Is titin a 'winding filament'? A new twist on muscle contraction

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1730, 2012, Pages 981-990

  Nishikawa, Kiisa C ^a   Monroy, Jenna A ^a   Uyeno, Theodore E ^b   Yeo, Sang Hoon ^c   Pai, Dinesh K ^c   Lindstedt, Stan L ^a  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

^b VALDOSTA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Connectin; Force depression; Force enhancement; History dependence of force production; Thin filament rotation; Titin actin interactions

Indexed keywords

CALCIUM; CATION; MUSCLE; POTENTIAL ENERGY; PROTEIN; SKELETON; STIFFNESS;

EID: 84856295953     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1304     Document Type: Article

References (78)

1. Huxley, A. F. & Niedergerke, R. 1954 Structural changes in muscle during contraction. Nature, 173, 971-973. (doi:10.1038/173971a0)
2. Huxley, H. & Hanson, J. 1954 Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature, 173, 973-976. (doi:10. 1038/173973a0)
3. Huxley, A. F. 2000 Mechanics and models of the myosin motor. Phil. Trans. R. Soc. Lond. B, 355, 433-440. (doi:10.1098/rstb.2000.0584)
4. Huxley, H. E. 2000 Past, present and future experiments on muscle. Phil. Trans. R. Soc. Lond. B, 355, 539-543. (doi:10.1098/rstb.2000.0595)
5. Herzog, W., Leonard, T. R., Joumaa, V. & Mehta, A. 2008 Mysteries of muscle contraction. J. Appl. Biomech., 24, 1-13.
6. Abbott, B. C. & Aubert, X. M. 1952 The force exerted by active striated muscle during and after change of length. J. Physiol., 117, 77-86.
7. Bigland-Ritchie, B. & Woods, J. J. 1976 Integrated electromyogram and oxygen uptake during positive and negative work. J. Physiol., (Lond.) 260, 267-277.
8. Kushmerick, M. J. & Davies, R. E. 1969 The chemical energetics of muscle contraction. II. The chemistry, efficiency and power of maximally working sartorius muscle. Proc. R. Soc. Lond. B, 174, 315-353. (doi:10.1098/rspb.1969.0096)
9. Julian, F. J. & Morgan, D. L. 1979 The effects of tension on non-uniform distribution of length changes applied to frog muscle fibres. J. Physiol., (Lond.) 293, 379-392.
10. Morgan, R. S. 1977 Actin rotates as myosin translates. J. Theor. Biol., 76, 769-771. (doi:10.1016/0022-5193 (77)90261-2)
11. Maruyama, K. 1976 Connectin, an elastic protein from myofibrils. J. Biochem., 80, 405-407.
12. Wang, K., McClure, J. & Tu, A. 1979 Titin: major myofibrillar components of striated muscle. Proc. Natl Acad. Sci. USA, 76, 3698-3702. (doi:10.1073/pnas.76.8.3698)
13. Horowitz, R. & Podolsky, R. J. 1987 The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: evidence for the role of titin filaments. J. Cell Biol., 105, 2217-2223. (doi:10. 1083/jcb.105.5.2217)
14. Linke, W. A., Ivemeyer, M., Mundel, P., Stockmeier, M. R. & Kolmerer, B. 1998 Nature of PEVK-titin elasticity in skeletal muscle. Proc. Natl Acad. Sci. USA, 95, 8052-8057. (doi:10.1073/pnas.95.14.8052)
15. Gregorio, C. C., Granzier, H., Sorimachi, H. & Labeit, S. 1999 Muscle assembly: a titanic achievement. Curr. Opin. Cell Biol., 11, 18-25. (doi:10.1016/S0955-0674 (99)80003-9)
16. Krüger, M. & Linke, W. A. 2011 The giant protein titin: a regulatory node that integrates myocyte signalling pathways. J. Biol. Chem., 286, 9905-9912. (doi:10.1074/jbc. R110.173260)
17. Reich, T. E., Lindstedt, S. L., LaStayo, P. C. & Pierotti, D. J. 2000 Is the spring quality of muscle plastic? Am J. Physiol., 278, R1661-R1666.
18. Herzog, W. & Leonard, T. R. 2002 Force enhancement following stretching of skeletal muscle: a new mechanism. J. Exp. Biol., 205, 1275-1283.
19. Campbell, K. S. & Moss, R. L. 2002 History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys. J., 82, 929-943. (doi:10.1016/S0006-3495(02)75454-4)
