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Physiol. Rev. 80: 853-924, 2000;
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Physiological Reviews, Vol. 80, No. 2, April 2000, pp. 853-924
Copyright ©2000 by the American Physiological Society

Regulation of Contraction in Striated Muscle

A. M. Gordon, E. Homsher, and M. Regnier

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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 J. Biol. Chem.Home page
T. Kobayashi and R. J. Solaro
Increased Ca2+ Affinity of Cardiac Thin Filaments Reconstituted with Cardiomyopathy-related Mutant Cardiac Troponin I
J. Biol. Chem., May 12, 2006; 281(19): 13471 - 13477.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
Y. Watanabe, H. Kokubo, S. Miyagawa-Tomita, M. Endo, K. Igarashi, K. i. Aisaki, J. Kanno, and Y. Saga
Activation of Notch1 signaling in cardiogenic mesoderm induces abnormal heart morphogenesis in mouse
Development, May 1, 2006; 133(9): 1625 - 1634.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
E. P. Debold, J. Romatowski, and R. H. Fitts
The depressive effect of Pi on the force-pCa relationship in skinned single muscle fibers is temperature dependent
Am J Physiol Cell Physiol, April 1, 2006; 290(4): C1041 - C1050.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
V. Saks, P. Dzeja, U. Schlattner, M. Vendelin, A. Terzic, and T. Wallimann
Cardiac system bioenergetics: metabolic basis of the Frank-Starling law
J. Physiol., March 1, 2006; 571(2): 253 - 273.
[Abstract] [Full Text] [PDF]

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 J BiochemHome page
H. Mizuno and H. Honda
Troponin Is a Potential Regulator for Actomyosin Interactions
J. Biochem., February 1, 2006; 139(2): 289 - 293.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
B. O'Connell, R. Blazev, and G. M. M. Stephenson
Electrophoretic and functional identification of two troponin C isoforms in toad skeletal muscle fibers
Am J Physiol Cell Physiol, February 1, 2006; 290(2): C515 - C523.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
M. A. Brotto, B. J. Biesiadecki, L. S. Brotto, T. M. Nosek, and J.-P. Jin
Coupled expression of troponin T and troponin I isoforms in single skeletal muscle fibers correlates with contractility
Am J Physiol Cell Physiol, February 1, 2006; 290(2): C567 - C576.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
W. D. Gao, T. Dai, and D. Nyhan
Increased cross-bridge cycling rate in stunned myocardium
Am J Physiol Heart Circ Physiol, February 1, 2006; 290(2): H886 - H893.
[Abstract] [Full Text] [PDF]

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 JGPHome page
J. E. Stelzer, L. Larsson, D. P. Fitzsimons, and R. L. Moss
Activation Dependence of Stretch Activation in Mouse Skinned Myocardium: Implications for Ventricular Function
J. Gen. Physiol., January 30, 2006; 127(2): 95 - 107.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
C. A. C. Ottenheijm, L. M. A. Heunks, M. C. P. Geraedts, and P. N. R. Dekhuijzen
Hypoxia-induced skeletal muscle fiber dysfunction: role for reactive nitrogen species
Am J Physiol Lung Cell Mol Physiol, January 1, 2006; 290(1): L127 - L135.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
G. Zhi, J. W. Ryder, J. Huang, P. Ding, Y. Chen, Y. Zhao, K. E. Kamm, and J. T. Stull
Myosin light chain kinase and myosin phosphorylation effect frequency-dependent potentiation of skeletal muscle contraction
PNAS, November 29, 2005; 102(48): 17519 - 17524.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
N. M. Kad, S. Kim, D. M. Warshaw, P. VanBuren, and J. E. Baker
Single-myosin crossbridge interactions with actin filaments regulated by troponin-tropomyosin
PNAS, November 22, 2005; 102(47): 16990 - 16995.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
O. M. Hernandez, D. Szczesna-Cordary, B. C. Knollmann, T. Miller, M. Bell, J. Zhao, S. G. Sirenko, Z. Diaz, G. Guzman, Y. Xu, et al.
F110I and R278C Troponin T Mutations That Cause Familial Hypertrophic Cardiomyopathy Affect Muscle Contraction in Transgenic Mice and Reconstituted Human Cardiac Fibers
J. Biol. Chem., November 4, 2005; 280(44): 37183 - 37194.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
O. Tchaicheeyan and A. Landesberg
Regulation of energy liberation during steady sarcomere shortening
Am J Physiol Heart Circ Physiol, November 1, 2005; 289(5): H2176 - H2182.
[Abstract] [Full Text] [PDF]

