Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity

Matsuda, Makoto; Takeshita, Kohei; Kurokawa, Tatsuki; Sakata, Souhei; Suzuki, Mamoru; Yamashita, Eiki; Okamura, Yasushi; Nakagawa, Atushi

doi:https://doi.org/10.1074/jbc.M110.214361

Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity

Matsuda, Makoto; Takeshita, Kohei; Kurokawa, Tatsuki et al.

Journal of Biological Chemistry, 2011, 286(26), 23368-23377

Number of Access:1,182（2025-07-18 10:23 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/73659

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Title	Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity
Creator	NRID 1000000354811 1000000354811 CreatorName Matsuda, Makoto
	NRID 1000080346808 1000080346808 CreatorName Takeshita, Kohei
	NRID 1000040527701 1000040527701 CreatorName Kurokawa, Tatsuki
	NRID 1000040528006 1000040528006 CreatorName Sakata, Souhei
	NRID 1000040280507 1000040280507 ORCID 0000-0001-7071-5093 0000-0001-7071-5093 researchmap permalink MamoruSUZUKI MamoruSUZUKI Scopus Author ID 55709928600 55709928600 CreatorName Suzuki, Mamoru
	NRID 1000000294132 1000000294132 ORCID 0000-0002-4278-0039 0000-0002-4278-0039 researchmap permalink eiki-yama eiki-yama Scopus Author ID 7005437913 7005437913 CreatorName Yamashita, Eiki
	NRID 1000080201987 1000080201987 researchmap permalink yasushiokamura yasushiokamura Scopus Author ID 55322083200 55322083200 ORCID 0000-0001-5386-7968 0000-0001-5386-7968 CreatorName Okamura, Yasushi
	NRID 1000020188890 1000020188890 ORCID 0000-0002-1700-7861 0000-0002-1700-7861 researchmap permalink atsushi_nakagawa atsushi_nakagawa Scopus Author ID 7202934909 7202934909 CreatorName Nakagawa, Atushi
Description	This research was originally published in Journal of Biological Chemistry. Makoto Matsuda, Kohei Takeshita, Tatsuki Kurokawa, Souhei Sakata, Mamoru Suzuki, Eiki Yamashita, Yasushi Okamura, and Atsushi Nakagawa. Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity. Journal of Biological Chemistry. 2011; 286, 23368-23377. © the American Society for Biochemistry and Molecular Biology.
Abstract	Ciona intestinalis voltage-sensing phosphatase (Ci-VSP) has a transmembrane voltage sensor domain and a cytoplasmic region sharing similarity to the phosphatase and tensin homolog (PTEN). It dephosphorylates phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 3,4,5-trisphosphate upon membrane depolarization. The cytoplasmic region is composed of a phosphatase domain and a putative membrane interaction domain, C2. Here we determined the crystal structures of the Ci-VSP cytoplasmic region in three distinct constructs, wildtype (248–576), wild-type (236–576), and G365A mutant (248–576). The crystal structure of WT-236 and G365A-248 had the disulfide bond between the catalytic residue Cys-363 and the adjacent residue Cys-310. On the other hand, the disulfide bond was not present in the crystal structure of WT-248. These suggest the possibility that Ci-VSP is regulated by reactive oxygen species as found in PTEN. These structures also revealed that the conformation of the TI loop in the active site of the Ci-VSP cytoplasmic region was distinct from the corresponding region of PTEN; Ci-VSP has glutamic acid (Glu-411) in the TI loop, orienting toward the center of active site pocket. Mutation of Glu-411 led to acquirement of increased activity toward phosphatidylinositol 3,5-bisphosphate, suggesting that this site is required for determining substrate specificity. Our results provide the basic information of the enzymatic mechanism of Ci-VSP.
Publisher	American Society for Biochemistry and Molecular Biology
Source Title	Journal of Biological Chemistry
Volume (Issue)	286(26)
Page	23368-23377
Date of Issued	2011-07
Language	English
Handle URL	https://hdl.handle.net/11094/73659
eISSN	1083351X
NCID	AA1202441X
Relation.isIdenticalTo	DOI (Publisher Version) https://doi.org/10.1074/jbc.M110.214361
Relation.isIdenticalTo	PMID 21543329
Access Rights	open access
CopyRight	© the American Society for Biochemistry and Molecular Biology.
oaire:version	Version of Record
Category	学術雑誌論文 Journal Article

