IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28587-z.html
   My bibliography  Save this article

Cytonemes coordinate asymmetric signaling and organization in the Drosophila muscle progenitor niche

Author

Listed:
  • Akshay Patel

    (University of Maryland)

  • Yicong Wu

    (National Institutes of Health)

  • Xiaofei Han

    (National Institutes of Health)

  • Yijun Su

    (National Institutes of Health
    National Institutes of Health)

  • Tim Maugel

    (University of Maryland)

  • Hari Shroff

    (National Institutes of Health
    National Institutes of Health)

  • Sougata Roy

    (University of Maryland)

Abstract

Asymmetric signaling and organization in the stem-cell niche determine stem-cell fates. Here, we investigate the basis of asymmetric signaling and stem-cell organization using the Drosophila wing-disc that creates an adult muscle progenitor (AMP) niche. We show that AMPs extend polarized cytonemes to contact the disc epithelial junctions and adhere themselves to the disc/niche. Niche-adhering cytonemes localize FGF-receptor to selectively adhere to the FGF-producing disc and receive FGFs in a contact-dependent manner. Activation of FGF signaling in AMPs, in turn, reinforces disc-specific cytoneme polarity/adhesion, which maintains their disc-proximal positions. Loss of cytoneme-mediated adhesion promotes AMPs to lose niche occupancy and FGF signaling, occupy a disc-distal position, and acquire morphological hallmarks of differentiation. Niche-specific AMP organization and diversification patterns are determined by localized expression and presentation patterns of two different FGFs in the wing-disc and their polarized target-specific distribution through niche-adhering cytonemes. Thus, cytonemes are essential for asymmetric signaling and niche-specific AMP organization.

Suggested Citation

  • Akshay Patel & Yicong Wu & Xiaofei Han & Yijun Su & Tim Maugel & Hari Shroff & Sougata Roy, 2022. "Cytonemes coordinate asymmetric signaling and organization in the Drosophila muscle progenitor niche," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28587-z
    DOI: 10.1038/s41467-022-28587-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28587-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28587-z?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. Mayu Inaba & Michael Buszczak & Yukiko M. Yamashita, 2015. "Nanotubes mediate niche–stem-cell signalling in the Drosophila testis," Nature, Nature, vol. 523(7560), pages 329-332, July.
    2. Panteleimon Rompolas & Kailin R. Mesa & Valentina Greco, 2013. "Spatial organization within a niche as a determinant of stem-cell fate," Nature, Nature, vol. 502(7472), pages 513-518, October.
    3. Yicong Wu & Xiaofei Han & Yijun Su & Melissa Glidewell & Jonathan S. Daniels & Jiamin Liu & Titas Sengupta & Ivan Rey-Suarez & Robert Fischer & Akshay Patel & Christian Combs & Junhui Sun & Xufeng Wu , 2021. "Multiview confocal super-resolution microscopy," Nature, Nature, vol. 600(7888), pages 279-284, December.
    4. Lindsey J. Macpherson & Emanuela E. Zaharieva & Patrick J. Kearney & Michael H. Alpert & Tzu-Yang Lin & Zeynep Turan & Chi-Hon Lee & Marco Gallio, 2015. "Dynamic labelling of neural connections in multiple colours by trans-synaptic fluorescence complementation," Nature Communications, Nature, vol. 6(1), pages 1-9, 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. Adrián Aguirre-Tamaral & Manuel Cambón & David Poyato & Juan Soler & Isabel Guerrero, 2022. "Predictive model for cytoneme guidance in Hedgehog signaling based on Ihog- Glypicans interaction," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Lijuan Du & Alex Sohr & Yujia Li & Sougata Roy, 2022. "GPI-anchored FGF directs cytoneme-mediated bidirectional contacts to regulate its tissue-specific dispersion," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Timo Kuhn & Amit N. Landge & David Mörsdorf & Jonas Coßmann & Johanna Gerstenecker & Daniel Čapek & Patrick Müller & J. Christof M. Gebhardt, 2022. "Single-molecule tracking of Nodal and Lefty in live zebrafish embryos supports hindered diffusion model," Nature Communications, Nature, vol. 13(1), pages 1-15, 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. Lijuan Du & Alex Sohr & Yujia Li & Sougata Roy, 2022. "GPI-anchored FGF directs cytoneme-mediated bidirectional contacts to regulate its tissue-specific dispersion," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Mami Nakamizo-Dojo & Kenichi Ishii & Jiro Yoshino & Masato Tsuji & Kazuo Emoto, 2023. "Descending GABAergic pathway links brain sugar-sensing to peripheral nociceptive gating in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Ning Xu & Sarah E. Bohndiek & Zexing Li & Cilong Zhang & Qiaofeng Tan, 2024. "Mechanical-scan-free multicolor super-resolution imaging with diffractive spot array illumination," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Sharif M. Ridwan & Autumn Twillie & Samaneh Poursaeid & Emma Kristine Beard & Muhammed Burak Bener & Matthew Antel & Ann E. Cowan & Shinya Matsuda & Mayu Inaba, 2024. "Diffusible fraction of niche BMP ligand safeguards stem-cell differentiation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Md Tauhidul Islam & Zixia Zhou & Hongyi Ren & Masoud Badiei Khuzani & Daniel Kapp & James Zou & Lu Tian & Joseph C. Liao & Lei Xing, 2023. "Revealing hidden patterns in deep neural network feature space continuum via manifold learning," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Matthew Antel & Romir Raj & Madona Y. G. Masoud & Ziwei Pan & Sheng Li & Barbara G. Mellone & Mayu Inaba, 2022. "Interchromosomal interaction of homologous Stat92E alleles regulates transcriptional switch during stem-cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-16, 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_s41467-022-28587-z. 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.