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F1FO ATP synthase molecular motor mechanisms

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Article Chemistry, Physical

Determinants of Directionality and Efficiency of the ATP Synthase Fo Motor at Atomic Resolution

Antoni Marciniak et al.

Summary: Through all-atom free energy simulations, we reveal the multifunctional role of arginine (R176) in the F-o subcomplex, which determines the direction of rotation, controls the protonation state, and separates the proton-access half-channels, leading to highly efficient energy conversion.

JOURNAL OF PHYSICAL CHEMISTRY LETTERS (2022)

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Structure of ATP synthase under strain during catalysis

Hui Guo et al.

Summary: ATP synthases are composed of F-1 and F-O motors, which are held together by a peripheral stalk. The peripheral stalk can resist the bending force caused by the rotation of the rotor during ATP hydrolysis or proton translocation. CryoEM imaging of yeast mitochondrial ATP synthase during ATP-hydrolysis-driven rotary catalysis reveals a large deformation of the peripheral stalk. This deformation is caused by the accumulation of strain in the stalk due to proton translocation, which drives the relative rotation of the rotor and enables efficient synthesis of ATP.

NATURE COMMUNICATIONS (2022)

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被撤回的出版物: Intrinsically unidirectional chemically fuelled rotary molecular motors (Retracted article. See JUL, 2023)

Ke Mo et al.

Summary: Scientists have designed synthetic molecular motors that can be driven by chemical energy and have intrinsic control over the direction of rotation, simple autonomous motion, and near-perfect unidirectionality. This study demonstrates the potential for future generations of multicomponent machines to perform mechanical functions.

NATURE (2022)

Article Chemistry, Physical

Determinants of Directionality and Efficiency of the ATP Synthase F-o Motor at Atomic Resolution

Antoni Marciniak et al.

Summary: Through extensive all-atom free energy simulations, it is shown that the directionality of the ATP synthase F-o subcomplex motor naturally arises from the interplay between intraprotein interactions and energetics of protonation. The strictly conserved arginine in the a-subunit is crucial for dictating rotation direction, controlling protonation state, and separating proton-access channels to ensure efficient energy conversion.

JOURNAL OF PHYSICAL CHEMISTRY LETTERS (2022)

Article Multidisciplinary Sciences

Structure of mycobacterial ATP synthase bound to the tuberculosis drug bedaquiline

Hui Guo et al.

Summary: The study of the ATP synthase structures in Mycobacterium smegmatis has provided insights into how the enzyme conserves energy through autoinhibition of ATP hydrolysis and the mechanism of action of the drug bedaquiline used in treating multidrug-resistant tuberculosis. Tuberculosis, caused by Mycobacterium tuberculosis, is increasingly resistant to first-line antibiotics, allowing infections to remain dormant and decreasing susceptibility to many antibiotics. Bedaquiline, developed from a lead compound identified in a screen against Mycobacterium smegmatis, targets the mycobacterial ATP synthase and is a cornerstone in the treatment of multidrug-resistant and extensively drug-resistant tuberculosis.

NATURE (2021)

Article Biology

pH-dependent 11° F1FO ATP synthase sub-steps reveal insight into the FO torque generating mechanism

Seiga Yanagisawa et al.

Summary: This study investigates the torque-generating mechanism in the F1FO ATP synthase, showing that mutations in the half-channels can change their pKa values and ultimately affect proton translocation. The experiments also reveal the ability of F-O to undergo single c-subunit rotational stepping, supporting a Grotthuss mechanism involving single water molecules in each half-channel linked by c-ring rotation. Furthermore, the pH-dependent 11-degree ATP synthase-direction sub-steps of the c(10)-ring were observed, providing evidence for a mechanism involving alternating proton translocation-dependent rotational sub-steps to sustain F1FO ATP synthesis.
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The six steps of the complete F1-ATPase rotary catalytic cycle

Meghna Sobti et al.

Summary: The study utilized cryo-electron microscopy to determine the structure of F-1-ATPase, revealing different conformational states during the catalytic cycle and providing a structural basis for the entire cycle.

NATURE COMMUNICATIONS (2021)

Article Multidisciplinary Sciences

Rotary catalysis of bovine mitochondrial F1-ATPase studied by single-molecule experiments

Ryohei Kobayashi et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2020)

Article Multidisciplinary Sciences

Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch

Meghna Sobti et al.

NATURE COMMUNICATIONS (2020)

Article Biochemistry & Molecular Biology

Cryo-EM structure of the entire mammalian F-type ATP synthase

Gergely Pinke et al.

NATURE STRUCTURAL & MOLECULAR BIOLOGY (2020)

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Structure of the dimeric ATP synthase from bovine mitochondria

Tobias E. Spikes et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2020)

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Cryo-EM and MD infer water-mediated proton transport and autoinhibition mechanisms of V-o complex

Soung-Hun Roh et al.

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The 3 x 120° rotary mechanism of Paracoccus denitrificans F1-ATPase is different from that of the bacterial and mitochondrial F1-ATPases

Mariel Zarco-Zavala et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2020)

Review Biochemistry & Molecular Biology

Structural Asymmetry and Kinetic Limping of Single Rotary F-ATP Synthases

Hendrik Sielaff et al.

MOLECULES (2019)

Review Biochemistry & Molecular Biology

Structure and Mechanisms of F-Type ATP Synthases

Werner Kuehlbrandt

ANNUAL REVIEW OF BIOCHEMISTRY, VOL 88 (2019)

Article Multidisciplinary Sciences

Rotary substates of mitochondrial ATP synthase reveal the basis of flexible F1-Fo coupling

Bonnie J. Murphy et al.

