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Transcription factor binding dynamics during human ES cell differentiation

Author

Listed:
  • Alexander M. Tsankov

    (Broad Institute of MIT and Harvard
    Harvard Stem Cell Institute
    Harvard University)

  • Hongcang Gu

    (Broad Institute of MIT and Harvard)

  • Veronika Akopian

    (Harvard Stem Cell Institute
    Harvard University)

  • Michael J. Ziller

    (Broad Institute of MIT and Harvard
    Harvard Stem Cell Institute
    Harvard University)

  • Julie Donaghey

    (Broad Institute of MIT and Harvard
    Harvard Stem Cell Institute
    Harvard University)

  • Ido Amit

    (Broad Institute of MIT and Harvard
    Weizmann Institute, Rehovot, 76100 Israel)

  • Andreas Gnirke

    (Broad Institute of MIT and Harvard)

  • Alexander Meissner

    (Broad Institute of MIT and Harvard
    Harvard Stem Cell Institute
    Harvard University)

Abstract

Pluripotent stem cells provide a powerful system to dissect the underlying molecular dynamics that regulate cell fate changes during mammalian development. Here we report the integrative analysis of genome-wide binding data for 38 transcription factors with extensive epigenome and transcriptional data across the differentiation of human embryonic stem cells to the three germ layers. We describe core regulatory dynamics and show the lineage-specific behaviour of selected factors. In addition to the orchestrated remodelling of the chromatin landscape, we find that the binding of several transcription factors is strongly associated with specific loss of DNA methylation in one germ layer, and in many cases a reciprocal gain in the other layers. Taken together, our work shows context-dependent rewiring of transcription factor binding, downstream signalling effectors, and the epigenome during human embryonic stem cell differentiation.

Suggested Citation

  • Alexander M. Tsankov & Hongcang Gu & Veronika Akopian & Michael J. Ziller & Julie Donaghey & Ido Amit & Andreas Gnirke & Alexander Meissner, 2015. "Transcription factor binding dynamics during human ES cell differentiation," Nature, Nature, vol. 518(7539), pages 344-349, February.
    • Handle: RePEc:nat:nature:v:518:y:2015:i:7539:d:10.1038_nature14233
    DOI: 10.1038/nature14233
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    Cited by:

    1. Pedro Madrigal & Siwei Deng & Yuliang Feng & Stefania Militi & Kim Jee Goh & Reshma Nibhani & Rodrigo Grandy & Anna Osnato & Daniel Ortmann & Stephanie Brown & Siim Pauklin, 2023. "Epigenetic and transcriptional regulations prime cell fate before division during human pluripotent stem cell differentiation," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    2. Yanting Luo & Jianlin He & Xiguang Xu & Ming-an Sun & Xiaowei Wu & Xuemei Lu & Hehuang Xie, 2018. "Integrative single-cell omics analyses reveal epigenetic heterogeneity in mouse embryonic stem cells," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-21, March.
    3. Lenny J. Negrón-Piñeiro & Yushi Wu & Sydney Popsuj & Diana S. José-Edwards & Alberto Stolfi & Anna Di Gregorio, 2024. "Cis-regulatory interfaces reveal the molecular mechanisms underlying the notochord gene regulatory network of Ciona," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Ishtiaque Hossain & Pierre Priam & Sofia C. Reynoso & Sahil Sahni & Xiao X. Zhang & Laurence Côté & Joelle Doumat & Candus Chik & Tianxin Fu & Julie A. Lessard & William A. Pastor, 2024. "ZIC2 and ZIC3 promote SWI/SNF recruitment to safeguard progression towards human primed pluripotency," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. Anat Kreimer & Tal Ashuach & Fumitaka Inoue & Alex Khodaverdian & Chengyu Deng & Nir Yosef & Nadav Ahituv, 2022. "Massively parallel reporter perturbation assays uncover temporal regulatory architecture during neural differentiation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Francesco Panariello & Onelia Gagliano & Camilla Luni & Antonio Grimaldi & Silvia Angiolillo & Wei Qin & Anna Manfredi & Patrizia Annunziata & Shaked Slovin & Lorenzo Vaccaro & Sara Riccardo & Valenti, 2023. "Cellular population dynamics shape the route to human pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Ke Shui & Chenwei Wang & Xuedi Zhang & Shanshan Ma & Qinyu Li & Wanshan Ning & Weizhi Zhang & Miaomiao Chen & Di Peng & Hui Hu & Zheng Fang & Anyuan Guo & Guanjun Gao & Mingliang Ye & Luoying Zhang & , 2023. "Small-sample learning reveals propionylation in determining global protein homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    8. M S Vijayabaskar & Debbie K Goode & Nadine Obier & Monika Lichtinger & Amber M L Emmett & Fatin N Zainul Abidin & Nisar Shar & Rebecca Hannah & Salam A Assi & Michael Lie-A-Ling & Berthold Gottgens & , 2019. "Identification of gene specific cis-regulatory elements during differentiation of mouse embryonic stem cells: An integrative approach using high-throughput datasets," PLOS Computational Biology, Public Library of Science, vol. 15(11), pages 1-29, November.
    9. Elizabeth D. Larson & Hideyuki Komori & Tyler J. Gibson & Cyrina M. Ostgaard & Danielle C. Hamm & Jack M. Schnell & Cheng-Yu Lee & Melissa M. Harrison, 2021. "Cell-type-specific chromatin occupancy by the pioneer factor Zelda drives key developmental transitions in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    10. Qiliang Ding & Matthew M. Edwards & Ning Wang & Xiang Zhu & Alexa N. Bracci & Michelle L. Hulke & Ya Hu & Yao Tong & Joyce Hsiao & Christine J. Charvet & Sulagna Ghosh & Robert E. Handsaker & Kevin Eg, 2021. "The genetic architecture of DNA replication timing in human pluripotent stem cells," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    11. Seth Teague & Gillian Primavera & Bohan Chen & Zong-Yuan Liu & LiAng Yao & Emily Freeburne & Hina Khan & Kyoung Jo & Craig Johnson & Idse Heemskerk, 2024. "Time-integrated BMP signaling determines fate in a stem cell model for early human development," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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