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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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    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.
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    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.

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