberg, M. E. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 31, 563-590 (2008).
25. Kandel, E. R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038 (2001).
26. Tsankova, N. M., Kumar, A. & Nestler, E. J. Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J. Neurosci. 24, 5603-5610 (2004).
27. Koshibu, K. et al. Protein phosphatase 1 regulates the histone code for long-term memory. J. Neurosci. 29, 13079-13089 (2009).
28. Kumar, A. et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48, 303-314 (2005).
29. Levenson, J. M. et al. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 279, 40545-40559 (2004).
30. Renthal, W. et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56, 517-529 (2007).
31. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M. & Tsai, L. H. Recovery of learning and memory is associated with chromatin remodelling. Nature 447, 178-182 (2007).
32. Guan, J. S. et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55-60 (2009).
33. Ptak, C. & Petronis, A. Epigenetics and complex disease: from etiology to new therapeutics. Annu. Rev. Pharmacol. Toxicol. 48, 257-276 (2008).
34. +/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42, 947-959 (2004).
35. Korzus, E., Rosenfeld, M. G. & Mayford, M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961-972 (2004).
36. Schaefer, A. et al. Control of cognition and adaptive behavior by the GLP/G9a epigenetic suppressor complex. Neuron 64, 678-691 (2009).
37. Bracken, A. P., Dietrich, N., Pasini, D., Hansen, K. H. & Helin, K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20, 1123-1136 (2006).
38. Hirabayashi, Y. et al. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 63, 600-613 (2009).
39. Maze, I. et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327, 213-216 (2010).
40. Katan-Khaykovich, Y. & Struhl, K. Dynamics of global histone acetylation and deacetylation in vivo: rapid restoration of normal histone acetylation status upon removal of activators and repressors. Genes Dev. 16, 743-752 (2002).
41. Radman-Livaja, M., Liu, C. L., Friedman, N., Schreiber, S. L. & Rando, O. J. Replication and active demethylation represent partially overlapping mechanisms for erasure of H3K4me3 in budding yeast. PLoS Genet. 6, e1000837 (2010).
42. Mohn, F. et al. Lineage-specific Polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766 (2008). This paper provides an insightful analysis of the changes in DNA and histone H3 methylation at promoter regions during cell-fate determination and early differentiation of neuronal progenitors.
43. Wong, A. H., Gottesman, I. I. & Petronis, A. Phenotypic differences in genetically identical organisms: the epigenetic perspective. Hum. Mol. Genet. 14, R11-R18 (2005).
44. Gartner, K. A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals? Lab. Anim. 24, 71-77 (1990).
45. Tamashiro, K. L. et al. Phenotype of cloned mice: development, behavior, and physiology. Exp. Biol. Med. 228, 1193-1200 (2003).
46. Weksberg, R. et al. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum. Mol. Genet. 11, 1317-1325 (2002).
47. Raj, A. & van Oudenaarden, A. Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-226 (2008).
48. Raj, A., Rifkin, S. A., Andersen, E. & van Oudenaarden, A. Variability in gene expression underlies incomplete penetrance. Nature 463, 913-918 (2010).
49. Francis, D. D., Szegda, K., Campbell, G., Martin, W. D. & Insel, T. R. Epigenetic sources of behavioral differences in mice. Nature Neurosci. 6, 445-446 (2003).
50. McMillen, I. C. & Robinson, J. S. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571-633 (2005).
51. Waterland, R. A. & Jirtle, R. L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 23, 5293-5300 (2003).
52. vy/a mice. FASEB J. 12, 949-957 (1998).
53. Waterland, R. A. & Jirtle, R. L. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20, 63-68 (2004).
54. Levine, S. Infantile experience and resistance to physiological stress. Science 126, 405 (1957).
55. Denenberg, V. H., Brumaghim, J. T., Haltmeyer, G. C. & Zarrow, M. X. Increased adrenocortical activity in the neonatal rat following handling. Endocrinology 81, 1047-1052 (1967).
56. Meaney, M. J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161-1192 (2001).
57. Weaver, I. C. et al. Epigenetic programming by maternal behavior. Nature Neurosci. 7, 847-854 (2004).
58. Murgatroyd, C. et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neurosci. 12, 1559-1566 (2009).
59. Cirulli, F. et al. Early life stress as a risk factor for mental health: role of neurotrophins from rodents to non-human primates. Neurosci. Biobehav. Rev. 33, 573-585 (2009).
60. Jirtle, R. L. & Skinner, M. K. Environmental epigenomics and disease susceptibility. Nature Rev. Genet. 8, 253-262 (2007).
61. Keverne, E. B. Genomic imprinting and the evolution of sex differences in mammalian reproductive strategies. Adv. Genet. 59, 217-243 (2007).
62. Wilkins, J. F. & Haig, D. What good is genomic imprinting: the function of parent-specific gene expression. Nature Rev. Genet. 4, 359-368 (2003).
