Abstract
Skeletal muscle is the source of human body motion. Many scholars have been studying in this field to reveal its contraction mechanism, and relevant achievements have been awarded the Nobel Prize. This paper reviewed the current researches on biomechanics of skeletal muscle, and concluded two strategies (top-down and bottom-up methods) for the biomechanical research of skeletal muscle. Moreover, this paper generalized two major aspects of muscle research: (1) the multi-force coupling mechanism and the collective operation mechanism of molecular motors; (2) the bioelectrochemical driving and control principium of muscle contraction. We discussed the solution for experimental verification and induced a novel idea to study the biomechanics of skeletal muscle based on the microscopic working mechanism of molecular motor, which is the origin of muscle contraction. Finally we analyzed the disadvantages in existent researches and explored future directions that need further studies.
Article PDF
Similar content being viewed by others
References
Hill A V. The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B, 1938, 126: 136–195
Huxley A F, Niedergerke R. Structural changes in muscle during contraction. Nature, 1954, 173: 971–973
Huxley H E, Hanson J. Changes in the cross-striations of muscle during contractions and stretch and their structural interpretation. Nature, 1954, 173: 973–976
Maclntosh B R, Gardiner P F, McComas A J. Skeletal Muscle: Form and Function. 2nd ed. Champaign, IL: Human Kinetics, 2005. 151–175
Li Y S, Chen W Y. Constitutive models of skeletal muscle contraction: I passive behaviors (in Chinese). Adv Mech, 2010, 40: 663–678
Linke W A, Ivemeyer M, Mundel P, et al. Nature of PEVK-titin elasticity in skeletal muscle. Proc Natl Acad Sci USA, 1998, 95: 8052–8057
Rayment I, Holden H M, Whittaker M. Structure of the actin-myosin complex and its implications for muscle contraction. Science, 1993, 261: 56–65
Rayment I, Rypniewski W R, Schmidt-Base K, et al. Three dimensional structure of myosin subfragment-1: A molecular motor. Science, 1993, 261: 50–58
Uyeda T Q, Abramson P D, Spudich J A. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc Natl Acad Sci USA, 1996, 93: 4459–4464
Holmes K C, Angert I, Jon K F, et al. Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide. Nature, 2003, 425: 423–427
Fung Y C. Biomechanics: Mechanical Properties of Living Tissues. New York: Springer-Verlag, 1993. 568
Li Y S, Zhang Y Q, Chen W Y. The constitute model of skeletal muscle contraction (in Chinese). J Taiyuan Univ Tech, 2005, 36: 760–764
Zajac F E. Muscle and tendon: Properties, models, scaling, and application to biomechanics and motor control. Crit Rev Biomed Eng, 1989, 17: 359–411
Huxley H E. The mechanism of muscular contraction. Science, 1969, 164: 1356–1366
Huxley A F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem, 1957, 7: 255–318
Huxley A F, Simmons R M. Proposed mechanism of force generation in striated muscle. Nature, 1971, 233: 533–538
Gordon A M, Huxley A F, Julian F J. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol, 1966, 184: 170–192
Zahalak G I, Motabarzadeh I. A re-examination of calcium activation in Huxley cross-bridge model. J Biomech Eng, 1997, 119: 20–29
Piazzesi G, Reconditi M, Linari M, et al. Mechanism of force generation by myosin heads in skeletal muscle. Nature, 2002, 415: 659–662
Finer J T, Simmons R M, Spudich J A. Single myosin molecule mechanics: Pico Newton forces and nano metre steps. Nature, 1994, 368: 113–119
Anderson F C, Pandy M G. Static and dynamic optimization solutions for gait are practically equivalent. J Biomech, 2001, 34: 153–161
Neptune R R, Burnfield J M, Mulroy S J. The neuromuscular demands of toe walking: A forward dynamics simulation analysis. J Biomech, 2007, 40: 1293–1300
Yang Y Y, Wang R C, Wang Y L, et al. Forward dynamics analysis of human lower limb neuromusculoskeletal system (in Chinese). J Tsinghua Univ (Sci Tech), 2006, 46: 1872–1875
Shu Y G, Ouyang Z C. Biological molecular motors (in Chinese). Physics, 2007, 36: 735–741
Yamakita Y, Iio T. Conformational change of skeletal muscle troponin. J Biochem, 1989, 105: 870–874
Spudich J A. The myosin swinging cross-bridge model. Nat Rev Mol Cell Biol, 2001, 2: 387–392
