XPaused Pol II coordinates tissue morphogenesis in the drosophila embryo

Cell

Volumn 153, Issue 5, 2013, Pages 976-

  Lagha, Mounia ^a   Bothma, Jacques P ^a   Esposito, Emilia ^a   Ng, Samuel ^a   Stefanik, Laura ^b   Tsui, Chiahao ^a   Johnston, Jeffrey ^c   Chen, Kai ^c   Gilmour, David S ^b   Zeitlinger, Julia ^c   Levine, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA POLYMERASE II; TRANSCRIPTION FACTOR SNAIL;

ARTICLE; CORRELATION ANALYSIS; DROSOPHILA; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; GAIN OF FUNCTION MUTATION; GASTRULATION; GENE ACTIVATION; GENE LOCUS; MESODERM; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN METABOLISM; QUANTITATIVE ANALYSIS; TRANSCRIPTION REGULATION; TRANSGENE; WILD TYPE;

GASTROPODA; MAMMALIA;

EID: 84878318299     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.04.045     Document Type: Article

References (67)

1. K. Adelman, and J.T. Lis Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans Nat. Rev. Genet. 13 2012 720 731
2. H.L. Ashe, M. Mannervik, and M. Levine Dpp signaling thresholds in the dorsal ectoderm of the Drosophila embryo Development 127 2000 3305 3312
3. N. Balaskas, A. Ribeiro, J. Panovska, E. Dessaud, N. Sasai, K.M. Page, J. Briscoe, and V. Ribes Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube Cell 148 2012 273 284
4. A.K. Boehm, A. Saunders, J. Werner, and J.T. Lis Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock Mol. Cell. Biol. 23 2003 7628 7637
5. A.N. Boettiger, and M. Levine Synchronous and stochastic patterns of gene activation in the Drosophila embryo Science 325 2009 471 473
6. A.N. Boettiger, and M. Levine Rapid transcription fosters coordinate snail expression in the Drosophila embryo Cell Rep 3 2013 8 15
7. J.P. Bothma, J. Magliocco, and M. Levine The snail repressor inhibits release, not elongation, of paused Pol II in the Drosophila embryo Curr. Biol. 21 2011 1571 1577
8. H. Chen, Z. Xu, C. Mei, D. Yu, and S. Small A system of repressor gradients spatially organizes the boundaries of Bicoid-dependent target genes Cell 149 2012 618 629
9. K.R. Duffy, C.J. Wellard, J.F. Markham, J.H. Zhou, R. Holmberg, E.D. Hawkins, J. Hasbold, M.R. Dowling, and P.D. Hodgkin Activation-induced B cell fates are selected by intracellular stochastic competition Science 335 2012 338 341
10. L. Dunipace, A. Ozdemir, and A. Stathopoulos Complex interactions between cis-regulatory modules in native conformation are critical for Drosophila snail expression Development 138 2011 4075 4084
11. A. Eldar, and M.B. Elowitz Functional roles for noise in genetic circuits Nature 467 2010 167 173
12. A. Fay, Z. Misulovin, J. Li, C.A. Schaaf, M. Gause, D.S. Gilmour, and D. Dorsett Cohesin selectively binds and regulates genes with paused RNA polymerase Curr. Biol. 21 2011 1624 1634
13. B. Gaertner, J. Johnston, K. Chen, N. Wallaschek, A. Paulson, A.S. Garruss, K. Gaudenz, B. De Kumar, R. Krumlauf, and J. Zeitlinger Poised RNA polymerase II changes over developmental time and prepares genes for future expression Cell Rep. 2 2012 1670 1683
14. D.A. Gilchrist, G. Dos Santos, D.C. Fargo, B. Xie, Y. Gao, L. Li, and K. Adelman Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation Cell 143 2010 540 551
15. D.A. Gilchrist, G. Fromm, G. dos Santos, L.N. Pham, I.E. McDaniel, A. Burkholder, D.C. Fargo, and K. Adelman Regulating the regulators: the pervasive effects of Pol II pausing on stimulus-responsive gene networks Genes Dev. 26 2012 933 944
16. M.G. Guenther, and R.A. Young Grounded: transcriptional pausing in naive mESCs Cell Stem Cell 10 2012 484 485
17. K. Hemavathy, X. Meng, and Y.T. Ip Differential regulation of gastrulation and neuroectodermal gene expression by Snail in the Drosophila embryo Development 124 1997 3683 3691
18. D.A. Hendrix, J.W. Hong, J. Zeitlinger, D.S. Rokhsar, and M.S. Levine Promoter elements associated with RNA Pol II stalling in the Drosophila embryo Proc. Natl. Acad. Sci. USA 105 2008 7762 7767
