The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase

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 Sakimura, Masahito Ikawa, Takehiko Sasaki and Yasushi Okamura
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Takafumi Kawai: Osaka University
Shin Morioka: Tokyo Medical and Dental University
Haruhiko Miyata: Osaka University
Rizki Tsari Andriani: Osaka University
Sharmin Akter: Osaka University
Gabriel Toma: Osaka University
Tatsuya Nakagawa: Osaka University
Yuki Oyama: Osaka University
Rie Iida-Norita: Osaka University
Junko Sasaki: Tokyo Medical and Dental University
Masahiko Watanabe: Hokkaido University
Kenji Sakimura: Niigata University
Masahito Ikawa: Osaka University
Takehiko Sasaki: Tokyo Medical and Dental University
Yasushi Okamura: Osaka University

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract Voltage-sensing phosphatase (VSP) exhibits voltage-dependent phosphatase activity toward phosphoinositides. VSP generates a specialized phosphoinositide environment in mammalian sperm flagellum. However, the voltage-sensing mechanism of VSP in spermatozoa is not yet characterized. Here, we found that VSP is activated during sperm maturation, indicating that electric signals in immature spermatozoa are essential. Using a heterologous expression system, we show the voltage-sensing property of mouse VSP (mVSP). The voltage-sensing threshold of mVSP is approximately −30 mV, which is sensitive enough to activate mVSP in immature spermatozoa. We also report several knock-in mice in which we manipulate the voltage-sensitivity or electrochemical coupling of mVSP. Notably, the V312R mutant, with a minor voltage-sensitivity change, exhibits abnormal sperm motility after, but not before, capacitation. Additionally, the V312R mutant shows a significant change in the acyl-chain profile of phosphoinositide. Our findings suggest that electrical signals during sperm maturation are crucial for establishing the optimal phosphoinositide environment in spermatozoa.

Date: 2024
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DOI: 10.1038/s41467-024-51755-2

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