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Subcellular second messenger networks drive distinct repellent-induced axon behaviors

Author

Listed:
  • Sarah Baudet

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Yvrick Zagar

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Fiona Roche

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Claudia Gomez-Bravo

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Sandrine Couvet

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Johann Bécret

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Morgane Belle

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Juliette Vougny

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Sinthuya Uthayasuthan

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

  • Oriol Ros

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision
    Universitat de Barcelona)

  • Xavier Nicol

    (Sorbonne Université, INSERM, CNRS, Institut de la Vision)

Abstract

Second messengers, including cAMP, cGMP and Ca2+ are often placed in an integrating position to combine the extracellular cues that orient growing axons in the developing brain. This view suggests that axon repellents share the same set of cellular messenger signals and that axon attractants evoke opposite cAMP, cGMP and Ca2+ changes. Investigating the confinement of these second messengers in cellular nanodomains, we instead demonstrate that two repellent cues, ephrin-A5 and Slit1, induce spatially segregated signals. These guidance molecules activate subcellular-specific second messenger crosstalk, each signaling network controlling distinct axonal morphology changes in vitro and pathfinding decisions in vivo.

Suggested Citation

  • Sarah Baudet & Yvrick Zagar & Fiona Roche & Claudia Gomez-Bravo & Sandrine Couvet & Johann Bécret & Morgane Belle & Juliette Vougny & Sinthuya Uthayasuthan & Oriol Ros & Xavier Nicol, 2023. "Subcellular second messenger networks drive distinct repellent-induced axon behaviors," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39516-z
    DOI: 10.1038/s41467-023-39516-z
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    References listed on IDEAS

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    1. Makoto Nishiyama & Akemi Hoshino & Lily Tsai & John R. Henley & Yoshio Goshima & Marc Tessier-Lavigne & Mu-ming Poo & Kyonsoo Hong, 2003. "Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning," Nature, Nature, vol. 423(6943), pages 990-995, June.
    2. Hariharan Subramanian & Alexander Froese & Peter Jönsson & Hannes Schmidt & Julia Gorelik & Viacheslav O. Nikolaev, 2018. "Distinct submembrane localisation compartmentalises cardiac NPR1 and NPR2 signalling to cGMP," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    3. Kyonsoo Hong & Makoto Nishiyama & John Henley & Marc Tessier-Lavigne & Mu-ming Poo, 2000. "Calcium signalling in the guidance of nerve growth by netrin-1," Nature, Nature, vol. 403(6765), pages 93-98, January.
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    5. Oleg Dyachok & Yegor Isakov & Jenny Sågetorp & Anders Tengholm, 2006. "Oscillations of cyclic AMP in hormone-stimulated insulin-secreting β-cells," Nature, Nature, vol. 439(7074), pages 349-352, January.
    6. Shiqiang Gao & Jatin Nagpal & Martin W. Schneider & Vera Kozjak-Pavlovic & Georg Nagel & Alexander Gottschalk, 2015. "Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp," Nature Communications, Nature, vol. 6(1), pages 1-12, November.
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    Cited by:

    1. Melody Atkins & Maud Wurmser & Michèle Darmon & Fiona Roche & Xavier Nicol & Christine Métin, 2023. "CXCL12 targets the primary cilium cAMP/cGMP ratio to regulate cell polarity during migration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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    1. Melody Atkins & Maud Wurmser & Michèle Darmon & Fiona Roche & Xavier Nicol & Christine Métin, 2023. "CXCL12 targets the primary cilium cAMP/cGMP ratio to regulate cell polarity during migration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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