RNA polymerase II pausing during development (original) (raw)

Abstract

The rapid expansion of genomics methods has enabled developmental biologists to address fundamental questions of developmental gene regulation on a genome-wide scale. These efforts have demonstrated that transcription of developmental control genes by RNA polymerase II (Pol II) is commonly regulated at the transition to productive elongation, resulting in the promoter-proximal accumulation of transcriptionally engaged but paused Pol II prior to gene induction. Here we review the mechanisms and possible functions of Pol II pausing and their implications for development.

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References (52)

  1. Adelman, K. and Lis, J. T. (2012). Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 13, 720-731.
  2. Adkins, N. L., Hagerman, T. A. and Georgel, P. (2006). GAGA protein: a multi- faceted transcription factor. Biochem. Cell Biol. 84, 559-567.
  3. Amir-Zilberstein, L., Ainbinder, E., Toube, L., Yamaguchi, Y., Handa, H. and Dikstein, R. (2007). Differential regulation of NF-kappaB by elongation factors is determined by core promoter type. Mol. Cell. Biol. 27, 5246-5259.
  4. Bai, X., Kim, J., Yang, Z., Jurynec, M. J., Akie, T. E., Lee, J., LeBlanc, J., Sessa, A., Jiang, H., DiBiase, A. et al. (2010). TIF1gamma controls erythroid cell fate by regulating transcription elongation. Cell 142, 133-143.
  5. Barboric, M., Nissen, R. M., Kanazawa, S., Jabrane-Ferrat, N. and Peterlin, B. M. (2001). NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell 8, 327-337.
  6. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
  7. Blau, J., Xiao, H., McCracken, S., O'Hare, P., Greenblatt, J. and Bentley, D. (1996). Three functional classes of transcriptional activation domain. Mol. Cell. Biol. 16, 2044-2055.
  8. Boettiger, A. N. and Levine, M. (2009). Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 325, 471-473.
  9. Bothma, J. P., Magliocco, J. and Levine, M. (2011) The snail repressor inhibits release, not elongation, of paused Pol II in the Drosophila embryo. Curr. Biol. 21, 1571-1577.
  10. Brown, S. A., Weirich, C. S., Newton, E. M. and Kingston, R. E. (1998). Transcriptional activation domains stimulate initiation and elongation at different times and via different residues. EMBO J. 17, 3146-3154.
  11. Chen, K., Johnston, J., Shao, W., Meier, S., Staber, C. and Zeitlinger, J. (2013). A global change in RNA polymerase II pausing during the Drosophila midblastula transition. Elife 2, e00861.
  12. Contreras, X., Barboric, M., Lenasi, T. and Peterlin, B. M. (2007). HMBA releases P- TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and activates HIV transcription. PLoS Pathog. 3, e146.
  13. Core, L. J., Waterfall, J. J. and Lis, J. T. (2008). Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322, 1845-1848.
  14. Danko, C. G., Hah, N., Luo, X., Martins, A. L., Core, L., Lis, J. T., Siepel, A. and Kraus, W. L. (2013). Signaling pathways differentially affect RNA polymerase II initiation, pausing, and elongation rate in cells. Mol. Cell 50, 212-222.
  15. Dikstein, R. (2011). The unexpected traits associated with core promoter elements. Transcription 2, 201-206.
  16. Gaertner, B., Johnston, J., Chen, K., Wallaschek, N., Paulson, A., Garruss, A. S., Gaudenz, K., De Kumar, B., Krumlauf, R. and Zeitlinger, J. (2012). Poised RNA polymerase II changes over developmental time and prepares genes for future expression. Cell Rep. 2, 1670-1683.
  17. Gilchrist, D. A., Dos Santos, G., Fargo, D. C., Xie, B., Gao, Y., Li, L. and Adelman, K. (2010). Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 143, 540-551.
  18. Gilchrist, D. A., Fromm, G., dos Santos, G., Pham, L. N., McDaniel, I. E., Burkholder, A., Fargo, D. C. and Adelman, K. (2012). Regulating the regulators: the pervasive effects of Pol II pausing on stimulus-responsive gene networks. Genes Dev. 26, 933-944.
  19. Gilmour, D. S. and Fan, R. (2009). Detecting transcriptionally engaged RNA polymerase in eukaryotic cells with permanganate genomic footprinting. Methods 48, 368-374.
  20. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. and Young, R. A. (2007). A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88.
  21. Guo, J. and Price, D. H. (2013). RNA polymerase ii transcription elongation control. Chem. Rev. 113, 8583-8603.
  22. Hendrix, D. A., Hong, J. W., Zeitlinger, J., Rokhsar, D. S. and Levine, M. S. (2008). Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc. Natl. Acad. Sci. USA 105, 7762-7767.
  23. Ivaldi, M. S., Karam, C. S. and Corces, V. G. (2007). Phosphorylation of histone H3 at Ser10 facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila. Genes Dev. 21, 2818-2831.
  24. Ji, X., Zhou, Y., Pandit, S., Huang, J., Li, H., Lin, C. Y., Xiao, R., Burge, C. B. and Fu, X. D. (2013). SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 153, 855-868.
  25. Kwak, H., Fuda, N. J., Core, L. J. and Lis, J. T. (2013). Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science 339, 950- 953.
