IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30624-w.html
   My bibliography  Save this article

Single-cell chromatin profiling of the primitive gut tube reveals regulatory dynamics underlying lineage fate decisions

Author

Listed:
  • Ryan J. Smith

    (The Hospital for Sick Children
    University of Toronto)

  • Hongpan Zhang

    (University of Virginia School of Medicine
    University of Virginia)

  • Shengen Shawn Hu

    (University of Virginia School of Medicine)

  • Theodora Yung

    (The Hospital for Sick Children
    University of Toronto)

  • Roshane Francis

    (The Hospital for Sick Children
    University of Toronto)

  • Lilian Lee

    (The Hospital for Sick Children)

  • Mark W. Onaitis

    (University of California San Diego Medical Center)

  • Peter B. Dirks

    (The Hospital for Sick Children
    University of Toronto)

  • Chongzhi Zang

    (University of Virginia School of Medicine
    University of Virginia
    University of Virginia)

  • Tae-Hee Kim

    (The Hospital for Sick Children
    University of Toronto)

Abstract

Development of the gastrointestinal system occurs after gut tube closure, guided by spatial and temporal control of gene expression. However, it remains unclear what forces regulate these spatiotemporal gene expression patterns. Here we perform single-cell chromatin profiling of the primitive gut tube to reveal organ-specific chromatin patterns that reflect the anatomical patterns of distinct organs. We generate a comprehensive map of epigenomic changes throughout gut development, demonstrating that dynamic chromatin accessibility patterns associate with lineage-specific transcription factor binding events to regulate organ-specific gene expression. Additionally, we show that loss of Sox2 and Cdx2, foregut and hindgut lineage-specific transcription factors, respectively, leads to fate shifts in epigenomic patterns, linking transcription factor binding, chromatin accessibility, and lineage fate decisions in gut development. Notably, abnormal expression of Sox2 in the pancreas and intestine impairs lineage fate decisions in both development and adult homeostasis. Together, our findings define the chromatin and transcriptional mechanisms of organ identity and lineage plasticity in development and adult homeostasis.

