Temperature-dependence of isometric tension and cross-bridge kinetics of cardiac muscle fibers reconstituted with a tropomyosin internal deletion mutant

Biophysical Journal

Volumn 91, Issue 11, 2006, Pages 4230-4240

  Lu, Xiaoying ^a   Tobacman, Larry S ^b   Kawai, Masataka ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; CALCIUM; MUSCLE PROTEIN; MUTANT PROTEIN; MYOSIN; RECOMBINANT PROTEIN; TROPOMYOSIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COW; HEART MUSCLE; MUSCLE ISOMETRIC CONTRACTION; MUSCLE RELAXATION; MUSCLE RIGIDITY; MUSCLE STIFFNESS; NONHUMAN; TEMPERATURE DEPENDENCE; THIN FILAMENT;

BOS TAURUS;

EID: 33845363591     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.084608     Document Type: Article

References (66)

1. Huxley, H. E. 1972. Structural changes in the actin- and myosin-containing filaments during contraction. Cold Spring Harb. Symp. Quant. Biol. 37:361-376.
2. Haselgrove, J. C. 1972. X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle. Cold Spring Harb. Symp. Quant. Biol. 37:341-352.
3. Chalovich, J. M. 1992. Actin-mediated regulation of muscle contraction. Pharmacol. Ther. 55:95-148.
4. Tobacman, L. S. 1996. Thin filament-mediated regulation of cardiac contraction. Annu. Rev. Physiol. 58:447-481.
5. Cooke, R. 1997. Actomyosin interaction in striated muscle. Physiol. Rev. 77:671-697.
6. McKillop, D. F., and M. A. Geeves. 1993. Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys. J. 65:693-701.
7. Parry, D. A., and J. M. Squire. 1973. Structural role of tropomyosin in muscle regulation: analysis of the x-ray diffraction patterns from relaxed and contracting muscles. J. Mol. Biol. 75:33-55.
8. Wakabayashi, T., H. E. Huxley, L. A. Amos, and A. Klug. 1975. Three-dimensional image reconstruction of actin-tropomyosin complex and actin-tropomyosin-troponin T-troponin I complex. J. Mol. Biol. 93:477-497.
9. Kress, M., H. E. Huxley, A. R. Faruqi, and J. Hendrix. 1986. Structural changes during activation of frog muscle studied by time-resolved x-ray diffraction. J. Mol. Biol. 188:325-342.
10. Vibert, P., R. Craig, and W. Lehman. 1997. Steric-model for activation of muscle thin filaments. J. Mol. Biol. 266:8-14.
11. Xu, C., R. Craig, L. Tobacman, R. Horowitz, and W. Lehman. 1999. Tropomyosin positions in regulated thin filaments revealed by cryoelectron microscopy. Biophys. J. 77:985-992.
12. Pirani, A., C. Xu, V. Hatch, R. Craig, L. S. Tobacman, and W. Lehman. 2005. Single particle analysis of relaxed and activated muscle thin filaments. J. Mol. Biol. 346:761-772.
13. Rosol, M., W. Lehman, R. Craig, C. Landis, C. Butters, and L. S. Tobacman. 2000. Three-dimensional reconstruction of thin filaments containing mutant tropomyosin. Biophys. J. 78:908-917.
14. Tobacman, L. S., and C. A. Butters. 2000. A new model of cooperative myosin-thin filament binding. J. Biol. Chem. 275:27587-27593.
15. Goldman, Y. E., J. A. McCray, and K. W. Ranatunga. 1987. Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres. J. Physiol. 392:71-95.
16. Ranatunga, K. W., B. Sharpe, and B. Turnbull. 1987. Contraction of human skeletal muscle at different temperatures. J. Physiol. 390:383-395.
17. Rall, J. A., and R. C. Woledge. 1990. Influence of temperature on mechanics and energetics of muscle contraction. Am. J. Physiol. 259:197-203.
18. Zhao, Y., and M. Kawai. 1994. Kinetic and thermodynamic studies of the cross-bridge cycle in rabbit psoas muscle fibers. Biophys. J. 67:1655-1668.
19. Coupland, M. E., E. Puchert, and K. W. Ranatunga. 2001. Temperature dependence of active tension in mammalian (rabbit psoas) muscle fibres: effect of inorganic phosphate. J. Physiol. 536.3:879-891.
20. Wang, G., and M. Kawai. 2001. Effect of temperature on elementary steps of the cross-bridge cycle in rabbit soleus slow-twitch muscle fibres. J. Physiol. (Lond.). 531.1:219-234.
