Cited by 207Genomics and Chromatin DynamicsGene Regulatory Network AnalysisDiffusion and Search Dynamics

Dynamic multifactor hubs interact transiently with sites of active transcription in Drosophila embryos

Open access
Mir, Mustafa, Stadler, Michael R, Ortiz, Stephan A, Hannon, Colleen E, Harrison, Melissa M, Darzacq, Xavier, Eisen, Michael B·2018·eLife

Published version of a preprint

Abstract

The regulation of transcription requires the coordination of numerous activities on DNA, yet how transcription factors mediate these activities remains poorly understood. Here, we use lattice light-sheet microscopy to integrate single-molecule and high-speed 4D imaging in developing Drosophila embryos to study the nuclear organization and interactions of the key transcription factors Zelda and Bicoid. In contrast to previous studies suggesting stable, cooperative binding, we show that both factors interact with DNA with surprisingly high off-rates. We find that both factors form dynamic subnuclear hubs, and that Bicoid binding is enriched within Zelda hubs. Remarkably, these hubs are both short lived and interact only transiently with sites of active Bicoid-dependent transcription. Based on our observations, we hypothesize that, beyond simply forming bridges between DNA and the transcription machinery, transcription factors can organize other proteins into hubs that transiently drive multiple activities at their gene targets. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.40497

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Zelda promotes the formation of local transcription factor hubs involving transcription factors required for developmental patterning, such as Bicoid and Dorsal.

    “For instance, Zelda promotes the formation of local TF hubs involving important transcription factors required for developmental patterning, such as Bicoid and Dorsal [51–54].”

    From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [52]

    The Results section ('Bicoid binding events are enriched in Zelda hubs'; page unavailable) reports Bicoid binding enriched within Zelda hubs, supporting that example. The cited paper does not establish Dorsal’s involvement in those hubs, so the Dorsal example is unsupported by this source. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 93