SCIENCE (2019)

Article Multidisciplinary Sciences

Structural basis for power stroke vs. Brownian ratchet mechanisms of motor proteins

Wonmuk Hwang et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2019)

Article Biochemistry & Molecular Biology

Single-molecule analysis reveals rotational substeps and chemo-mechanical coupling scheme of Enterococcus hirae V1-ATPase

Tatsuya Iida et al.

JOURNAL OF BIOLOGICAL CHEMISTRY (2019)

Article Multidisciplinary Sciences

Elastic coupling power stroke mechanism of the F1-ATPase molecular motor

James L. Martin et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2018)

Article Multidisciplinary Sciences

High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane

Anurag P. Srivastava et al.

SCIENCE (2018)

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Structure, mechanism, and regulation of the chloroplast ATP synthase

Alexander Hahn et al.

SCIENCE (2018)

Article Biochemistry & Molecular Biology

The uniqueness of subunit α of mycobacterial F-ATP synthases: An evolutionary variant for niche adaptation

Priya Ragunathan et al.

JOURNAL OF BIOLOGICAL CHEMISTRY (2017)

Article Biochemistry & Molecular Biology

Protonation-dependent stepped rotation of the F-type ATP synthase c-ring observed by single-molecule measurements

Seiga Yanagisawa et al.

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Power Stroke Angular Velocity Profiles of Archaeal A-ATP Synthase Versus Thermophilic and Mesophilic F-ATP Synthase Molecular Motors

Hendrik Sielaff et al.

JOURNAL OF BIOLOGICAL CHEMISTRY (2016)

Article Multidisciplinary Sciences

Load-dependent destabilization of the γ-rotor shaft in FOF1 ATP synthase revealed by hydrogen/deuterium-exchange mass spectrometry

Siavash Vahidi et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2016)

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How release of phosphate from mammalian F1-ATPase generates a rotary substep

John V. Bason et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2015)

Article Multidisciplinary Sciences

Dissecting the role of the γ-subunit in the rotary-chemical coupling and torque generation of F1-ATPase

Shayantani Mukherjee et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2015)

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Simple mechanism whereby the F1-ATPase motor rotates with near-perfect chemomechanical energy conversion

Ei-ichiro Saita et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2015)

Review Biochemistry & Molecular Biology

Half channels mediating H transport and the mechanism of gating in the Fo sector of Escherichia coli F1Fo ATP synthase

Robert H. Fillingame et al.

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None of the Rotor Residues of F1-ATPase Are Essential for Torque Generation

Ryohei Chiwata et al.

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Chemomechanical coupling of human mitochondrial F1-ATPase motor

Toshiharu Suzuki et al.

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Anatomy of F1-ATPase powered rotation

James L. Martin et al.

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Thermodynamic analysis of F1-ATPase rotary catalysis using high-speed imaging

Rikiya Watanabe et al.

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High-resolution single-molecule characterization of the enzymatic states in Escherichia coli F1-ATPase

Thomas Bilyard et al.

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Structural evidence of a new catalytic intermediate in the pathway of ATP hydrolysis by F1-ATPase from bovine heart mitochondria

David M. Rees et al.

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Controlled rotation of the F1-ATPase reveals differential and continuous binding changes for ATP synthesis

Kengo Adachi et al.

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Structure of the ATP synthase catalytic complex (F1) from Escherichia coli in an autoinhibited conformation

Gino Cingolani et al.

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Torsional elasticity and energetics of F1-ATPase

Jacek Czub et al.

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Electrostatic origin of the mechanochemical rotary mechanism and the catalytic dwell of F1-ATPase

Shayantani Mukherjee et al.

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Resolving stepping rotation in Thermus thermophilus H+-ATPase/synthase with an essentially drag-free probe

Shou Furuike et al.

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Direct observation of stepped proteolipid ring rotation in E. coli FoF1-ATP synthase

Robert Ishmukhametov et al.

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Single Molecule Behavior of Inhibited and Active States of Escherichia coli ATP Synthase F1 Rotation

Mizuki Sekiya et al.

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Microscopic rotary mechanism of ion translocation in the F0 complex of ATP synthases

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ATP Synthase with Its γ Subunit Reduced to the N-terminal Helix Can Still Catalyze ATP Synthesis

Nelli Mnatsakanyan et al.

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Torque generation and elastic power transmission in the rotary F0F1-ATPase

Wolfgang Junge et al.

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Determination of torque generation from the power stroke of Escherichia coli F1-ATPase

Tassilo Hornung et al.

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How subunit coupling produces the γ-subunit rotary motion in F1-ATPase

Jingzhi Pu et al.

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Domain compliance and elastic power transmission in rotary FOFl-ATPase

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Axle-less F1-ATPase rotates in the correct direction

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Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 a resolution

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Et tu, Grotthuss! and other unfinished stories

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The rotor tip inside a bearing of a thermophilic F1-ATPase is dispensable for torque generation

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Folding-based molecular simulations reveal mechanisms of the rotary motor F1-ATPase

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Microsecond time scale rotation measurements of single F1-ATPase molecules

D Spetzler et al.

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Stochastic high-speed rotation of Escherichia coli ATP synthase F1 sector -: The ε subunit-sensitive rotation

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Proton-powered subunit rotation in single membrane-bound F0F1-ATP synthase

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F1-ATPase, the C-terminal end of subunit γ is not required for ATP hydrolysis-driven rotation

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Pause and rotation of F1-ATPase during catalysis

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The participation of metals in the mechanism of the F1-ATPase

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The role of the DELSEED motif of the β subunit in rotation of F1-ATPase

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A rotary molecular motor that can work at near 100% efficiency

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