Interactions between connected half-sarcomeres produce emergent mechanical behavior in a mathematical model of muscle

PLoS Computational Biology

Volumn 5, Issue 11, 2009, Pages

  Campbell, Kenneth S ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; FIBERS; MAMMALS;

A.FIBRES; CA 2+; CONDITION; FORCE RESPONSE; MAMMALIAN MUSCLES; MECHANICAL BEHAVIOR; MECHANICAL COMPONENTS; MUSCLE FIBER; MYOFIBRILS; PROPERTY;

MUSCLE;

CONNECTIN; DESMIN; ACTIN; MYOSIN;

ANIMAL EXPERIMENT; ARTICLE; CELL ISOLATION; CELL MEMBRANE PERMEABILITY; COMPUTER MODEL; COMPUTER SIMULATION; CONTROLLED STUDY; ENERGY ABSORPTION; MATHEMATICAL MODEL; MECHANICS; MOUSE; MUSCLE; MUSCLE CELL; MUSCLE FIBRIL; MUSCLE ISOMETRIC CONTRACTION; MUSCLE STRETCHING; NONHUMAN; PSOAS MUSCLE; QUANTITATIVE ANALYSIS; SARCOMERE; THEORY; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; MECHANICAL STRESS; METHODOLOGY; NONLINEAR SYSTEM; PHYSIOLOGY; RABBIT; STATISTICAL MODEL; SYSTEMS BIOLOGY;

MAMMALIA; MUS; ORYCTOLAGUS CUNICULUS;

ACTINS; ANIMALS; BIOMECHANICS; COMPUTER SIMULATION; LINEAR MODELS; MODELS, BIOLOGICAL; MYOFIBRILS; MYOSINS; NONLINEAR DYNAMICS; PSOAS MUSCLES; RABBITS; SARCOMERES; STRESS, MECHANICAL; SYSTEMS BIOLOGY;

EID: 73449088381     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000560     Document Type: Article

References (47)

