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A K+-selective cGMP-gated ion channel controls chemosensation of sperm

Nature Cell Biology volume 8, pages 1149–1154 (2006)Cite this article

Abstract

Eggs attract sperm by chemical factors, a process called chemotaxis. Sperm from marine invertebrates use cGMP signalling to transduce incident chemoattractants into changes in the Ca2+ concentration in the flagellum, which control the swimming behaviour during chemotaxis1,2,3. The signalling pathway downstream of the synthesis of cGMP by a guanylyl cyclase is ill-defined. In particular, the ion channels that are involved in Ca2+ influx and their mechanisms of gating are not known4. Using rapid voltage-sensitive dyes and kinetic techniques, we record the voltage response that is evoked by the chemoattractant in sperm from the sea urchin Arbacia punctulata. We show that the chemoattractant evokes a brief hyperpolarization followed by a sustained depolarization. The hyperpolarization is caused by the opening of K+-selective cyclic-nucleotide-gated (CNG) channels in the flagellum. Ca2+ influx commences at the onset of recovery from hyperpolarization. The voltage threshold of Ca2+ entry indicates the involvement of low-voltage-activated Cav channels. These results establish a model of chemosensory transduction in sperm whereby a cGMP-induced hyperpolarization opens Cav channels by a 'recovery-from-inactivation' mechanism and unveil an evolutionary kinship between transduction mechanisms in sperm and photoreceptors.

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Figure 1: Resact-induced changes in membrane voltage.
Figure 2: The K+ channel is directly gated by cyclic nucleotides.
Figure 3: Mechanism of Ca2+ entry.
Figure 4: Model of chemotactic signalling events in sperm.

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Acknowledgements

This work was supported by the Deutsche Forschungsgemeinschaft, KA 545/10-4 and the Fonds der Chemischen Industrie. We thank members of the Kaupp lab for critical reading of the manuscript, and A. Eckert and H.D. Grammig for preparing the manuscript and figures. We thank M. Gomez and E. Nasi for continous supply of material.

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  1. Abteilung Zelluläre Signalverarbeitung, Institut für Neurowissenschaft und Biophysik, INB-1, Forschungszentrum Jülich, Jülich, 52425, Germany

    Timo Strünker, Ingo Weyand, Wolfgang Bönigk, Qui Van, Astrid Loogen, Nachiket Kashikar & U.Benjamin Kaupp

  2. Marine Biological Laboratory, Woods Hole, 02543, MA, USA

    Timo Strünker, Ingo Weyand, Joel E. Brown & U.Benjamin Kaupp

  3. Forschungsinstitut für Molekulare Pharmakologie, Robert-Rössle-Str., Berlin, 13125, Germany

    Volker Hagen & Eberhard Krause

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Strünker, T., Weyand, I., Bönigk, W. et al. A K+-selective cGMP-gated ion channel controls chemosensation of sperm. Nat Cell Biol 8, 1149–1154 (2006). https://doi.org/10.1038/ncb1473

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