  1. Altmeyer M Neelsen KJ Teloni F Pozdnyakova I Pellegrino S Grøfte M Rask MB Streicher W Jungmichel S Nielsen ML Lukas J 2015 Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose) Nature Communications 6 8088 10.1038/ncomms9088 26286827 PMC4560800 · DOI
  2. Anderson KV Lengyel JA 1981 Changing rates of DNA and RNA synthesis in Drosophila embryos Developmental Biology 82 127 138 10.1016/0012-1606(81)90434-6 6164584 · DOI
  3. Baena-Lopez LA Alexandre C Mitchell A Pasakarnis L Vincent JP 2013 Accelerated homologous recombination and subsequent genome modification in Drosophila Development 140 4818 4825 10.1242/dev.100933 24154526 PMC3833436 · DOI
  4. Bassett AR Tibbit C Ponting CP Liu J-L 2013 Highly efficient targeted mutagenesis of drosophila with the CRISPR/Cas9 System Cell Reports 4 220 228 10.1016/j.celrep.2013.06.020 23827738 PMC3714591 · DOI
  5. Bassett AR Tibbit C Ponting CP Liu JL 2014 Mutagenesis and homologous recombination in Drosophila cell lines using CRISPR/Cas9 Biology Open 3 42 49 10.1242/bio.20137120 24326186 PMC3892159 · DOI
  6. Bhattacharya D Talwar S Mazumder A Shivashankar GV 2009 Spatio-temporal plasticity in chromatin organization in mouse cell differentiation and during drosophila embryogenesis Biophysical Journal 96 3832 3839 10.1016/j.bpj.2008.11.075 19413989 PMC3297759 · DOI
  7. Blythe SA Wieschaus EF 2016 Establishment and maintenance of heritable chromatin structure during early Drosophila embryogenesis eLife 5 e20148 10.7554/eLife.20148 27879204 PMC5156528 · DOI
  8. Boehning M Dugast-Darzacq C Rankovic M Hansen AS Yu T-K Marie-Nelly H McSwiggen DT 2018 RNA Polymerase II Clustering through CTD Phase Separation bioRxiv 10.1101/316372 30127355 · DOI
  9. Boija A Mannervik M 2016 Initiation of diverse epigenetic states during nuclear programming of the Drosophila body plan PNAS 113 8735 8740 10.1073/pnas.1516450113 27439862 PMC4978291 · DOI
  10. Bothma JP Garcia HG Ng S Perry MW Gregor T Levine M 2015 Enhancer additivity and non-additivity are determined by enhancer strength in the Drosophila embryo eLife 4 e07956 10.7554/eLife.07956 PMC4532966 26267217 · DOI · Paper page
  11. Brangwynne CP Eckmann CR Courson DS Rybarska A Hoege C Gharakhani J Julicher F Hyman AA 2009 Germline P granules are liquid droplets that localize by controlled dissolution/Condensation Science 324 1729 1732 10.1126/science.1172046 19460965 · DOI
  12. Burke KA Janke AM Rhine CL Fawzi NL 2015 Residue-by-residue view of in vitro fus granules that bind the c-terminal domain of RNA polymerase II Molecular Cell 60 231 241 10.1016/j.molcel.2015.09.006 26455390 PMC4609301 · DOI
  13. Chen B Gilbert LA Cimini BA Schnitzbauer J Zhang W Li GW Park J Blackburn EH Weissman JS Qi LS Huang B 2013 Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system Cell 155 1479 1491 10.1016/j.cell.2013.12.001 24360272 PMC3918502 · DOI
  14. Chen BC Legant WR Wang K Shao L Milkie DE Davidson MW Janetopoulos C Wu XS Hammer JA Liu Z English BP Mimori-Kiyosue Y Romero DP Ritter AT Lippincott-Schwartz J Fritz-Laylin L Mullins RD Mitchell DM Bembenek JN Reymann AC Böhme R Grill SW Wang JT Seydoux G Tulu US Kiehart DP Betzig E 2014a Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution Science 346 1257998 10.1126/science.1257998 25342811 PMC4336192 · DOI
  15. Chong S Dugast-Darzacq C Liu Z Dong P Dailey GM Cattoglio C Heckert A Banala S Lavis L Darzacq X Tjian R 2018 Imaging dynamic and selective low-complexity domain interactions that control gene transcription Science 361 eaar2555 10.1126/science.aar2555 29930090 PMC6961784 · DOI · Paper page
  16. Cisse II Izeddin I Causse SZ Boudarene L Senecal A Muresan L Dugast-Darzacq C Hajj B Dahan M Darzacq X 2013 Real-Time dynamics of rna polymerase ii clustering in live human cells Science 341 664 667 10.1126/science.1239053 23828889 · DOI
  17. Combs PA Eisen MB 2013 Sequencing mRNA from cryo-sliced Drosophila embryos to determine genome-wide spatial patterns of gene expression PLOS ONE 8 e71820 10.1371/journal.pone.0071820 23951250 PMC3741199 · DOI
  18. Combs PA Eisen MB 2017 Genome-wide measurement of spatial expression in patterning mutants of Drosophila melanogaster F1000Research 6 41 10.12688/f1000research.9720.1 28299188 PMC5325077 · DOI