20. 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, 13 716-13 721. (doi:10.1073/pnas.2235652100)
21. Warren, C. M., Krzesinski, P. R. & Greaser, M. L. 2003 Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis, 24, 1695-1702. (doi:10.1002/elps.200305392)
22. Wang, K., Ramirez-Mitchell, R. & Palter, D. 1984 Titin is an extraordinarily long, flexible, and slender myofibrillar protein. Proc. Natl Acad. Sci. USA, 81, 3685-3689. (doi:10.1073/pnas.81.12.3685)
23. Funatsu, T., Kono, E., Higuchi, H., Kimura, S., Ishiwata, S., Yoshioka, T., Maruyama, K. & Tsukita, S. 1993 Elastic filaments in situ, in cardiac muscle: deepetch replica analysis in combination with selective removal of actin and myosin filaments. J. Cell Biol., 120, 711-724. (doi:10.1083/jcb.120.3.711)
24. Bennett, P. M., Hodkin, T. E. & Hawkins, C. 1997 Evidence that the tandem Ig domains near the end of the muscle thick filament form an inelastic part of the I-band titin. J. Struct. Biol., 120, 93-104. (doi:10.1006/ jsbi.1997.3898)
25. Muhle-Goll, C., Habeck, M., Cazorla, O., Nilges, M., Labeit, S. & Granzier, H. 2001 Structural and functional studies of titin's fn3 modules reveal conserved surface patterns and binding to myosin S1: a possible role in the Frank-Starling mechanism of the heart. J. Mol. Biol., 313, 431-477. (doi:10.1006/jmbi.2001.5017)
26. Gautel, M. & Goulding, G. 1996 A molecular map of titin/connectin elasticity reveals two different mechanisms acting in series. FEBS Lett., 385, 11-14. (doi:10. 1016/0014-5793(96)00338-9)
27. Linke, W. A., Ivemeyer, M., Labeit, S., Hinssen, H., Rüegg, 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)
28. Wang, K., McCarter, R., Wright, J., Beverly, J. & Ramirez-Mitchell, R. 1991 Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension. Proc. Natl Acad. Sci. USA, 88, 7101-7105. (doi:10.1073/ pnas.88.16.7101)
29. Granzier, H. L. & Labeit, S. 2004 The giant protein titin: a major player in myocardial mechanics, signaling and disease. Circ. Res., 94, 284-295. (doi:10.1161/01.RES.0000117769.88862.F8)
30. Trombitas, K., Greaser, M., French, G. & Granzier, H. 1998 PEVK extension of human soleus muscle titin revealed by immunolabeling with the anti-titin antibody 9D10. J. Struct. Biol., 122, 188-196. (doi:10.1006/jsbi.1998.3984)
31. 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)
32. Magid, A. & Law, D. J. 1985 Myofibrils bear most of the resting tension in frog skeletal muscle. Science, 230, 1280-1282. (doi:10.1126/science.4071053)
33. Edman, K. A. P. & Tsuchiya, T. 1996 Strain of passive elements during force enhancement by stretch in frog muscle fibres. J. Physiol., 490, 191-205.
34. Joumaa, V., Leonard, T. & Herzog, W. 2008 Residual force enhancement in myofibrils and sarcomeres. Proc. R. Soc. B, 275, 1411-1419. (doi:10.1098/rspb.2008.0142)
35. Leonard, T. R. & Herzog, W. 2010 Regulation of muscle force in the absence of actin-myosin based cross-bridge interaction. Am. J. Physiol. Cell Physiol., 299, 14-20. (doi:10.1152/ajpcell.00049.2010)
36. Kellermayer, M. S. Z. & 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)
37. Suzuki, J., Kimura, S. & Maruyama, K. 1994 Electron microscopic filament lengths of connectin and its fragments. J. Biochem., (Tokyo) 116, 406-410.
38. Hayashi, C. et al., 2008 Multiple molecular interactions implicate the connectin/titin N2A region as a modulating scaffold for p94/calpain 3 activity in skeletal muscle. J. Biol. Chem., 283, 14 801-14 814.
39. Monroy, J. A., Powers, K. L., Gilmore, L. A., Uyeno, T. A. & Nishikawa, K. C. 2011 Ca2{thorn}-activation of skeletal muscle: not just the thin filament? Integr. Comp. Biol., 51, e94. (doi:10.1093/icb/icr008)
