DNA methylation changes in plasticity genes accompany the formation and maintenance of memory

Nature Neuroscience

Volumn 19, Issue 1, 2015, Pages 102-110

  Halder, Rashi ^a   Hennion, Magali ^a   Vidal, Ramon O ^a   Shomroni, Orr ^a   Rahman, Raza Ur ^a   Rajput, Ashish ^a   Centeno, Tonatiuh Pena ^a   Van Bebber, Frauke ^a   Capece, Vincenzo ^a   Vizcaino, Julio C Garcia ^a   Schuetz, Anna Lena ^a   Burkhardt, Susanne ^a   Benito, Eva ^a   Sala, Magdalena Navarro ^a   Javan, Sanaz Bahari ^a   Haass, Christian ^a,b,c   Schmid, Bettina ^a,c   Fischer, Andre ^a,d   Bonn, Stefan ^a  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c Ludwig Maximilians University Munich ^*  (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; CHROMATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; ASSOCIATIVE MEMORY; BRAIN NERVE CELL; CELL FUNCTION; CELLS BY BODY ANATOMY; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEAR CONDITIONING TEST; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HISTONE METHYLATION; HISTONE MODIFICATION; LEARNING; LONG TERM MEMORY; MALE; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; RNA SPLICING; SHORT TERM MEMORY; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMISTRY; CINGULATE GYRUS; CONDITIONING; FEAR; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CA1 REGION, HIPPOCAMPAL; CHROMATIN; CONDITIONING (PSYCHOLOGY); DNA METHYLATION; EPIGENESIS, GENETIC; FEAR; GENE EXPRESSION; GYRUS CINGULI; HISTONES; MALE; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY;

EID: 84953836674     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4194     Document Type: Article

References (66)

