A K+-selective CNG channel orchestrates Ca2+ signalling in zebrafish sperm

  1. Sylvia Fechner
  2. Luis Alvarez
  3. Wolfgang Bönigk
  4. Astrid Müller
  5. Thomas Berger
  6. Rene Pascal
  7. Christian Trötschel
  8. Ansgar Poetsch
  9. Gabriel Stölting
  10. Kellee R Siegfried
  11. Elisabeth Kremmer
  12. Reinhard Seifert
  13. U Benjamin Kaupp  Is a corresponding author
  1. Center of Advanced European Studies and Research, United States
  2. Center of Advanced European Studies and Research, Germany
  3. Ruhr-Universität Bochum, Germany
  4. Forschungszentrum Jülich, Germany
  5. University of Massachusetts Boston, United States
  6. Helmholtz-Zentrum München, Germany

Abstract

Calcium in the flagellum controls sperm navigation. In sperm of marine invertebrates and mammals, Ca2+ signalling has been intensely studied, whereas for fish little is known. In sea urchin sperm, a cyclic nucleotide-gated K+ channel (CNGK) mediates a cGMP-induced hyperpolarization that evokes Ca2+ influx. Here, we identify in sperm of the freshwater fish Danio rerio a novel CNGK family member featuring non-canonical properties. It is located in the sperm head rather than the flagellum and is controlled by intracellular pH, but not cyclic nucleotides. Alkalization hyperpolarizes sperm and produces Ca2+ entry. Ca2+ induces spinning-like swimming, different from swimming of sperm from other species. The 'spinning' mode probably guides sperm into the micropyle, a narrow entrance on the surface of fish eggs. A picture is emerging of sperm channel orthologues that employ different activation mechanisms and serve different functions. The channel inventories probably reflect adaptations to species-specific challenges during fertilization.

Article and author information

Author details

  1. Sylvia Fechner

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Luis Alvarez

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Wolfgang Bönigk

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Astrid Müller

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Thomas Berger

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Rene Pascal

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Christian Trötschel

    Lehrstuhl Biochemie der Pflanzen, Ruhr-Universität Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Ansgar Poetsch

    Lehrstuhl Biochemie der Pflanzen, Ruhr-Universität Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Gabriel Stölting

    Institute of Complex Systems 4, Forschungszentrum Jülich, Jülich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Kellee R Siegfried

    Biology Department, University of Massachusetts Boston, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Elisabeth Kremmer

    Institut für Molekulare Immunologie, Helmholtz-Zentrum München, München, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Reinhard Seifert

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. U Benjamin Kaupp

    Abteilung Molekulare Neurosensorik, Center of Advanced European Studies and Research, Bonn, Germany
    For correspondence
    U.B.Kaupp@caesar.de
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Richard Aldrich, The University of Texas at Austin, United States

Version history

  1. Received: March 20, 2015
  2. Accepted: December 9, 2015
  3. Accepted Manuscript published: December 9, 2015 (version 1)
  4. Version of Record published: January 30, 2016 (version 2)

Copyright

© 2015, Fechner et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sylvia Fechner
  2. Luis Alvarez
  3. Wolfgang Bönigk
  4. Astrid Müller
  5. Thomas Berger
  6. Rene Pascal
  7. Christian Trötschel
  8. Ansgar Poetsch
  9. Gabriel Stölting
  10. Kellee R Siegfried
  11. Elisabeth Kremmer
  12. Reinhard Seifert
  13. U Benjamin Kaupp
(2015)
A K+-selective CNG channel orchestrates Ca2+ signalling in zebrafish sperm
eLife 4:e07624.
https://doi.org/10.7554/eLife.07624

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https://doi.org/10.7554/eLife.07624