  19. Doidy J Li Y Neymotin B Edwards MB Varala K Gresham D Coruzzi GM 2016 "Hit-and-Run" transcription: de novo transcription initiated by a transient bZIP1 "hit" persists after the "run" BMC Genomics 17 10.1186/s12864-016-2410-2 26843062 PMC4738784 · DOI
  20. Driever W Nüsslein-Volhard C 1988 The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner Cell 54 95 104 10.1016/0092-8674(88)90183-3 3383245 · DOI
  21. Dufourt J Trullo A Hunter J Fernandez C Lazaro J Dejean M Morales L 2018 Temporal control of transcription by zelda in living drosophila embryo bioRxiv 10.1101/282426 · DOI
  22. Edgar BA Kiehle CP Schubiger G 1986 Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development Cell 44 365 372 10.1016/0092-8674(86)90771-3 3080248 · DOI
  23. Edgar BA Schubiger G 1986 Parameters controlling transcriptional activation during early Drosophila development Cell 44 871 877 10.1016/0092-8674(86)90009-7 2420468 · DOI
  24. Foe VE Alberts BM 1983 Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in drosophila embryogenesis Journal of Cell Science 61 31 70 6411748
  25. Foo SM Sun Y Lim B Ziukaite R O’Brien K Nien C-Y Kirov N Shvartsman SY Rushlow CA 2014 Zelda potentiates morphogen activity by increasing chromatin accessibility Current Biology 24 1341 1346 10.1016/j.cub.2014.04.032 24909324 PMC4075064 · DOI
  26. Fradin C 2017 On the importance of protein diffusion in biological systems: The example of the Bicoid morphogen gradient Biochimica Et Biophysica Acta (BBA) - Proteins and Proteomics 1865 1676 1686 10.1016/j.bbapap.2017.09.002 28919007 · DOI
  27. Friedman MJ Shah AG Fang ZH Ward EG Warren ST Li S Li XJ 2007 Polyglutamine domain modulates the TBP-TFIIB interaction: implications for its normal function and neurodegeneration Nature Neuroscience 10 1519 1528 10.1038/nn2011 17994014 · DOI
  28. Frohnhöfer HG Nüsslein-Volhard C 1986 Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid Nature 324 120 125 10.1038/324120a0 · DOI
  29. Garcia HG Tikhonov M Lin A Gregor T 2013 Quantitative imaging of transcription in living Drosophila embryos links polymerase activity to patterning Current Biology 23 2140 2145 10.1016/j.cub.2013.08.054 24139738 PMC3828032 · DOI
  30. Gratz SJ Cummings AM Nguyen JN Hamm DC Donohue LK Harrison MM Wildonger J O'Connor-Giles KM 2013 Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease Genetics 194 1029 1035 10.1534/genetics.113.152710 23709638 PMC3730909 · DOI
  31. Gratz SJ Ukken FP Rubinstein CD Thiede G Donohue LK Cummings AM O'Connor-Giles KM 2014 Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila Genetics 196 961 971 10.1534/genetics.113.160713 24478335 PMC3982687 · DOI
  32. Gregor T Wieschaus EF McGregor AP Bialek W Tank DW 2007 Stability and Nuclear Dynamics of the Bicoid Morphogen Gradient Cell 130 141 152 10.1016/j.cell.2007.05.026 17632061 PMC2253672 · DOI
  33. Groth AC Fish M Nusse R Calos MP 2004 Construction of transgenic drosophila by using the site-specific integrase from phage C31 Genetics 166 1775 1782 10.1534/genetics.166.4.1775 15126397 PMC1470814 · DOI
  34. Hamm DC Larson ED Nevil M Marshall KE Bondra ER Harrison MM 2017 A conserved maternal-specific repressive domain in Zelda revealed by Cas9-mediated mutagenesis in Drosophila melanogaster PLOS Genetics 13 e1007120 10.1371/journal.pgen.1007120 29261646 PMC5752043 · DOI
  35. Hannon CE Blythe SA Wieschaus EF 2017 Concentration dependent chromatin states induced by the bicoid morphogen gradient eLife 6 e28275 10.7554/eLife.28275 28891464 PMC5624782 · DOI
  36. Hansen AS Pustova I Cattoglio C Tjian R Darzacq X 2017 CTCF and cohesin regulate chromatin loop stability with distinct dynamics eLife 6 e25776 10.7554/eLife.25776 28467304 PMC5446243 · DOI · Paper page
  37. Hansen AS Woringer M Grimm JB Lavis LD Tjian R Darzacq X 2018 Robust model-based analysis of single-particle tracking experiments with Spot-On eLife 7 e33125 10.7554/eLife.33125 29300163 PMC5809147 · DOI
  38. Harrison MM Eisen MB 2015 Transcriptional activation of the zygotic genome in drosophila Current Topics in Developmental Biology 113 85 112 10.1016/bs.ctdb.2015.07.028 26358871 · DOI
