Short-Range Mechanical Properties of Skeletal and Cardiac Muscles

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 682)

Abstract

Striated muscles are disproportionately stiff for small movements. This facet of their behavior can be demonstrated by measuring the force produced when the muscle is stretched more than about 1% of its initial length. When this is done, it can be seen that force rises rapidly during the initial phases of the movement and much less rapidly during the latter stages of the stretch. Experiments performed using chemically permeabilized skeletal and cardiac muscles show that the initial stiffness of the preparations increases in proportion with isometric force as the free Ca2+ concentration in the bathing solution is raised from a minimal to a saturating value. This is strong evidence that the short-range mechanical properties of activated muscle result from stretching myosin cross-bridges that are attached between the thick and thin filaments. Relaxed intact muscles also exhibit short-range mechanical properties but the molecular mechanisms underlying this behavior are less clear. This chapter summarizes some of the interesting features of short-range mechanical properties in different types of muscle preparation, describes some of the likely underlying mechanisms and discusses the potential physiological significance of the behavior.

Keywords

Muscle stiffness Muscle mechanics Myosin SREC 

Notes

Acknowledgements

This work was supported by American Heart Association Scientist Development Grant 0630079N, NIH AG021862, NIH HL090749 and the University of Kentucky Research Challenge Trust Fund.

