Abstract
Muscle is a machine that converts metabolic energy into mechanical work by cyclic ATP-driven interactions of the molecular motor, myosin II, with the actin filament. Muscle can also act as a brake, generating a high resistive force with reduced ATP consumption, when the load is increased above the isometric force. To investigate the molecular basis of the braking action of muscle, we used time-resolved X-ray diffraction from intact cells isolated from skeletal muscle of the frog. The results indicate that a stretch of 2–6nm per half-sarcomere imposed on the actively contracting cell induces a rapid attachment to actin of the second motor domain of the myosin molecules that have the first motor domain already attached before the stretch. This mechanism allows skeletal muscle to almost instantaneously resist an external stretch, while minimising the stress on an individual motor.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Brunello E, Reconditi M, Elangovan R, Linari M, Sun YB, Narayanan T, Panine P, Piazzesi G, Irving M, Lombardi V (2007) Skeletal muscle resists stretch by rapid binding of the second motor domain of myosin to actin. Proc Natl Acad Sci U S A 104:20114–20119
Ford LE, Huxley AF, Simmons RM (1981) The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol 311:219–249
Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318
Huxley HE (1969) The mechanism of muscular contraction. Science 164:1356–1365
Huxley HE, Brown W (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol 30:383–434
Huxley AF, Lombardi V (1980) A sensitive force transducer with resonant frequency 50 kHz. J Physiol 305:15–16
Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538
Huxley AF, Lombardi V, Peachey LD (1981) A system for fast recording of longitudinal displacement of a striated muscle fibre. J Physiol 317:12P–13P
Infante AA, Klaupiks D, Davies RE (1964) Adenosine triphosphate: changes in muscles doing negative work. Science 144:1577–1578
Irving M, Piazzesi G, Lucii L, Sun YB, Harford JJ, Dobbie IM, Ferenczi MA, Reconditi M, Lombardi V (2000) Conformation of the myosin motor during force generation in skeletal muscle. Nat Struct Biol 7:482–485
Katz B (1939) The relation between force and speed in muscular contraction. J Physiol 96:45
Kushmerick MJ, Davies RE (1969) The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscles. Appendix. Free energy and enthalpy of atp hydrolysis in the sarcoplasm. Proc R Soc Lond B Biol Sci 174:315–353
Linari M, Woledge RC (1995) Comparison of energy output during ramp and staircase shortening in frog muscle fibres. J Physiol 487(Pt 3):699–710
Linari M, Lucii L, Reconditi M, Casoni ME, Amenitsch H, Bernstorff S, Piazzesi G, Lombardi V (2000) A combined mechanical and X-ray diffraction study of stretch potentiation in single frog muscle fibres. J Physiol 526(Pt 3):589–596
Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–4624
Piazzesi G, Reconditi M, Linari M, Lucii L, Sun YB, Narayanan T, Boesecke P, Lombardi V, Irving M (2002) Mechanism of force generation by myosin heads in skeletal muscle. Nature 415:659–662
Piazzesi G, Reconditi M, Linari M, Lucii L, Bianco P, Brunello E, Decostre V, Stewart A, Gore DB, Irving TC, Irving M, Lombardi V (2007) Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 131:784–795
Reconditi M, Linari M, Lucii L, Stewart A, Sun YB, Boesecke P, Narayanan T, Fischetti RF, Irving T, Piazzesi G, Irving M, Lombardi V (2004) The myosin motor in muscle generates a smaller and slower working stroke at higher load. Nature 428:578–581
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Berlin Heidelberg
About this chapter
Cite this chapter
Fusi, L. et al. (2011). Interference X-ray Diffraction from Single Muscle Cells Reveals the Molecular Basis of Muscle Braking. In: Diaspro, A. (eds) Optical Fluorescence Microscopy. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-15175-0_11
Download citation
DOI: https://doi.org/10.1007/978-3-642-15175-0_11
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-15174-3
Online ISBN: 978-3-642-15175-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)