  39. Hostettler L Grundy L Käser-Pébernard S Wicky C Schafer WR Glauser DA 2017 The Bright fluorescent protein mneongreen facilitates protein expression analysis in vivo G3: Genes|Genomes|Genetics 7 607 615 10.1534/g3.116.038133 28108553 PMC5295605 · DOI
  40. Hug CB Grimaldi AG Kruse K Vaquerizas JM 2017 Chromatin architecture emerges during zygotic genome activation independent of transcription Cell 169 216 228 10.1016/j.cell.2017.03.024 28388407 · DOI · Paper page
  41. Izeddin I Récamier V Bosanac L Cissé II Boudarene L Dugast-Darzacq C Proux F Bénichou O Voituriez R Bensaude O Dahan M Darzacq X 2014 Single-molecule tracking in live cells reveals distinct target-search strategies of transcription factors in the nucleus eLife 3 e02230 10.7554/eLife.02230 PMC4095940 24925319 · DOI
  42. Kato M McKnight SL 2018 A Solid-State conceptualization of information transfer from gene to message to protein Annual Review of Biochemistry 87 351 390 10.1146/annurev-biochem-061516-044700 29195049 · DOI
  43. Kepten E Weron A Sikora G Burnecki K Garini Y 2015 Guidelines for the fitting of anomalous diffusion mean square displacement graphs from single particle tracking experiments PLOS ONE 10 e0117722 10.1371/journal.pone.0117722 25680069 PMC4334513 · DOI
  44. Kondo S Ueda R 2013 Highly improved gene targeting by germline-specific cas9 expression in Drosophila Genetics 195 715 721 10.1534/genetics.113.156737 24002648 PMC3813859 · DOI
  45. Kovar H 2011 Dr. Jekyll and Mr. Hyde: The two faces of the fus/ews/taf15 protein family Sarcoma 2011 1 13 10.1155/2011/837474 PMC3005952 21197473 · DOI
  46. Lécuyer E Yoshida H Parthasarathy N Alm C Babak T Cerovina T Hughes TR Tomancak P Krause HM 2007 Global Analysis of mrna localization reveals a prominent role in organizing cellular architecture and function Cell 131 174 187 10.1016/j.cell.2007.08.003 17923096 · DOI · Paper page
  47. Li XY MacArthur S Bourgon R Nix D Pollard DA Iyer VN Hechmer A Simirenko L Stapleton M Luengo Hendriks CL Chu HC Ogawa N Inwood W Sementchenko V Beaton A Weiszmann R Celniker SE Knowles DW Gingeras T Speed TP Eisen MB Biggin MD 2008 Transcription Factors Bind Thousands of Active and Inactive Regions in the Drosophila Blastoderm PLOS Biology 6 e27 10.1371/journal.pbio.0060027 18271625 PMC2235902 · DOI
  48. Li X-Y Harrison MM Villalta JE Kaplan T Eisen MB 2014 Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition eLife 3 e03737 10.7554/eLife.03737 PMC4358338 25313869 · DOI
  49. Liang HL Nien CY Liu HY Metzstein MM Kirov N Rushlow C 2008 The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila Nature 456 400 403 10.1038/nature07388 18931655 PMC2597674 · DOI · Paper page
  50. Liu Z Legant WR Chen BC Li L Grimm JB Lavis LD Betzig E Tjian R 2014 3D imaging of Sox2 enhancer clusters in embryonic stem cells eLife 3 e04236 10.7554/eLife.04236 25537195 PMC4381973 · DOI
  51. Mazza D Abernathy A Golob N Morisaki T McNally JG 2012 A benchmark for chromatin binding measurements in live cells Nucleic Acids Research 40 e119 10.1093/nar/gks701 22844090 PMC3424588 · DOI
  52. Miné-Hattab J Recamier V Izeddin I Rothstein R Darzacq X 2017 Multi-scale tracking reveals scale-dependent chromatin dynamics after DNA damage Molecular Biology of the Cell 28 3323 3332 10.1091/mbc.e17-05-0317 PMC5687033 28794266 · DOI
  53. Mir M Reimer A Haines JE Li X-Y Stadler M Garcia H Eisen MB Darzacq X 2017 Dense Bicoid hubs accentuate binding along the morphogen gradient Genes & Development 31 1784 1794 10.1101/gad.305078.117 28982761 PMC5666676 · DOI · Paper page
  54. Mir M Reimer A Stadler M Tangara A Hansen AS Hockemeyer D Eisen MB Garcia H Darzacq X 2018 single molecule imaging in live embryos using lattice light-sheet microscopy Methods in Molecular Biology 1814 541 559 10.1007/978-1-4939-8591-3_32 29956254 PMC6225527 · DOI
  55. Nien C-Y Liang H-L Butcher S Sun Y Fu S Gocha T Kirov N Manak JR Rushlow C 2011 Temporal coordination of gene networks by zelda in the early Drosophila embryo PLOS Genetics 7 e1002339 10.1371/journal.pgen.1002339 22028675 PMC3197689 · DOI
  56. Normanno D Boudarène L Dugast-Darzacq C Chen J Richter C Proux F Bénichou O Voituriez R Darzacq X Dahan M 2015 Probing the target search of DNA-binding proteins in mammalian cells using TetR as model searcher Nature Communications 6 7357 10.1038/ncomms8357 26151127 PMC4507003 · DOI