References

  1. Allinger TL, Epstein M, Herzog W (1996) Stability of muscle fibers on the descending limb of the force-length relation. A theoretical consideration. J Biomech 29:627–633PubMedCrossRefGoogle Scholar
  2. Axelson HW, Hagbarth KE (2001) Human motor control consequences of thixotropic changes in muscular short-range stiffness. J Physiol 535(1):279–288PubMedCrossRefGoogle Scholar
  3. Axelson HW, Hagbarth KE (2003) Human motor compensations for thixotropy-dependent changes in resting wrist joint position after large joint movements. Acta Physiol Scand 179:389–398PubMedCrossRefGoogle Scholar
  4. Bagni MA, Cecchi G, Colombini B, Colomo F (2002) A non-cross-bridge stiffness in activated frog muscle fibers. Biophys J 82:3118–3127PubMedCrossRefGoogle Scholar
  5. Bagni MA, Colombini B, Geiger P, Berlinguer Palmini R, Cecchi G (2004) A non cross-bridge calcium-dependent stiffness in frog muscle fibers. Am J Physiol Cell Physiol 286:C1353–C1357PubMedCrossRefGoogle Scholar
  6. Bers DM (1991) Excitation-contraction coupling and cardiac contractile force. Kluwer, DordrechtGoogle Scholar
  7. Bianco P, Nagy A, Kengyel A, Szatmári D, Mártonfalvi Z, Huber T, Kellermayer MSZ (2007) Interaction forces between F-actin and titin PEVK domain measured with optical tweezers. Biophys J 93:2102–2109PubMedCrossRefGoogle Scholar
  8. Blair GWS (1969) Elementary rheology, Academic, LondonGoogle Scholar
  9. Brenner B (1988) Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: Implications for regulation of muscle contraction. Proc Natl Acad Sci USA 85:3265–3269PubMedCrossRefGoogle Scholar
  10. Buchthal F, Kaiser E (1951) The rheology of the cross striated muscle fibre with particular reference to isotonic conditions. Vol. 21.7. Det Kongelige Danske Videnskabernes Selskab Biologiske Meddelser, CopenhagenGoogle Scholar
  11. Campbell KS (2006) Filament compliance effects can explain tension overshoots during force development. Biophys J 91:4102–4109PubMedCrossRefGoogle Scholar
  12. Campbell KS (2009) Short-range mechanical properties simulated with a mechanical mdoel incorporating multiple half-sarcomeres. Biophys J 96:615aCrossRefGoogle Scholar
  13. Campbell KS, Holbrook AM (2006) Myocardial stiffness in experimental conditions that mimic ischemia. Biophys J 90:1270ACrossRefGoogle Scholar
  14. Campbell KS, Lakie M (1995) Tension responses to imposed length changes in isolated relaxed muscle fibre bundles from Rana temporaria. J Physiol 487:155–156PGoogle Scholar
  15. Campbell KS, Lakie M (1998) A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol 510.3:941–962PubMedCrossRefGoogle Scholar
  16. Campbell KS, Lakie M (2008) Response to Bianco et al.: Interaction forces between F-actin and titin PEVK domain measured with optical tweezers. Biophys J 94:327–328; 329–330PubMedCrossRefGoogle Scholar
  17. 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):531–548PubMedCrossRefGoogle Scholar
  18. Campbell KS, Moss RL (2002) History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J 82:929–943PubMedCrossRefGoogle Scholar
  19. Campbell KS, Moss RL (2003) SLControl: PC-based data acquisition and analysis for muscle mechanics. Am J Physiol Heart Circ Physiol 285:H2857–H2864PubMedGoogle Scholar
  20. Campbell KS, Patel JR, Moss RL (2003) Cycling cross-bridges increase myocardial stiffness at sub-maximal levels of Ca2+ activation. Biophys J 84:3807–3815PubMedCrossRefGoogle Scholar
  21. Carnes CA, Geisbuhler TP, Reiser PJ (2004) Age-dependent changes in contraction and regional myocardial myosin heavy chain isoform expression in rats. J Appl Physiol 97:446–453PubMedCrossRefGoogle Scholar
  22. Denny-Brown D (1929) On the nature of postural reflexes. Proc R Soc Lond B Biol Sci 104:252–301CrossRefGoogle Scholar
  23. Edman KA, Elzinga G, Noble MI (1981) Critical sarcomere extension required to recruit a decaying component of extra force during stretch in tetanic contractions of frog skeletal muscle fibers. J Gen Physiol 78:365–382PubMedCrossRefGoogle Scholar
  24. Endo M (1973) Length dependence of activation of skinned muscle fibres by calcium. Cold Spring Harb Symp Quant Biol 37:505–510CrossRefGoogle Scholar
  25. Farman GP, Tachampa K, Mateja R, Cazorla O, Lacampagne A, de Tombe PP (2008) Blebbistatin: use as inhibitor of muscle contraction. Pflugers Arch 455:995–1005PubMedCrossRefGoogle Scholar
  26. Feng TP (1932) The thermo-elastic properties of muscle. J Physiol 74:455–470PubMedGoogle Scholar
  27. Ford LE, Huxley AF, Simmons RM (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol 269:441–515PubMedGoogle Scholar
  28. Fujita H, Labeit D, Gerull B, Labeit S, Granzier HL (2004) Titin isoform-dependent effect of calcium on passive myocardial tension. Am J Physiol Heart Circ Physiol 287:H2528–H2534PubMedCrossRefGoogle Scholar
  29. Gao WD, Backx PH, Azan-Backz M, Marban E (1994) Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle. Circ Res 74:408–415PubMedCrossRefGoogle Scholar
  30. Getz EB, Cooke R, Lehman SL (1998) Phase transition in force during ramp stretches of skeletal muscle. Biophys J 75:2971–2983PubMedCrossRefGoogle Scholar
  31. Granzier HL, Irving TC (1995) Passive tension in cardiac muscles: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68:1027–1044PubMedCrossRefGoogle Scholar