19. T. Juven-Gershon, and J.T. Kadonaga Regulation of gene expression via the core promoter and the basal transcriptional machinery Dev. Biol. 339 2010 225 229
20. T. Kalmar, C. Lim, P. Hayward, S. Muñoz-Descalzo, J. Nichols, J. Garcia-Ojalvo, and A. Martinez Arias Regulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cells PLoS Biol. 7 2009 e1000149
21. J.S. Kanodia, R. Rikhy, Y. Kim, V.K. Lund, R. DeLotto, J. Lippincott-Schwartz, and S.Y. Shvartsman Dynamics of the Dorsal morphogen gradient Proc. Natl. Acad. Sci. USA 106 2009 21707 21712
22. J.S. Kanodia, Y. Kim, R. Tomer, Z. Khan, K. Chung, J.D. Storey, H. Lu, P.J. Keller, and S.Y. Shvartsman A computational statistics approach for estimating the spatial range of morphogen gradients Development 138 2011 4867 4874
23. D. Kosman, Y.T. Ip, M. Levine, and K. Arora Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo Science 254 1991 118 122
24. H. Lee, K.W. Kraus, M.F. Wolfner, and J.T. Lis DNA sequence requirements for generating paused polymerase at the start of hsp70 Genes Dev. 6 1992 284 295
25. C. Lee, X. Li, A. Hechmer, M. Eisen, M.D. Biggin, B.J. Venters, C. Jiang, J. Li, B.F. Pugh, and D.S. Gilmour NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila Mol. Cell. Biol. 28 2008 3290 3300
26. M. Leptin Gastrulation movements: the logic and the nuts and bolts Dev. Cell 8 2005 305 320
27. M. Levine Paused RNA polymerase II as a developmental checkpoint Cell 145 2011 502 511
28. M. Leptin, and B. Grunewald Cell shape changes during gastrulation in Drosophila Development 110 1990 73 84
29. J. Li, and D.S. Gilmour Promoter proximal pausing and the control of gene expression Curr. Opin. Genet. Dev. 21 2011 231 235
30. L.M. Liberman, G.T. Reeves, and A. Stathopoulos Quantitative imaging of the Dorsal nuclear gradient reveals limitations to threshold-dependent patterning in Drosophila Proc. Natl. Acad. Sci. USA 106 2009 22317 22322
31. C. Lin, A.S. Garrett, B. De Kumar, E.R. Smith, M. Gogol, C. Seidel, R. Krumlauf, and A. Shilatifard Dynamic transcriptional events in embryonic stem cells mediated by the super elongation complex (SEC) Genes Dev. 25 2011 1486 1498
32. R. Losick, and C. Desplan Stochasticity and cell fate Science 320 2008 65 68
33. J.M. Morachis, C.M. Murawsky, and B.M. Emerson Regulation of the p53 transcriptional response by structurally diverse core promoters Genes Dev. 24 2010 135 147
34. J. Nichols, and A. Smith The origin and identity of embryonic stem cells Development 138 2011 3 8
35. C.T. Ong, and V.G. Corces Enhancer function: new insights into the regulation of tissue-specific gene expression Nat. Rev. Genet. 12 2011 283 293
36. M.W. Perry, A.N. Boettiger, J.P. Bothma, and M. Levine Shadow enhancers foster robustness of Drosophila gastrulation Curr. Biol. 20 2010 1562 1567
37. G.T. Reeves, N. Trisnadi, T.V. Truong, M. Nahmad, S. Katz, and A. Stathopoulos Dorsal-ventral gene expression in the Drosophila embryo reflects the dynamics and precision of the dorsal nuclear gradient Dev. Cell 22 2012 544 557
38. C.A. Rushlow, and S.Y. Shvartsman Temporal dynamics, spatial range, and transcriptional interpretation of the Dorsal morphogen gradient Curr. Opin. Genet. Dev. 22 2012 542 546
39. Y. Saga The synchrony and cyclicity of developmental events Cold Spring Harb. Perspect. Biol. 4 2012 a008201
40. D.S. Schneider, K.L. Hudson, T.Y. Lin, and K.V. Anderson Dominant and recessive mutations define functional domains of Toll, a transmembrane protein required for dorsal-ventral polarity in the Drosophila embryo Genes Dev. 5 1991 797 807
41. B. Schuettengruber, M. Ganapathi, B. Leblanc, M. Portoso, R. Jaschek, B. Tolhuis, M. van Lohuizen, A. Tanay, and G. Cavalli Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos PLoS Biol. 7 2009 e13
42. L.S. Shopland, K. Hirayoshi, M. Fernandes, and J.T. Lis 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. 9 1995 2756 2769
43. D. Sweeton, S. Parks, M. Costa, and E. Wieschaus Gastrulation in Drosophila: the formation of the ventral furrow and posterior midgut invaginations Development 112 1991 775 789