  57. Ozdemir A Ma L White KP Stathopoulos A 2014 Su(H)-mediated repression positions gene boundaries along the dorsal-ventral axis of drosophila embryos Developmental Cell 31 100 113 10.1016/j.devcel.2014.08.005 25313963 PMC4201238 · DOI
  58. Para A Li Y Marshall-Colón A Varala K Francoeur NJ Moran TM Edwards MB Hackley C Bargmann BO Birnbaum KD McCombie WR Krouk G Coruzzi GM 2014 Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis PNAS 111 10371 10376 10.1073/pnas.1404657111 24958886 PMC4104873 · DOI
  59. Pearson JC Watson JD Crews ST 2012 Drosophila melanogaster Zelda and Single-minded collaborate to regulate an evolutionarily dynamic CNS midline cell enhancer Developmental Biology 366 420 432 10.1016/j.ydbio.2012.04.001 22537497 PMC3358474 · DOI
  60. Pritchard DK Schubiger G 1996 Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio Genes & Development 10 1131 1142 10.1101/gad.10.9.1131 8654928 · DOI
  61. Reichardt I Bonnay F Steinmann V Loedige I Burkard TR Meister G Knoblich JA 2018 The tumor suppressor Brat controls neuronal stem cell lineages by inhibiting Deadpan and Zelda EMBO Reports 19 102 117 10.15252/embr.201744188 29191977 PMC5757284 · DOI
  62. Ren X Sun J Housden BE Hu Y Roesel C Lin S Liu LP Yang Z Mao D Sun L Wu Q Ji JY Xi J Mohr SE Xu J Perrimon N Ni JQ 2013 Optimized gene editing technology for Drosophila melanogaster using germ line-specific Cas9 PNAS 110 19012 19017 10.1073/pnas.1318481110 24191015 PMC3839733 · DOI
  63. Schaffner W 1988 Gene regulation. A hit-and-run mechanism for transcriptional activation? Nature 336 427 428 10.1038/336427a0 3194030 · DOI
  64. Schulz KN Bondra ER Moshe A Villalta JE Lieb JD Kaplan T McKay DJ Harrison MM 2015 Zelda is differentially required for chromatin accessibility, transcription factor binding, and gene expression in the early Drosophila embryo Genome Research 25 1715 1726 10.1101/gr.192682.115 26335634 PMC4617967 · DOI · Paper page
  65. Sebo ZL Lee HB Peng Y Guo Y 2013 A simplified and efficient germline-specific CRISPR/Cas9 system for drosophila genomic engineering Fly 8 1 6 PMC3974895 24141137
  66. Sergé A Bertaux N Rigneault H Marguet D 2008 Dynamic multiple-target tracing to probe spatiotemporal cartography of cell membranes Nature Methods 5 687 694 10.1038/nmeth.1233 18604216 · DOI
  67. Shin D-H Hong J-W 2016 Transcriptional activity of the short gastrulation primary enhancer in the ventral midline requires its early activity in the presumptive neurogenic ectoderm BMB Reports 49 572 577 10.5483/BMBRep.2016.49.10.119 27616358 PMC5227300 · DOI
  68. Spiluttini B Gu B Belagal P Smirnova AS Nguyen VT Hébert C Schmidt U Bertrand E Darzacq X Bensaude O 2010 Splicing-independent recruitment of U1 snRNP to a transcription unit in living cells Journal of Cell Science 123 2085 2093 10.1242/jcs.061358 20519584 · DOI
  69. Sprague BL Pego RL Stavreva DA McNally JG 2004 Analysis of binding reactions by fluorescence recovery after photobleaching Biophysical Journal 86 3473 3495 10.1529/biophysj.103.026765 15189848 PMC1304253 · DOI
  70. Staller MV Fowlkes CC Bragdon MD Wunderlich Z Estrada J DePace AH 2015 A gene expression atlas of a bicoid-depleted Drosophila embryo reveals early canalization of cell fate Development 142 587 596 10.1242/dev.117796 25605785 PMC4302997 · DOI
  71. Staudt N Fellert S Chung H-R Jäckle H Vorbrüggen G 2006 Mutations of the Drosophila zinc finger-encoding gene vielfältig impair mitotic cell divisions and cause improper chromosome segregation Molecular Biology of the Cell 17 2356 2365 10.1091/mbc.e05-11-1056 16525017 PMC1446075 · DOI
  72. Strom AR Emelyanov AV Mir M Fyodorov DV Darzacq X Karpen GH 2017 Phase separation drives heterochromatin domain formation Nature 547 241 245 10.1038/nature22989 28636597 PMC6022742 · DOI
  73. Struhl G Struhl K Macdonald PM 1989 The gradient morphogen bicoid is a concentration-dependent transcriptional activator Cell 57 1259 1273 10.1016/0092-8674(89)90062-7 2567637 · DOI