Lymn R W, Taylor E W. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry, 1971, 10: 4617–4624
Zhao Y P. Some physical mechanical problems in Nano-electromechanical Systems (in Chinese). Chin Mech Abst, 2007, 21: 1–21
Munday J N, Capasso F, Parsegian V A. Measured long-range repulsive Casimir-Lifshitz forces. Nature, 2009, 457: 170–173
Liu Y M, Scolari M, Im W, et al. Protein-protein interactions in actinmyosin binding and structural effects of R405Q mutation: A molecular dynamics study. Proteins: Struct Funct Bioinform, 2006, 64: 156–166
Nakajima H, Kunioka Y, Nakano K, et al. Scanning force microscopy of the interaction events between a single molecule of heavy meromyosin and actin. Biochem Biophys Res Commun, 1997, 234: 178–182
Guo Z, Yin Y H. Coupling mechanism of multi-force interactions in the myosin molecular motor. Chin Sci Bull, 2010, 55: 3538–3544
Guo Z, Yin Y H. Casimir effect on adhesion interaction between myosin molecular motor and actin filament. Inter J Nanosyst, 2010, 3: 9–15
Yanagida S, Kitamura K, Tanaka H, et al. Single molecule analysis of the actomyosin motor. Curr Opin Cell Biol, 2000, 12: 20–25
Huxley A F. Cross-bridge action: Present views, prospects, and unknowns. J Biomech, 2000, 33: 1189–1195
Kaya M, Higuchi H. Nonlinear elasticity and an 8-nm working stroke of single myosin molecules in myofilaments. Science, 2010, 329: 686–689
Sellers J R, Veigel C. Direct observation of the myosin-Va power stroke and its reversal. Nat Struct Mol Biol, 2010, 17: 590–595
Uyeda T Q P, Abramson P D, Spudich J A. The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc Natl Acad Sci USA, 1996, 93: 4459–4464
Ishijima A, Kojima H, Funatsu T, et al. Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell, 1998, 92: 161–171
Yanagida T, Iwaki M, Ishii Y. Single molecule measurements and molecular motors. Phil Trans R Soc B, 2008, 363: 2123–2134
Li G H, Cui Q. Mechanochemical coupling in myosin: A theoretical analysis with molecular dynamics and combined QM/MM reaction path calculations. J Phys Chem B, 2004, 108: 3342–3357
Yang Z, Zhao Y P. QM/MM and classical molecular dynamics simulation of His-tagged peptide immobilization on nickel surface. Mat Sci Eng A-Struct, 2006, 423: 84–91
Yang Z, Zhao Y P. Adsorption of His-tagged peptide to Ni, Cu and Au (100) surfaces: Molecular dynamics simulation. Eng Anal Bound Elem, 2007, 31: 402–409
Feynman R P, Leighton R B, Sands M. The Feynman Lectures on Physics. Boston: Addison-Wesley Longman, 1970
Astumian R D. Thermodynamics and kinetics of a Brownian motor. Science, 1997, 276: 917–922
Julicher F, Ajdari A, Prost J. Modeling molecular motors. Rev Mod Phys, 1997, 69: 1269–1281
Esaki S, Ishii Y, Yanagida T. Model describing the biased Brownian movement of myosin. Proc Japan Acad, 2003, 79: 9–14
Ai B Q, Wang X J, Liu G T, et al. Theoretical study for muscle contraction (in Chinese). Chin J Med Phys, 2003, 20: 107–109
Bao J D, Zhou Y Z. Biased fluctuation model for the unidirectional stepping motion of molecular motor (in Chinese). Chin Sci Bull (Chin Ver), 1998, 43: 1493–1496
Li C P, Hang Y R, Zhan Y, et al. Study the directional motion of myosin VI with the dipole model (in Chinese). Chin Sci Bull (Chin Ver), 2008, 53: 528–532
Spudich J A, Sivaramakrishnan S. Myosin VI: An innovative motor that challenged the swinging lever arm hypothesis. Nat Rev Mol Cell Biol, 2010, 11: 128–137
Sweeney H L, Houdusse A. Myosin VI rewrites the rules for myosin motors. Cell, 2010, 141: 573–582
Montemagno C, Bachand G. Constructing nanomechanical devices powered by biomolecular motors. Nanotechnology, 1999, 10: 225–231
Van Delden R A, Ter Wiel M K J, Pollard M M, et al. Unidirectional molecular motor on a gold surface. Nature, 2005, 437: 1337–1340
Ren Q, Zhao Y P, Yuek J C, et al. Biological application of multi-component nanowires in hybrid devices powered by F1-ATPase motors. Biomed Microdevices, 2006, 8: 201–208
Cui Y B, Zhang Y H, Yue J C, et al. Direct observation of the clockwise light-driven rotation of F0F1-ATP synthase complex. Chin Sci Bull, 2009, 49: 1235–1237
Qi W, Duan L, Wang K, et al. Motor protein CF0F1 reconstituted in lipid-coated hemoglobin microcapsules for ATP synthesis. Adv Mater, 2008, 20: 601–605
