Trading force for speed: Why superfast crossbridge kinetics leads to superlow forces

Trading force for speed: Why superfast crossbridge kinetics leads to superlow forces

^*Biology Department, Leidy Laboratories, University of Pennsylvania, Philadelphia, PA 19104; ^§Department of Physiology, Pennsylvania Muscle Institute, University of Pennsylvania School of Medicine, Philadelphia, PA 19104-6083; and ^†Marine Biological Laboratories, Woods Hole, MA 02543

Communicated by Clara Franzini-Armstrong, University of Pennsylvania School of Medicine, Philadelphia, PA (received for review January 25, 1999)

Abstract

Superfast muscles power high-frequency motions such as sound production and visual tracking. As a class, these muscles also generate low forces. Using the toadfish swimbladder muscle, the fastest known vertebrate muscle, we examined the crossbridge kinetic rates responsible for high contraction rates and how these might affect force generation. Swimbladder fibers have evolved a 10-fold faster crossbridge detachment rate than fast-twitch locomotory fibers, but surprisingly the crossbridge attachment rate has remained unchanged. These kinetics result in very few crossbridges being attached during contraction of superfast fibers (only ≈1/6 of that in locomotory fibers) and thus low force. This imbalance between attachment and detachment rates is likely to be a general mechanism that imposes a tradeoff of force for speed in all superfast fibers.

Footnotes

↵ ‡ To whom reprint requests should be addressed. e-mail: lrome{at}mail.sas.upenn.edu.
¶ In a steady state, the overall rate of crossbridge attachment equals the overall rate of crossbridge detachment. Each of these terms, in turn, is equal to the rate at which the crossbridges are going through the attachment–detachment cycle, which we measure by the ATPase rate. Because the overall rate of crossbridge detachment = g × number of attached bridges and crossbridge attachment = f × number of detached bridges, these can be rearranged (Eq. 1 and Eq. 2) to solve for the rate constants. Note that in the case that all of the myosin heads are attached and contribute to stiffness in rigor, (ATPase/number of attached bridges) is equivalent to the quotient of the values of ATPase and proportion of attached bridges presented in Table 2. This is because the ATPase values are normalized for myosin head concentration, and the number of attached heads can be estimated as the product of myosin head concentration and the proportion of attached crossbridges. Similarly, (ATPase/number of detached heads) is equivalent to the quotient of the values of ATPase and (1−proportion of attached bridges).
ABBREVIATIONS:

SR,

sarcoplasmic reticulum;

NP-EGTA,

nitrophenyl-EGTA