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CXCL12 targets the primary cilium cAMP/cGMP ratio to regulate cell polarity during migration

Author

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  • Melody Atkins

    (Sorbonne Université)

  • Maud Wurmser

    (Sorbonne Université, INSERM CNRS)

  • Michèle Darmon

    (Sorbonne Université)

  • Fiona Roche

    (Sorbonne Université, INSERM CNRS)

  • Xavier Nicol

    (Sorbonne Université, INSERM CNRS)

  • Christine Métin

    (Sorbonne Université)

Abstract

Directed cell migration requires sustained cell polarisation. In migrating cortical interneurons, nuclear movements are directed towards the centrosome that organises the primary cilium signalling hub. Primary cilium-elicited signalling, and how it affects migration, remain however ill characterised. Here, we show that altering cAMP/cGMP levels in the primary cilium by buffering cAMP, cGMP or by locally increasing cAMP, influences the polarity and directionality of migrating interneurons, whereas buffering cAMP or cGMP in the apposed centrosome compartment alters their motility. Remarkably, we identify CXCL12 as a trigger that targets the ciliary cAMP/cGMP ratio to promote sustained polarity and directed migration. We thereby uncover cAMP/cGMP levels in the primary cilium as a major target of extrinsic cues and as the steering wheel of neuronal migration.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43645-w
    DOI: 10.1038/s41467-023-43645-w
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    References listed on IDEAS

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    1. Franck Polleux & Theresa Morrow & Anirvan Ghosh, 2000. "Semaphorin 3A is a chemoattractant for cortical apical dendrites," Nature, Nature, vol. 404(6778), pages 567-573, April.
    2. 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.
    3. Stefania Averaimo & Ahlem Assali & Oriol Ros & Sandrine Couvet & Yvrick Zagar & Ioana Genescu & Alexandra Rebsam & Xavier Nicol, 2016. "A plasma membrane microdomain compartmentalizes ephrin-generated cAMP signals to prune developing retinal axon arbors," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    4. 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.
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