Suggested Citation

  • Ryan J. Smith & Hongpan Zhang & Shengen Shawn Hu & Theodora Yung & Roshane Francis & Lilian Lee & Mark W. Onaitis & Peter B. Dirks & Chongzhi Zang & Tae-Hee Kim, 2022. "Single-cell chromatin profiling of the primitive gut tube reveals regulatory dynamics underlying lineage fate decisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30624-w
    DOI: 10.1038/s41467-022-30624-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30624-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-30624-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Lu Han & Praneet Chaturvedi & Keishi Kishimoto & Hiroyuki Koike & Talia Nasr & Kentaro Iwasawa & Kirsten Giesbrecht & Phillip C. Witcher & Alexandra Eicher & Lauren Haines & Yarim Lee & John M. Shanno, 2020. "Single cell transcriptomics identifies a signaling network coordinating endoderm and mesoderm diversification during foregut organogenesis," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Jean-Leon Chong & Pamela L. Wenzel & M. Teresa Sáenz-Robles & Vivek Nair & Antoney Ferrey & John P. Hagan & Yorman M. Gomez & Nidhi Sharma & Hui-Zi Chen & Madhu Ouseph & Shu-Huei Wang & Prashant Trikh, 2009. "E2f1–3 switch from activators in progenitor cells to repressors in differentiating cells," Nature, Nature, vol. 462(7275), pages 930-934, December.
    3. Sonja Nowotschin & Manu Setty & Ying-Yi Kuo & Vincent Liu & Vidur Garg & Roshan Sharma & Claire S. Simon & Nestor Saiz & Rui Gardner & Stéphane C. Boutet & Deanna M. Church & Pamela A. Hoodless & Anna, 2019. "The emergent landscape of the mouse gut endoderm at single-cell resolution," Nature, Nature, vol. 569(7756), pages 361-367, May.
    4. Ronan Russell & Phichitpol P. Carnese & Thomas G. Hennings & Emily M. Walker & Holger A. Russ & Jennifer S. Liu & Simone Giacometti & Roland Stein & Matthias Hebrok, 2020. "Loss of the transcription factor MAFB limits β-cell derivation from human PSCs," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Shengen Shawn Hu & Lin Liu & Qi Li & Wenjing Ma & Michael J. Guertin & Clifford A. Meyer & Ke Deng & Tingting Zhang & Chongzhi Zang, 2022. "Intrinsic bias estimation for improved analysis of bulk and single-cell chromatin accessibility profiles using SELMA," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Sina Schumacher & Max Fernkorn & Michelle Marten & Rui Chen & Yung Su Kim & Ivan Bedzhov & Christian Schröter, 2024. "Tissue-intrinsic beta-catenin signals antagonize Nodal-driven anterior visceral endoderm differentiation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Luke Simpson & Andrew Strange & Doris Klisch & Sophie Kraunsoe & Takuya Azami & Daniel Goszczynski & Triet Minh & Benjamin Planells & Nadine Holmes & Fei Sang & Sonal Henson & Matthew Loose & Jennifer, 2024. "A single-cell atlas of pig gastrulation as a resource for comparative embryology," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Karin D. Prummel & Helena L. Crowell & Susan Nieuwenhuize & Eline C. Brombacher & Stephan Daetwyler & Charlotte Soneson & Jelena Kresoja-Rakic & Agnese Kocere & Manuel Ronner & Alexander Ernst & Zahra, 2022. "Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    4. Joyce J. Thompson & Daniel J. Lee & Apratim Mitra & Sarah Frail & Ryan K. Dale & Pedro P. Rocha, 2022. "Extensive co-binding and rapid redistribution of NANOG and GATA6 during emergence of divergent lineages," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Lu Han & Yongxia Wu & Kun Fang & Sean Sweeney & Ulyss K. Roesner & Melodie Parrish & Khushbu Patel & Tom Walter & Julia Piermattei & Anthony Trimboli & Julia Lefler & Cynthia D. Timmers & Xue-Zhong Yu, 2023. "The splanchnic mesenchyme is the tissue of origin for pancreatic fibroblasts during homeostasis and tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Simon Andrews & Christel Krueger & Maravillas Mellado-Lopez & Myriam Hemberger & Wendy Dean & Vicente Perez-Garcia & Courtney W. Hanna, 2023. "Mechanisms and function of de novo DNA methylation in placental development reveals an essential role for DNMT3B," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Nimrod Rappoport & Elad Chomsky & Takashi Nagano & Charlie Seibert & Yaniv Lubling & Yael Baran & Aviezer Lifshitz & Wing Leung & Zohar Mukamel & Ron Shamir & Peter Fraser & Amos Tanay, 2023. "Single cell Hi-C identifies plastic chromosome conformations underlying the gastrulation enhancer landscape," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Jong Geol Lee & Jung-Min Yon & Globinna Kim & Seul-Gi Lee & C-Yoon Kim & Seung-A Cheong & Hyun-Yi Kim & Jiyoung Yu & Kyunggon Kim & Young Hoon Sung & Hyun Ju Yoo & Dong-Cheol Woo & Jin Kyung Rho & Cha, 2024. "PIBF1 regulates trophoblast syncytialization and promotes cardiovascular development," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. Shengyong Yu & Chunhua Zhou & Jiangping He & Zhaokai Yao & Xingnan Huang & Bowen Rong & Hong Zhu & Shijie Wang & Shuyan Chen & Xialian Wang & Baomei Cai & Guoqing Zhao & Yuhan Chen & Lizhan Xiao & He , 2022. "BMP4 drives primed to naïve transition through PGC-like state," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Andrea B. Alber & Hector A. Marquez & Liang Ma & George Kwong & Bibek R. Thapa & Carlos Villacorta-Martin & Jonathan Lindstrom-Vautrin & Pushpinder Bawa & Feiya Wang & Yongfeng Luo & Laertis Ikonomou , 2023. "Directed differentiation of mouse pluripotent stem cells into functional lung-specific mesenchyme," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Jeremy Lotto & Rebecca Cullum & Sibyl Drissler & Martin Arostegui & Victoria C. Garside & Bettina M. Fuglerud & Makenna Clement-Ranney & Avinash Thakur & T. Michael Underhill & Pamela A. Hoodless, 2023. "Cell diversity and plasticity during atrioventricular heart valve EMTs," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. Ran Wang & Xianfa Yang & Jiehui Chen & Lin Zhang & Jonathan A. Griffiths & Guizhong Cui & Yingying Chen & Yun Qian & Guangdun Peng & Jinsong Li & Liantang Wang & John C. Marioni & Patrick P. L. Tam & , 2023. "Time space and single-cell resolved tissue lineage trajectories and laterality of body plan at gastrulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Charles Petitpré & Louis Faure & Phoebe Uhl & Paula Fontanet & Iva Filova & Gabriela Pavlinkova & Igor Adameyko & Saida Hadjab & Francois Lallemend, 2022. "Single-cell RNA-sequencing analysis of the developing mouse inner ear identifies molecular logic of auditory neuron diversification," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Andrea Toth & Paranthaman Kannan & John Snowball & Matthew Kofron & Joseph A. Wayman & James P. Bridges & Emily R. Miraldi & Daniel Swarr & William J. Zacharias, 2023. "Alveolar epithelial progenitor cells require Nkx2-1 to maintain progenitor-specific epigenomic state during lung homeostasis and regeneration," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    15. Zeyang Wang & Rui Fan & Angela Russo & Filippo M. Cernilogar & Alexander Nuber & Silvia Schirge & Irina Shcherbakova & Iva Dzhilyanova & Enes Ugur & Tobias Anton & Lisa Richter & Heinrich Leonhardt & , 2022. "Dominant role of DNA methylation over H3K9me3 for IAP silencing in endoderm," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. William R. Reay & Dylan J. Kiltschewskij & Maria A. Biase & Zachary F. Gerring & Kousik Kundu & Praveen Surendran & Laura A. Greco & Erin D. Clarke & Clare E. Collins & Alison M. Mondul & Demetrius Al, 2024. "Genetic influences on circulating retinol and its relationship to human health," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    17. Nicolas Allègre & Sabine Chauveau & Cynthia Dennis & Yoan Renaud & Dimitri Meistermann & Lorena Valverde Estrella & Pierre Pouchin & Michel Cohen-Tannoudji & Laurent David & Claire Chazaud, 2022. "NANOG initiates epiblast fate through the coordination of pluripotency genes expression," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    18. Shunsuke Tanigawa & Etsuko Tanaka & Koichiro Miike & Tomoko Ohmori & Daisuke Inoue & Chen-Leng Cai & Atsuhiro Taguchi & Akio Kobayashi & Ryuichi Nishinakamura, 2022. "Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. Mariana A. Branco & Tiago P. Dias & Joaquim M. S. Cabral & Perpetua Pinto-do-Ó & Maria Margarida Diogo, 2022. "Human multilineage pro-epicardium/foregut organoids support the development of an epicardium/myocardium organoid," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    20. Paraskevi Athanasouli & Martina Balli & Anchel Jaime-Soguero & Annekatrien Boel & Sofia Papanikolaou & Bernard K. Veer & Adrian Janiszewski & Tijs Vanhessche & Annick Francis & Youssef El Laithy & Ant, 2023. "The Wnt/TCF7L1 transcriptional repressor axis drives primitive endoderm formation by antagonizing naive and formative pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30624-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.