1. Guzman-Karlsson M.C., Meadows J.P., Gavin C.F., Hablitz J.J., & Sweatt J.D. Transcriptional and epigenetic regulation of Hebbian and non-Hebbian plasticity. Neuropharmacology. 80, 3-17 (2014).
2. Gräff J., & Tsai L.-H. Histone acetylation: molecular mnemonics on the chromatin. Nat. Rev. Neurosci. 14, 97-111 (2013).
3. Zovkic I.B., Guzman-Karlsson M.C., & Sweatt J.D. Epigenetic regulation of memory formation and maintenance. Learn. Mem. 20, 61-74 (2013).
4. Sweatt J.D. The emerging field of neuroepigenetics. Neuron. 80, 624-632 (2013).
5. Lopez-Atalaya J.P., & Barco A. Can Changes in Histone Acetylation Contribute to Memory Formation? Trends Genet. 30, 529-539 (2014).
6. Levenson J.M., et al. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 279, 40545-40559 (2004).
7. Gupta S., et al. Histone methylation regulates memory formation. J. Neurosci. 30, 3589-3599 (2010).
8. Miller C.A., & Sweatt J.D. Covalent modification of DNA regulates memory formation. Neuron. 53, 857-869 (2007).
9. Miller C.A., et al. Cortical DNA methylation maintains remote memory. Nat. Neurosci. 13, 664-666 (2010).
10. Strahl B.D., & Allis C.D. The language of covalent histone modifications. Nature. 403, 41-45 (2000).
11. Day J.J., & Sweatt J.D. Epigenetic mechanisms in cognition. Neuron. 70, 813-829 (2011).
12. Fischer A. Epigenetic memory: the Lamarckian brain. EMBO J. 33, 945-967 (2014).
13. Fanselow M.S. Factors governing one-Trial contextual conditioning. Anim. Learn. Behav. 18, 264-270 (1990).
14. Kim J.J., & Fanselow M.S. Modality-specific retrograde amnesia of fear. Science. 256, 675-677 (1992).
15. Runyan J.D., Moore A.N., & Dash P.K. A role for prefrontal cortex in memory storage for trace fear conditioning. J. Neurosci. 24, 1288-1295 (2004).
16. Einarsson E.O., & Nader K. Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory. Learn. Mem. 19, 449-452 (2012).
17. Bonn S., et al. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development. Nat. Genet. 44, 148-156 (2012).
18. Bonn S., et al. Cell type-specific chromatin immunoprecipitation from multicellular complex samples using BiTS-ChIP. Nat. Protoc. 7, 978-994 (2012).
19. Jiang Y., Matevossian A., Huang H.-S., Straubhaar J., & Akbarian S. Isolation of neuronal chromatin from brain tissue. BMC Neurosci. 9, 42 (2008).
20. Peleg S., et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science. 328, 753-756 (2010).
21. Barski A., et al. High-resolution profiling of histone methylations in the human genome. Cell. 129, 823-837 (2007).
22. Zhou V.W., Goren A., & Bernstein B.E. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12, 7-18 (2010).
23. Cahoy J.D., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28, 264-278 (2008).
24. Ko Y., et al. Cell type-specific genes show striking and distinct patterns of spatial expression in the mouse brain. Proc. Natl. Acad. Sci. USA. 110, 3095-3100 (2013).
25. Guo J.U., et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 14, 1345-1351 (2011).
26. Guo J.U., et al. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat. Neurosci. 17, 215-222 (2014).
27. Lister R., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 462, 315-322 (2009).
28. Kim T.-K., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature. 465, 182-187 (2010).
29. Malik A.N., et al. Genome-wide identification and characterization of functional neuronal activity-dependent enhancers. Nat. Neurosci. 17, 1330-1339 (2014).
30. Heintzman N.D., et al. Histone modifications at human enhancers reflect global cell-Type-specific gene expression. Nature. 459, 108-112 (2009).
31. Lyons G.E., Micales B.K., Schwarz J., Martin J.F., & Olson E.N. Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J. Neurosci. 15, 5727-5738 (1995).
32. Gao Z., et al. Neurod1 is essential for the survival and maturation of adult-born neurons. Nat. Neurosci. 12, 1090-1092 (2009).
33. Nakayama A., et al. Role for RFX transcription factors in non-neuronal cell-specific inactivation of the microtubule-Associated protein MAP1A promoter. J. Biol. Chem. 278, 233-240 (2003).
34. Reiprich S., & Wegner M. From CNS stem cells to neurons and glia: Sox for everyone. Cell Tissue Res. 359, 111-124 (2015).
35. Lesburguères E., et al. Early tagging of cortical networks is required for the formation of enduring associative memory. Science. 331, 924-928 (2011).
36. Reijmers L.G., Perkins B.L., Matsuo N., & Mayford M. Localization of a stable neural correlate of associative memory. Science. 317, 1230-1233 (2007).
37. Garner A.R., et al. Generation of a synthetic memory trace. Science. 335, 1513-1516 (2012).
38. Silva A.J., Zhou Y., Rogerson T., Shobe J., & Balaji J. Molecular and cellular approaches to memory allocation in neural circuits. Science. 326, 391-395 (2009).
39. Ramirez S., et al. Creating a false memory in the hippocampus. Science. 341, 387-391 (2013).
40. Park C.S., Rehrauer H., & Mansuy I.M. Genome-wide analysis of H4K5 acetylation associated with fear memory in mice. BMC Genomics. 14, 539 (2013).
41. Bero A.W., et al. Early remodeling of the neocortex upon episodic memory encoding. Proc. Natl. Acad. Sci. USA. 111, 11852-11857 (2014).
42. Heyward F.D., & Sweatt J.D. DNA methylation in memory formation: emerging insights. Neuroscientist. 21, 475-489 (2015).
43. Shukla S., et al. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature. 479, 74-79 (2011).
44. Fosque B.F., et al. Neural circuits. Labeling of active neural circuits in vivo with designed calcium integrators. Science. 347, 755-760 (2015).
45. Peng X., et al. Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics. 4, 26 (2003).
46. Kendziorski C., Irizarry R.A., Chen K.S., Haag J.D., & Gould M.N. On the utility of pooling biological samples in microarray experiments. Proc. Natl. Acad. Sci. USA. 102, 4252-4257 (2005).
47. Kendziorski C.M., Zhang Y., Lan H., & Attie A.D. The efficiency of pooling mRNA in microarray experiments. Biostatistics. 4, 465-477 (2003).
48. Egelhofer T.A., et al. An assessment of histone-modification antibody quality. Nat. Struct. Mol. Biol. 18, 91-93 (2011).
49. Proudhon C., et al. Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol. Cell. 47, 909-920 (2012).
50. Bessa J., et al. Zebrafish enhancer detection (ZED) vector: a new tool to facilitate transgenesis and the functional analysis of cis-regulatory regions in zebrafish. Dev. Dyn. 238, 2409-2417 (2009).
51. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., & Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310 (1995).
52. Andrews S. FastQC A Quality Control Tool for High Throughput Sequence Data http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.(2010).
53. Li H., et al. The sequence alignment/map format and SAMtools. Bioinformatics. 25, 2078-2079 (2009).
54. Lienhard M., Grimm C., Morkel M., Herwig R., & Chavez L. MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics. 30, 284-286 (2014).
55. Capece V., et al. Oasis: online analysis of small RNA deep sequencing data. Bioinformatics. 31, 2205-2207 (2015).
56. Landt S.G., et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 22, 1813-1831 (2012).
57. Salzberg S.L., & Langmead B. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 9, 357-359 (2012).
58. Dobin A., et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 29, 15-21 (2013).
59. Shen L., Shao N., Liu X., & Nestler E. ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics. 15, 284 (2014).
60. Love M.I., Huber W., & Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
61. Wang J., Duncan D., Shi Z., & Zhang B. WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res. 41, W77-W83 (2013).
62. Rajagopal N., et al. RFECS: a random-forest based algorithm for enhancer identification from chromatin state. PLoS Comput. Biol. 9, e1002968 (2013).
63. Quinlan A.R., & Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 26, 841-842 (2010).
64. Zhang Y., et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
65. Song Q., & Smith A.D. Identifying dispersed epigenomic domains from ChIP-Seq data. Bioinformatics. 27, 870-871 (2011).
66. Anders S., Reyes A., & Huber W. Detecting differential usage of exons from RNA-seq data. Genome Res. 22, 2008-2017 (2012).