Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation

Cell

Volumn 143, Issue 4, 2010, Pages 540-551

  Gilchrist, Daniel A ^a   Dos Santos, Gilberto ^a   Fargo, David C ^a   Xie, Bin ^b   Gao, Yuan ^b,c   Li, Leping ^a   Adelman, Karen ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ELONGATION FACTOR; NEGATIVE ELONGATION FACTOR; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA SEQUENCE; ENZYME BINDING; GENE ACTIVATION; GENE CONTROL; HOUSEKEEPING GENE; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION;

METAZOA;

EID: 78149477660     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.10.004     Document Type: Article

References (42)

1. Albert I., Mavrich T.N., Tomsho L.P., Qi J., Zanton S.J., Schuster S.C., Pugh B.F. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 2007, 446:572-576.
2. Basehoar A.D., Zanton S.J., Pugh B.F. Identification and distinct regulation of yeast TATA box-containing genes. Cell 2004, 116:699-709.
3. Boettiger A.N., Levine M. Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 2009, 325:471-473.
4. Cairns B.R. The logic of chromatin architecture and remodelling at promoters. Nature 2009, 461:193-198.
5. Cheng B., Price D.H. Properties of RNA polymerase II elongation complexes before and after the P-TEFb-mediated transition into productive elongation. J. Biol. Chem. 2007, 282:21901-21912.
6. Core L.J., Waterfall J.J., Lis J.T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
7. Dimarcq J.L., Imler J.L., Lanot R., Ezekowitz R.A., Hoffmann J.A., Janeway C.A., Lagueux M. Treatment of l(2)mbn Drosophila tumorous blood cells with the steroid hormone ecdysone amplifies the inducibility of antimicrobial peptide gene expression. Insect Biochem. Mol. Biol. 1997, 27:877-886.
8. Gilchrist D.A., Fargo D.C., Adelman K. Using ChIP-chip and ChIP-seq to study the regulation of gene expression: genome-wide localization studies reveal widespread regulation of transcription elongation. Methods 2009, 48:398-408.
9. Gilchrist D.A., Nechaev S., Lee C., Ghosh S.K., Collins J.B., Li L., Gilmour D.S., Adelman K. NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev. 2008, 22:1921-1933.
10. Hendrix D.A., Hong J.W., Zeitlinger J., Rokhsar D.S., Levine M.S. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 2008, 105:7762-7767.
11. Iyer V., Struhl K. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 1995, 14:2570-2579.
12. Izban M.G., Luse D.S. Factor-stimulated RNA polymerase II transcribes at physiological elongation rates on naked DNA but very poorly on chromatin templates. J. Biol. Chem. 1992, 267:13647-13655.
13. Juven-Gershon T., Hsu J.Y., Theisen J.W., Kadonaga J.T. The RNA polymerase II core promoter-the gateway to transcription. Curr. Opin. Cell Biol. 2008, 20:253-259.
14. Kaplan N., Moore I.K., Fondufe-Mittendorf Y., Gossett A.J., Tillo D., Field Y., LeProust E.M., Hughes T.R., Lieb J.D., Widom J., et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458:362-366.
15. Kim T.H., Barrera L.O., Zheng M., Qu C., Singer M.A., Richmond T.A., Wu Y., Green R.D., Ren B. A high-resolution map of active promoters in the human genome. Nature 2005, 436:876-880.
16. Lee C., Li X., Hechmer A., Eisen M., Biggin M.D., Venters B.J., Jiang C., Li J., Pugh B.F., Gilmour D.S. NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol. Cell. Biol. 2008, 28:3290-3300.
17. Lis J. Promoter-associated pausing in promoter architecture and postinitiation transcriptional regulation. Cold Spring Harb. Symp. Quant. Biol. 1998, 63:347-356.
18. Marshall N.F., Price D.H. Control of formation of two distinct classes of RNA polymerase II elongation complexes. Mol. Cell. Biol. 1992, 12:2078-2090.
19. Marshall N.F., Price D.H. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J. Biol. Chem. 1995, 270:12335-12338.
20. Mavrich T.N., Jiang C., Ioshikhes I.P., Li X., Venters B.J., Zanton S.J., Tomsho L.P., Qi J., Glaser R.L., Schuster S.C., et al. Nucleosome organization in the Drosophila genome. Nature 2008, 453:358-362.
21. Mito Y., Henikoff J.G., Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat. Genet. 2005, 37:1090-1097.
22. Muse G.W., Gilchrist D.A., Nechaev S., Shah R., Parker J.S., Grissom S.F., Zeitlinger J., Adelman K. RNA polymerase is poised for activation across the genome. Nat. Genet. 2007, 39:1507-1511.
23. Nechaev S., Fargo D.C., dos Santos G., Liu L., Gao Y., Adelman K. Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 2010, 327:335-338.
24. Ozsolak F., Song J.S., Liu X.S., Fisher D.E. High-throughput mapping of the chromatin structure of human promoters. Nat. Biotechnol. 2007, 25:244-248.
25. Peterlin B.M., Price D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 2006, 23:297-305.
26. Rahl P.B., Lin C.Y., Seila A.C., Flynn R.A., McCuine S., Burge C.B., Sharp P.A., Young R.A. c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
27. Roeder R.G. Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett. 2005, 579:909-915.
28. Rougvie A.E., Lis J.T. The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 1988, 54:795-804.
29. Schones D.E., Cui K., Cuddapah S., Roh T.Y., Barski A., Wang Z., Wei G., Zhao K. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008, 132:887-898.
30. Schwartz S., Meshorer E., Ast G. Chromatin organization marks exon-intron structure. Nat. Struct. Mol. Biol. 2009, 16:990-995.
31. Sekinger E.A., Moqtaderi Z., Struhl K. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol. Cell 2005, 18:735-748.
32. Shopland L.S., Hirayoshi K., Fernandes M., Lis J.T. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites. Genes Dev. 1995, 9:2756-2769.
33. Tillo D., Kaplan N., Moore I.K., Fondufe-Mittendorf Y., Gossett A.J., Field Y., Lieb J.D., Widom J., Segal E., Hughes T.R. High nucleosome occupancy is encoded at human regulatory sequences. PLoS ONE 2010, 5:e9129.
34. Tirosh I., Barkai N. Two strategies for gene regulation by promoter nucleosomes. Genome Res. 2008, 18:1084-1091.
35. Tsukiyama T., Becker P.B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 1994, 367:525-532.
36. Weiner A., Hughes A., Yassour M., Rando O.J., Friedman N. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res. 2009, 20:90-100.
37. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 1980, 286:854-860.
38. Wu C.H., Yamaguchi Y., Benjamin L.R., Horvat-Gordon M., Washinsky J., Enerly E., Larsson J., Lambertsson A., Handa H., Gilmour D. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev. 2003, 17:1402-1414.
39. Yamaguchi Y., Inukai N., Narita T., Wada T., Handa H. Evidence that negative elongation factor represses transcription elongation through binding to a DRB sensitivity-inducing factor/RNA polymerase II complex and RNA. Mol. Cell. Biol. 2002, 22:2918-2927.
40. Yuan G.C., Liu Y.J., Dion M.F., Slack M.D., Wu L.F., Altschuler S.J., Rando O.J. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309:626-630.
41. Zeitlinger J., Stark A., Kellis M., Hong J.W., Nechaev S., Adelman K., Levine M., Young R.A. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat. Genet. 2007, 39:1512-1516.
42. Zhang Y., Moqtaderi Z., Rattner B.P., Euskirchen G., Snyder M., Kadonaga J.T., Liu X.S., Struhl K. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol. 2009, 16:847-852.