The mechanisms of the residual force enhancement after stretch of skeletal muscle: Non-uniformity in half-sarcomeres and stiffness of titin

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1739, 2012, Pages 2705-2713

  Rassier, Dilson E ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Cross bridge kinetics; Force enhancement; Sarcomere; Titin

Indexed keywords

CALCIUM; FORCE; GENE; ION; LITERATURE REVIEW; MUSCLE; STEADY-STATE EQUILIBRIUM;

EID: 84862118003     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.0467     Document Type: Review

References (76)

1. Abbot, B. C. & Aubert, X. 1952 The force exerted by active striated muscle during and after change of length. J. Physiol. 117, 77-86.
2. Fenn, W. O. 1924 The relation between the work performed and the energy liberated in muscular contraction. J. Physiol. 58, 373-395.
3. Flitney, F. W. & Hirst, D. G. 1978 Cross-bridge detachment and sarcomere 'give' during stretch of active frog's muscle. J. Physiol. 276, 449-465.
4. Katz, B. 1939 The relation between force and speed in muscular contraction. J. Physiol. 96, 45-64.
5. Abbott, B. C., Aubert, X. M. & Hill, A. V. 1951 The absorption of work by a muscle stretched during a single twitch or a short tetanus. Proc. R. Soc. Lond. B 139, 86-104. (doi:10.1098/rspb.1951.0048)
6. Fenn, W. O. 1923 A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J. Physiol. 58, 175-203.
7. Edman, K. A., Elzinga, G. & Noble, M. I. 1982 Residual force enhancement after stretch of contracting frog single muscle fibers. J. Gen. Physiol. 80, 769-784. (doi:10. 1085/jgp.80.5.769)
8. Edman, K. A. & Tsuchiya, T. 1996 Strain of passive elements during force enhancement by stretch in frog muscle fibres. J. Physiol. 490, 191-205.
9. Julian, F. J. & Morgan, D. L. 1979 The effect on tension of non-uniform distribution of length changes applied to frog muscle fibres. J. Physiol. 293, 379-392.
10. Pun, C., Syed, A. & Rassier, D. E. 2010 Historydependent properties of skeletal muscle myofibrils contracting along the ascending limb of the force-length relationship. Proc. R. Soc. B 277, 475-484. (doi:10. 1098/rspb.2009.1579)
11. Rassier, D. E. & Pavlov, I. 2012 Force produced by isolated sarcomeres and half-sarcomeres after an imposed stretch. Am. J. Physiol. Cell Physiol. 302, C240-C248. (doi:10.1152/ajpcell.00208.2011)
12. Sugi, H. & Tsuchiya, T. 1988 Stiffness changes during enhancement and deficit of isometric force by slow length changes in frog skeletal muscle fibres. J. Physiol. 407, 215-229.
13. Gordon, A. M., Huxley, A. F. & Julian, F. J. 1966 The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. 184, 170-192.
14. Joumaa, V., Leonard, T. R. & Herzog, W. 2008 Residual force enhancement in myofibrils and sarcomeres. Proc. R. Soc. B 275, 1411-1419. (doi:10.1098/rspb.2008.0142)
15. Bagni, M. A., Colombini, B., Colomo, F., Palmini, R. B. & Cecchi, G. 2005 Non cross-bridge stiffness in skeletal muscle fibres at rest and during activity. Adv. Exp. Med. Biol. 565, 141-154. (doi:10.1007/0-387-24990-7_11)
16. Cornachione, A. S. & Rassier, D. E. 2012 A noncross-bridge, static tension is present in permeabilized skeletal muscle fibers after active force inhibition or actin extraction. Am. J. Physiol. Cell Physiol. 302, C566-C574. (doi:10.1152/ajpcell.00355.2011)
17. Labeit, D., Watanabe, K., Witt, C., Fujita, H., Wu, Y., Lahmers, S., Funck, T., Labeit, S. & Granzier, H. 2003 Calcium-dependent molecular spring elements in the giant protein titin. Proc. Natl Acad. Sci. USA 100, 13716-13 721. (doi:10.1073/pnas.2235652100)
18. Telley, I. A., Stehle, R., Ranatunga, K. W., Pfitzer, G., Stussi, E. & Denoth, J. 2006 Dynamic behaviour of half-sarcomeres during and after stretch in activated rabbit psoas myofibrils: sarcomere asymmetry but no 'sarcomere popping'. J. Physiol. 573, 173-185. (doi:10. 1113/jphysiol.2006.105809)
