Cited by 126Genomics and Chromatin DynamicsEpigenetics and DNA MethylationChromatin Remodeling and Cancer

Widespread activation of developmental gene expression characterized by PRC1-dependent chromatin looping

Open access
Loubiere, V., Papadopoulos, G. L., Szabo, Q., Martinez, A-M., Cavalli, G.·2020·Science Advances

Abstract

Polycomb repressive complex 1 shapes 3D loops associated with transcription of key developmental genes.

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 · 10.1126/sciadv.aax4001

Cites

4 of 4 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?

  • PRC1 mediates chromatin interactions between a subset of active developmental enhancers and promoters in Drosophila.

    “Moreover, PRC1 was recently found to mediate chromatin interactions between a subset of active developmental enhancers and promoters in Drosophila [361].”

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: 44

  1. [1]Schuettengruber B., Bourbon H. M., Di Croce L., Cavalli G., Genome regulation by polycomb and trithorax: 70 years and counting. Cell 171, 34– 57 (2017). 28938122
  2. [2]Loubiere V., Martinez A. M., Cavalli G., Cell fate and developmental regulation dynamics by polycomb proteins and 3D genome architecture. BioEssays 41, e1800222 (2019). 30793782
  3. [3]Loubiere V., Delest A., Thomas A., Bonev B., Schuettengruber B., Sati S., Martinez A.-M., Cavalli G., Coordinate redeployment of PRC1 proteins suppresses tumor formation during Drosophila development. Nat. Genet. 48, 1436– 1442 (2016). 27643538 PMC5407438
  4. [4]Pherson M., Misulovin Z., Gause M., Mihindukulasuriya K., Swain A., Dorsett D., Polycomb repressive complex 1 modifies transcription of active genes. Sci. Adv. 3, e1700944 (2017). 28782042 PMC5540264
  5. [5]Morey L., Santanach A., Blanco E., Aloia L., Nora E. P., Bruneau B. G., Croce L. D., Polycomb regulates mesoderm cell fate-specification in embryonic stem cells through activation and repression mechanisms. Cell Stem Cell 17, 300– 315 (2015). 26340528
  6. [6]Cohen I., Zhao D., Bar C., Valdes V. J., Dauber-Decker K. L., Nguyen M. B., Nakayama M., Rendl M., Bickmore W. A., Koseki H., Zheng D., Ezhkova E., PRC1 fine-tunes gene repression and activation to safeguard skin development and stem cell specification. Cell Stem Cell 22, 726– 739.e7 (2018). 29727681 PMC5944606
  7. [7]Eagen K. P., Aiden E. L., Kornberg R. D., Polycomb-mediated chromatin loops revealed by a subkilobase-resolution chromatin interaction map. Proc. Natl. Acad. Sci. U.S.A. 114, 8764– 8769 (2017). 28765367 PMC5565414
  8. [8]Ogiyama Y., Schuettengruber B., Papadopoulos G. L., Chang J.-M., Cavalli G., Polycomb-dependent chromatin looping contributes to gene silencing during Drosophila development. Mol. Cell 71, 73– 88 (2018). 30008320
  9. [9]Mortazavi A., Pepke S., Jansen C., Marinov G. K., Ernst J., Kellis M., Hardison R. C., Myers R. M., Wold B. J., Integrating and mining the chromatin landscape of cell-type specificity using self-organizing maps. Genome Res. 23, 2136– 2148 (2013). 24170599 PMC3847782
  10. [10]Filion G. J., van Bemmel J. G., Braunschweig U., Talhout W., Kind J., Ward L. D., Brugman W., de Castro I. J., Kerkhoven R. M., Bussemaker H. J., van Steensel B., Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143, 212– 224 (2010). 20888037 PMC3119929
  11. [11]Lee H.-G., Kahn T. G., Simcox A., Schwartz Y. B., Pirrotta V., Genome-wide activities of Polycomb complexes control pervasive transcription. Genome Res. 25, 1170– 1181 (2015). 25986499 PMC4510001
  12. [13]Sexton T., Yaffe E., Kenigsberg E., Bantignies F., Leblanc B., Hoichman M., Parrinello H., Tanay A., Cavalli G., Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458– 472 (2012). 22265598
  13. [14]Lieberman-Aiden E., van Berkum N. L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B. R., Sabo P. J., Dorschner M. O., Sandstrom R., Bernstein B., Bender M. A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L. A., Lander E. S., Dekker J., Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289– 293 (2009). 19815776 PMC2858594
  14. [15]Davie K., Jacobs J., Atkins M., Potier D., Christiaens V., Halder G., Aerts S., Discovery of transcription factors and regulatory regions driving in vivo tumor development by ATAC-seq and FAIRE-seq open chromatin profiling. PLOS Genet. 11, e1004994 (2015). 25679813 PMC4334524
  15. [16]McKay D. J., Lieb J. D., A common set of DNA regulatory elements shapes Drosophila appendages. Dev. Cell 27, 306– 318 (2013). 24229644 PMC3866527
  16. [17]Yanez-Cuna J. O., Arnold C. D., Stampfel G., Boryń Ł. M., Gerlach D., Rath M., Stark A., Dissection of thousands of cell type-specific enhancers identifies dinucleotide repeat motifs as general enhancer features. Genome Res. 24, 1147– 1156 (2014). 24714811 PMC4079970
  17. [19]Erceg J., Pakozdi T., Marco-Ferreres R., Ghavi-Helm Y., Girardot C., Bracken A. P., Furlong E. E. M., Dual functionality of cis-regulatory elements as developmental enhancers and Polycomb response elements. Genes Dev. 31, 590– 602 (2017). 28381411 PMC5393054
