Structural basis for cofilin binding and actin filament disassembly

Kotaro Tanaka; Shuichi Takeda; Kaoru Mitsuoka; Toshiro Oda; Chieko Kimura-Sakiyama; Yuichiro Maéda; Akihiro Narita

doi:10.1038/s41467-018-04290-w

Structural basis for cofilin binding and actin filament disassembly

Kotaro Tanaka, Shuichi Takeda, Kaoru Mitsuoka, Toshiro Oda, Chieko Kimura-Sakiyama, Yuichiro Maéda, Akihiro Narita

Research output: Contribution to journal › Article › peer-review

101 Citations (Scopus)

Abstract

Actin depolymerizing factor (ADF) and cofilin accelerate actin dynamics by severing and disassembling actin filaments. Here, we present the 3.8 Å resolution cryo-EM structure of cofilactin (cofilin-decorated actin filament). The actin subunit structure of cofilactin (C-form) is distinct from those of F-actin (F-form) and monomeric actin (G-form). During the transition between these three conformations, the inner domain of actin (subdomains 3 and 4) and the majority of subdomain 1 move as two separate rigid bodies. The cofilin-actin interface consists of three distinct parts. Based on the rigid body movements of actin and the three cofilin-actin interfaces, we propose models for the cooperative binding of cofilin to actin, preferential binding of cofilin to ADP-bound actin filaments and cofilin-mediated severing of actin filaments.

Original language	English
Article number	1860
Journal	Nature communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-04290-w
Publication status	Published - Dec 1 2018
Externally published	Yes

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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10.1038/s41467-018-04290-w

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@article{b2b85afb06b443098262cf515a93208b,

title = "Structural basis for cofilin binding and actin filament disassembly",

abstract = "Actin depolymerizing factor (ADF) and cofilin accelerate actin dynamics by severing and disassembling actin filaments. Here, we present the 3.8 {\AA} resolution cryo-EM structure of cofilactin (cofilin-decorated actin filament). The actin subunit structure of cofilactin (C-form) is distinct from those of F-actin (F-form) and monomeric actin (G-form). During the transition between these three conformations, the inner domain of actin (subdomains 3 and 4) and the majority of subdomain 1 move as two separate rigid bodies. The cofilin-actin interface consists of three distinct parts. Based on the rigid body movements of actin and the three cofilin-actin interfaces, we propose models for the cooperative binding of cofilin to actin, preferential binding of cofilin to ADP-bound actin filaments and cofilin-mediated severing of actin filaments.",

author = "Kotaro Tanaka and Shuichi Takeda and Kaoru Mitsuoka and Toshiro Oda and Chieko Kimura-Sakiyama and Yuichiro Ma{\'e}da and Akihiro Narita",

note = "Funding Information: This research was supported by JSPS KAKENHI (JP26251017 to Y.M. and A.N.; JP16H06280 to K.M.), JST PRESTO, Japan (10404 to A.N.), a Grant-in-Aid for JSPS Research Fellow (13J02335 to K.T.), Takeda Science Foundation, a Grant-in-Aid for Scientific Research on Innovative Areas—Platforms for Advanced Technologies and Research Resources “Advanced Bioimaging Support” and by Grants-in-Aid from “Nanotechnology Platform” (Project No. 12024046) of the Ministry of Education, Culture, Sports, Science and Technology (MEXT). We also acknowledge Prof. Hiroshi Abe of Chiba University, Japan, for advice on selecting cofilin species and providing expression systems. We thank Dr. Ryotaro Koike and Prof. Motonori Ota of Nagoya University, Japan, for sharing unpublished results concerning molecular dynamics simulations. We thank Prof. Robert Robinson (A*STAR and Okayama University) for polishing and editing a draft of this manuscript. We thank Prof. Koh Saito and Assoc. Prof. Makoto Kuwahara of Nagoya University, Japan, for granting us use of the FEI Polara, a cryo-EM. We also thank Michal Bell, PhD, from Edanz Group (www. edanzediting.com/ac) for editing a draft of this manuscript. Funding Information: This research was supported by JSPS KAKENHI (JP26251017 to Y.M. and A.N.; JP16H06280 to K.M.), JST PRESTO, Japan (10404 to A.N.), a Grant-in-Aid for JSPS Research Fellow (13J02335 to K.T.), Takeda Science Foundation, a Grant-in-Aid for Scientific Research on Innovative Areas Platforms for Advanced Technologies and Research Resources {"}Advanced Bioimaging Support{"} and by Grants-in-Aid from {"}Nanotechnology Platform{"} (Project No. 12024046) of the Ministry of Education, Culture, Sports, Science and Technology (MEXT). Publisher Copyright: {\textcopyright} 2018 The Author(s).",

year = "2018",

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doi = "10.1038/s41467-018-04290-w",

language = "English",

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T1 - Structural basis for cofilin binding and actin filament disassembly