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 Mol Biol EvolHome page
R. Herranz, J. Mateos, J. A. Mas, E. Garcia-Zaragoza, M. Cervera, and R. Marco
The Coevolution of Insect Muscle TpnT and TpnI Gene Isoforms
Mol. Biol. Evol., November 1, 2005; 22(11): 2231 - 2242.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
E. W. Clemmens, M. Entezari, D. A Martyn, and M. Regnier
Different effects of cardiac versus skeletal muscle regulatory proteins on in vitro measures of actin filament speed and force
J. Physiol., August 1, 2005; 566(3): 737 - 746.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
C. A. C. Ottenheijm, L. M. A. Heunks, G. C. Sieck, W.-Z. Zhan, S. M. Jansen, H. Degens, T. de Boo, and P. N. R. Dekhuijzen
Diaphragm Dysfunction in Chronic Obstructive Pulmonary Disease
Am. J. Respir. Crit. Care Med., July 15, 2005; 172(2): 200 - 205.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
S. J. Dixon and P. J. Roy
Muscle arm development in Caenorhabditis elegans
Development, July 1, 2005; 132(13): 3079 - 3092.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
T. E. Gillis, B. Liang, F. Chung, and G. F. Tibbits
Increasing mammalian cardiomyocyte contractility with residues identified in trout troponin C
Physiol Genomics, June 16, 2005; 22(1): 1 - 7.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
C. R. Hancock, E. Janssen, and R. L. Terjung
Skeletal muscle contractile performance and ADP accumulation in adenylate kinase-deficient mice
Am J Physiol Cell Physiol, June 1, 2005; 288(6): C1287 - C1297.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
E. Verburg, R. M. Murphy, D. G. Stephenson, and G. D. Lamb
Disruption of excitation-contraction coupling and titin by endogenous Ca2+-activated proteases in toad muscle fibres
J. Physiol., May 1, 2005; 564(3): 775 - 790.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
M Kruger, S Zittrich, C Redwood, N Blaudeck, J James, J Robbins, G Pfitzer, and R Stehle
Effects of the mutation R145G in human cardiac troponin I on the kinetics of the contraction-relaxation cycle in isolated cardiac myofibrils
J. Physiol., April 15, 2005; 564(2): 347 - 357.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
X. Wang, Q.-Q. Huang, M. T. Breckenridge, A. Chen, T. O. Crawford, D. H. Morton, and J.-P. Jin
Cellular Fate of Truncated Slow Skeletal Muscle Troponin T Produced by Glu180 Nonsense Mutation in Amish Nemaline Myopathy
J. Biol. Chem., April 8, 2005; 280(14): 13241 - 13249.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. V. Vinogradova, D. B. Stone, G. G. Malanina, C. Karatzaferi, R. Cooke, R. A. Mendelson, and R. J. Fletterick
Ca2+-regulated structural changes in troponin
PNAS, April 5, 2005; 102(14): 5038 - 5043.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
J.-i. Okada, S. Sugiura, S. Nishimura, and T. Hisada
Three-dimensional simulation of calcium waves and contraction in cardiomyocytes using the finite element method
Am J Physiol Cell Physiol, March 1, 2005; 288(3): C510 - C522.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
R. Nassar, N. N. Malouf, L. Mao, H. A. Rockman, A. E. Oakeley, J. R. Frye, J. R. Herlong, S. P. Sanders, and P. A. W. Anderson
cTnT1, a cardiac troponin T isoform, decreases myofilament tension and affects the left ventricular pressure waveform
Am J Physiol Heart Circ Physiol, March 1, 2005; 288(3): H1147 - H1156.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. C. Barbato, Q.-Q. Huang, M. M. Hossain, M. Bond, and J.-P. Jin
Proteolytic N-terminal Truncation of Cardiac Troponin I Enhances Ventricular Diastolic Function
J. Biol. Chem., February 25, 2005; 280(8): 6602 - 6609.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
P. Graceffa and A. Mazurkie
Effect of Caldesmon on the Position and Myosin-induced Movement of Smooth Muscle Tropomyosin Bound to Actin
J. Biol. Chem., February 11, 2005; 280(6): 4135 - 4143.
[Abstract] [Full Text] [PDF]

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 J. Physiol.Home page
A. Moreno-Gonzalez, J. Fredlund, and M. Regnier
Cardiac troponin C (TnC) and a site I skeletal TnC mutant alter Ca2+ versus crossbridge contribution to force in rabbit skeletal fibres
J. Physiol., February 1, 2005; 562(3): 873 - 884.
[Abstract] [Full Text] [PDF]


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