  32. Granzier H, Labeit S (2002) Cardiac titin: an adjustable multi-functional spring. J Physiol 541:335–342PubMedCrossRefGoogle Scholar
  33. Gunst SJ (1983) Contractile force of canine airway smooth muscle during cyclical length changes. J Appl Physiol 55:759–769PubMedGoogle Scholar
  34. Harris J (1977) Rheology and non-Newtonian flow. Longman, London and New YorkGoogle Scholar
  35. Harris SP, Shaffer JF, Bezold KL, Kensler RW (2009) Switching gears with myosin binding protein-C. Biophys J 96:4ACrossRefGoogle Scholar
  36. Haugen P, Sten-Knudsen O (1981) The dependence of the short-range elasticity on sarcomere length in resting isolated frog muscle fibres. Acta Physiol Scand 112:113–120PubMedCrossRefGoogle Scholar
  37. Herbst M (1976) Studies on the relation between latency relaxation and resting cross-bridges of frog skeletal muscle. Pflugers Arch 364:71–76PubMedCrossRefGoogle Scholar
  38. Hill AV (1965) Trails and trials in physiology. Edward Arnold, LondonGoogle Scholar
  39. Hill DK (1968) Tension due to interaction between the sliding filaments in resting striated muscle. The effect of stimulation. J Physiol 199:637–684PubMedGoogle Scholar
  40. 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 67:2411–2421PubMedCrossRefGoogle Scholar
  41. Kellermayer MS, Bianco P, Martonfalvi Z, Nagy A, Kengyel A, Szatmari D, Huber T, Linari M, Caremani M, Lombardi V (2008) Muscle thixotropy: more than just cross-bridges? Biophys J 94:329–330CrossRefGoogle Scholar
  42. King NMP, Helmes M, Granzier H (2009) A direct method to measure the restoring force and slack sarcomere length of intact cardiomyocytes. Biophys J 96:498aCrossRefGoogle Scholar
  43. Lakie M, Walsh EG, Wright GW (1984) Resonance at the wrist demonstrated by the use of a torque motor: an instrumental analysis of muscle tone in man. J Physiol 353:265–285PubMedGoogle Scholar
  44. Liddell EGT, Sherrington C (1924) Reflexes in response to stretch (myotatic reflexes). Proc R Soc Lond B Biol Sci 96:212–242CrossRefGoogle Scholar
  45. Lombardi V, Piazzesi G (1990) The contractile response during steady lengthening of stimulated frog muscle fibres. J Physiol 431:141–171PubMedGoogle Scholar
  46. Loram ID, Maganaris CN, Lakie M (2007) The passive, human calf muscles in relation to standing: the short range stiffness lies in the contractile component. J Physiol 584:677–692PubMedCrossRefGoogle Scholar
  47. Meiss RA (1987) Stiffness of active smooth muscle during forced elongation. Am J Physiol Cell Physiol 253:C484–C493Google Scholar
  48. Mitov MI, Holbrook AM, Campbell KS (2009) Myocardial short-range force responses increase with age in F344 rats. J Mol Cell Cardiol 46:39–46PubMedCrossRefGoogle Scholar
  49. Morgan DL (1990) New insights into the behavior of muscle during active lengthening. Biophys J 57:209–221PubMedCrossRefGoogle Scholar
  50. Mutungi G, Ranatunga KW (1996) The viscous, viscoelastic and elastic characteristics of resting fast and slow mammalian (rat) muscle fibres. J Physiol 496.3:827–836PubMedGoogle Scholar
  51. Mutungi G, Ranatunga KW (2000) Do cross-bridges contribute to the tension response during stretch of passive muscle? A response. J Muscle Res Cell Motil 21:301–302PubMedCrossRefGoogle Scholar
  52. Proske U, Morgan DL (1999) Do cross-bridges contribute to the tension during stretch of passive muscle? J Muscle Res Cell Motil 20:433–442PubMedCrossRefGoogle Scholar
  53. Proske U, Morgan DL, Gregory JE (1993) Thixotropy in skeletal muscle and in muscle spindles: a review. Prog Neurobiol 41:705–721PubMedCrossRefGoogle Scholar
  54. Rack PMH, Westbury DR (1974) The short range stiffness of active mammalian muscle and its effect on mechanical properties. J Physiol 240:331–350PubMedGoogle Scholar
  55. Sandow A (1970) Skeletal muscle. Ann Rev Physiol 32:87–138CrossRefGoogle Scholar
  56. Stienen GJ, Versteeg PG, Papp Z, Elzinga G (1992) Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2+. J Physiol 451:503–523PubMedGoogle Scholar
  57. Tikunov BA, Sweeney HL, Rome LC (2001) Quantitative electrophoretic analysis of myosin heavy chains in single muscle fibers. J Appl Physiol 90:1927–1935PubMedGoogle Scholar
  58. Vieth E (1989) Fitting piecewise linear regression functions to biological responses. J Appl Physiol 67:390–396PubMedGoogle Scholar
  59. Wakabayashi K, Sugimoto Y, Tanaka H, Ueno Y, Takezawa Y, Amemiya Y (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67:2422–2435PubMedCrossRefGoogle Scholar
  60. Wu Y, Cazorla O, Labeit D, Labeit S, Granzier H (2000) Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J Mol Cell Cardiol 32:2151–2162PubMedCrossRefGoogle Scholar
  61. Zahalak GI (1997) Can muscle fibers be stable on the descending limbs of their sarcomere length-tension relations? J Biomech 30:1179–1182PubMedCrossRefGoogle Scholar
  62. Zile MR, Baicu CF, Gaasch WH (2004) Diastolic heart failure – abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 350:1953–1959PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Physiology & Center for Muscle BiologyUniversity of KentuckyLexingtonUSA

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