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Enhancer redundancy provides phenotypic robustness in mammalian development

Author

Listed:
  • Marco Osterwalder

    (Environmental Genomics and Systems Biology Division)

  • Iros Barozzi

    (Environmental Genomics and Systems Biology Division)

  • Virginie Tissières

    (University of Basel
    Centro Andaluz de Biología del Desarrollo, CSIC/JA/Universidad Pablo de Olavide)

  • Yoko Fukuda-Yuzawa

    (Environmental Genomics and Systems Biology Division)

  • Brandon J. Mannion

    (Environmental Genomics and Systems Biology Division)

  • Sarah Y. Afzal

    (Environmental Genomics and Systems Biology Division)

  • Elizabeth A. Lee

    (Environmental Genomics and Systems Biology Division)

  • Yiwen Zhu

    (Environmental Genomics and Systems Biology Division)

  • Ingrid Plajzer-Frick

    (Environmental Genomics and Systems Biology Division)

  • Catherine S. Pickle

    (Environmental Genomics and Systems Biology Division)

  • Momoe Kato

    (Environmental Genomics and Systems Biology Division)

  • Tyler H. Garvin

    (Environmental Genomics and Systems Biology Division)

  • Quan T. Pham

    (Environmental Genomics and Systems Biology Division)

  • Anne N. Harrington

    (Environmental Genomics and Systems Biology Division)

  • Jennifer A. Akiyama

    (Environmental Genomics and Systems Biology Division)

  • Veena Afzal

    (Environmental Genomics and Systems Biology Division)

  • Javier Lopez-Rios

    (University of Basel
    Centro Andaluz de Biología del Desarrollo, CSIC/JA/Universidad Pablo de Olavide)

  • Diane E. Dickel

    (Environmental Genomics and Systems Biology Division)

  • Axel Visel

    (Environmental Genomics and Systems Biology Division
    US Department of Energy Joint Genome Institute
    School of Natural Sciences, University of California)

  • Len A. Pennacchio

    (Environmental Genomics and Systems Biology Division
    US Department of Energy Joint Genome Institute
    Comparative Biochemistry Program, University of California)

Abstract

Gene enhancer knockout phenotypes and analysis of enhancer activity patterns show that developmental genes are regulated by multiple redundant enhancers in mouse embryos.

Suggested Citation

  • Marco Osterwalder & Iros Barozzi & Virginie Tissières & Yoko Fukuda-Yuzawa & Brandon J. Mannion & Sarah Y. Afzal & Elizabeth A. Lee & Yiwen Zhu & Ingrid Plajzer-Frick & Catherine S. Pickle & Momoe Kat, 2018. "Enhancer redundancy provides phenotypic robustness in mammalian development," Nature, Nature, vol. 554(7691), pages 239-243, February.
    • Handle: RePEc:nat:nature:v:554:y:2018:i:7691:d:10.1038_nature25461
    DOI: 10.1038/nature25461
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    Citations

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    Cited by:

    1. Fabrice Darbellay & Anna Ramisch & Lucille Lopez-Delisle & Michael Kosicki & Antonella Rauseo & Zahra Jouini & Axel Visel & Guillaume Andrey, 2024. "Pre-hypertrophic chondrogenic enhancer landscape of limb and axial skeleton development," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Naoko Koyano-Nakagawa & Wuming Gong & Satyabrata Das & Joshua W. M. Theisen & Tran B. Swanholm & Daniel Ly & Nikita Dsouza & Bhairab N. Singh & Hiroko Kawakami & Samantha Young & Katherine Q. Chen & Y, 2022. "Etv2 regulates enhancer chromatin status to initiate Shh expression in the limb bud," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Markus Götz & Olivier Messina & Sergio Espinola & Jean-Bernard Fiche & Marcelo Nollmann, 2022. "Multiple parameters shape the 3D chromatin structure of single nuclei at the doc locus in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Matthieu Santos & Stéphanie Backer & Frédéric Auradé & Matthew Man-Kin Wong & Maud Wurmser & Rémi Pierre & Francina Langa & Marcio Cruzeiro & Alain Schmitt & Jean-Paul Concordet & Athanassia Sotiropou, 2022. "A fast Myosin super enhancer dictates muscle fiber phenotype through competitive interactions with Myosin genes," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Samuel Abassah-Oppong & Matteo Zoia & Brandon J. Mannion & Raquel Rouco & Virginie Tissières & Cailyn H. Spurrell & Virginia Roland & Fabrice Darbellay & Anja Itum & Julie Gamart & Tabitha A. Festa-Da, 2024. "A gene desert required for regulatory control of pleiotropic Shox2 expression and embryonic survival," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    6. Raquel Rouco & Olimpia Bompadre & Antonella Rauseo & Olivier Fazio & Rodrigue Peraldi & Fabrizio Thorel & Guillaume Andrey, 2021. "Cell-specific alterations in Pitx1 regulatory landscape activation caused by the loss of a single enhancer," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    7. Daniela Michelatti & Sven Beyes & Chiara Bernardis & Maria Luce Negri & Leonardo Morelli & Naiara Garcia Bediaga & Vittoria Poli & Luca Fagnocchi & Sara Lago & Sarah D’Annunzio & Nicole Cona & Ilaria , 2024. "Oncogenic enhancers prime quiescent metastatic cells to escape NK immune surveillance by eliciting transcriptional memory," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    8. Andrea Wilderman & Eva D’haene & Machteld Baetens & Tara N. Yankee & Emma Wentworth Winchester & Nicole Glidden & Ellen Roets & Jo Dorpe & Sandra Janssens & Danny E. Miller & Miranda Galey & Kari M. B, 2024. "A distant global control region is essential for normal expression of anterior HOXA genes during mouse and human craniofacial development," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    9. Arthur S. Lee & Lauren J. Ayers & Michael Kosicki & Wai-Man Chan & Lydia N. Fozo & Brandon M. Pratt & Thomas E. Collins & Boxun Zhao & Matthew F. Rose & Alba Sanchis-Juan & Jack M. Fu & Isaac Wong & X, 2024. "A cell type-aware framework for nominating non-coding variants in Mendelian regulatory disorders," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    10. Vincent Loubiere & Bernardo P. Almeida & Michaela Pagani & Alexander Stark, 2024. "Developmental and housekeeping transcriptional programs display distinct modes of enhancer-enhancer cooperativity in Drosophila," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    11. Sandra Kessler & Maryline Minoux & Onkar Joshi & Yousra Zouari & Sebastien Ducret & Fiona Ross & Nathalie Vilain & Adwait Salvi & Joachim Wolff & Hubertus Kohler & Michael B. Stadler & Filippo M. Rijl, 2023. "A multiple super-enhancer region establishes inter-TAD interactions and controls Hoxa function in cranial neural crest," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    12. Jan-Renier Moonen & James Chappell & Minyi Shi & Tsutomu Shinohara & Dan Li & Maxwell R. Mumbach & Fan Zhang & Ramesh V. Nair & Joseph Nasser & Daniel H. Mai & Shalina Taylor & Lingli Wang & Ross J. M, 2022. "KLF4 recruits SWI/SNF to increase chromatin accessibility and reprogram the endothelial enhancer landscape under laminar shear stress," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    13. Jin Woo Oh & Michael A. Beer, 2024. "Gapped-kmer sequence modeling robustly identifies regulatory vocabularies and distal enhancers conserved between evolutionarily distant mammals," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Xuemeng Zhou & Tsz Wing Sam & Ah Young Lee & Danny Leung, 2021. "Mouse strain-specific polymorphic provirus functions as cis-regulatory element leading to epigenomic and transcriptomic variations," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    15. Matthew J Harder & Julie Hix & Wendy M Reeves & Michael T Veeman, 2021. "Ciona Brachyury proximal and distal enhancers have different FGF dose-response relationships," PLOS Genetics, Public Library of Science, vol. 17(1), pages 1-23, January.
    16. Christopher Chase Bolt & Lucille Lopez-Delisle & Aurélie Hintermann & Bénédicte Mascrez & Antonella Rauseo & Guillaume Andrey & Denis Duboule, 2022. "Context-dependent enhancer function revealed by targeted inter-TAD relocation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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