  74. Sun Y Nien CY Chen K Liu HY Johnston J Zeitlinger J Rushlow C 2015 Zelda overcomes the high intrinsic nucleosome barrier at enhancers during Drosophila zygotic genome activation Genome Research 25 1703 1714 10.1101/gr.192542.115 26335633 PMC4617966 · DOI
  75. Tarantino N Tinevez JY Crowell EF Boisson B Henriques R Mhlanga M Agou F Israël A Laplantine E 2014 TNF and IL-1 exhibit distinct ubiquitin requirements for inducing NEMO-IKK supramolecular structures The Journal of Cell Biology 204 231 245 10.1083/jcb.201307172 24446482 PMC3897181 · DOI
  76. Tautz D 1988 Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres Nature 332 281 284 10.1038/332281a0 2450283 · DOI
  77. ten Bosch JR Benavides JA Cline TW 2006 The TAGteam DNA motif controls the timing of Drosophila pre-blastoderm transcription Development 133 1967 1977 10.1242/dev.02373 16624855 · DOI · Paper page
  78. Teves SS An L Hansen AS Xie L Darzacq X Tjian R 2016 A dynamic mode of mitotic bookmarking by transcription factors eLife 5 e22280 10.7554/eLife.22280 27855781 PMC5156526 · DOI
  79. Tomancak P Berman BP Beaton A Weiszmann R Kwan E Hartenstein V Celniker SE Rubin GM 2007 Global analysis of patterns of gene expression during Drosophila embryogenesis Genome Biology 8 R145 10.1186/gb-2007-8-7-r145 17645804 PMC2323238 · DOI
  80. Tsai A Muthusamy AK Alves MRP Lavis LD Singer RH Stern DL Crocker J 2017 Nuclear microenvironments modulate transcription from low-affinity enhancers eLife 6 e28975 10.7554/eLife.28975 29095143 PMC5695909 · DOI
  81. Venken KJ Carlson JW Schulze KL Pan H He Y Spokony R Wan KH Koriabine M de Jong PJ White KP Bellen HJ Hoskins RA 2009 Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster Nature Methods 6 431 434 10.1038/nmeth.1331 19465919 PMC2784134 · DOI
  82. Watanabe N Mitchison TJ 2002 Single-molecule speckle analysis of actin filament turnover in lamellipodia Science 295 1083 1086 10.1126/science.1067470 11834838 · DOI
  83. Wilk R Hu J Blotsky D Krause HM 2016 Diverse and pervasive subcellular distributions for both coding and long noncoding RNAs Genes & Development 30 594 609 10.1101/gad.276931.115 26944682 PMC4782052 · DOI
  84. Wollman AJ Shashkova S Hedlund EG Friemann R Hohmann S Leake MC 2017 Transcription factor clusters regulate genes in eukaryotic cells eLife 6 e27451 10.7554/eLife.27451 28841133 PMC5602325 · DOI
  85. Woringer M Darzacq X 2018 Protein motion in the nucleus: from anomalous diffusion to weak interactions arXiv https://arxiv.org/abs/1802.06275 PMC6103463 30065106 · arXiv
  86. Xiang S Kato M Wu LC Lin Y Ding M Zhang Y Yu Y McKnight SL 2015 The LC domain of hnrnpa2 adopts similar conformations in hydrogel polymers, liquid-like droplets, and nuclei Cell 163 829 839 10.1016/j.cell.2015.10.040 26544936 PMC4879888 · DOI
  87. Xu Z Chen H Ling J Yu D Struffi P Small S 2014 Impacts of the ubiquitous factor Zelda on Bicoid-dependent DNA binding and transcription in Drosophila Genes & Development 28 608 621 10.1101/gad.234534.113 24637116 PMC3967049 · DOI
  88. Xu H Sepúlveda LA Figard L Sokac AM Golding I 2015 Combining protein and mRNA quantification to decipher transcriptional regulation Nature Methods 12 739 742 10.1038/nmeth.3446 26098021 PMC4521975 · DOI
  89. Yu Z Ren M Wang Z Zhang B Rong YS Jiao R Gao G 2013 Highly Efficient Genome Modifications Mediated by CRISPR/Cas9 in Drosophila Genetics 195 289 291 10.1534/genetics.113.153825 23833182 PMC3761309 · DOI
  90. Zalokar M 1976 Autoradiographic study of protein and RNA formation during early development of Drosophila eggs Developmental Biology 49 425 437 10.1016/0012-1606(76)90185-8 817947 · DOI
  91. Zaret KS Mango SE 2016 Pioneer transcription factors, chromatin dynamics, and cell fate control Current Opinion in Genetics & Development 37 76 81 10.1016/j.gde.2015.12.003 26826681 PMC4914445 · DOI
  92. Zhang M Chang H Zhang Y Yu J Wu L Ji W Chen J Liu B Lu J Liu Y Zhang J Xu P Xu T 2012 Rational design of true monomeric and bright photoactivatable fluorescent proteins Nature Methods 9 727 729 10.1038/nmeth.2021 22581370 · DOI
  93. Zhang Y Arcia S Perez B Fernandez-Funez P Rincon-Limas DE 2013 p∆TubHA4C, a new versatile vector for constitutive expression in Drosophila Molecular Biology Reports 40 5407 5415 10.1007/s11033-013-2639-7 23681549 · DOI

