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Diffusible fraction of niche BMP ligand safeguards stem-cell differentiation

Author

Listed:
  • Sharif M. Ridwan

    (University of Connecticut Health Center)

  • Autumn Twillie

    (University of Connecticut Health Center)

  • Samaneh Poursaeid

    (University of Connecticut Health Center)

  • Emma Kristine Beard

    (University of Connecticut Health Center)

  • Muhammed Burak Bener

    (University of Connecticut Health Center)

  • Matthew Antel

    (University of Connecticut Health Center)

  • Ann E. Cowan

    (University of Connecticut Health Center
    University of Connecticut Health Center)

  • Shinya Matsuda

    (Biozentrum, University of Basel
    Department of Biological Sciences, Graduate School of Science, The University of Tokyo)

  • Mayu Inaba

    (University of Connecticut Health Center)

Abstract

Drosophila male germline stem cells (GSCs) reside at the tip of the testis and surround a cluster of niche cells. Decapentaplegic (Dpp) is one of the well-established ligands and has a major role in maintaining stem cells located in close proximity. However, the existence and the role of the diffusible fraction of Dpp outside of the niche have been unclear. Here, using genetically-encoded nanobodies called Morphotraps, we physically block Dpp diffusion without interfering with niche-stem cell signaling and find that a diffusible fraction of Dpp is required to ensure differentiation of GSC daughter cells, opposite of its role in maintenance of GSC in the niche. Our work provides an example in which a soluble niche ligand induces opposed cellular responses in stem cells versus in differentiating descendants to ensure spatial control of the niche. This may be a common mechanism to regulate tissue homeostasis.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45408-7
    DOI: 10.1038/s41467-024-45408-7
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    References listed on IDEAS

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    1. Stefan Harmansa & Fisun Hamaratoglu & Markus Affolter & Emmanuel Caussinus, 2015. "Dpp spreading is required for medial but not for lateral wing disc growth," Nature, Nature, vol. 527(7578), pages 317-322, November.
    2. Thomas A. Rando, 2006. "Stem cells, ageing and the quest for immortality," Nature, Nature, vol. 441(7097), pages 1080-1086, June.
    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. Jun Cheng & Nezaket Türkel & Nahid Hemati & Margaret T. Fuller & Alan J. Hunt & Yukiko M. Yamashita, 2008. "Centrosome misorientation reduces stem cell division during ageing," Nature, Nature, vol. 456(7222), pages 599-604, December.
    5. Shinya Matsuda & Jonas V. Schaefer & Yusuke Mii & Yutaro Hori & Dimitri Bieli & Masanori Taira & Andreas Plückthun & Markus Affolter, 2021. "Asymmetric requirement of Dpp/BMP morphogen dispersal in the Drosophila wing disc," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    6. Xiaomeng Wang & Robin E. Harris & Laura J. Bayston & Hilary L. Ashe, 2008. "Type IV collagens regulate BMP signalling in Drosophila," Nature, Nature, vol. 455(7209), pages 72-77, September.
    7. Sean J. Morrison & Judith Kimble, 2006. "Asymmetric and symmetric stem-cell divisions in development and cancer," Nature, Nature, vol. 441(7097), pages 1068-1074, June.
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