40. Garvey, S. M., Rajan, C., Lerner, A. P., Frankel, W. N. & Cox, G. A. 2002 The muscular dystrophy with myositis (mdm) mouse mutation disrupts skeletal muscle-specific domain of titin. Genom, 79, 146-149. (doi:10.1006/ geno.2002.6685)
41. Edman, K. A. P. 1979 The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibers. J. Physiol., 291, 143-159.
42. Allen, D. G. & Kentish, J. C. 1985 The cellular basis of the length-tension relation in cardiac muscle. J. Mol. Cell. Cardiol., 17, 821-840. (doi:10.1016/S0022-2828 (85)80097-3)
43. Robinson, T. F. & Winegrad, S. 1979 The measurement and dynamic implications of thin filament lengths in heart muscle. J. Physiol., 286, 607-619.
44. Cazorla, O., Freiburg, A., Helmes, M., Centner, T., McNabb, M., Wu, Y., Trombitas, K., Labeit, S. & Granzier, H. 2000 Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ. Res., 86, 59-67.
45. 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)
46. Weiwad, W. K. K., Linke, W. A. &Wussling, M. H. P. 2000 Sarcomere length-tension relationship of rat cardiac myocytes at lengths greater than optimum. J. Mol. Cell. Cardiol., 32, 247-259. (doi:10.1006/jmcc.1999.1069)
47. Shiels, H. A. & White, E. 2008 The Frank-Starling mechanism in vertebrate cardiac myocytes. J. Exp. Biol., 211, 2005-2013. (doi:10.1242/jeb.003145)
48. Patrick, S. M., Hoskins, A. C., Kentish, J. C., White, E., Shiels, H. A. & Cazorla, O. 2010 Enhanced lengthdependent Ca2{thorn} activation in fish cardiomyocytes permits a large operating range of sarcomere lengths. J. Mol. Cell. Cardiol., 48, 917-924. (doi:10.1016/j. yjmcc.2010.02.008)
49. King, N. M., Mathawasin, M., Nedrud, J., Harrell, N., Chung, C. S., Helmes, M. & Granzier, H. 2010 Mouse intact cardiac myocyte mechanics: cross-bridge and titin-based stress in unactivated cells. J. Gen. Physiol., 137, 81-91. (doi:10.1085/jgp.201010499)
50. Biewener, A. & Roberts, T. J. 2000 Muscle and tendon contributions to force, work and elastic energy savings: a comparative perspective. Exerc. Sports Sci. Rev., 28, 99-107.
51. Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R., Kram, R. & Lehman, S. 2000 How animals move: an integrative view. Science, 288, 100-106. (doi:10.1126/science.288.5463.100)
52. Tanaka, Y., Ishijima, A. & Ishiwata, S. 1992 Super helix formation of actin filaments in an in vitro, motile system. Biochim. Biophys. Acta, 159, 94-98. (doi:10.1016/0167-4838(92)90079-S)
53. Nishizaka, T., Yagi, T., Tanaka, Y. & Ishiwata, S. 1993 Right-handed rotation of an actin filament in an in vitro, motile system. Nature, 361, 269-271. (doi:10.1038/ 361269a0)
54. Sase, I., Miyata, H., Ishiwata, S. & Kinosita, K. 1997 Axial rotation of sliding actin filaments revealed by single-fluorophore imaging. Proc. Natl Acad. Sci. USA, 94, 5646-5650. (doi:10.1073/pnas.94.11.5646)
55. Bordas, J., Svensson, A., Rothery, M., Lowy, J., Diakun, G. P. & Boesecke, P. 1999 Extensibility and symmetry of actin filaments in contracting muscles. Biophys. J., 77, 3197-3207. (doi:10.1016/S0006-3495(99)77150-X)
56. Tsaturyan, A. K., Koubassova, N., Ferenczi, M. A., Narayanan, T., Roessle, M. & Bershitsky, S. Y. 2005 Strong binding of myosin heads stretches and twists the actin helix. Biophys. J., 88, 1902-1910. (doi:10. 1529/biophysj.104.050047)
57. Goldstein, M. A., Schroeter, J. P. & Sass, R. L. 1990 Two structural states of the vertebrate Z band. Electron Microsc. Rev., 3, 227-248. (doi:10.1016/0892-0354(90) 90003-B)
58. Jarosch, R. 2000 Muscle force arises by actin filament rotation and torque in the Z-filaments. Biochem. Biophys. Res. Commun., 270, 677-682. (doi:10.1006/bbrc.1999.1971)
