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Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning

Author

Listed:
  • Makoto Nishiyama

    (New York University School of Medicine)

  • Akemi Hoshino

    (New York University School of Medicine)

  • Lily Tsai

    (New York University School of Medicine)

  • John R. Henley

    (University of California at Berkeley)

  • Yoshio Goshima

    (Yokohama City University School of Medicine)

  • Marc Tessier-Lavigne

    (Stanford University)

  • Mu-ming Poo

    (University of California at Berkeley)

  • Kyonsoo Hong

    (New York University School of Medicine)

Abstract

Signalling by intracellular second messengers such as cyclic nucleotides and Ca2+ is known to regulate attractive and repulsive guidance of axons by extracellular factors1,2. However, the mechanism of interaction among these second messengers in determining the polarity of the guidance response is largely unknown. Here, we report that the ratio of cyclic AMP to cyclic GMP activities sets the polarity of netrin-1-induced axon guidance: high ratios favour attraction, whereas low ratios favour repulsion. Whole-cell recordings of Ca2+ currents at Xenopus spinal neuron growth cones indicate that cyclic nucleotide signalling directly modulates the activity of L-type Ca2+ channels (LCCs) in axonal growth cones. Furthermore, cGMP signalling activated by an arachidonate 12-lipoxygenase metabolite3 suppresses LCC activity triggered by netrin-1, and is required for growth-cone repulsion mediated by the DCC–UNC5 receptor complex4. By linking cAMP and cGMP signalling and modulation of Ca2+ channel activity in growth cones, these findings delineate an early membrane-associated event responsible for signal transduction during bi-directional axon guidance.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:423:y:2003:i:6943:d:10.1038_nature01751
    DOI: 10.1038/nature01751
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    Cited by:

    1. 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.
    2. 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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