Widespread transcription at neuronal activity-regulated enhancers

Nature

Volumn 465, Issue 7295, 2010, Pages 182-187

  Kim, Tae Kyung ^a,h   Hemberg, Martin ^a   Gray, Jesse M ^a   Costa, Allen M ^a   Bear, Daniel M ^a   Wu, Jing ^b   Harmin, David A ^a,c   Laptewicz, Mike ^a   Barbara Haley, Kellie ^d   Kuersten, Scott ^e   Markenscoff Papadimitriou, Eirene ^a,i   Kuhl, Dietmar ^f   Bito, Haruhiko ^g   Worley, Paul F ^b   Kreiman, Gabriel ^a   Greenberg, Michael E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e ILLUMINA INC   (United States)

^f UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^g UNIVERSITY OF TOKYO   (Japan)

^h UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCER RNA; HISTONE ACETYLTRANSFERASE PCAF; HISTONE H3; LYSINE; MESSENGER RNA; RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG;

GENE EXPRESSION; GENETIC ANALYSIS; GENOME; NEUROLOGY; PROTEIN; RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; ENZYME BINDING; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; GENOME; MESSENGER RNA SYNTHESIS; METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA SYNTHESIS;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CONSENSUS SEQUENCE; CREB-BINDING PROTEIN; CYTOSKELETAL PROTEINS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENES, FOS; GENES, REPORTER; HISTONES; METHYLATION; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; RNA POLYMERASE II; RNA, UNTRANSLATED; TRANSCRIPTION, GENETIC;

EID: 77952367798     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09033     Document Type: Article

References (40)

1. Banerji, J., Rusconi, S. & Schaffner, W. Expression of a b-globin gene is enhanced by remote SV40 DNA sequences. Cell 27, 299-308 (1981).
2. Greer, P. L. & Greenberg, M. E. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59, 846-860 (2008).
3. Heintzman, N. D. et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nature Genet. 39, 311-318 (2007).
4. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009).
5. Xi, H. et al. Identification and characterization of cell type-specific and ubiquitous chromatin regulatory structures in the human genome. PLoS Genet. 3, e136 (2007)
6. Park, P. J. ChIP-seq: advantages and challenges of a maturing technology. Nature Rev. Genet. 10, 669-680 (2009).
7. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
8. Robertson, A. G. et al. Genome-wide relationship between histone H3 lysine 4 mono-and tri-methylation and transcription factor binding. Genome Res. 18, 1906-1917 (2008).
9. Chowdhury, S. et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52, 445-459 (2006).
10. Plath, N. et al. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52, 437-444 (2006).
11. Shepherd, J. D. et al. Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52, 475-484 (2006).
12. 21 and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J. Neurosci. 21, 5484-5493 (2001).
13. Kawashima, T. et al. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc. Natl Acad. Sci. USA 106, 316-321 (2009).
14. Pintchovski, S. A., Peebles, C. L., Kim, H. J., Verdin, E. & Finkbeiner, S. The serum response factor and a putative novel transcription factor regulate expression of the immediate-early gene Arc/Arg3.1 in neurons. J. Neurosci. 29, 1525-1537 (2009).
15. 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).
16. Lin, Y. et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198-1204 (2008).
17. Kee, B. L., Arias, J. & Montminy, M. R. Adaptor-mediated recruitment of RNA polymerase II to a signal-dependent activator. J. Biol. Chem. 271, 2373-2375 (1996).
18. Brodsky, A. S. et al. Genomic mapping of RNA polymerase II reveals sites of co-transcriptional regulation in human cells. Genome Biol. 6, R64 (2005).
19. Kim, T. H. et al. A high-resolution map of active promoters in the human genome. Nature 436, 876-880 (2005).
20. Koch, F., Jourquin, F., Ferrier, P. & Andrau, J. C. Genome-wide RNA polymerase II: not genes only! Trends Biochem. Sci. 33, 265-273 (2008).
21. Szutorisz, H., Dillon, N. & Tora, L. The role of enhancers as centres for general transcription factor recruitment. Trends Biochem. Sci. 30, 593-599 (2005).
22. Abeel, T., Saeys, Y., Rouze, P. & Van de Peer, Y. ProSOM: core promoter prediction based on unsupervised clustering of DNA physical profiles. Bioinformatics 24, i24-i31 (2008).
23. Ling, J. et al. HS2 enhancer function is blocked by a transcriptional terminator inserted between the enhancer and the promoter. J. Biol. Chem. 279, 51704-51713 (2004).
24. Zhao, H. & Dean, A. An insulator blocks spreading of histone acetylation and interferes with RNA polymerase II transfer between an enhancer and gene. Nucleic Acids Res. 32, 4903-4919 (2004).
25. Heintzman, N. D. et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112 (2009).
26. Gerber, M. & Shilatifard, A. Transcriptional elongation by RNA polymerase II and histone methylation. J. Biol. Chem. 278, 26303-26306 (2003). (Pubitemid 36876764)
27. Kawashima, T. et al. Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc. Natl Acad. Sci. USA 106, 316-321 (2009).
28. Couttlet, P. et al. Messenger RNA deadenylation precedes decapping in mammalian cells. Proc. Natl Acad. Sci. USA 94, 5628-5633 (1997).
29. Flavell, S. W. et al. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60, 1022-1038 (2008).
30. Kharchenko, P. V., Tolstorukov, M. Y. & Park, P. J. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nature Biotechnol. 26, 1351-1359 (2008).
31. Rozowsky, J. et al. PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nature Biotechnol. 27, 66-75 (2009).
32. Robertson, A. G. et al. Genome-wide relationship between histone H3 lysine 4 mono-and tri-methylation and transcription factor binding. Genome Res. 18, 1906-1917 (2008).
33. Skellam, J. G. The frequency distribution of the difference between two Poisson variates belonging to different populations. J. R. Stat. Soc. A 109, 296 (1946).
34. Efron, B. Microarrays, empirical Bayes and the two-groups model. Stat. Sci. 23, 1-22 (2008).
35. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B. Methodol. 57, 289-300 (1995).
36. Jothi, R., Cuddapah, S., Barski, A., Cui, K. & Zhao, K. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res. 36, 5221-5231 (2008).
37. Ooe, N. et al. Identification of a novel basic helix-loop-helix-PAS factor, NXF, reveals a Sim2 competitive, positive regulatory role in dendritic-cytoskeleton modulator drebrin gene expression. Mol. Cell. Biol. 24, 608-616 (2004).
38. Lin, Y. et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198-1204 (2008).
39. Huang, D. W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protocols 4, 44-57 (2009).
40. Dennis, G. Jr et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 4, 3 (2003).