  18. [21]Curtiss J., Burnett M., Mlodzik M., distal antenna and distal antenna-related function in the retinal determination network during eye development in Drosophila. Dev. Biol. 306, 685– 702 (2007). 17493605 PMC1986786
  19. [22]Davis T. L., Rebay I., Master regulators in development: Views from the Drosophila retinal determination and mammalian pluripotency gene networks. Dev. Biol. 421, 93– 107 (2017). 27979656 PMC5496713
  20. [23]Kondo T., Isono K., Kondo K., Endo T. A., Itohara S., Vidal M., Koseki H., Polycomb potentiates meis2 activation in midbrain by mediating interaction of the promoter with a tissue-specific enhancer. Dev. Cell 28, 94– 101 (2014). 24374176
  21. [25]Kloet S. L., Makowski M. M., Baymaz H. I., van Voorthuijsen L., Karemaker I. D., Santanach A., Jansen P. W. T. C., Croce L. D., Vermeulen M., The dynamic interactome and genomic targets of Polycomb complexes during stem-cell differentiation. Nat. Struct. Mol. Biol. 23, 682– 690 (2016). 27294783 PMC4939079
  22. [26]Stowers R. S., Schwarz T. L., A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152, 1631– 1639 (1999). 10430588 PMC1460682
  23. [27]Loubiere V., Delest A., Schuettengruber B., Martinez A.-M., Cavalli G., Chromatin immunoprecipitation experiments from whole drosophila embryos or larval imaginal discs. Bio Protoc. 7, e2327 (2017). PMC8410254 34541088
  24. [28]Strutt H., Paro R., The polycomb group protein complex of Drosophila melanogaster has different compositions at different target genes. Mol. Cell. Biol. 17, 6773– 6783 (1997). 9372908 PMC232533
  25. [29]Bantignies F., Cavalli G., Topological organization of Drosophila Hox genes using DNA fluorescent in situ hybridization. Methods Mol. Biol. 1196, 103– 120 (2014). 25151160
  26. [30]Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.-Y., White D. J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676– 682 (2012). 22743772 PMC3855844
  27. [31]Langmead B., Salzberg S. L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357– 359 (2012). 22388286 PMC3322381
  28. [32]Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R.; Genome Project Data Processing Subgroup, The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078– 2079 (2009). 19505943 PMC2723002
  29. [33]Zhang Y., Liu T., Meyer C. A., Eeckhoute J., Johnson D. S., Bernstein B. E., Nusbaum C., Myers R. M., Brown M., Li W., Liu X. S., Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008). 18798982 PMC2592715
  30. [34]Ramirez F., Ryan D. P., Grüning B., Bhardwaj V., Kilpert F., Richter A. S., Heyne S., Dündar F., Manke T., deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160– W165 (2016). 27079975 PMC4987876
  31. [35]Kent W. J., Zweig A. S., Barber G., Hinrichs A. S., Karolchik D., BigWig and BigBed: enabling browsing of large distributed datasets. Bioinformatics 26, 2204– 2207 (2010). 20639541 PMC2922891
  32. [36]Robinson J. T., Thorvaldsdóttir H., Winckler W., Guttman M., Lander E. S., Getz G., Mesirov J. P., Integrative genomics viewer. Nat. Biotechnol. 29, 24– 26 (2011). 21221095 PMC3346182
  33. [37]Stempor P., Ahringer J., SeqPlots - Interactive software for exploratory data analyses, pattern discovery and visualization in genomics. Wellcome Open Res. 1, 14 (2016). 27918597 PMC5133382
  34. [38]Pohl A., Beato M., bwtool: A tool for bigWig files. Bioinformatics 30, 1618– 1619 (2014). 24489365 PMC4029031
  35. [39]Kohonen T., Self-organizing neural projections. Neural Netw. 19, 723– 733 (2006). 16774731
  36. [40]R. Wehrens, L. M. C. Buydens, Self- and Super-organizing Maps in R: The kohonen Package. 2007 21, 19%J Journal of Statistical Software (2007).
  37. [41]Nagano T., Lubling Y., Várnai C., Dudley C., Leung W., Baran Y., Cohen N. M., Wingett S., Fraser P., Tanay A., Cell-cycle dynamics of chromosomal organization at single-cell resolution. Nature 547, 61– 67 (2017). 28682332 PMC5567812
  38. [42]N. M. Cohen, P. Olivares-Chauvet, Y. Lubling, Y. Baran, A. Lifshitz, M. Hoichman, A. Tanay, SHAMAN: bin-free randomization, normalization and screening of Hi-C matrices. bioRxiv 187203; doi: 10.1101/187203 · DOI
  39. [43]Dobin A., Davis C. A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., Gingeras T. R., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15– 21 (2013). 23104886 PMC3530905
  40. [44]Anders S., Pyl P. T., Huber W., HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166– 169 (2015). 25260700 PMC4287950
  41. [45]Love M. I., Huber W., Anders S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014). 25516281 PMC4302049
  42. [46]Huang D. W., Sherman B. T., Lempicki R. A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44– 57 (2009). 19131956
  43. [47]Yu G., Wang L.-G., Han Y., He Q.-Y., clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS 16, 284– 287 (2012). 22455463 PMC3339379
  44. [48]Quinlan A. R., Hall I. M., BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841– 842 (2010). 20110278 PMC2832824

