Titin elasticity and mechanism of passive force development in rat cardiac myocytes probed by thin-filament extraction

Biophysical Journal

Volumn 73, Issue 4, 1997, Pages 2043-2053

  Granzier, Henk ^a   Kellermayer, Miklós ^a,b   Helmes, Michiel ^a   Trombitás, Károly ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CONNECTIN; GELSOLIN;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; ELASTICITY; HEART CONTRACTION; HEART MUSCLE CELL; IMMUNOELECTRON MICROSCOPY; MYOFILAMENT; NONHUMAN; PROTEIN PROTEIN INTERACTION; RAT; SARCOMERE;

ANIMALIA;

EID: 0030855930     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78234-1     Document Type: Article

References (51)

1. Bustamante, C., J. Marko, E. Siggia, and S. Smith. 1994. Entropic elasticity of λ-phage DNA. Science. 265:1599-1600.
2. Erickson, H. 1994. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin in fibronectin. Proc. Natl Acad. Sci. USA. 91:10114-10118.
3. 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.
4. Funatsu, T., H. Higuchi, and S. Ishiwata. 1990. Elastic filaments in skeletal muscle revealed by selective removal of thin filaments with plasma gelsolin. J. Cell Biol. 110:53-62.
5. Funatsu, T., E. Kono, H. Higuchi, S. Kimura, S. Ishiwata, T. Yoshioka, K. Maruyama, S. Tsukita. 1993. Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. J. Cell Biol. 120:711-724.
6. Fürst, D., M. Osborn, M. Nave, and K. Weber. 1988. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z-line extends close to the M-line. J. Cell Biol. 106: 1563-1572.
7. Gautel, M., and D. Goulding. 1996. A molecular map of titin/connectin elasticity reveals two different mechanisms acting in series. FEBS Lett. 385:11-14.
8. Granzier, H., M. Helmes, and K. Trombitás. 1996. Nonuniform elasticity of titin in cardiac myocytes: a study using immunoelectron microscopy and cellular mechanics. Biophys. J. 70:430-442.
9. Granzier, H., and T. Irving. 1995. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J. 68:1027-1044.
10. Granzier, H. L. M., and K. Wang. 1993. Passive tension and stiffness of vertebrate skeletal muscle and insect flight muscle: the contribution of weak crossbridges and elastic filaments. Biophys. J. 65:2141-2159.
11. Gutierrez, G., A. van Heerden, J. Wright, and K. Wang. 1997. Titin elasticity: interaction and extensibility of PEVK segment of human fetal skeletal titin. Biophys. J. 72:A279 (Abstr.).
12. 2+ and segment length dependence of isometric force kinetics in intact ferret cardiac muscle. Circ. Res. 73:603-611.
13. Helmes, M., K. Trombitás, and H. Granzier. 1996. Titin develops restoring force in rat cardiac myocytes. Circ. Res. 79:619-626.
14. Higuchi, H. 1992. Changes in contractile properties with selective digestion of connectin (titin) in skinned fibers of frog skeletal muscle. J. Biochem. 111:291-295.
15. Higuchi, H., N. Nakauchi, K. Maruyama, and S. Fujime. 1993. Characterization of β-connectin (titin 2) from striated muscle by dynamic light scattering. Biophys. J. 65:1906-1915.
16. Horowits, R., E. S. Kempner, M. E. Bisher, and R. Podolsky. 1986. A physiological role for titin and nebulin in skeletal muscle. Nature. 323:160-164.
17. Horowits, R., K. Maruyama, and R. Podolsky. 1989. Elastic behavior of connectin filaments during thick filament movement in activated skeletal muscle. J. Cell Biol. 109:2169-2176.
18. Itoh, Y., T. Suzuki, S. Kimura, K. Ohashi, H. Higuchi, H. Sawada, T. Shinizu, M. Shibata, and K. Maruyama. 1988. Extensible and less-extensible domains of connectin filaments in stretched vertebrate skeletal muscle sarcomeres as detected by immunofluorescence and immunoelectron microscopy using monoclonal antibodies. J. Biochem. 104: 504-508.
19. Jin, J.-P. 1995. Cloned rat cardiac titin class I and class II motifs: expression, purification, characterization, and interaction with F-actin. J. Biol. Chem. 270:6908-6916.
20. Keller, T. 1995. Structure and function of titin and nebulin. Curr. Opin. Cell Biol. 7:32-38.
21. Kellermayer, M., and H. Granzier. 1996a. Calcium-dependent inhibition of in vitro thin-filament motility by native titin. FEBS Lett. 380:281-286.
22. Kellermayer, M., and H. Granzier. 1996b. Elastic properties of single titin molecules made visible through fluorescent F-actin binding. Biochem. Biophys. Res. Commun. 221:491-497.
23. Kellermayer, M., S. Smith, H. Granzier, and C. Bustamante. 1997. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science. 276:1112-1116.
24. Kimura, S., K. Maruyama, and Y. Huang. 1984. Interactions of muscle β-connectin with myosin, actin, and actomyosin at low ionic strength. J. Biochem. 96:499-506.