Cited by

Sorted by citations

Authors
Mir, M., Stadler, M. R., Ortiz, S. A., Hannon, C. E., Harrison, M. M., Darzacq, X., & Eisen, M. B.
Affiliations
  • University of California, Berkeley (US)
  • Howard Hughes Medical Institute (US)
  • University of Wisconsin–Madison (US)
Corresponding author
  • Darzacq, Xavier
  • Eisen, Michael B
Venue
eLife
Published
2018-12-27
Volume
7
ISSN
2050-084X (ISSN-L)
OpenAlex
W2949107687
Cited by
207
References
5
Citations by year
2026: 17 · 2025: 24 · 2024: 37 · 2023: 37 · 2022: 21 · 2021: 28 · 2020: 23 · 2019: 16 · 2018: 4
FWCI
6.31
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
Funders
  • American Cancer Society
  • National Institutes of Health (GM111694, UO1-EB021236, U54-DK107980)
  • California Institute for Regenerative Medicine (LA1-08013)
  • Howard Hughes Medical Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Diffusion and Search Dynamics
Keywords
transcription factor-DNA binding, Zelda, Bicoid, transient protein interactions, transcriptional regulation, Drosophila embryo, nuclear organization, lattice light-sheet microscopy, 4D imaging, single-molecule imaging, dissociation rate constant
MeSH terms
Animals, Binding Sites, Cell Nucleus, Drosophila melanogaster, Embryo, Nonmammalian, Nuclear Proteins, Protein Binding, Transcription Factors, Trans-Activators, Homeodomain Proteins, Gene Expression Regulation, Developmental, Microscopy, Confocal, Imaging, Three-Dimensional, Drosophila Proteins, Time-Lapse Imaging

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review