  26. Lagha, M., Bothma, J. P., Esposito, E., Ng, S., Stefanik, L., Tsui, C., Johnston, J., Chen, K., Gilmour, D. S., Zeitlinger, J. et al. (2013). Paused Pol II coordinates tissue morphogenesis in the Drosophila embryo. Cell 153, 976-987.
  27. Lee, C., Li, X., Hechmer, A., Eisen, M., Biggin, M. D., Venters, B. J., Jiang, C., Li, J., Pugh, B. F. and Gilmour, D. S. (2008). NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol. Cell. Biol. 28, 3290- 3300.
  28. Lenhard, B., Sandelin, A. and Carninci, P. (2012). Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat. Rev. Genet. 13, 233- 245.
  29. Levine, M. (2011). Paused RNA polymerase II as a developmental checkpoint. Cell 145, 502-511.
  30. Li, J. and Gilmour, D. S. (2013). Distinct mechanisms of transcriptional pausing orchestrated by GAGA factor and M1BP, a novel transcription factor. EMBO J. 32, 1829-1841.
  31. Li, J., Liu, Y., Rhee, H. S., Ghosh, S. K., Bai, L., Pugh, B. F. and Gilmour, D. S. (2013). Kinetic competition between elongation rate and binding of NELF controls promoter-proximal pausing. Mol. Cell 50, 711-722.
  32. Lin, C., Garrett, A. S., De Kumar, B., Smith, E. R., Gogol, M., Seidel, C., Krumlauf, R. and Shilatifard, A. (2011). Dynamic transcriptional events in embryonic stem cells mediated by the super elongation complex (SEC). Genes Dev. 25, 1486- 1498.
  33. Lis, J. (1998). Promoter-associated pausing in promoter architecture and postinitiation transcriptional regulation. Cold Spring Harb. Symp. Quant. Biol. 63, 347-356.
  34. Little, S. C., Tikhonov, M. and Gregor, T. (2013). Precise developmental gene expression arises from globally stochastic transcriptional activity. Cell 154, 789- 800.
  35. Luse, D. S. (2013). Promoter clearance by RNA polymerase II. Biochim. Biophys. Acta 1829, 63-68.
  36. Marbach-Bar, N., Ben-Noon, A., Ashkenazi, S., Tamarkin-Ben Harush, A., Avnit- Sagi, T., Walker, M. D. and Dikstein, R. (2013). Disparity between microRNA levels and promoter strength is associated with initiation rate and Pol II pausing. Nat. Commun. 4, 2118.
  37. Montanuy, I., Torremocha, R., Hernández-Munain, C. and Suñé, C. (2008). Promoter influences transcription elongation: TATA-box element mediates the assembly of processive transcription complexes responsive to cyclin-dependent kinase 9. J. Biol. Chem. 283, 7368-7378.
  38. Muse, G. W., Gilchrist, D. A., Nechaev, S., Shah, R., Parker, J. S., Grissom, S. F., Zeitlinger, J. and Adelman, K. (2007). RNA polymerase is poised for activation across the genome. Nat. Genet. 39, 1507-1511.
  39. Nechaev, S., Fargo, D. C., dos Santos, G., Liu, L., Gao, Y. and Adelman, K. (2010). Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 327, 335-338.
  40. Ohler, U., Liao, G. C., Niemann, H. and Rubin, G. M. (2002). Computational analysis of core promoters in the Drosophila genome. Genome Biol. 3, RESEARCH0087.
  41. Pokholok, D. K., Zeitlinger, J., Hannett, N. M., Reynolds, D. B. and Young, R. A. (2006). Activated signal transduction kinases frequently occupy target genes. Science 313, 533-536.
  42. Rach, E. A., Winter, D. R., Benjamin, A. M., Corcoran, D. L., Ni, T., Zhu, J. and Ohler, U. (2011). Transcription initiation patterns indicate divergent strategies for gene regulation at the chromatin level. PLoS Genet. 7, e1001274.
  43. Rahl, P. B., Lin, C. Y., Seila, A. C., Flynn, R. A., McCuine, S., Burge, C. B., Sharp, P. A. and Young, R. A. (2010). c-Myc regulates transcriptional pause release. Cell 141, 432-445.
  44. Schwartz, Y. B., Kahn, T. G., Stenberg, P., Ohno, K., Bourgon, R. and Pirrotta, V. (2010). Alternative epigenetic chromatin states of polycomb target genes. PLoS Genet. 6, e1000805.
  45. Takahashi, H., Parmely, T. J., Sato, S., Tomomori-Sato, C., Banks, C. A., Kong, S. E., Szutorisz, H., Swanson, S. K., Martin-Brown, S., Washburn, M. P. et al. (2011). Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146, 92-104.
  46. Voigt, P., Tee, W. W. and Reinberg, D. (2013). A double take on bivalent promoters. Genes Dev. 27, 1318-1338.
  47. Yamaguchi, Y., Shibata, H. and Handa, H. (2013). Transcription elongation factors DSIF and NELF: promoter-proximal pausing and beyond. Biochim. Biophys. Acta 1829, 98-104.
  48. Yankulov, K., Blau, J., Purton, T., Roberts, S. and Bentley, D. L. (1994). Transcriptional elongation by RNA polymerase II is stimulated by transactivators. Cell 77, 749-759.
  49. Zeitlinger, J., Stark, A., Kellis, M., Hong, J. W., Nechaev, S., Adelman, K., Levine, M. and Young, R. A. (2007). RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat. Genet. 39, 1512-1516.
  50. Zhang, Y., Feng, Y., Chatterjee, S., Tuske, S., Ho, M. X., Arnold, E. and Ebright, R. H. (2012). Structural basis of transcription initiation. Science 338, 1076-1080.
  51. Zhou, Q., Li, T. and Price, D. H. (2012). RNA polymerase II elongation control. Annu. Rev. Biochem. 81, 119-143.
  52. Zippo, A., Serafini, R., Rocchigiani, M., Pennacchini, S., Krepelova, A. and Oliviero, S. (2009). Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138, 1122-1136.