25. Kruger, M., J. Wright, and K. Wang. 1991. Nebulin as a length regulator of thin filaments of vertebrate skeletal muscles: correlation of thin filament length, nebulin size, and epitope profile. J. Cell Biol. 115: 97-107.
26. Labeit, S., and B. Kolmerer. 1995. Titins, giant proteins in charge of muscle ultrastructure and elasticity. Science. 270:293-296.
27. Labeit, S., B. Kolmerer, and W. Linke. 1997. The giant protein titin. Emerging roles in physiology and pathophysiology. Circ. Res. 80: 290-294.
28. Li, Q., J.-P. Jin, and H. Granzier. 1995. The effect of genetically expressed cardiac titin fragments on in vitro actin motility. Biophys. J. 69: 1508-1518.
29. Linke, W., M. Ivemeyer, M. Olivieri, B. Kolmerer, J. Rüegg, and S. Labeit. 1996. Towards a molecular understanding of the elasticity of titin. J. Mol Biol. 261:62-71.
30. Linke, W., V. Popov, and G. Pollack. 1994. Passive and active tension in single cardiac myofibrils. Biophys. J. 67:782-792.
31. Linke, W., M. Ivemeyer, S. Labeit, H. Hinnsen, J. Rüegg, and M. Gautel. 1997. Actin-titin interaction in cardiac myofibrils: probing a physiological role. Biophys. J. 73:905-919.
32. Marko, J., and E. Siggia. 1995. Stretching DNA. Macromolecules. 28: 8759-8770.
33. Maruyama, K. 1997. Connectin/titin, giant elastic protein of muscle. FASEB J. 11:341-345.
34. Maruyama, K., T. Endo, H. Kume, Y. Kawamura, N. Kanzawa, Y. Nakauchi, S. Kimura, and K. Maruyama. 1993. A novel domain sequence of connectin localised at the I-band of skeletal muscle sarcomous: homology to neurofilament subunits. Biochem. Biophys. Res. Commun. 194:1288-1291.
35. Maruyama, K., D. Hu, T. Suzuki, and S. Kimura. 1987. Binding of actin filaments to connectin. J. Biochem. 101:1339-1346.
36. Ohtsuka, H., H. Yajima, K. Maruyama, and S. Kimura. 1997. Binding of the N-terminal 63 kDa portion of connectin/titin to α-actinin as revealed by the yeast two-hybrid system. FEBS Lett. 401:65-67.
37. Rief, M., M. Gautel, F. Oesterhelt, J. Fernandez, and H. Gaubb. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112.
38. Sebestyén, M., J. Wolff, and M. Greaser. 1995. Characterization of a novel 5.4 kb cDNA fragment coding for the N-terminal region of rabbit cardiac titin. Biophys. J. 68:A65.
39. Sorimachi, H., A. Freiburg, B. Kolmerer, S. Ishiura, G. Stier, C. Gregorio, D. Labeit, W. Linke, K. Suzuki, and S. Labeit. 1997. Tissue-specific expression and α-actinin binding properties of the Z-disc titin. Implications for the nature of vertebrate z-discs. J. Mol. Biol. 270:688-695.
40. ter Keurs, H. 1983. Calcium and contractility. In Cardiac Metabolism, A. J. Drake-Holland and M. Noble, editors. John Wiley and Sons, New York.
41. Trinick, J. 1996. Cytoskeleton: titin as scaffold and spring. Curr. Biol. 6:258-260.
42. Trombitás, K., P. Baatsen, M. Kellermayer, and G. Pollack. 1991. Nature and origin of gap filaments in striated muscle. J. Cell Sci. 100:809-814.
43. Trombitás, K., M. Greaser, and H. Pollack. 1997. Interaction between titin and thin filaments in intact cardiac muscle. J. Muscle Res. Cell Motil. 18:345-351.
44. Trombitás, K., and H. Granzier. 1997. Actin removal from cardiac myocytes shows that near the Z-line titin attaches to actin while under tension. Am. J. Physiol. (Cell). 42:C662-C670.
45. Trombitás, K., J.-P. Jin, and H. Granzier. 1995. The mechanically active domain of titin in cardiac muscle. Circ Res. 77:856-861.
46. Trombitás, K., and G. Pollack. 1993. Elastic properties of the titin filament in the Z-line region of vertebrate striated muscle. J. Muscle Res. Cell Motil. 14:416-422.
47. Tskhovrebova, L., and J. Trinick. 1997. Direct visualization of extensibility in isolated titin molecules. J. Mol. Biol. 265:100-106.
48. Tskhovrebova, L., J. Trinick, J. Sleep, and R. Simmons. 1997. Elasticity and unfolding of single molecules of the giant muscle protein of titin. Nature. 387:308-312.
49. Wang, K., R. McCarter, J. Wright, B. Jennate, and R. Ramirez-Mitchell. 1993. Viscoelasticity of the sarcomere matrix of skeletal muscles: the titin-myosin composite filament is a dual-range molecular spring. Biophys. J. 64:1161-1177.
50. Wang, S.-M., and M. Greaser. 1985. Immunocytochemical studies using a monoclonal antibody to bovine cardiac titin on intact and extracted myofibrils. J. Muscle Res. Cell Motil. 6:293-312.
51. Yu, F., D. Zhou, and H. Yin. 1991. Chimeric and truncated gCap39 elucidate the requirements for actin filament severing and end capping by the gelsolin family of proteins. J. Biol. Chem. 266:19269-19275.