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None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation

F(1)-ATPase is a powerful rotary molecular motor that can rotate an object several hundred times as large as the motor itself against the viscous friction of water. Forced reverse rotation has been shown to lead to ATP synthesis, implying that the mechanical work against the motor’s high torque can...

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Autores principales: Chiwata, Ryohei, Kohori, Ayako, Kawakami, Tomonari, Shiroguchi, Katsuyuki, Furuike, Shou, Adachi, Kengo, Sutoh, Kazuo, Yoshida, Masasuke, Kinosita, Kazuhiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Biophysical Society 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4052266/
https://www.ncbi.nlm.nih.gov/pubmed/24853745
http://dx.doi.org/10.1016/j.bpj.2014.04.013
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author Chiwata, Ryohei
Kohori, Ayako
Kawakami, Tomonari
Shiroguchi, Katsuyuki
Furuike, Shou
Adachi, Kengo
Sutoh, Kazuo
Yoshida, Masasuke
Kinosita, Kazuhiko
author_facet Chiwata, Ryohei
Kohori, Ayako
Kawakami, Tomonari
Shiroguchi, Katsuyuki
Furuike, Shou
Adachi, Kengo
Sutoh, Kazuo
Yoshida, Masasuke
Kinosita, Kazuhiko
author_sort Chiwata, Ryohei
collection PubMed
description F(1)-ATPase is a powerful rotary molecular motor that can rotate an object several hundred times as large as the motor itself against the viscous friction of water. Forced reverse rotation has been shown to lead to ATP synthesis, implying that the mechanical work against the motor’s high torque can be converted into the chemical energy of ATP. The minimal composition of the motor protein is α(3)β(3)γ subunits, where the central rotor subunit γ turns inside a stator cylinder made of alternately arranged α(3)β(3) subunits using the energy derived from ATP hydrolysis. The rotor consists of an axle, a coiled coil of the amino- and carboxyl-terminal α-helices of γ, which deeply penetrates the stator cylinder, and a globular protrusion that juts out from the stator. Previous work has shown that, for a thermophilic F(1), significant portions of the axle can be truncated and the motor still rotates a submicron sized bead duplex, indicating generation of up to half the wild-type (WT) torque. Here, we inquire if any specific interactions between the stator and the rest of the rotor are needed for the generation of a sizable torque. We truncated the protruding portion of the rotor and replaced part of the remaining axle residues such that every residue of the rotor has been deleted or replaced in this or previous truncation mutants. This protrusionless construct showed an unloaded rotary speed about a quarter of the WT, and generated one-third to one-half of the WT torque. No residue-specific interactions are needed for this much performance. F(1) is so designed that the basic rotor-stator interactions for torque generation and control of catalysis rely solely upon the shape and size of the rotor at very low resolution. Additional tailored interactions augment the torque to allow ATP synthesis under physiological conditions.
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spelling pubmed-40522662015-05-20 None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation Chiwata, Ryohei Kohori, Ayako Kawakami, Tomonari Shiroguchi, Katsuyuki Furuike, Shou Adachi, Kengo Sutoh, Kazuo Yoshida, Masasuke Kinosita, Kazuhiko Biophys J Molecular Machines, Motors and Nanoscale Biophysics F(1)-ATPase is a powerful rotary molecular motor that can rotate an object several hundred times as large as the motor itself against the viscous friction of water. Forced reverse rotation has been shown to lead to ATP synthesis, implying that the mechanical work against the motor’s high torque can be converted into the chemical energy of ATP. The minimal composition of the motor protein is α(3)β(3)γ subunits, where the central rotor subunit γ turns inside a stator cylinder made of alternately arranged α(3)β(3) subunits using the energy derived from ATP hydrolysis. The rotor consists of an axle, a coiled coil of the amino- and carboxyl-terminal α-helices of γ, which deeply penetrates the stator cylinder, and a globular protrusion that juts out from the stator. Previous work has shown that, for a thermophilic F(1), significant portions of the axle can be truncated and the motor still rotates a submicron sized bead duplex, indicating generation of up to half the wild-type (WT) torque. Here, we inquire if any specific interactions between the stator and the rest of the rotor are needed for the generation of a sizable torque. We truncated the protruding portion of the rotor and replaced part of the remaining axle residues such that every residue of the rotor has been deleted or replaced in this or previous truncation mutants. This protrusionless construct showed an unloaded rotary speed about a quarter of the WT, and generated one-third to one-half of the WT torque. No residue-specific interactions are needed for this much performance. F(1) is so designed that the basic rotor-stator interactions for torque generation and control of catalysis rely solely upon the shape and size of the rotor at very low resolution. Additional tailored interactions augment the torque to allow ATP synthesis under physiological conditions. The Biophysical Society 2014-05-20 /pmc/articles/PMC4052266/ /pubmed/24853745 http://dx.doi.org/10.1016/j.bpj.2014.04.013 Text en © 2014 The Authors http://creativecommons.org/licenses/by/3.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).
spellingShingle Molecular Machines, Motors and Nanoscale Biophysics
Chiwata, Ryohei
Kohori, Ayako
Kawakami, Tomonari
Shiroguchi, Katsuyuki
Furuike, Shou
Adachi, Kengo
Sutoh, Kazuo
Yoshida, Masasuke
Kinosita, Kazuhiko
None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation
title None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation
title_full None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation
title_fullStr None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation
title_full_unstemmed None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation
title_short None of the Rotor Residues of F(1)-ATPase Are Essential for Torque Generation
title_sort none of the rotor residues of f(1)-atpase are essential for torque generation
topic Molecular Machines, Motors and Nanoscale Biophysics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4052266/
https://www.ncbi.nlm.nih.gov/pubmed/24853745
http://dx.doi.org/10.1016/j.bpj.2014.04.013
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