21. Ranatunga, K. W. 1999. Endothermic force generation in skinned cardiac muscle from rat. J. Muscle Res. Cell Motil. 20:489-496.
22. Fujita, H., and M. Kawai. 2002. Temperature effect on isometric tension is mediated by regulatory proteins tropomyosin and troponin in bovine myocardium. J. Physiol. (Lond.). 539.1:267-276.
23. Hitchcock-DeGregori, S. E., and T. A. Varnell. 1990. Tm has discrete actin-binding sites with sevenfold and 14-fold periodicities. J. Mol. Biol. 214:885-896.
24. Hitchcock-DeGregori, S. E., and Y. An. 1996. Integral repeats and a continuous coiled coil are required for binding of striated muscle tropomyosin to the regulated actin filament. J. Biol. Chem. 16:3600-3603.
25. Landis, C., N. Back, E. Homsher, and L. S. Tobacman. 1999. Effects of tropomyosin internal deletions on thin filament function. J. Biol. Chem. 274:31279-31285.
26. Kawai, M., T. Kido, M. Vogel, R. H. Fink, and S. Ishiwata. 2006. Temperature change does not affect force between regulated actin filaments and heavy meromyosin in single-molecule experiments. J. Physiol. (Lond.). 574.3:877-887.
27. Lu, X., L. S. Tobacman, and M. Kawai. 2003. Effect of tropomyosin internal deletion AS-Δ23 Tm on isometric tension and the cross-bridge kinetics in bovine myocardium. J. Physiol. (Lond.). 553.2:457-471.
28. Kawai, M., and S. Ishiwata. 2006. Use of thin-filament reconstituted muscle fibres to probe the mechanism of force generation. J. Muscle Res. Cell Motil. 27:455-468.
29. Tobacman, L. S., and R. S. Adelstein. 1986. Mechanism of regulation of cardiac actin-myosin subfragment 1 by troponin-tropomyosin. Biochem. Biophys. Res. Commun. 25:798-802.
30. Monteiro, P. B., R. C. Lataro, J. A. Ferro, and C. Reinach Fde. 1994. Functional α-tropomyosin produced in Escherichia coli. A dipeptide extension can substitute the amino-terminal acetyl group. J. Biol. Chem. 269:10461-10466.
31. Fujita, H., K. Yasuda, S. Niitsu, T. Funatsu, and S. Ishiwata. 1996. Structural and functional reconstitution of thin filaments in the contractile apparatus of cardiac muscle. Biophys. J. 71:2307-2318.
32. Fujita, H., D. Sasaki, S. Ishiwata, and M. Kawai. 2002. Elementary steps of the cross-bridge cycle in bovine myocardium with and without regulatory proteins. Biophys. J. 82:915-928.
33. Kawai, M., and P. W. Brandt. 1980. Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J. Muscle Res. Cell Motil. 1:279-303.
34. Homsher, E., D. M. Lee, C. Morris, D. Pavlov, and L. S. Tobacman. 2000. Regulation of force and unloaded sliding speed in single thin filaments: effects of regulatory proteins and calcium. J. Physiol. (Lond.). 524.1:233-243.
35. Ranatunga, K. W., and S. R. Wylie. 1983. Temperature-dependent transition in isometric contraction of rat muscle. J. Physiol. 339:87-95.
36. Kawai, M., and P. W. Brandt. 1976. Two rigor states in skinned crayfish single muscle fibers. J. Gen. Physiol. 68:267-280.
37. Reference deleted in proof.
38. Heald, R. W., and S. E. Hitchcock-DeGregori. 1988. The structure of the amino terminus of tropomyosin is critical for binding to actin in the absence and presence of troponin. J. Biol. Chem. 263:5254-5259.
39. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
40. Kraft, T., and B. Brenner. 1997. Force enhancement without changes in cross-bridge turnover kinetics: the effect of EMD 57033. Biophys. J. 72:272-281.
41. Bershitsky, S. Y., and A. K. Tsaturyan. 2002. The elementary force generation process probed by temperature and length perturbations in muscle fibres from the rabbit. J. Physiol. 540.3:971-988.
42. Piazzesi, G., M. Reconditi, N. Koubassova, V. Decostre, M. Linari, L. Lucii, and V. Lombardi. 2003. Temperature dependence of the force-generating process in single fibres from frog skeletal muscle. J. Physiol. 549.1:93-106.
43. Kawai, M. 2003. What do we learn by studying the temperature effect on isometric tension and tension transients in mammalian striated muscle fibres? J. Muscle Res. Cell Mot. 24:127-138.
