Modulation of Passive (Visco-) Elasticity in Cyclic Stretch-Shortening Experiments of Skeletal Muscle Myofibrils
Keywords:
skeletal muscle, titin, actin, myosin, stretch-shortening cycles, passive properties, stiffness, elastic, visco-elastic, energy loss, hysteresis, muscle properties, cross-bridge theory, sliding filament theory, sarcomere, sarcomere mechanics.Abstract
Titin is the third most abundant protein in sarcomeres and fulfills a number of mechanical and signaling functions. Specifically, titin is responsible for most of the passive forces in sarcomeres and the passive visco-elastic behaviour of myofibrils and muscles. It has been suggested, based on mechanical testing of isolated titin molecules, that titin is an essentially elastic spring if Ig domain un/refolding is prevented either by working at short titin lengths, prior to any unfolding of Ig domains, or at long sarcomere (and titin) lengths when Ig domain un/refolding is effectively prevented. However, these properties of titin, and by extension of muscles, have not been tested with titin in its natural structural environment within a sarcomere. The purpose of this study was to gain insight into the Ig domain un/refolding kinetics and test the idea that titin could behave essentially elastically at any sarcomere length by preventing Ig domain un/refolding during passive stretch-shortening cycles. Although not completely successful, we demonstrate here that titin’s visco-elastic properties appear to depend on the Ig domain un/refolding kinetics and that indeed, titin (and thus myofibrils) can become virtually elastic when Ig domain un/refolding is prevented.
References
1. Wilkie, D. R. Studies in Biology, No. 11, Muscle. 1968. London, Edward Arnold Publishers Ltd.
2. Herzog, W., in Biomechanics of the Musculoskeletal System, Nigg, B. M. and Herzog, W., Eds. John Wiley & Sons Ltd. ed. 2nd , 1999 , p.p. 148-188.
3. Woledge, R. C., Curtin, N. A., and Homsher, E. Energetic aspects of muscle contraction. 245. 1985. London, Academic Press.
4. Wang, K., Mcclure, J., and Tu, A., Proc Natl.Acad.Sci U.S.A 76 (8), 1979
5. Maruyama, K., J Biochem. 80 (2), 1976
6. Maruyama, K., FASEB J. 11 , 1997
7. Duvall, M. M., Gifford, J. L., Amrein, M., and Herzog, W., Eur.Biophys.J. 42 , 2012
8. Joumaa, V., Rassier, D. E., Leonard, T. R., and Herzog, W., Am J Physiol Cell Physiol 294 (1), 2008
9. Labeit, D., Watanabe, K., Witt, C., Fujita, H., Wu, Y., Lahmers, S., Funck, T., Labeit, S., and Granzier, H. L. M., Proc Natl Acad Sci U S A
100 , 2003
10. Astier, C., Raynaud, F., Lebart, M. C., Roustan, C., and Benyamin, Y., FEBS Lett. 429 (1), 1998
11. Kulke, M., Fujita-Becker, S., Rostkova, E., Neagoe, C., Labeit, D., Manstein, D. J., Gautel, M., and Linke, W. A., Circ.Res. 89 (10), 2001
12. Linke, W. A., Kulke, M., Li, H., Fujita-Becker, S., Neagoe, C., Manstein, D. J., Gautel, M., and Fernandez, J. M., Journal of Structural Biology 137 , 2002
13. Nagy, A., Cacciafesta, P., Grama, L., Kengyel, A., Malnasi-Csizmadia, A., and Kellermayer, M. S. Z., J Cell Sci 117 (Pt 24), 2004
