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An atlas of dynamic chromatin landscapes in mouse fetal development

Author

Listed:
  • David U. Gorkin

    (Ludwig Institute for Cancer Research
    University of California, San Diego School of Medicine)

  • Iros Barozzi

    (Lawrence Berkeley National Laboratory
    Imperial College London)

  • Yuan Zhao

    (Ludwig Institute for Cancer Research
    University of California, San Diego)

  • Yanxiao Zhang

    (Ludwig Institute for Cancer Research)

  • Hui Huang

    (Ludwig Institute for Cancer Research
    University of California, San Diego School of Medicine)

  • Ah Young Lee

    (Ludwig Institute for Cancer Research)

  • Bin Li

    (Ludwig Institute for Cancer Research)

  • Joshua Chiou

    (University of California, San Diego School of Medicine
    University of California, San Diego School of Medicine)

  • Andre Wildberg

    (University of California, San Diego School of Medicine)

  • Bo Ding

    (University of California, San Diego School of Medicine)

  • Bo Zhang

    (Penn State School of Medicine)

  • Mengchi Wang

    (University of California, San Diego School of Medicine)

  • J. Seth Strattan

    (Stanford University School of Medicine, Department of Genetics)

  • Jean M. Davidson

    (Stanford University School of Medicine, Department of Genetics)

  • Yunjiang Qiu

    (Ludwig Institute for Cancer Research
    University of California, San Diego)

  • Veena Afzal

    (Lawrence Berkeley National Laboratory)

  • Jennifer A. Akiyama

    (Lawrence Berkeley National Laboratory)

  • Ingrid Plajzer-Frick

    (Lawrence Berkeley National Laboratory)

  • Catherine S. Novak

    (Lawrence Berkeley National Laboratory)

  • Momoe Kato

    (Lawrence Berkeley National Laboratory)

  • Tyler H. Garvin

    (Lawrence Berkeley National Laboratory)

  • Quan T. Pham

    (Lawrence Berkeley National Laboratory)

  • Anne N. Harrington

    (Lawrence Berkeley National Laboratory)

  • Brandon J. Mannion

    (Lawrence Berkeley National Laboratory)

  • Elizabeth A. Lee

    (Lawrence Berkeley National Laboratory)

  • Yoko Fukuda-Yuzawa

    (Lawrence Berkeley National Laboratory)

  • Yupeng He

    (University of California, San Diego
    Salk Institute for Biological Studies)

  • Sebastian Preissl

    (Ludwig Institute for Cancer Research
    University of California, San Diego School of Medicine)

  • Sora Chee

    (Ludwig Institute for Cancer Research)

  • Jee Yun Han

    (University of California, San Diego School of Medicine)

  • Brian A. Williams

    (California Institute of Technology)

  • Diane Trout

    (California Institute of Technology)

  • Henry Amrhein

    (California Institute of Technology)

  • Hongbo Yang

    (Penn State School of Medicine)

  • J. Michael Cherry

    (Stanford University School of Medicine, Department of Genetics)

  • Wei Wang

    (University of California, San Diego School of Medicine)

  • Kyle Gaulton

    (University of California, San Diego School of Medicine)

  • Joseph R. Ecker

    (Salk Institute for Biological Studies
    Salk Institute for Biological Studies)

  • Yin Shen

    (Institute for Human Genetics and University of California, San Francisco
    University of California, San Francisco)

  • Diane E. Dickel

    (Lawrence Berkeley National Laboratory)

  • Axel Visel

    (Lawrence Berkeley National Laboratory
    US Department of Energy Joint Genome Institute
    University of California, Merced)

  • Len A. Pennacchio

    (Lawrence Berkeley National Laboratory
    US Department of Energy Joint Genome Institute
    University of California, Berkeley)

  • Bing Ren

    (Ludwig Institute for Cancer Research
    University of California, San Diego School of Medicine
    University of California, San Diego School of Medicine
    University of California, San Diego School of Medicine)

Abstract

The Encyclopedia of DNA Elements (ENCODE) project has established a genomic resource for mammalian development, profiling a diverse panel of mouse tissues at 8 developmental stages from 10.5 days after conception until birth, including transcriptomes, methylomes and chromatin states. Here we systematically examined the state and accessibility of chromatin in the developing mouse fetus. In total we performed 1,128 chromatin immunoprecipitation with sequencing (ChIP–seq) assays for histone modifications and 132 assay for transposase-accessible chromatin using sequencing (ATAC–seq) assays for chromatin accessibility across 72 distinct tissue-stages. We used integrative analysis to develop a unified set of chromatin state annotations, infer the identities of dynamic enhancers and key transcriptional regulators, and characterize the relationship between chromatin state and accessibility during developmental gene regulation. We also leveraged these data to link enhancers to putative target genes and demonstrate tissue-specific enrichments of sequence variants associated with disease in humans. The mouse ENCODE data sets provide a compendium of resources for biomedical researchers and achieve, to our knowledge, the most comprehensive view of chromatin dynamics during mammalian fetal development to date.

