Abstract
Stretching of active muscles leads to a great enhancement of the force developed without increased ATP consumption. The mechanism of force enhancement is still debated and it is not clear if it is due to increased crossbridge strain or to a stretch-induced increase in crossbridge number. The present study, performed on single fibres from tibialis anterior or interosseus muscles of the frog at 5 °C, was aimed at clarifying this point. A striation follower device was used to measure sarcomere length changes. Force was measured during the application of stretches (0.15–3.9 ms duration, 3–7.8 nm per half-sarcomere amplitude) to activated fibres. Small 4 kHz sinusoidal length oscillations, superimposed on the stretches, were used to calculate fibre stiffness with high time resolution. Stiffness increased during the stretch then subsequently decayed, all in parallel with tension. Likewise, during quick releases, stiffness decreased during the release then subsequently recovered in parallel with tension. Comparison of tension and stiffness both during the tetanus rise and also during stretches which doubled tension, imposed on the tetanus rise, indicated that stretch-induced crossbridge recruitment was only about 11 %, suggesting that force enhancement by stretching is mainly due to an increase of individual crossbridge force, whereas crossbridge recruitment plays only a minor role. The accompanying stiffness changes can be explained by non-linearity of myofilament compliance.
Similar content being viewed by others
References
Abbott BC, Aubert XM (1952) The force exerted by active striated muscle during and after change of length. J Physiol 117:77–86
Bagni MA, Cecchi G, Colomo F, Tesi C (1988) Plateau and descending limb of the sarcomere length-tension relation in short length-clamped segments of frog muscle fibres. J Physiol 401:581–595
Bagni MA, Cecchi G, Colomo F, Poggesi C (1990) Tension and stiffness of frog muscle fibres at full filament overlap. J Muscle Res Cell Motil 11:371–377
Bagni MA, Cecchi G, Colombini B, Colomo F (1999) Sarcomere tension-stiffness relation during the tetanus rise in single frog muscle fibres. J Muscle Res Cell Motil 20:469–476
Bagni MA, Cecchi G, Colombini B, Colomo F (2002) A non-cross-bridge stiffness in activated frog muscle fibers. Biophys J 82:3118–3127
Bagni MA, Colombini B, Geiger P, Berlinguer Palmini R, Cecchi G (2004) Non-cross-bridge calcium-dependent stiffness in frog muscle fibers. Am J Physiol Cell Physiol 286:C1353–C1357
Bagni MA, Cecchi G, Colombini B (2005) Crossbridge properties investigated by fast ramp stretching of activated frog muscle fibres. J Physiol 565:261–268
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 USA 104:20114–20119
Cavagna GA (1993) Effect of temperature and velocity of stretching on stress relaxation of contracting frog muscle fibres. J Physiol 462:161–173
Cavagna GA, Citterio G (1974) Effect of stretching on the elastic characteristics and the contractile component of frog striated muscle. J Physiol 239:1–14
Cecchi G, Griffiths PJ, Taylor S (1982) Muscular contraction: kinetics of crossbridge attachment studied by high-frequency stiffness measurements. Science 217:70–72
Cecchi G, Griffiths PJ, Taylor S (1986) Stiffness and force in activated frog skeletal muscle fibers. Biophys J 49:437–451
Cecchi G, Colomo F, Lombardi V, Piazzesi G (1987) Stiffness of frog muscle fibres during rise of tension and relaxation in fixed-end or length-clamped tetani. Pflugers Arch 409:39–46
Chakrabarty T, Xiao M, Cooke R, Selvin PR (2002) Holding two heads together: stability of the myosin II rod measured by resonance energy transfer between the heads. Proc Natl Acad Sci USA 99:6011–6016
Colombini B, Benelli G, Nocella M, Musarò A, Cecchi G, Bagni MA (2009a) Mechanical properties of intact single fibres from wild-type and MLC/mIGF-1 transgenic mouse muscle. J Muscle Res Cell Motil 30:199–207
Colombini B, Nocella M, Benelli G, Cecchi G, Griffiths PJ, Bagni MA (2009b) Reversal of the myosin power stroke induced by fast stretching of intact skeletal muscle fibers. Biophys J 97:2922–2929
Colombini B, Nocella M, Bagni MA, Griffiths PJ, Cecchi G (2010a) Is the cross-bridge stiffness proportional to tension during muscle fiber activation? Biophys J 98:2582–2590
Colombini B, Nocella M, Benelli G, Cecchi G, Bagni MA (2010b) Crossbridge properties during force enhancement by slow stretching in single intact frog muscle fibres. J Physiol 585:607–615
Curtin NA, Davies RE (1973) Chemical and mechanical changes during stretching of activated frog skeletal muscle. Cold Spring Harbor Symp Quant Biol 37:619–626
