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GPI-anchored FGF directs cytoneme-mediated bidirectional contacts to regulate its tissue-specific dispersion

Author

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  • Lijuan Du

    (University of Maryland)

  • Alex Sohr

    (University of Maryland
    Center for Biologics Evaluation and Research, Food and Drug Administration)

  • Yujia Li

    (University of Maryland)

  • Sougata Roy

    (University of Maryland)

Abstract

How signaling proteins generate a multitude of information to organize tissue patterns is critical to understanding morphogenesis. In Drosophila, FGF produced in wing-disc cells regulates the development of the disc-associated air-sac-primordium (ASP). Here, we show that FGF is Glycosylphosphatidylinositol-anchored to the producing cell surface and that this modification both inhibits free FGF secretion and promotes target-specific cytoneme contacts and contact-dependent FGF release. FGF-source and ASP cells extend cytonemes that present FGF and FGFR on their surfaces and reciprocally recognize each other over distance by contacting through cell-adhesion-molecule (CAM)-like FGF-FGFR binding. Contact-mediated FGF-FGFR interactions induce bidirectional responses in ASP and source cells that, in turn, polarize FGF-sending and FGF-receiving cytonemes toward each other to reinforce signaling contacts. Subsequent un-anchoring of FGFR-bound-FGF from the source membrane dissociates cytoneme contacts and delivers FGF target-specifically to ASP cytonemes for paracrine functions. Thus, GPI-anchored FGF organizes both source and recipient cells and self-regulates its cytoneme-mediated tissue-specific dispersion.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30417-1
    DOI: 10.1038/s41467-022-30417-1
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    References listed on IDEAS

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    1. Eliana Stanganello & Anja I. H. Hagemann & Benjamin Mattes & Claude Sinner & Dana Meyen & Sabrina Weber & Alexander Schug & Erez Raz & Steffen Scholpp, 2015. "Filopodia-based Wnt transport during vertebrate tissue patterning," Nature Communications, Nature, vol. 6(1), pages 1-14, May.
    2. 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.
    3. Cyrille Alexandre & Alberto Baena-Lopez & Jean-Paul Vincent, 2014. "Patterning and growth control by membrane-tethered Wingless," Nature, Nature, vol. 505(7482), pages 180-185, January.
    4. 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.
    5. Darren Gilmour & Martina Rembold & Maria Leptin, 2017. "From morphogen to morphogenesis and back," Nature, Nature, vol. 541(7637), pages 311-320, January.
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