Suggested Citation

  • David U. Gorkin & Iros Barozzi & Yuan Zhao & Yanxiao Zhang & Hui Huang & Ah Young Lee & Bin Li & Joshua Chiou & Andre Wildberg & Bo Ding & Bo Zhang & Mengchi Wang & J. Seth Strattan & Jean M. Davidson, 2020. "An atlas of dynamic chromatin landscapes in mouse fetal development," Nature, Nature, vol. 583(7818), pages 744-751, July.
  • Handle: RePEc:nat:nature:v:583:y:2020:i:7818:d:10.1038_s41586-020-2093-3
    DOI: 10.1038/s41586-020-2093-3
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    Cited by:

    1. Ye Cai & Huifen Cao & Fang Wang & Yufei Zhang & Philipp Kapranov, 2022. "Complex genomic patterns of abasic sites in mammalian DNA revealed by a high-resolution SSiNGLe-AP method," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    2. Raúl F. Pérez & Patricia Tezanos & Alfonso Peñarroya & Alejandro González-Ramón & Rocío G. Urdinguio & Javier Gancedo-Verdejo & Juan Ramón Tejedor & Pablo Santamarina-Ojeda & Juan José Alba-Linares & , 2024. "A multiomic atlas of the aging hippocampus reveals molecular changes in response to environmental enrichment," Nature Communications, Nature, vol. 15(1), pages 1-26, December.
    3. Zhangyuan Pan & Yuelin Yao & Hongwei Yin & Zexi Cai & Ying Wang & Lijing Bai & Colin Kern & Michelle Halstead & Ganrea Chanthavixay & Nares Trakooljul & Klaus Wimmers & Goutam Sahana & Guosheng Su & M, 2021. "Pig genome functional annotation enhances the biological interpretation of complex traits and human disease," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Yael Aylon & Noa Furth & Giuseppe Mallel & Gilgi Friedlander & Nishanth Belugali Nataraj & Meng Dong & Ori Hassin & Rawan Zoabi & Benjamin Cohen & Vanessa Drendel & Tomer Meir Salame & Saptaparna Mukh, 2022. "Breast cancer plasticity is restricted by a LATS1-NCOR1 repressive axis," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    5. Renata Bordeira-Carriço & Joana Teixeira & Marta Duque & Mafalda Galhardo & Diogo Ribeiro & Rafael D. Acemel & Panos. N. Firbas & Juan J. Tena & Ana Eufrásio & Joana Marques & Fábio J. Ferreira & Telm, 2022. "Multidimensional chromatin profiling of zebrafish pancreas to uncover and investigate disease-relevant enhancers," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    6. 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.
    7. Adriana Arneson & Amin Haghani & Michael J. Thompson & Matteo Pellegrini & Soo Bin Kwon & Ha Vu & Emily Maciejewski & Mingjia Yao & Caesar Z. Li & Ake T. Lu & Marco Morselli & Liudmilla Rubbi & Bret B, 2022. "A mammalian methylation array for profiling methylation levels at conserved sequences," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. 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.
    9. Phoebe Lut Fei Tam & Ming Fung Cheung & Lu Yan Chan & Danny Leung, 2024. "Cell-type differential targeting of SETDB1 prevents aberrant CTCF binding, chromatin looping, and cis-regulatory interactions," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Sudha Sunil Rajderkar & Kitt Paraiso & Maria Luisa Amaral & Michael Kosicki & Laura E. Cook & Fabrice Darbellay & Cailyn H. Spurrell & Marco Osterwalder & Yiwen Zhu & Han Wu & Sarah Yasmeen Afzal & Ma, 2024. "Dynamic enhancer landscapes in human craniofacial development," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Jennifer P. Nguyen & Timothy D. Arthur & Kyohei Fujita & Bianca M. Salgado & Margaret K. R. Donovan & Hiroko Matsui & Ji Hyun Kim & Agnieszka D’Antonio-Chronowska & Matteo D’Antonio & Kelly A. Frazer, 2023. "eQTL mapping in fetal-like pancreatic progenitor cells reveals early developmental insights into diabetes risk," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    12. Ze Yan & Ji Yang & Wen-Tian Wei & Ming-Liang Zhou & Dong-Xin Mo & Xing Wan & Rui Ma & Mei-Ming Wu & Jia-Hui Huang & Ya-Jing Liu & Feng-Hua Lv & Meng-Hua Li, 2024. "A time-resolved multi-omics atlas of transcriptional regulation in response to high-altitude hypoxia across whole-body tissues," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    13. Christopher T. Rhodes & Joyce J. Thompson & Apratim Mitra & Dhanya Asokumar & Dongjin R. Lee & Daniel J. Lee & Yajun Zhang & Eva Jason & Ryan K. Dale & Pedro P. Rocha & Timothy J. Petros, 2022. "An epigenome atlas of neural progenitors within the embryonic mouse forebrain," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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