Cited by

Sorted by citations

Authors
Loubiere, V., Papadopoulos, G. L., Szabo, Q., Martinez, A.-M., & Cavalli, G.
Affiliations
  • Institute of Human Genetics, UMR 9002, CNRS–University of Montpellier, 34396 Montpellier, France.
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
  • Martinez, A-M.
  • Cavalli, G.
Venue
Science Advances
Published
2020-01-10
Volume
6
Issue
2
Pages
eaax4001-eaax4001
ISSN
2375-2548 (ISSN-L)
OpenAlex
W2999808884
Cited by
126
References
4
Citations by year
2026: 13 · 2025: 24 · 2024: 16 · 2023: 24 · 2022: 21 · 2021: 22 · 2020: 6
FWCI
5.97
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Science Advances (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by-nc)
Funders
  • H2020 European Research Council (2017-AdG No 788972)
  • European Research Council (ERC-2008-AdG No 232947)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords
PRC1, chromatin looping, developmental gene expression, RING1B, 3D genome organization, neuronal differentiation, transcriptional regulation, chromatin interactions
MeSH terms
Animals, Cell Differentiation, Chromatin, Drosophila melanogaster, Enhancer Elements, Genetic, Promoter Regions, Genetic, Protein Binding, Gene Expression Regulation, Developmental, Response Elements, Genes, Developmental, Mice, Genetic Loci, Neural Stem Cells, Imaginal Discs, Polycomb Repressive Complex 1

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