1. Noble D (2006) The music of life : biology beyond the genome. Oxford: Oxford University Press.
2. Stoecker U, Telley IA, Stussi E, Denoth J (2009) A multisegmental cross-bridge kinetics model of the myofibril. J Theor Biol 259: 714-726.
3. Huxley AF (1957) Muscle structure and theories of contraction. Prog in Biophys and Biophys Chem 7: 255-318.
4. Huxley AF, Tideswell S (1996) Filament compliance and tension transients in muscle. J Muscle Res Cell Motil 17: 507-511.
5. Huxley AF, Tideswell S (1997) Rapid regeneration of power stroke in contracting muscle by attachment of second myosin head. J Muscle Res Cell Motil 18: 111-114.
6. Tskhovrebova L, Trinick J (2003) Titin: properties and family relationships. Nat Rev Mol Cell Biol 4: 679-689.
7. Campbell KS, Moss RL (2000) A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch. J Physiol 525.2: 531-548.
8. del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, et al. (2009) Stretching single talin rod molecules activates vinculin binding. Science 323: 638-641.
9. Labeit D, Watanabe K, Witt C, Fujita H, Wu Y, et al. (2003) Calcium-dependent molecular spring elements in the giant protein titin. Proc Natl Acad Sci USA 100: 13716-13721.
10. Edman KA, Tsuchiya T (1996) Strain of passive elements during force enhancement by stretch in frog muscle fibres. J Physiol 490(Pt 1): 191-205.
11. Getz EB, Cooke R, Lehman SL (1998) Phase transition in force during ramp stretches of skeletal muscle. Biophys J 75: 2971-2983.
12. Morgan DL (1990) New insights into the behavior of muscle during active lengthening. Biophys J 57(2): 209-221.
13. Sam M, Shah S, Fridén J, Milner DJ, Capetanaki Y, et al. (2000) Desmin knockout muscles generate lower stress and are less vulnerable to injury compared with wild-type muscles. Am J Physiol, Cell Physiol 279: C1116-C1122.
14. Campbell KS, Moss RL (2002) History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J 82: 929-943.
15. Lombardi V, Piazzesi G (1990) The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol 431: 141-171.
16. Horiuti K, Higuchi H, Umazume Y, Konishi M, Okazaki O, et al. (1988) Mechanism of action of 2,3-butanedione 2-monoxime on contraction of frog skeletal muscle fibres. J Muscle Res Cell Motil 9: 156-164.
17. Limouze J, Straight AF, Mitchison T, Sellers JR (2004) Specificity of blebbistatin, an inhibitor of myosin II. J Muscle Res Cell Motil 25: 337-341.
18. Swartz DR, Moss RL, Greaser ML (1997) Characteristics of Troponin C binding to the myofibrillar thin filament: Extraction of Troponin C is not random along the length of the thin filament. Biophys J 73: 293-305.
19. Pavlov I, Novinger R, Rassier DE (2009) The mechanical behavior of individual sarcomeres of myofibrils isolated from rabbit psoas muscle. Am J Physiol, Cell Physiol.
20. Julian FJ, Morgan DL (1979) The effect on tension of non-uniform distribution of length changes applied to frog muscle fibres. J Physiol 293: 379-392.
21. Julian FJ, Morgan DL (1979) Intersarcomere dynamics during fixed-end tetanic contractions of frog muscle fibres. J Physiol 293: 365-378.
22. Edman KA, Reggiani C (1984) Redistribution of sarcomere length during isometric contraction of frog muscle fibres and its relation to tension creep. J Physiol 351: 169-198.
23. Telley IA, Denoth J, Stussi E, Pfitzer G, Stehle R (2006) Half-sarcomere dynamics in myofibrils during activation and relaxation studied by tracking fluorescent markers. Biophys J 90: 514-530.
24. Rassier DE, Herzog W, Pollack GH (2003) Dynamics of individual sarcomeres during and after stretch in activated single myofibrils. Proc Biol Sci 270: 1735-1740.
25. Shimamoto Y, Suzuki M, Mikhailenko SV, Yasuda K, Ishiwata S (2009) Intersarcomere coordination in muscle revealed through individual sarcomere response to quick stretch. Proc Natl Acad Sci USA.
26. Edman KA, Elzinga G, Noble MI (1982) Residual force enhancement after stretch of contracting frog single muscle fibers. J Gen Physiol 80: 769-784.
27. Huxley AF, Lombardi V, Peachey LD (1981) A system for fast recording of longitudinal displacement of a striated muscle fiber. J Physiol 317: 12-13P.
28. Campbell KS, Moss RL (2003) SLControl: PC-based data acquisition and analysis for muscle mechanics. Am J Physiol Heart Circ Physiol 285: H2857-H2864.
29. McLoon LK, Rios L, Wirtschafter JD (1999) Complex three-dimensional patterns of myosin isoform expression: differences between and within specific extraocular muscles. J Muscle Res Cell Motil 20: 771-783.
30. Huxley AF, Peachey LD (1961) The maximum length for contraction in vertebrate striated muscle. J Physiol 156: 150-165.
31. Huxley AF (1974) Review Lecture - Muscular Contraction. J Physiol 243: 1-43.
32. Blake DJ, Weir A, Newey SE, Davies KE (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 82: 291-329.
33. Balogh J, Li Z, Paulin D, Arner A (2005) Desmin filaments influence myofilament spacing and lateral compliance of slow skeletal muscle fibers. Biophys J 88: 1156-1165.
34. Mitov MI, Holbrook AM, Campbell KS (2009) Myocardial short-range force responses increase with age in F344 rats. J Mol Cell Cardiol 46: 39-46.
35. Campbell KS, Lakie M (1998) A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol 510.3: 941-962.
36. Linari M, Caremani M, Piperio C, Brandt P, Lombardi V (2007) Stiffness and fraction of myosin motors responsible for active force in permeabilized muscle fibers from rabbit psoas. Biophys J 92: 2476-2490.
37. Lewalle A, Steffen W, Stevenson O, Ouyang Z, Sleep J (2008) Single-molecule measurement of the stiffness of the rigor myosin head. Biophys J 94: 2160-2169.
38. Pate E, Cooke R (1989) A model of crossbridge action: the effects of ATP, ADP and Pi. J Muscle Res Cell Motil 10: 181-196.
39. Huxley HE, Stewart A, Sosa H, Irving T (1994) X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J 67: 2411-2421.
40. Wakabayashi K, Sugimoto Y, Tanaka H, Ueno Y, Takezawa Y, et al. (1994) Xray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67: 2422-2435.
41. Daniel TL, Trimble AC, Chase PB (1998) Compliant realignment of binding sites in muscle: Transient behavior and mechanical tuning. Biophys J 74: 1611-1621.
42. Tanner BCW, Danser AH, Regnier M (2007) Sarcomere lattice geometry influences cooperative myosin binding in muscle. PLoS Computat Biol 3: e115.
43. Mijailovich SM, Fredberg JJ, Butler JP (1996) On the theory of muscle contraction: filament extensibility and the development of isometric force and stiffness. Biophys J 71: 1475-1484.
44. Campbell KS (2006) Filament compliance effects can explain tension overshoots during force development. Biophys J 91: 4102-4109.
45. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical Recipes in C - The Art of Scientific Computing. Cambridge: Cambridge University Press.
46. Matsumoto M, Nishimura T (1998) Mersenne Twister: A 623-dimensionally equidistributed uniform pseudorandom number generator. TOMACS 8: 3-30.
47. Kennedy JF, Eberhart RC, Shi Y (2001) Swarm intelligence. San Francisco; London: Morgan Kaufmann Publishers. 512 p.