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

Kawai, Takafumi; Morioka, Shin; Miyata, Haruhiko; Andriani, Rizki Tsari; Akter, Sharmin; Toma, Gabriel; Nakagawa, Tatsuya; Oyama, Yuki; Iida-Norita, Rie; Sasaki, Junko; Watanabe, Masahiko; Sakimura, Kenji; Ikawa, Masahito; Sasaki, Takehiko; Okamura, Yasushi

doi:https://doi.org/10.1038/s41467-024-51755-2

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

Kawai, Takafumi; Morioka, Shin; Miyata, Haruhiko et al.

Nature Communications, 2024, 15, 7289

Number of Access:1,415（2025-07-18 09:57 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/98256

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Title	The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase
Creator	NRID 1000070614915 1000070614915 researchmap permalink t_kawa t_kawa Scopus Author ID 55465095900 55465095900 CreatorName Kawai, Takafumi
	NRID 1000000973364 1000000973364 CreatorName Morioka, Shin
	NRID 1000050604732 1000050604732 ORCID 0000-0003-4758-5803 0000-0003-4758-5803 researchmap permalink hmiyata hmiyata Scopus Author ID 37161837000 37161837000 CreatorName Miyata, Haruhiko
	NRID 1000060935667 1000060935667 CreatorName Andriani, Rizki Tsari
	CreatorName Akter, Sharmin
	CreatorName Toma, Gabriel
	CreatorName Nakagawa, Tatsuya
	ORCID 0000-0003-4579-5487 0000-0003-4579-5487 CreatorName Oyama, Yuki
	NRID 1000010816771 1000010816771 ORCID 0000-0003-0104-1974 0000-0003-0104-1974 researchmap permalink 7000029591 7000029591 CreatorName Iida-Norita, Rie
	NRID 1000030333371 1000030333371 CreatorName Sasaki, Junko
	NRID 1000070210945 1000070210945 CreatorName Watanabe, Masahiko
	NRID 1000040162325 1000040162325 CreatorName Sakimura, Kenji
	NRID 1000020304066 1000020304066 ORCID 0000-0001-9859-6217 0000-0001-9859-6217 researchmap permalink read0054910 read0054910 Scopus Author ID 16689054500 16689054500 CreatorName Ikawa, Masahito
	NRID 1000050333365 1000050333365 CreatorName Sasaki, Takehiko
	NRID 1000080201987 1000080201987 researchmap permalink yasushiokamura yasushiokamura Scopus Author ID 55322083200 55322083200 ORCID 0000-0001-5386-7968 0000-0001-5386-7968 CreatorName Okamura, Yasushi
Description	Kawai T., Morioka S., Miyata H., et al. The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase. Nature Communications 15, 7289 (2024); https://doi.org/10.1038/s41467-024-51755-2.
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.
Publisher	Nature Research
Source Title	Nature Communications
Volume (Issue)	15
Page	7289
Date of Issued	2024-08-24
Language	English
Handle URL	https://hdl.handle.net/11094/98256
eISSN	20411723
Relation.isIdenticalTo	DOI (Publisher Version) https://doi.org/10.1038/s41467-024-51755-2
Access Rights	open access
CopyRight	This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
oaire:version	Version of Record
Category	学術雑誌論文 Journal Article

Resource Type	journal article
Local Type	Journal Article
DCTERMS.bibliographicCitation	Nature Communications. 2024, 15, p. 7289
DC.title	The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase
DC.creator	Kawai, Takafumi
	Morioka, Shin
	Miyata, Haruhiko
	Andriani, Rizki Tsari
	Akter, Sharmin
	Toma, Gabriel
	Nakagawa, Tatsuya
	Oyama, Yuki
	Iida-Norita, Rie
	Sasaki, Junko
	Watanabe, Masahiko
	Sakimura, Kenji
	Ikawa, Masahito
	Sasaki, Takehiko
	Okamura, Yasushi
DC.publisher	Nature Research
DC.language' scheme='DCTERMS.RFC1766	English
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2024-08-24
DC.identifier	https://doi.org/10.1038/s41467-024-51755-2
DC.description	Kawai T., Morioka S., Miyata H., et al. The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase. Nature Communications 15, 7289 (2024); https://doi.org/10.1038/s41467-024-51755-2.
DCTERMS.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.
DC.rights	This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
DC.format	98256
citation_title	The significance of electrical signals in maturing spermatozoa for phosphoinositide regulation through voltage-sensing phosphatase
citation_author	Kawai, Takafumi
	Morioka, Shin
	Miyata, Haruhiko
	Andriani, Rizki Tsari
	Akter, Sharmin
	Toma, Gabriel
	Nakagawa, Tatsuya
	Oyama, Yuki
	Iida-Norita, Rie
	Sasaki, Junko
	Watanabe, Masahiko
	Sakimura, Kenji
	Ikawa, Masahito
	Sasaki, Takehiko
	Okamura, Yasushi
citation_publisher	Nature Research
citation_language	English
citation_date	2024-08-24
citation_journal_title	Nature Communications
citation_volume	15
citation_firstpage	7289
citation_doi	https://doi.org/10.1038/s41467-024-51755-2
citation_public_url	https://hdl.handle.net/11094/98256

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

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