Edman KA (2009) Non-linear myofilament elasticity in frog intact muscle fibres. J Exp Biol 212:1115–1119
Edman KA, Elzinga G, Noble MIM (1978) Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J Physiol 281:139–155
Ford LE, Huxley AF, Simmons RM (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol 269:441–515
Fusi L, Reconditi M, Linari M, Brunello E, Elangovan R, Lombardi V, Piazzesi G (2010) The mechanism of the resistance to stretch of isometrically contracting single muscle fibres. J Physiol 588:495–510
Getz EB, Cooke R, Lehman SL (1998) Phase transition in force during ramp stretches of skeletal muscle. Biophys J 75:2971–2983
Higuchi H, Yanagida T, Goldman YE (1995) Compliance of thin filaments in skinned fibers of rabbit skeletal muscle. Biophys J 69:1000–1010
Hill AV, Howarth JV (1959) The reversal of chemical reactions in contracting muscle during an applied stretch. Proc R Soc Lond B Biol Sci 151:169–193
Irving T, Wu Y, Bekyarova T, Farman GP, Fukuda N, Granzier H (2011) Thick-filament strain and interfilament spacing in passive muscle: effect of titin-based passive tension. Biophys J 100:1499–1508
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
Julian FJ, Morgan DL (1981) Variation of muscle stiffness with tension during tension transients and constant velocity shortening in the frog. J Physiol 319:193–203
Katz B (1939) The relation between force and speed in muscular contraction. J Physiol 96:45–64
Kaya M, Higuchi H (2010) Nonlinear elasticity and an 8-nm working stroke of single myosin molecules in myofilaments. Science 329(5992):686–689
Linari M, Woledge RC, Curtin NA (2003) Energy storage during stretch of active single fibres from frog skeletal muscle. J Physiol 548:461–474
Loiselle DS, Tran K, Crampin EJ, Curtin NA (2010) Why has reversal of the actin-myosin cross-bridge cycle not been observed experimentally? J Appl Physiol 108:1465–1471
Lombardi V, Piazzesi G (1990) The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol 431:141–171
Månsson A (1993) Tension transients in skeletal muscle fibres of the frog at varied tonicity of the extracellular medium. J Muscle Res Cell Motil 14:15–25
Månsson A (2010a) Actomyosin-ADP states, interhead cooperativity, and the force-velocity relation of skeletal muscle. Biophys J 98:1237–1246
Månsson A (2010b) Significant impact on muscle mechanics of small nonlinearities in myofilament elasticity. Biophys J 99:1869–1875
Nocella M, Colombini B, Benelli G, Cecchi G, Bagni MA, Bruton J (2011) Force decline during fatigue is due to both a decrease in the force per individual cross-bridge and the number of cross-bridges. J Physiol 589:3371–3381
Nocella M, Colombini B, Bagni MA, Bruton J, Cecchi G (2012) Non-crossbridge calcium-dependent stiffness in slow and fast skeletal fibres from mouse muscle. J Muscle Res Cell Motil 32:403–409
Offer G, Ranatunga KW (2010) Crossbridge and filament compliance in muscle: implications for tension generation and lever arm swing. J Muscle Res Cell Motil 31:245–265
Piazzesi G, Linari M, Reconditi M, Vanzi F, Lombardi V (1997) Cross-bridge detachment and attachment following a step stretch imposed on active single frog muscle fibres. J Physiol 498:3–15
Podolsky RJ, Naylor GRS, Arata T (1982) Cross-bridge properties in the rigor state. In: Twarog BM, Levine RJC, Dewey MM (eds) Basic biology of muscles: a comparative approach. Raven, New York
Reconditi M (2010) There is no experimental evidence for non-linear myofilament elasticity in skeletal muscle. J Exp Biol 213:658–659
Stienen GJM, Versteeg PGA, Papp Z, Elzinga G (1992) Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2+. J Physiol 451:503–523
Sugi H (1972) Tension changes during and after stretch in frog muscle fibres. J Physiol 225:237–253
van der Heide U, Ketelaars M, Treijtel BW, de Beer EL, Blangé T (1997) Strain dependence of the elastic properties of force-producing cross-bridges in rigor skeletal muscle. Biophys J 72:814–821
Acknowledgments
This study was supported by the Università di Firenze, Ministero della Ricerca Scientifica (PRIN) and Ente Cassa di Risparmio di Firenze CRF 2010.0256 and CRF 2011.0302.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nocella, M., Bagni, M.A., Cecchi, G. et al. Mechanism of force enhancement during stretching of skeletal muscle fibres investigated by high time-resolved stiffness measurements. J Muscle Res Cell Motil 34, 71–81 (2013). https://doi.org/10.1007/s10974-012-9335-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10974-012-9335-4