14. Herzog, W., Duvall, M., and Leonard, T. R., Exerc.Sport Sci.Rev. 40 (1), 2012
15. Granzier, H. L. M. and Labeit, S., Muscle Nerve 36 (6), 2007
16. Herzog, J. A., Leonard, T. R., Jinha, A., and Herzog, W., J.Biomech. 45 (11), 2012
17. Granzier, H. L. M. and Labeit, S., Exerc Sport Sci Rev 34 (2), 2006
18. Maruyama, K., Kimura, S, Kuroda, M, and Handa, S, J.Biochem 82 , 1977
19. Granzier, H. L. M., Kellermayer, M. S. Z., Helmes, M., and Trombitás, K., Biophys J 73 , 1997
20. Linke, W. A., Popov, V. I., and Pollack, G. H., Biophys J 67 (2), 1994
21. Horowits, R. and Podolsky, R. J., J Cell Biol 105 , 1987
22. Horowits, R., Kempner, E. S., Bisher, M. E., and Podolsky, R., Nature 323 , 1986
23. Joumaa, V., Rassier, D. E., Leonard, T. R., and Herzog, W., Pflügers Arch - Eur J Physiol 455 , 2007
24. Herzog, W. and Leonard, T. R., J Exp Biol 205 , 2002
25. Leonard, T. R. and Herzog, W., Am.J Physiol Cell Physiol 299 , 2010
26. Leonard, T. R., Duvall, M., and Herzog, W., Am J Physiol Cell Physiol 299(6) , 2010
27. Herzog, W., Leonard, T., Joumaa, V., Duvall, M., and Panchangam, A., Mol.Cell Biomech. 9 (3), 2012
28. Rassier, D. E., Herzog, W., and Pollack, G. H., Proc.R.Soc.Lond.B 270 , 2003
29. Kellermayer, M. S. Z., Smith, S. B., Granzier, H. L. M., and Bustamante, C., Science 276 (5315), 1997
30. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M., and Gaub, H. E., Science 276 (5315), 1997
31. Tskhovrebova, L., Trinick, J., Sleep, J. A., and Simmons, R. A., Nature 387 , 1997
32. Kellermayer, M. S., Smith, S. B., Bustamante, C., and Granzier, H. L., J.Struct.Biol. 122 (1-2), 1998
33. Minajeva, A., Neagoe, C., Kulke, M., and Linke, W. A., J Physiol (Lond) 540.1 , 2002
34. Joumaa, V., Leonard, T. R., and Herzog, W., Proc R Soc B 275 , 2008
35. Bartoo, M. L., Linke, W. A., and Pollack, G. H., Am J Physiol 273 , 1997
36. Hinkle, D. F., Wiersma, W., and Jurs, S. G., in Applied Statistics for the Behavioural Sciences Rand McNally College Publishing Co , 1979 , p.p. 332-367.
37. Alexander, R. M. and Bennet-Clark, H. C., Nature 265 , 1977
38. Best, R. B., Fowler, S. B., Herrera, J. L., Steward, A., Paci, E., and Clarke, J., J Mol Biol 330 (4), 2003
39. Best, R. B., Brockwell, D. J., Toca-Herrera, J. L., Blake, A. W., Smith, D. A., Radford, S. E., and Clarke, J., Anal.Chim.Acta 479 , 2003
40. Leonard, T. R., Joumaa, V., and Herzog, W., J.Biomech. 43 (15), 2010
41. Coulis, G., Becila, S., Herrera-Mendez, C. H., Sentandreu, M. A., Raynaud, F., Richard, I., Benyamin, Y., and Ouali, A., Biochemistry (Mosc). 47 (35), 2008
42. Funatsu, T., Higuchi, H., and Ishiwata, S., J Cell Biol 110 (1), 1990
43. Tatsumi, R., Maeda, K., Hattori, A., and Takahashi, K., J Muscle Res Cell Motil 22(2) , 2001
44. Anderson, B. R., Bogomolovas, J., Labeit, S., and Granzier, H. L. M., J.Struct.Biol. 170 , 2010
45. Yamasaki, R., Wu, Y., McNabb, M., Greaser, M., Labeit, S., and Granzier, H. L. M., Circ.Res. 90 (11), 2002
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