AU - Tanaka, Kotaro

AU - Takeda, Shuichi

AU - Mitsuoka, Kaoru

AU - Oda, Toshiro

AU - Kimura-Sakiyama, Chieko

AU - Maéda, Yuichiro

AU - Narita, Akihiro

N1 - Funding Information: This research was supported by JSPS KAKENHI (JP26251017 to Y.M. and A.N.; JP16H06280 to K.M.), JST PRESTO, Japan (10404 to A.N.), a Grant-in-Aid for JSPS Research Fellow (13J02335 to K.T.), Takeda Science Foundation, a Grant-in-Aid for Scientific Research on Innovative Areas—Platforms for Advanced Technologies and Research Resources “Advanced Bioimaging Support” and by Grants-in-Aid from “Nanotechnology Platform” (Project No. 12024046) of the Ministry of Education, Culture, Sports, Science and Technology (MEXT). We also acknowledge Prof. Hiroshi Abe of Chiba University, Japan, for advice on selecting cofilin species and providing expression systems. We thank Dr. Ryotaro Koike and Prof. Motonori Ota of Nagoya University, Japan, for sharing unpublished results concerning molecular dynamics simulations. We thank Prof. Robert Robinson (A*STAR and Okayama University) for polishing and editing a draft of this manuscript. We thank Prof. Koh Saito and Assoc. Prof. Makoto Kuwahara of Nagoya University, Japan, for granting us use of the FEI Polara, a cryo-EM. We also thank Michal Bell, PhD, from Edanz Group (www. edanzediting.com/ac) for editing a draft of this manuscript. Funding Information: This research was supported by JSPS KAKENHI (JP26251017 to Y.M. and A.N.; JP16H06280 to K.M.), JST PRESTO, Japan (10404 to A.N.), a Grant-in-Aid for JSPS Research Fellow (13J02335 to K.T.), Takeda Science Foundation, a Grant-in-Aid for Scientific Research on Innovative Areas Platforms for Advanced Technologies and Research Resources "Advanced Bioimaging Support" and by Grants-in-Aid from "Nanotechnology Platform" (Project No. 12024046) of the Ministry of Education, Culture, Sports, Science and Technology (MEXT). Publisher Copyright: © 2018 The Author(s).

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Actin depolymerizing factor (ADF) and cofilin accelerate actin dynamics by severing and disassembling actin filaments. Here, we present the 3.8 Å resolution cryo-EM structure of cofilactin (cofilin-decorated actin filament). The actin subunit structure of cofilactin (C-form) is distinct from those of F-actin (F-form) and monomeric actin (G-form). During the transition between these three conformations, the inner domain of actin (subdomains 3 and 4) and the majority of subdomain 1 move as two separate rigid bodies. The cofilin-actin interface consists of three distinct parts. Based on the rigid body movements of actin and the three cofilin-actin interfaces, we propose models for the cooperative binding of cofilin to actin, preferential binding of cofilin to ADP-bound actin filaments and cofilin-mediated severing of actin filaments.

AB - Actin depolymerizing factor (ADF) and cofilin accelerate actin dynamics by severing and disassembling actin filaments. Here, we present the 3.8 Å resolution cryo-EM structure of cofilactin (cofilin-decorated actin filament). The actin subunit structure of cofilactin (C-form) is distinct from those of F-actin (F-form) and monomeric actin (G-form). During the transition between these three conformations, the inner domain of actin (subdomains 3 and 4) and the majority of subdomain 1 move as two separate rigid bodies. The cofilin-actin interface consists of three distinct parts. Based on the rigid body movements of actin and the three cofilin-actin interfaces, we propose models for the cooperative binding of cofilin to actin, preferential binding of cofilin to ADP-bound actin filaments and cofilin-mediated severing of actin filaments.

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Structural basis for cofilin binding and actin filament disassembly

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