19. Getz, E. B., Cooke, R. & Lehman, S. L. 1998 Phase transition in force during ramp stretches of skeletal muscle. Biophys. J. 75, 2971-2983. (doi:10.1016/S0006-3495 (98)77738-0)
20. Lombardi, V. & Piazzesi, G. 1990 The contractile response during steady lengthening of stimulated frog muscle fibres. J. Physiol. 431, 141-171.
21. Edman, K. A., Elzinga, G. & Noble, M. I. 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, 365-382. (doi:10.1085/jgp.78.4.365)
22. Minozzo, F. C. & Rassier, D. E. 2010 Effects of blebbistatin and Ca2{thorn} concentration on force produced during stretch of skeletal muscle fibers. Am. J. Physiol. Cell Physiol. 299, C1127-C1135. (doi:10.1152/ajpcell. 00073.2010)
23. Pinniger, G. J., Ranatunga, K. W. & Offer, G. W. 2006 Crossbridge and non-crossbridge contributions to tension in lengthening rat muscle: force-induced reversal of the power stroke. J. Physiol. 573, 627-643. (doi:10. 1113/jphysiol.2005.095448)
24. Stienen, G. J., Versteeg, P. G., Papp, Z. & Elzinga, G. 1992 Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2{thorn}. J. Physiol. 451, 503-523.
25. 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.
26. Ranatunga, K. W., Roots, H., Pinniger, G. J. & Offer, G. W. 2010 Crossbridge and non-crossbridge contributions to force in shortening and lengthening muscle. Adv. Exp. Med. Biol. 682, 207-221. (doi:10.1007/978-1-4419-6366-6_12)
27. Edman, K. A., Elzinga, G. & Noble, M. I. 1978 Enhancement of mechanical performance by stretch during tetanic contractions of vertebrate skeletal muscle fibres. J. Physiol. 281, 139-155.
28. Rassier, D. E., Herzog, W. & Pollack, G. H. 2003 Dynamics of individual sarcomeres during and after stretch in activated single myofibrils. Proc. R. Soc. B 270, 1735-1740. (doi:10.1098/rspb.2003.2418)
29. Leonard, T. R., DuVall, M. & Herzog, W. 2010 Force enhancement following stretch in a single sarcomere. Am. J. Physiol. Cell Physiol. 299, C1398-C1401. (doi:10.1152/ajpcell.00222.2010)
30. Edman, K. A. & Reggiani, C. 1984 Absence of plateau of the sarcomere length-tension relation in frog muscle fibres. Acta Physiol. Scand. 122, 213-216. (doi:10.1111/j.1748-1716.1984.tb07502.x)
31. Edman, K. A. & 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.
32. Julian, F. J. & Morgan, D. L. 1979 Intersarcomere dynamics during fixed-end tetanic contractions of frog muscle fibres. J. Physiol. 293, 365-378.
33. Pavlov, I., Novinger, R. & Rassier, D. E. 2009 Sarcomere dynamics in skeletal muscle myofibrils during isometric contractions. J. Biomech. 42, 2808-2812. (doi:10.1016/j.jbiomech.2009.08.011)
34. Telley, I. A., 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. (doi:10.1529/biophysj.105.070334)
35. Gordon, A. M., Huxley, A. F. & Julian, F. J. 1966 Tension development in highly stretched vertebrate muscle fibres. J. Physiol. 184, 143-169.
36. Granzier, H. L. & Pollack, G. H. 1990 The descending limb of the force-sarcomere length relation of the frog revisited. J. Physiol. 421, 595-615.
37. Edman, K. A. & Flitney, F. W. 1982 Laser diffraction studies of sarcomere dynamics during 'isometric' relaxation in isolated muscle fibres of the frog. J. Physiol. 329, 1-20.
38. Stehle, R., Kruger, M. & Pfitzer, G. 2002 Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid Ca(2{thorn}) changes. Biophys. J. 83, 2152-2161. (doi:10.1016/S0006-3495(02)73975-1)
39. Morgan, D. L. 1990 New insights into the behavior of muscle during active lengthening. Biophys. J. 57, 209-221. (doi:10.1016/S0006-3495(90)82524-8)
40. Morgan, D. L. 1994 An explanation for residual increased tension in striated muscle after stretch during contraction. Exp. Physiol. 79, 831-838.
