mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility

Sakamoto, Satoko; Thumkeo, Dean; Ohta, Hiroshi; Zhang, Zhen; Huang, Shuangru; Kanchanawong, Pakorn; Fuu, Takayoshi; Watanabe, Sadanori; Shimada, Kentaro; Fujihara, Yoshitaka; Yoshida, Shosei; Ikawa, Masahito; Watanabe, Naoki; Saitou, Mitinori; Narumiya, Shuh

doi:https://doi.org/10.1371/journal.pbio.2004874

mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility

Sakamoto, Satoko; Thumkeo, Dean; Ohta, Hiroshi et al.

PLoS Biology, 2018, 16(9), e2004874

Number of Access:1,236（2025-08-22 01:08 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/78570

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Title	mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility
Creator	NRID 1000070648427 1000070648427 CreatorName Sakamoto, Satoko
	NRID 1000040372594 1000040372594 CreatorName Thumkeo, Dean
	NRID 1000050391892 1000050391892 CreatorName Ohta, Hiroshi
	CreatorName Zhang, Zhen
	CreatorName Huang, Shuangru
	CreatorName Kanchanawong, Pakorn
	CreatorName Fuu, Takayoshi
	CreatorName Watanabe, Sadanori
	CreatorName Shimada, Kentaro
	NRID 1000070578848 1000070578848 CreatorName Fujihara, Yoshitaka
	NRID 1000060294138 1000060294138 CreatorName Yoshida, Shosei
	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 1000080303816 1000080303816 CreatorName Watanabe, Naoki
	NRID 1000080373306 1000080373306 CreatorName Saitou, Mitinori
	NRID 1000070144350 1000070144350 CreatorName Narumiya, Shuh
Description	mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility. Sakamoto S, Thumkeo D, Ohta H, Zhang Z, Huang S, et al. PLOS Biology. 2018. 16(9) : e2004874. doi:10.1371/journal.pbio.2004874
Abstract	Formin is one of the two major classes of actin binding proteins (ABPs) with nucleation and polymerization activity. However, despite advances in our understanding of its biochemical activity, whether and how formins generate specific architecture of the actin cytoskeleton and function in a physiological context in vivo remain largely obscure. It is also unknown how actin filaments generated by formins interact with other ABPs in the cell. Here, we combine genetic manipulation of formins mammalian diaphanous homolog1 (mDia1) and 3 (mDia3) with superresolution microscopy and single-molecule imaging, and show that the formins mDia1 and mDia3 are dominantly expressed in Sertoli cells of mouse seminiferous tubule and together generate a highly dynamic cortical filamentous actin (F-actin) meshwork that is continuous with the contractile actomyosin bundles. Loss of mDia1/3 impaired these F-actin architectures, induced ectopic noncontractile espin1-containing F-actin bundles, and disrupted Sertoli cell–germ cell interaction, resulting in impaired spermatogenesis. These results together demonstrate the previously unsuspected mDia-dependent regulatory mechanism of cortical F-actin that is indispensable for mammalian sperm development and male fertility.
Publisher	Public Library of Science
Source Title	PLoS Biology
Volume (Issue)	16(9)
Page	e2004874
Date of Issued	2018-09-26
Language	English
Handle URL	https://hdl.handle.net/11094/78570
PISSN	15449173
eISSN	15457885
NCID	AA11886145
Relation.isIdenticalTo	DOI (Publisher Version) https://doi.org/10.1371/journal.pbio.2004874
Relation.isIdenticalTo	PMID 30256801
Access Rights	open access
CopyRight	© 2018 Sakamoto et al. This article is licensed under a Creative Commons Attribution 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	PLoS Biology. 2018, 16(9), p. e2004874
DC.title	mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility
DC.creator	Sakamoto, Satoko
	Thumkeo, Dean
	Ohta, Hiroshi
	Zhang, Zhen
	Huang, Shuangru
	Kanchanawong, Pakorn
	Fuu, Takayoshi
	Watanabe, Sadanori
	Shimada, Kentaro
	Fujihara, Yoshitaka
	Yoshida, Shosei
	Ikawa, Masahito
	Watanabe, Naoki
	Saitou, Mitinori
	Narumiya, Shuh
DC.publisher	Public Library of Science
DC.language' scheme='DCTERMS.RFC1766	English
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2018-09-26
DC.identifier	https://doi.org/10.1371/journal.pbio.2004874
DC.description	mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility. Sakamoto S, Thumkeo D, Ohta H, Zhang Z, Huang S, et al. PLOS Biology. 2018. 16(9) : e2004874. doi:10.1371/journal.pbio.2004874
DCTERMS.abstract	Formin is one of the two major classes of actin binding proteins (ABPs) with nucleation and polymerization activity. However, despite advances in our understanding of its biochemical activity, whether and how formins generate specific architecture of the actin cytoskeleton and function in a physiological context in vivo remain largely obscure. It is also unknown how actin filaments generated by formins interact with other ABPs in the cell. Here, we combine genetic manipulation of formins mammalian diaphanous homolog1 (mDia1) and 3 (mDia3) with superresolution microscopy and single-molecule imaging, and show that the formins mDia1 and mDia3 are dominantly expressed in Sertoli cells of mouse seminiferous tubule and together generate a highly dynamic cortical filamentous actin (F-actin) meshwork that is continuous with the contractile actomyosin bundles. Loss of mDia1/3 impaired these F-actin architectures, induced ectopic noncontractile espin1-containing F-actin bundles, and disrupted Sertoli cell–germ cell interaction, resulting in impaired spermatogenesis. These results together demonstrate the previously unsuspected mDia-dependent regulatory mechanism of cortical F-actin that is indispensable for mammalian sperm development and male fertility.
DC.rights	© 2018 Sakamoto et al. This article is licensed under a Creative Commons Attribution 4.0 International License.
DC.format	78570
citation_title	mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility
citation_author	Sakamoto, Satoko
	Thumkeo, Dean
	Ohta, Hiroshi
	Zhang, Zhen
	Huang, Shuangru
	Kanchanawong, Pakorn
	Fuu, Takayoshi
	Watanabe, Sadanori
	Shimada, Kentaro
	Fujihara, Yoshitaka
	Yoshida, Shosei
	Ikawa, Masahito
	Watanabe, Naoki
	Saitou, Mitinori
	Narumiya, Shuh
citation_publisher	Public Library of Science
citation_language	English
citation_date	2018-09-26
citation_journal_title	PLoS Biology
citation_volume	16
citation_issue	9
citation_firstpage	e2004874
citation_doi	https://doi.org/10.1371/journal.pbio.2004874
citation_pmid	30256801
citation_public_url	https://hdl.handle.net/11094/78570

mDia1/3 generate cortical F-actin meshwork in Sertoli cells that is continuous with contractile F-actin bundles and indispensable for spermatogenesis and male fertility

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