Resource Type	journal article
Local Type	Journal Article
DCMI Type	Text
DCTERMS.bibliographicCitation	Journal of Biological Chemistry. 2011, 286(26), p. 23368-23377
DC.title	Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity
DC.creator	Matsuda, Makoto
	Takeshita, Kohei
	Kurokawa, Tatsuki
	Sakata, Souhei
	Suzuki, Mamoru
	Yamashita, Eiki
	Okamura, Yasushi
	Nakagawa, Atushi
DC.publisher	American Society for Biochemistry and Molecular Biology
DC.language' scheme='DCTERMS.RFC1766	English
DC.type' scheme='DCTERMS.DCMIType	Text
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2011-07
DC.identifier	https://doi.org/10.1074/jbc.M110.214361
DC.description	This research was originally published in Journal of Biological Chemistry. Makoto Matsuda, Kohei Takeshita, Tatsuki Kurokawa, Souhei Sakata, Mamoru Suzuki, Eiki Yamashita, Yasushi Okamura, and Atsushi Nakagawa. Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity. Journal of Biological Chemistry. 2011; 286, 23368-23377. © the American Society for Biochemistry and Molecular Biology.
DCTERMS.abstract	Ciona intestinalis voltage-sensing phosphatase (Ci-VSP) has a transmembrane voltage sensor domain and a cytoplasmic region sharing similarity to the phosphatase and tensin homolog (PTEN). It dephosphorylates phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 3,4,5-trisphosphate upon membrane depolarization. The cytoplasmic region is composed of a phosphatase domain and a putative membrane interaction domain, C2. Here we determined the crystal structures of the Ci-VSP cytoplasmic region in three distinct constructs, wildtype (248–576), wild-type (236–576), and G365A mutant (248–576). The crystal structure of WT-236 and G365A-248 had the disulfide bond between the catalytic residue Cys-363 and the adjacent residue Cys-310. On the other hand, the disulfide bond was not present in the crystal structure of WT-248. These suggest the possibility that Ci-VSP is regulated by reactive oxygen species as found in PTEN. These structures also revealed that the conformation of the TI loop in the active site of the Ci-VSP cytoplasmic region was distinct from the corresponding region of PTEN; Ci-VSP has glutamic acid (Glu-411) in the TI loop, orienting toward the center of active site pocket. Mutation of Glu-411 led to acquirement of increased activity toward phosphatidylinositol 3,5-bisphosphate, suggesting that this site is required for determining substrate specificity. Our results provide the basic information of the enzymatic mechanism of Ci-VSP.
DC.rights	© the American Society for Biochemistry and Molecular Biology.
DC.format	73659
citation_title	Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity
citation_author	Matsuda, Makoto
	Takeshita, Kohei
	Kurokawa, Tatsuki
	Sakata, Souhei
	Suzuki, Mamoru
	Yamashita, Eiki
	Okamura, Yasushi
	Nakagawa, Atushi
citation_publisher	American Society for Biochemistry and Molecular Biology
citation_language	English
citation_date	2011-07
citation_journal_title	Journal of Biological Chemistry
citation_volume	286
citation_issue	26
citation_firstpage	23368
citation_lastpage	23377
citation_doi	https://doi.org/10.1074/jbc.M110.214361
citation_pmid	21543329
citation_public_url	https://hdl.handle.net/11094/73659

Crystal structure of the cytoplasmic phosphatase and tensin homolog (PTEN)-like region of Ciona intestinalis voltage-sensing phosphatase provides insight into substrate specificity and redox regulation of the phosphoinositide phosphatase activity

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