44. K.J. Venken, Y. He, R.A. Hoskins, and H.J. Bellen P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster Science 314 2006 1747 1751
45. S.D. Vincent, and M.E. Buckingham How to make a heart: the origin and regulation of cardiac progenitor cells Curr. Top. Dev. Biol. 90 2010 1 41
46. J. Zeitlinger, A. Stark, M. Kellis, J.W. Hong, S. Nechaev, K. Adelman, M. Levine, and R.A. Young RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo Nat. Genet. 39 2007 1512 1516
47. H. Acloque, O.H. Ocaña, A. Matheu, K. Rizzoti, C. Wise, R. Lovell-Badge, and M.A. Nieto Reciprocal repression between Sox3 and snail transcription factors defines embryonic territories at gastrulation Dev. Cell 21 2011 546 558
48. U. Alon An Introduction to Systems Biology: Design Principles of Biological Circuits 2006 Chapman & Hall/CRC Boca Raton, FL
49. K.V. Anderson, and J.A. Lengyel Changing rates of histone mRNA synthesis and turnover in Drosophila embryos Cell 21 1980 717 727
50. B.R. Daniels, R. Rikhy, M. Renz, T.M. Dobrowsky, and J. Lippincott-Schwartz Multiscale diffusion in the mitotic Drosophila melanogaster syncytial blastoderm Proc. Natl. Acad. Sci. USA 109 2012 8588 8593
51. B.A. Edgar, M.P. Weir, G. Schubiger, and T. Kornberg Repression and turnover pattern fushi tarazu RNA in the early Drosophila embryo Cell 47 1986 747 754
52. C.C. Fowlkes, C.L. Hendriks, S.V.E. Keränen, G.H. Weber, O. Rübel, M.Y. Huang, S. Chatoor, A.H. DePace, L. Simirenko, and C. Henriquez A quantitative spatiotemporal atlas of gene expression in the Drosophila blastoderm Cell 133 2008 364 374
53. N. Friedman, L. Cai, and X.S. Xie Linking stochastic dynamics to population distribution: an analytical framework of gene expression Phys. Rev. Lett. 97 2006 168302
54. S.K. Ghosh, A. Missra, and D.S. Gilmour Negative elongation factor accelerates the rate at which heat shock genes are shut off by facilitating dissociation of heat shock factor Mol. Cell. Biol. 31 2011 4232 4243
55. D.S. Gilmour, and R. Fan Detecting transcriptionally engaged RNA polymerase in eukaryotic cells with permanganate genomic footprinting Methods 48 2009 368 374
56. T. Gregor, D.W. Tank, E.F. Wieschaus, and W. Bialek Probing the limits to positional information Cell 130 2007 153 164
57. T. Gregor, E.F. Wieschaus, A.P. McGregor, W. Bialek, and D.W. Tank Stability and nuclear dynamics of the bicoid morphogen gradient Cell 130 2007 141 152
58. R.V. Hogg, and A.T. Craig Introduction to Mathematical Statistics 4th Edition 1978 Macmillan New York
59. Y.T. Ip, R.E. Park, D. Kosman, K. Yazdanbakhsh, and M. Levine dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo Genes Dev. 6 1992 1518 1530
60. J. Jaeger, S. Surkova, M. Blagov, H. Janssens, D. Kosman, K.N. Kozlov, Manu, E. Myasnikova, C.E. Vanario-Alonso, and M. Samsonova Dynamic control of positional information in the early Drosophila embryo Nature 430 2004 368 371
61. D. Kosman, C.M. Mizutani, D. Lemons, W.G. Cox, W. McGinnis, and E. Bier Multiplex detection of RNA expression in Drosophila embryos Science 305 2004 846
62. R. Lehmann, and C. Nüsslein-Volhard hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo Dev. Biol. 119 1987 402 417
63. X. Ma, D. Yuan, K. Diepold, T. Scarborough, and J. Ma The Drosophila morphogenetic protein Bicoid binds DNA cooperatively Development 122 1996 1195 1206
64. P. McHale, C.M. Mizutani, D. Kosman, D.L. MacKay, M. Belu, A. Hermann, W. McGinnis, E. Bier, and T. Hwa Gene length may contribute to graded transcriptional responses in the Drosophila embryo Dev. Biol. 360 2011 230 240
65. T. O'Brien, and J.T. Lis RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp70 gene Mol. Cell. Biol. 11 1991 5285 5290
66. A. Stathopoulos, and M. Levine Whole-genome analysis of Drosophila gastrulation Curr. Opin. Genet. Dev. 14 2004 477 484
67. C. Zhao, A. York, F. Yang, D.J. Forsthoefel, V. Dave, D. Fu, D. Zhang, M.S. Corado, S. Small, M.A. Seeger, and J. Ma The activity of the Drosophila morphogenetic protein Bicoid is inhibited by a domain located outside its homeodomain Development 129 2002 1669 1680