63. Wolf, J. B. & Hager, R. A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol. 4, e380 (2006).
64. DeChiara, T. M., Robertson, E. J. & Efstratiadis, A. Parental imprinting of the mouse insulinlike growth factor II gene. Cell 64, 849-859 (1991).
65. Barlow, D. P., Stoger, R., Herrmann, B. G., Saito, K. & Schweifer, N. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the T m e locus. Nature 349, 84-87 (1991).
66. Fowden, A. L., Sibley, C., Reik, W. & Constancia, M. Imprinted genes, placental development and fetal growth. Horm. Res. 65 (suppl. 3), 50-58 (2006).
67. Reik, W. & Walter, J. Genomic imprinting: parental influence on the genome. Nature Rev. Genet. 2, 21-32 (2001).
68. Luedi, P. P., Hartemink, A. J. & Jirtle, R. L. Genome-wide prediction of imprinted murine genes. Genome Res. 15, 875-884 (2005).
69. Davies, W. et al. Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nature Genet. 37, 625-629 (2005).
70. Raefski, A. S. & O'Neill, M. J. Identification of a cluster of X-linked imprinted genes in mice. Nature Genet. 37, 620-624 (2005).
71. Wilkinson, L. S., Davies, W. & Isles, A. R. Genomic imprinting effects on brain development and function. Nature Rev. Neurosci. 8, 832-843 (2007).
72. Kozlov, S. V. et al. The imprinted gene Magel2 regulates normal circadian output. Nature Genet. 39, 1266-1272 (2007).
73. Richards, E. J. Inherited epigenetic variation\revisiting soft inheritance. Nature Rev. Genet. 7, 395-401 (2006).
74. Lim, A. L. & Ferguson-Smith, A. C. Genomic imprinting effects in a compromised in utero environment: implications for a healthy pregnancy. Semin. Cell Dev. Biol. 21, 201-208 (2010).
75. Patisaul, H. B. & Adewale, H. B. Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior. Front. Behav. Neurosci. 3, 10 (2009).
76. Weaver, I. C. et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 25, 11045-11054 (2005).
77. Whitelaw, N. C. & Whitelaw, E. Transgenerational epigenetic inheritance in health and disease. Curr. Opin. Genet. Dev. 18, 273-279 (2008).
78. Agalioti, T., Chen, G. & Thanos, D. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111, 381-392 (2002).
79. Matzke, M., Kanno, T., Huettel, B., Daxinger, L. & Matzke, A. J. RNA-directed DNA methylation and Pol IVb in Arabidopsis. Cold Spring Harb. Symp. Quant. Biol. 71, 449-459 (2006).
80. Rinn, J. L. et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129, 1311-1323 (2007).
81. Francis, N. J., Follmer, N. E., Simon, M. D., Aghia, G. & Butler, J. D. Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137, 110-122 (2009).
82. Creppe, C. et al. Elongator controls the migration and differentiation of cortical neurons through acetylation of α-tubulin. Cell 136, 551-564 (2009).
83. Kim, A. H. et al. A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 136, 322-336 (2009).
84. Deato, M. D. & Tjian, R. Switching of the core transcription machinery during myogenesis. Genes Dev. 21, 2137-2149 (2007).
85. De Bustos, C. et al. Tissue-specific variation in DNA methylation levels along human chromosome 1. Epigenetics Chromatin 2, 7 (2009).
86. Lister, R. et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322 (2009).
87. Meissner, A. et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770 (2008).
88. Mikkelsen, T. S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560 (2007).
89. Goll, M. G. & Bestor, T. H. Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481-514 (2005).
90. Gehring, M., Reik, W. & Henikoff, S. DNA demethylation by DNA repair. Trends Genet. 25, 82-90 (2009).
91. Jost, J. P. et al. 5-Methylcytosine DNA glycosylase participates in the genome-wide loss of DNA methylation occurring during mouse myoblast differentiation. Nucleic Acids Res. 29, 4452-4461 (2001).
92. Kangaspeska, S. et al. Transient cyclical methylation of promoter DNA. Nature 452, 112-115 (2008).
93. Metivier, R. et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 45-50 (2008).
94. Popp, C. et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105 (2010).
95. Bhutani, N. et al. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463, 1042-1047 (2010).
96. Allis, C. D. et al. New nomenclature for chromatin-modifying enzymes. Cell 131, 633-636 (2007).
97. Campos, E. I. & Reinberg, D. Histones: annotating chromatin. Annu. Rev. Genet. 43, 559-599 (2009).
98. Ruthenburg, A. J., Li, H., Patel, D. J. & Allis, C. D. Multivalent engagement of chromatin modifications by linked binding modules. Nature Rev. Mol. Cell Biol. 8, 983-994 (2007)
99. References 96 and 97 are insightful reviews on the functional significance of individual, or patterns of, histone modifications, with a debate on a revised histone-code hypothesis.
100. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000).
101. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
102. Wang, Z. et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nature Genet. 40, 897-903 (2008).