41. Herzog, W. & Leonard, T. R. 2007 Response to the (Morgan and Proske) Letter to the Editor by Walter Herzog (on behalf of the authors) and Tim Leonard. J. Physiol. 578(2), 617-620.
42. Morgan, D. L. & Proske, U. 2006 Sarcomere popping requires stretch over a range where total tension decreases with length. J. Physiol. 574, 627-628. (doi:10.1113/jphysiol.2006.574201)
43. Morgan, D. L. & Proske, U. 2007 Can all residual force enhancement be explained by sarcomere nonuniformities? J. Physiol. 578, 613-615. (doi:10.1113/jphysiol.2006.125039)
44. Brown, L. M. & Hill, L. 1991 Some observations on variations in filament overlap in tetanized muscle fibres and fibres stretched during a tetanus, detected in the electron microscope after rapid fixation. J. Muscle Res. Cell Motil. 12, 171-182. (doi:10.1007/BF01774036)
45. Talbot, J. A. & Morgan, D. L. 1996 Quantitative analysis of sarcomere non-uniformities in active muscle following a stretch. J. Muscle Res. Cell Motil. 17, 261-268. (doi:10. 1007/BF00124247)
46. Pavlov, I., Novinger, R. & Rassier, D. E. 2009 The mechanical behavior of individual sarcomeres of myofibrils isolated from rabbit psoas muscle. Am. J. Physiol. Cell Physiol. 297, C1211-C1219. (doi:10.1152/ajpcell. 00233.2009)
47. Campbell, S.G., Hatfield, P. C. & Campbell, K. S. 2011 A mathematical model of muscle containing heterogeneous half-sarcomeres exhibits residual force enhancement. PLoS Comput. Biol. 7, e1002156. (doi:10.1371/journal. pcbi.1002156)
48. Colomo, F., Lombardi, V. & Piazzesi, G. 1989 The recovery of tension in transients during steady lengthening of frog muscle fibres. Pflugers Arch. 414, 245-247. (doi:10.1007/BF00580970)
49. Linari, M., Lucii, L., Reconditi, M., Casoni, M. E., 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, 589-596. (doi:10.1111/j.1469-7793. 2000.00589.x)
50. Colombini, B., Bagni, M. A., Cecchi, G. & Griffiths, P. J. 2007 Effects of solution tonicity on crossbridge properties and myosin lever arm disposition in intact frog muscle fibres. J. Physiol. 578, 337-346. (doi:10.1113/jphysiol.2006.117770)
51. Colombini, B., Nocella, M., Benelli, G., Cecchi, G. & Bagni, M. A. 2007 Crossbridge properties during force enhancement by slow stretching in single intact frog muscle fibres. J. Physiol. 585, 607-615. (doi:10.1113/jphysiol.2007.141440)
52. Rassier, D. E. 2008 Pre-power stroke cross bridges contribute to force during stretch of skeletal muscle myofibrils. Proc. R. Soc. B 275, 2577-2586. (doi:10. 1098/rspb.2008.0719)
53. 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. (doi:10.1113/jphysiol.2009.178137)
54. Herzog, W., Lee, E. J. & Rassier, D. E. 2006 Residual force enhancement in skeletal muscle. J. Physiol. 574, 635-642. (doi:10.1113/jphysiol.2006.107748)
55. Joumaa, V., Rassier, D. E., Leonard, T. R. & Herzog, W. 2008 The origin of passive force enhancement in skeletal muscle. Am. J. Physiol. Cell Physiol. 294, C74-C78. (doi:10.1152/ajpcell.00218.2007)
56. Neagoe, C., Opitz, C. A., Makarenko, I. & Linke, W. A. 2003 Gigantic variety: expression patterns of titin isoforms in striated muscles and consequences for myofibrillar passive stiffness. J. Muscle Res. Cell Motil. 24, 175-189. (doi:10.1023/A:1026053530766)
57. Bagni, M. A., Cecchi, G., Colombini, B. & Colomo, F. 2002 A non-cross-bridge stiffness in activated frog muscle fibers. Biophys. J. 82, 3118-3127. (doi:10.1016/S0006-3495(02)75653-1)
58. Bagni, M. A., Cecchi, G., Colomo, F. & Garzella, P. 1994 Development of stiffness precedes cross-bridge attachment during the early tension rise in single frog muscle fibres. J. Physiol. 481, 273-278.
