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Physiological Reviews, Vol. 80, No. 2, April 2000, pp. 853-924
Copyright ©2000 by the American Physiological Society
Departments of Physiology and Biophysics and of Bioengineering, University of Washington, Seattle, Washington; and Department of Physiology, University of California at Los Angeles, Los Angeles, California
Gordon, A. M.,
E. Homsher, and
M. Regnier.
Regulation of Contraction in Striated Muscle. Physiol. Rev. 80: 853-924, 2000.
Ca2+ regulation of contraction in vertebrate striated
muscle is exerted primarily through effects on the thin filament, which regulate strong cross-bridge binding to actin. Structural and biochemical studies suggest that the position of tropomyosin (Tm) and
troponin (Tn) on the thin filament determines the interaction of myosin
with the binding sites on actin. These binding sites can be
characterized as blocked (unable to bind to cross bridges), closed
(able to weakly bind cross bridges), or open (able to bind cross
bridges so that they subsequently isomerize to become strongly bound
and release ATP hydrolysis products). Flexibility of the Tm may allow
variability in actin (A) affinity for myosin along the thin filament
other than through a single 7 actin:1 tropomyosin:1 troponin
(A7TmTn) regulatory unit. Tm position on the actin filament is regulated by the occupancy of NH-terminal Ca2+
binding sites on TnC, conformational changes resulting from
Ca2+ binding, and changes in the interactions among Tn, Tm,
and actin and as well as by strong S1 binding to actin.
Ca2+ binding to TnC enhances TnC-TnI interaction,
weakens TnI attachment to its binding sites on 1-2 actins of the
regulatory unit, increases Tm movement over the actin surface, and
exposes myosin-binding sites on actin previously blocked by Tm.
Adjacent Tm are coupled in their overlap regions where Tm movement is
also controlled by interactions with TnT. TnT also interacts with
TnC-TnI in a Ca2+-dependent manner. All these
interactions may vary with the different protein isoforms. The movement
of Tm over the actin surface increases the "open" probability of
myosin binding sites on actins so that some are in the open
configuration available for myosin binding and cross-bridge
isomerization to strong binding, force-producing states. In
skeletal muscle, strong binding of cycling cross bridges promotes
additional Tm movement. This movement effectively stabilizes Tm in the
open position and allows cooperative activation of additional actins in
that and possibly neighboring A7TmTn regulatory units. The
structural and biochemical findings support the physiological observations of steady-state and transient mechanical behavior. Physiological studies suggest the following. 1)
Ca2+ binding to Tn/Tm exposes sites on actin to which
myosin can bind. 2) Ca2+ regulates the strong
binding of M·ADP·Pi to actin, which precedes the
production of force (and/or shortening) and release of hydrolysis products. 3) The initial rate of force development depends
mostly on the extent of Ca2+ activation of the thin
filament and myosin kinetic properties but depends little on the
initial force level. 4) A small number of strongly attached
cross bridges within an A7TmTn regulatory unit can activate
the actins in one unit and perhaps those in neighboring units. This
results in additional myosin binding and isomerization to strongly
bound states and force production. 5) The rates of the
product release steps per se (as indicated by the unloaded shortening
velocity) early in shortening are largely independent of the extent of
thin filament activation ([Ca2+]) beyond a given baseline
level. However, with a greater extent of shortening, the rates depend
on the activation level. 6) The cooperativity between
neighboring regulatory units contributes to the activation by strong
cross bridges of steady-state force but does not affect the rate of
force development. 7) Strongly attached, cycling cross
bridges can delay relaxation in skeletal muscle in a cooperative
manner. 8) Strongly attached and cycling cross bridges can
enhance Ca2+ binding to cardiac TnC, but influence skeletal
TnC to a lesser extent. 9) Different Tn subunit isoforms can
modulate the cross-bridge detachment rate as shown by studies with
mutant regulatory proteins in myotubes and in in vitro motility assays.
These results and conclusions suggest possible explanations for
differences between skeletal and cardiac muscle regulation and
delineate the paths future research may take toward a better
understanding of striated muscle regulation.
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