59. Bianco, P., Nagy, A., Kengyel, A., Szatmari, D., Martonfalvi, Z., Huber, T. & Kellermayer, M. S. Z. 2007 Interaction forces between F-actin and titin PEVK domain measured with optical tweezers. Biophys. J., 93, 2102-2109. (doi:10.1529/biophysj.107.106153)
60. Pavlov, I., Novinger, R. & Rassier, D. 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)
61. Shi, D., Somlyo, A. V., Somlyo, A. P. & Shao, Z. 2001 Visualizing filamentous actin on lipid bilayers by atomic force microscopy in solution. J. Microsc., 201, 377-382. (doi:10.1046/j.1365-2818.2001.00844.x)
62. Higuchi, H., Nakauchi, Y., Maruyama, K. & Fujime, S. 1993 Characterization of beta-connectin (titin 2) from striated muscle by dynamic light scattering. Biophys. J., 65, 1906-1915. (doi:10.1016/S0006-3495 (93)81261-X)
63. Edman, K. A. P., Elzinga, G. & Noble, M. I. M. 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)
64. Finer, J. T., Mehta, A. D. & Spudich, J. A. 1995 Characterization of single actin-myosin interactions. Biophys. J., 68, S291-S296. (doi:10.1016/S0006-3495 (95)80187-6)
65. Reconditi, M. et al., 2004 The myosin motor in muscle generates a smaller and slower working stroke at higher load. Nature, 428, 578-581. (doi:10.1038/nature02380)
66. Hill, A. V. 1938 The heat of shortening and the dynamic constants of muscle. Proc. R. Soc. Lond. B, 126, 136-195. (doi:10.1098/rspb.1938.0050)
67. Hill, A. V. 1964 The effect of load on the heat of shortening of muscle. Proc. R. Soc. Lond. B, 159, 297-318. (doi:10.1098/rspb.1964.0004)
68. Huxley, A. F. 1973 A note suggesting that the crossbridge attachment during muscle contraction may take place in two stages. Proc. R. Soc. Lond. B, 183, 83-86. (doi:10.1098/rspb.1973.0006)
69. Huxley, A. F. & Simmons, R. M. 1971 Proposed mechanism of force generation in striated muscle. Nature, 233, 533-538. (doi:10.1038/233533a0)
70. Ford, L. E., Huxley, A. F. & Simmons, R. M. 1977 Tension responses to sudden length change in stimulated frog muscle fibers near slack length. J. Physiol., 269, 441-515.
71. Lappin, A. K., Monroy, J. A., Pilarski, J. Q., Zepnewski, E. D., Pierotti, D. J. & Nishikawa, K. C. 2006 Storage and recovery of elastic potential energy powers ballistic prey capture in toads. J. Exp. Biol., 209, 2535-2553. (doi:10.1242/jeb.02276)
72. Galler, S. & Hilber, K. 1998 Tension/stiffness ratio of skinned rat skeletal muscle fibre types at various temperatures. Acta Physiol. Scand., 162, 119-126. (doi:10.1046/j. 1365-201X.1998.0272f.x)
73. Sugi, H., Akimoto, T., Kobayashi, T., Suzuki, S. & Shimada, S. 2000 Possible contribution of titin filaments to the compliant series elastic component in horseshoe crab skeletal muscle fibers. Adv. Exp. Med. Biol., 481, 371-380. (doi:10.1007/978-1-4615-4267-4_22)
74. Telley, I. A., Stehle, R., Ranatunga, K. W., Pfitzer, G., Stüssi, 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)
75. Daniel, T. L., Trimble, A. C. & Chase, P. B. 1998 Compliant realignment of binding sites in muscle: transient behavior and mechanical tuning. Biophys. J., 74, 1611-1621. (doi:10.1016/S0006-3495(98)77875-0)
76. Shimamoto, Y., Suzuki, M., Mikhailenko, S. V., Yasuda, K. & Ishiwata, S. 2009 Inter-sarcomere coordination in muscle revealed though individual sarcomere response to quick stretch. Proc. Natl Acad. Sci. USA, 106, 11 954-11 959. (doi:10.1073/pnas.0813288106)
77. Edman, K. A. 1975 Mechanical deactivation induced by active shortening in isolated muscle fibers of the frog. J. Physiol., 246, 255-275.
78. Monroy, J. A., Lappin, A. K. & Nishikawa, K. C. 2007 Elastic properties of active muscle: on the rebound? Exerc. Sports Sci. Rev., 35, 174-179. (doi:10.1097/jes. 0b013e318156e0e6)