59. Bagni, M. A., Colombini, B., Geiger, P., Berlinguer, P. R. & Cecchi, G. 2004 Non-cross-bridge calcium-dependent stiffness in frog muscle fibers. Am. J. Physiol. Cell Physiol. 286, C1353-C1357. (doi:10.1152/ajpcell.00493.2003)
60. Colombini, B., Benelli, G., Nocella, M., Musaro, A., Cecchi, G. & Bagni, M. A. 2009 Mechanical properties of intact single fibres from wild-type and MLC/mIgf-1 transgenic mouse muscle. J. Muscle Res. Cell Motil. 97, 2922-2929.
61. Nocella, M., Colombini, B., Bagni, M. A., 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. (doi:10. 1007/s10974-011-9274-5)
62. Joumaa, V., Rassier, D. E., Leonard, T. R. & Herzog, W. 2007Passive force enhancement in singlemyofibrils. Pflugers Arch. 455, 367-371. (doi:10.1007/s00424-007-0287-2)
63. Rassier, D. E., Lee, E. J. & Herzog, W. 2005 Modulation of passive force in single skeletal muscle fibres. Biol. Lett. 1, 342-345. (doi:10.1098/rsbl.2005.0337)
64. Bang, M. L. et al. 2001 The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 89, 1065-1072. (doi:10.1161/hh2301.100981)
65. Kellermayer, M. S. & Granzier, H. L. 1996 Calciumdependent inhibition of in vitro thin-filament motility by native titin. FEBS Lett. 380, 281-286. (doi:10.1016/0014-5793(96)00055-5)
66. Kellermayer, M. S. & Granzier, H. L. 1996 Elastic properties of single titin molecules made visible through fluorescent F-actin binding. Biochem. Biophys. Res. Commun. 221, 491-497. (doi:10.1006/bbrc.1996.0624)
67. Linke, W. A., Ivemeyer, M., Labeit, S., Hinssen, H., Ruegg, J. C. & Gautel, M. 1997 Actin-titin interaction in cardiac myofibrils: probing a physiological role. Biophys. J. 73, 905-919. (doi:10.1016/S0006-3495(97) 78123-2)
68. Trombitas, K., Greaser, M. L. & Pollack, G. H. 1997 Interaction between titin and thin filaments in intact cardiac muscle. J. Muscle Res. Cell Motil. 18, 345-351. (doi:10.1023/A:1018626210300)
69. Ma, K. & Wang, K. 2003 Malleable conformation of the elastic PEVK segment of titin: non-co-operative interconversion of polyproline II helix, beta-turn and unordered structures. Biochem. J. 374, 687-695. (doi:10.1042/BJ20030702)
70. Kulke, M., Fujita-Becker, S., Rostkova, E., Neagoe, C., Labeit, D., Manstein, D. J., Gautel, M. & Linke, W. A. 2001 Interaction between PEVK-titin and actin filaments: origin of a viscous force component in cardiac myofibrils. Circ. Res. 89, 874-881. (doi:10.1161/hh2201.099453)
71. Linke, W. A., Kulke, M., Li, H., Fujita-Becker, S., Neagoe, C., Manstein, D. J., Gautel, M. & Fernandez, J. M. 2002 PEVK domain of titin: an entropic spring with actin-binding properties. J. Struct. Biol. 137, 194-205. (doi:10.1006/jsbi.2002.4468)
72. Nagy, A., Cacciafesta, P., Grama, L., Kengyel, A., Malnasi-Csizmadia, A. & Kellermayer, M. S. 2004 Differential actin binding along the PEVK domain of skeletal muscle titin. J. Cell Sci. 117, 5781-5789. (doi:10.1242/jcs.01501)
73. Yamasaki, R. et al. 2001 Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys. J. 81, 2297-2313. (doi:10.1016/S0006-3495(01)75876-6)
74. Kato, K. & Kimura, S. 1985 S100ao (alpha alpha) protein is mainly located in the heart and striated muscles. Biochim. Biophys. Acta 842, 146-150. (doi:10. 1016/0304-4165(85)90196-5)
75. Stuyvers, B. D., Miura, M., Jin, J. P. & ter Keurs, H. E. 1998 Ca(2{thorn})-dependence of diastolic properties of cardiac sarcomeres: involvement of titin. Prog. Biophys. Mol. Biol. 69, 425-443. (doi:10.1016/S0079-6107(98) 00018-2)
76. Chandra, M., Mamidi, R., Ford, S., Hidalgo, C., Witt, C., Ottenheijm, C., Labeit, S. & Granzier, H. 2009 Nebulin alters cross-bridge cycling kinetics and increases thin filament activation: a novel mechanism for increasing tension and reducing tension cost. J. Biol. Chem. 284, 30 889-30 896. (doi:10.1074/jbc. M109.049718)