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A single-cell atlas of Drosophila trachea reveals glycosylation-mediated Notch signaling in cell fate specification

Author

Listed:
  • Yue Li

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Tianfeng Lu

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Pengzhen Dong

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Jian Chen

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Qiang Zhao

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Yuying Wang

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Tianheng Xiao

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Honggang Wu

    (Zhejiang University School of Medicine)

  • Quanyi Zhao

    (Stanford University)

  • Hai Huang

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

Abstract

The Drosophila tracheal system is a favorable model for investigating the program of tubular morphogenesis. This system is established in the embryo by post-mitotic cells, but also undergoes remodeling by adult stem cells. Here, we provide a comprehensive cell atlas of Drosophila trachea using the single-cell RNA-sequencing (scRNA-seq) technique. The atlas documents transcriptional profiles of tracheoblasts within the Drosophila airway, delineating 9 major subtypes. Further evidence gained from in silico as well as genetic investigations highlight a set of transcription factors characterized by their capacity to switch cell fate. Notably, the transcription factors Pebbled, Blistered, Knirps, Spalt and Cut are influenced by Notch signaling and determine tracheal cell identity. Moreover, Notch signaling orchestrates transcriptional activities essential for tracheoblast differentiation and responds to protein glycosylation that is induced by high sugar diet. Therefore, our study yields a single-cell transcriptomic atlas of tracheal development and regeneration, and suggests a glycosylation-responsive Notch signaling in cell fate determination.

Suggested Citation

  • Yue Li & Tianfeng Lu & Pengzhen Dong & Jian Chen & Qiang Zhao & Yuying Wang & Tianheng Xiao & Honggang Wu & Quanyi Zhao & Hai Huang, 2024. "A single-cell atlas of Drosophila trachea reveals glycosylation-mediated Notch signaling in cell fate specification," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46455-w
    DOI: 10.1038/s41467-024-46455-w
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    References listed on IDEAS

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    1. Craig A. Micchelli & Norbert Perrimon, 2006. "Evidence that stem cells reside in the adult Drosophila midgut epithelium," Nature, Nature, vol. 439(7075), pages 475-479, January.
    2. Katja Brückner & Lidia Perez & Henrik Clausen & Stephen Cohen, 2000. "Glycosyltransferase activity of Fringe modulates Notch–Delta interactions," Nature, Nature, vol. 406(6794), pages 411-415, July.
    3. Katja Brücker & Lidia Perez & Henrik Clausen & Stephen Cohen, 2000. "Erratum: Glycosyltransferase activity of Fringe modulates Notch–Delta interactions," Nature, Nature, vol. 407(6804), pages 654-654, October.
    4. 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.
    5. Yuta Sakaidani & Tomoko Nomura & Aiko Matsuura & Makiko Ito & Emiko Suzuki & Kosuke Murakami & Daita Nadano & Tsukasa Matsuda & Koichi Furukawa & Tetsuya Okajima, 2011. "O-Linked-N-acetylglucosamine on extracellular protein domains mediates epithelial cell–matrix interactions," Nature Communications, Nature, vol. 2(1), pages 1-9, September.
    6. Yue Li & Pengzhen Dong & Yang Yang & Tianyu Guo & Quanyi Zhao & Dan Miao & Huanle Li & Tianfeng Lu & Fanning Xia & Jialan Lyu & Jun Ma & Thomas B. Kornberg & Qiang Zhang & Hai Huang, 2022. "Metabolic control of progenitor cell propagation during Drosophila tracheal remodeling," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    7. Katja Rust & Lauren E. Byrnes & Kevin Shengyang Yu & Jason S. Park & Julie B. Sneddon & Aaron D. Tward & Todd G. Nystul, 2020. "A single-cell atlas and lineage analysis of the adult Drosophila ovary," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    8. 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.
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