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The working stroke upon myosin-nucleotide complexes binding to actin.

Walter Steffen¹, David Smith, John Sleep

¹Randall Centre, King's College, London SE1 1UL, United Kingdom.

Proceedings of the National Academy of Sciences of the United States of America

|May 17, 2003

Summary

The actomyosin crossbridge cycle

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Area of Science:

Muscle physiology
Molecular motor function
Biophysics

Background:

Myosin's tight binding to actin is well-established.
Direct coupling of binding energy to the working stroke remained experimentally elusive.
Previous muscle fiber experiments could not resolve this question.

Purpose of the Study:

To determine if myosin-actin binding energy directly fuels the actomyosin crossbridge working stroke.
To investigate the mechanical states of myosin during the ATPase cycle at the single-molecule level.

Main Methods:

Utilized single-molecule optical tweezers to measure the actomyosin crossbridge cycle.
Compared the working stroke of four myosin complexes (myosin, myosin-ADP, myosin-pyrophosphate, myosin-adenyl-5'yl imidodiphosphate) with ATP hydrolysis.
Analyzed myosin conformations upon binding to actin.

Main Results:

A significant working stroke (5.4 nm) was observed exclusively during ATP hydrolysis.
Myosin complexes without ATP hydrolysis exhibited minimal to no working stroke, indicating a rigor-like conformation.
The myosin products state (M.ADP.Pi) binds actin in a distinct prestroke conformation.

Conclusions:

Myosin exists in at least two distinct mechanical conformations when dissociated from actin.
These conformations correlate with high-resolution structural states (open and closed nucleotide binding pockets).
The working stroke is powered by ATP hydrolysis, not solely by myosin-actin binding energy.

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