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Deciphering early human pancreas development at the single-cell level

Author

Listed:
  • Zhuo Ma

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Xiaofei Zhang

    (Chinese Academy of Sciences
    Huazhong University of Science and Technology
    The First Affiliated Hospital of Hainan Medical University, Hainan Medical University)

  • Wen Zhong

    (Linköping University
    Karolinska Institutet)

  • Hongyan Yi

    (The First Affiliated Hospital of Hainan Medical University, Hainan Medical University)

  • Xiaowei Chen

    (Chinese Academy of Sciences)

  • Yinsuo Zhao

    (Chinese Academy of Sciences)

  • Yanlin Ma

    (The First Affiliated Hospital of Hainan Medical University, Hainan Medical University)

  • Eli Song

    (Chinese Academy of Sciences)

  • Tao Xu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Guangzhou Laboratory
    Central Hospital Affiliated to Shandong First Medical University)

Abstract

Understanding pancreas development can provide clues for better treatments of pancreatic diseases. However, the molecular heterogeneity and developmental trajectory of the early human pancreas are poorly explored. Here, we performed large-scale single-cell RNA sequencing and single-cell assay for transposase accessible chromatin sequencing of human embryonic pancreas tissue obtained from first-trimester embryos. We unraveled the molecular heterogeneity, developmental trajectories and regulatory networks of the major cell types. The results reveal that dorsal pancreatic multipotent cells in humans exhibit different gene expression patterns than ventral multipotent cells. Pancreato-biliary progenitors that generate ventral multipotent cells in humans were identified. Notch and MAPK signals from mesenchymal cells regulate the differentiation of multipotent cells into trunk and duct cells. Notably, we identified endocrine progenitor subclusters with different differentiation potentials. Although the developmental trajectories are largely conserved between humans and mice, some distinct gene expression patterns have also been identified. Overall, we provide a comprehensive landscape of early human pancreas development to understand its lineage transitions and molecular complexity.

Suggested Citation

  • Zhuo Ma & Xiaofei Zhang & Wen Zhong & Hongyan Yi & Xiaowei Chen & Yinsuo Zhao & Yanlin Ma & Eli Song & Tao Xu, 2023. "Deciphering early human pancreas development at the single-cell level," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40893-8
    DOI: 10.1038/s41467-023-40893-8
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    References listed on IDEAS

    as
    1. Qiao Zhou & Douglas A. Melton, 2018. "Author Correction: Pancreas regeneration," Nature, Nature, vol. 560(7720), pages 34-34, August.
    2. Qiao Zhou & Douglas A. Melton, 2018. "Pancreas regeneration," Nature, Nature, vol. 557(7705), pages 351-358, May.
    3. Gioele La Manno & Ruslan Soldatov & Amit Zeisel & Emelie Braun & Hannah Hochgerner & Viktor Petukhov & Katja Lidschreiber & Maria E. Kastriti & Peter Lönnerberg & Alessandro Furlan & Jean Fan & Lars E, 2018. "RNA velocity of single cells," Nature, Nature, vol. 560(7719), pages 494-498, August.
    4. Lauren E. Byrnes & Daniel M. Wong & Meena Subramaniam & Nathaniel P. Meyer & Caroline L. Gilchrist & Sarah M. Knox & Aaron D. Tward & Chun J. Ye & Julie B. Sneddon, 2018. "Lineage dynamics of murine pancreatic development at single-cell resolution," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    5. Åsa Apelqvist & Hao Li & Lukas Sommer & Paul Beatus & David J. Anderson & Tasuku Honjo & Martin Hrabě de Angelis & Urban Lendahl & Helena Edlund, 1999. "Notch signalling controls pancreatic cell differentiation," Nature, Nature, vol. 400(6747), pages 877-881, August.
    6. Mette Bentsen & Philipp Goymann & Hendrik Schultheis & Kathrin Klee & Anastasiia Petrova & René Wiegandt & Annika Fust & Jens Preussner & Carsten Kuenne & Thomas Braun & Johnny Kim & Mario Looso, 2020. "ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    7. Marissa A. Scavuzzo & Matthew C. Hill & Jolanta Chmielowiec & Diane Yang & Jessica Teaw & Kuanwei Sheng & Yuelin Kong & Maria Bettini & Chenghang Zong & James F. Martin & Malgorzata Borowiak, 2018. "Endocrine lineage biases arise in temporally distinct endocrine progenitors during pancreatic morphogenesis," Nature Communications, Nature, vol. 9(1), pages 1-21, December.
    8. David Willnow & Uwe Benary & Anca Margineanu & Maria Lillina Vignola & Fabian Konrath & Igor M. Pongrac & Zahra Karimaddini & Alessandra Vigilante & Jana Wolf & Francesca M. Spagnoli, 2021. "Quantitative lineage analysis identifies a hepato-pancreato-biliary progenitor niche," Nature, Nature, vol. 597(7874), pages 87-91, September.
    9. Junyue Cao & Malte Spielmann & Xiaojie Qiu & Xingfan Huang & Daniel M. Ibrahim & Andrew J. Hill & Fan Zhang & Stefan Mundlos & Lena Christiansen & Frank J. Steemers & Cole Trapnell & Jay Shendure, 2019. "The single-cell transcriptional landscape of mammalian organogenesis," Nature, Nature, vol. 566(7745), pages 496-502, February.
    10. Suoqin Jin & Christian F. Guerrero-Juarez & Lihua Zhang & Ivan Chang & Raul Ramos & Chen-Hsiang Kuan & Peggy Myung & Maksim V. Plikus & Qing Nie, 2021. "Inference and analysis of cell-cell communication using CellChat," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    11. Eiji Yoshihara & Carolyn O’Connor & Emanuel Gasser & Zong Wei & Tae Gyu Oh & Tiffany W. Tseng & Dan Wang & Fritz Cayabyab & Yang Dai & Ruth T. Yu & Christopher Liddle & Annette R. Atkins & Michael Dow, 2020. "Immune-evasive human islet-like organoids ameliorate diabetes," Nature, Nature, vol. 586(7830), pages 606-611, October.
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    1. Lihua Chen & Nannan Wang & Tongran Zhang & Feng Zhang & Wei Zhang & Hao Meng & Jingyi Chen & Zhiying Liao & Xiaopeng Xu & Zhuo Ma & Tao Xu & Huisheng Liu, 2024. "Directed differentiation of pancreatic δ cells from human pluripotent stem cells," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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