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Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor

Author

Listed:
  • Yoshimichi Murata

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences)

  • Hirohide Iwasaki

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    The Graduate University for Advanced Studies)

  • Mari Sasaki

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    The Graduate University for Advanced Studies)

  • Kazuo Inaba

    (University of Tsukuba)

  • Yasushi Okamura

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    The Graduate University for Advanced Studies
    National Institute of Advanced Industrial Science and Technology)

Abstract

Changes in membrane potential affect ion channels and transporters, which then alter intracellular chemical conditions. Other signalling pathways coupled to membrane potential have been suggested1,2,3 but their underlying mechanisms are unknown. Here we describe a novel protein from the ascidian Ciona intestinalis that has a transmembrane voltage-sensing domain homologous to the S1–S4 segments of voltage-gated channels and a cytoplasmic domain similar to phosphatase and tensin homologue. This protein, named C. intestinalis voltage-sensor-containing phosphatase (Ci-VSP), displays channel-like ‘gating’ currents and directly translates changes in membrane potential into the turnover of phosphoinositides. The activity of the phosphoinositide phosphatase in Ci-VSP is tuned within a physiological range of membrane potential. Immunocytochemical studies show that Ci-VSP is expressed in Ciona sperm tail membranes, indicating a possible role in sperm function or morphology. Our data demonstrate that voltage sensing can function beyond channel proteins and thus more ubiquitously than previously realized.

Suggested Citation

  • Yoshimichi Murata & Hirohide Iwasaki & Mari Sasaki & Kazuo Inaba & Yasushi Okamura, 2005. "Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor," Nature, Nature, vol. 435(7046), pages 1239-1243, June.
    • Handle: RePEc:nat:nature:v:435:y:2005:i:7046:d:10.1038_nature03650
    DOI: 10.1038/nature03650
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    Cited by:

    1. Chang Zhao & Parker D. Webster & Alexis Angeli & Francesco Tombola, 2023. "Mechanically-primed voltage-gated proton channels from angiosperm plants," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Spencer C. Guo & Rong Shen & Benoît Roux & Aaron R. Dinner, 2024. "Dynamics of activation in the voltage-sensing domain of Ciona intestinalis phosphatase Ci-VSP," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Yawei Yu & Lin Zhang & Baobin Li & Zhu Fu & Stephen G. Brohawn & Ehud Y. Isacoff, 2024. "Coupling sensor to enzyme in the voltage sensing phosphatase," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    4. Takafumi Kawai & Shin Morioka & Haruhiko Miyata & Rizki Tsari Andriani & Sharmin Akter & Gabriel Toma & Tatsuya Nakagawa & Yuki Oyama & Rie Iida-Norita & Junko Sasaki & Masahiko Watanabe & Kenji Sakim, 2024. "The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Woori Ko & Euna Lee & Jung-Eun Kim & Hyun-Ho Lim & Byung-Chang Suh, 2024. "The plasma membrane inner leaflet PI(4,5)P2 is essential for the activation of proton-activated chloride channels," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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