Lan G, Sun S X. Dynamics of myosin-driven skeletal muscle contraction I. Steady-state force generation. Biophys J, 2005, 88: 4107–4117
Chin L, Yue P, Feng J J, et al. Mathematical simulation of muscle cross-bridge cycle and force-velocity relationship. Biophys J, 2006, 91: 3653–3663
Guo W S, Luo L F. A new model of the mechanochemical actin activated myosin ATPase cycle (in Chinese). Prog Biochem Biophys, 2003, 30: 216–220
Shu Y G, Shi H L. Cooperative effects on the kinetics of ATP hydrolysis in collective molecular motors. Phys Rev E, 2004, 69: 021912
Vermeulen K C, Stienen G J M, Schmid C F, et al. Cooperative behavior of molecular motors. J Muscle Res Cell Mot, 2002, 23: 71–79
Veigel C, Molloy J E. Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nat Cell Biol, 2003, 5: 980–986
Brugues J, Casademunt J. Self-organization and cooperativity of weakly coupled molecular motors under unequal loading. Phys Rev Lett, 2009, 102: 118104
Campas O, Kafri Y, Zeldovich K B, et al. Collective dynamics of interacting molecular motors. Phys Rev Lett, 2006, 97: 038101
Yin Y H, Guo Z. Collective mechanism of molecular motors and a dynamic mechanical model for sarcomere. Sci China Tech Sci, 2011, 54: 2130–2137
Alencar A M, Butler J P, Mijailovich S M. Thermodynamic origin of cooperativity in acto-myosin interactions: The coupling of short-range interactions with actin bending stiffness in an Ising-like model. Phys Rev E, 2009, 79: 041906
Stein R B, Bobet J, Owuztoreli M N, el al. The kinetics relating calcium and force in skeletal muscle. Biophys J, 1988, 54: 705–717
Guo Z, Yin Y H. A dynamic model of skeletal muscle based on collective behavior of myosin motors-Biomechanics of skeletal muscle based on working mechanism of myosin motors (I). Sci China Tech Sci, 2012, 55: 1589–1595
Sanes J R, Lichtman J W. Development of the vertebrate neuromuscular junction. Ann Rev Neurosci, 1999, 22: 389–442
Toyoshima C, Nakasako M, Nomura H, et al. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature, 2000, 405: 647–655
Yin C C, D’Cruz L G, Lai F A. Ryanodine receptor arrays: Not just a pretty pattern? Cell, 2008, 18: 149–156
Stern M D, Pizzaro G, Rios E. Local control model of excitation-contraction coupling in skeletal muscle. J Gen Physiol, 1997, 110: 415–440
Cannel M B, Allen D G. Model of calcium movements during activation in the sarcomere of frog skeletal muscle. Biophys J, 1984, 45: 913–925
Stuyvers B D, McCulloch A D, Guo J, et al. Effect of stimulation rate, sarcomere length and Ca2+ on force generation by mouse cardiac muscle. J Physiol, 2002, 544: 817–830
Edwards R H T, Hill D K, Jones D A. Fatigue of long duration in human skeletal muscle after exercise. J Physiol, 1977, 272: 769–778
Yin Y H, Chen X. Bioelectrochemical control mechanism with variable-frequency regulation for skeletal muscle contraction-Biomechanics of skeletal muscle based on the working mechanism of myosin motors (II). Sci China Tech Sci, 2012, 55: 2115–2125
Hodgkin A L, Huxley A F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol, 1952, 117: 500–544
Luscher H R, Shiner J S. Simulation of action potential propagation in complex terminal arborizations. Biophys J, 1990, 58: 1389–1399
Smith D O. Mechanisms of action potential propagation failure at sites of axon branching in the crayfish. J Physiol, 1980, 301: 243–259
Rogers J M, McCulloch A D. A collocation-Galerkin finite element model of cardiac action potential propagation. IEEE Trans Biomed Eng, 1994, 41: 743–757
Kandel E R, Schwartz J H, Jessell T M. Principles of Neural Science. 4th ed. New York: Elsevier, 2000
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
This article is published under an open access license. Please check the 'Copyright Information' section either on this page or in the PDF for details of this license and what re-use is permitted. If your intended use exceeds what is permitted by the license or if you are unable to locate the licence and re-use information, please contact the Rights and Permissions team.
About this article
Cite this article
Yin, Y., Guo, Z., Chen, X. et al. Studies on biomechanics of skeletal muscle based on the working mechanism of myosin motors: An overview. Chin. Sci. Bull. 57, 4533–4544 (2012). https://doi.org/10.1007/s11434-012-5438-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11434-012-5438-y