44. Kawai, M., K. Kawaguchi, M. Saito, and S. Ishiwata. 2000. Temperature change does not affect force between single actin filaments and HMM from rabbit muscles. Biophys. J. 78:3112-3119.
45. Kawaguchi, K., and S. Ishiwata. 2000. Temperature dependence of force, velocity, and processivity of single kinesin molecules. Biochem. Biophys. Res. Commun. 272:895-899.
46. Oosawa, F., S. Fujime, S. Ishiwata, and K. Mihashi. 1972. Dynamic property of F-actin and thin filament. Cold Spr. Harbor Symp. Quant. Biol. 37:277-285.
47. Bagni, M. A., G. Cecchi, F. Colomo, and C. Poggesi. 1990. Tension and stiffness of frog muscle fibres at full filament overlap. J. Muscle Res. Cell Motil. 11:371-377.
48. Kojima, H., A. Ishijima, and T. Yanagida. 1994. Free in PMC direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc. Natl. Acad. Sci. USA. 91:12962-12966.
49. Wakabayashi, K., Y. Sugimito, H. Tanaka, Y. Ueno, Y. Takezawa, and Y. Amemiya. 1994. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys. J. 67:2422-2435.
50. Huxley, H. E., A. Stewart, H. Sosa, and T. Irving. 1994. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys. J. 67:2411-2421.
51. Higuchi, H., T. Yanagida, and Y. E. Goldman. 1995. Compliance of thin filaments in skinned fibers of rabbit skeletal muscle. Biophys. J. 69:1000-1010.
52. Fortune, N. S., M. A. Geeves, and K. W. Ranatunga. 1991. Tension responses to rapid pressure release in glycerinated rabbit muscle fibres. Proc. Natl. Acad. Sci. USA. 80:7323-7327.
53. Kawai, M., and H. R. Halvorson. 1991. Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned fibers of rabbit psoas muscle. Biophys. J. 59:329-342.
54. Dantzig, J. A., Y. E. Goldman, N. C. Millar, J. Lacktis, and E. Homsher. 1992. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J. Physiol. (Lond.). 451:247-278.
55. Murphy, K. P., Y. Zhao, and M. Kawai. 1996. Molecular forces involved in force generation during skeletal muscle contraction. J. Exp. Biol. 199:2565-2571.
56. Van Holde, K. E., W. C. Johnson, and P. S. Ho. 1998. Principles of Physical Biochemistry, 3rd Ed. Prentice Hall, Upper Saddle River, NJ.
57. Tonomura, Y., S. Tokura, and K. Sekiya. 1962. Binding of myosin A to F-actin. J. Biol. Chem. 237:1074-1081.
58. Highsmith, S. 1977. The effects of temperature and salts on myosin subfragment-1 and F-actin association. Arch. Biochem. Biophys. 180:404-408.
59. Ishiwata, S., B. A. Manuck, J. C. Seidel, and J. Gergely. 1986. Saturation transfer electron paramagnetic resonance study of the mobility of myosin heads in myofibrils under conditions of partial dissociation. Biophys. J. 49:821-828.
60. Eaton, B. L. 1976. Tropomyosin binding to F-actin induced by myosin heads. Science. 192:1337-1339.
61. Cassell, M., and L. S. Tobacman. 1996. Opposite effects of myosin subfragment 1 on binding of cardiac troponin and tropomyosin to the thin filament. J. Biol. Chem. 271:12867-12872.
62. Geeves, M. A., and D. J. Halsall. 1986. The dynamics of the interaction between myosin subfragment 1 and pyrene-labelled thin filaments, from rabbit skeletal muscle. Proc. R. Soc. Lond. B Biol. Sci. 229:85-95.
63. Williams, D. L., and L. E. Greene. 1983. Comparison of the effects of tropomyosin and troponin-tropomyosin on the binding of myosin subfragment 1 to actin. Biochem. Biophys. Res. Commun. 22:2770-2774.
64. Malnasi-Csizmadia, A., D. S. Pearson, M. Kovacs, R. J. Woolley, M. A. Geeves, and C. R. Bagshaw. 2001. Kinetic resolution of a conformational transition and the ATP hydrolysis step using relaxation methods with a Dictyostelium myosin II mutant containing a single tryptophan residue. Biochemistry. 40:12727-12737.
65. Xu, S., G. Offer, J. Gu, H. D. White, and L. C. Yu. 2003. Temperature and ligand dependence of conformation and helical order in myosin filaments. Biochemistry. 42:390-401.
66. 2+-saturated form. Nature. 424:35-41.