The elasticity of single titin molecules using a two-bead optical tweezers assay

Biophysical Journal

Volumn 87, Issue 2, 2004, Pages 1112-1135

  Leake, Mark C ^a,c   Wilson, David ^a   Gautel, Mathias ^a,b   Simmons, Robert M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; IMMUNOGLOBULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSAY; DEVICE; ELASTICITY; ENTROPY; HEART MUSCLE; HYSTERESIS; IONIC STRENGTH; NONHUMAN; OPTICAL TWEEZERS ASSAY; PROTEIN ANALYSIS; SARCOMERE; SKELETAL MUSCLE; STRESS; TEMPERATURE;

ANIMALIA;

EID: 4143147307     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.103.033571     Document Type: Article

References (68)

1. Ariel, G., and Andelman, D. 2003. Persistence length of a strongly charged rodlike polyelectrolyte in the presence of salt. Phys. Rev. E. 67:011805.
2. Carrion-Vazquez, M., A. F. Oberhauser, S. B. Fowler, P. E. Marszalek, S. E. Broedel, and J. Clarke. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA. 96: 3694-3699.
3. Chung, S. H., and R. A. Kennedy. 1991. Forward-backward non-linear filtering technique for extracting small biological signals from noise. J. Neurosci. Methods. 40:71-86.
4. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
5. Evans, E., and K. Ritchie. 1999. Strength of a weak bond connecting flexible polymer chains. Biophys. J. 76:2439-2447.
6. Florey, P. J. 1969. Statistical Mechanics of Chain Molecules. Interscience Publishers, New York.
7. Fratemali, F., and Pastore, A. 1999. Modularity and homology: modeling of the type II module family from titin. J. Mol. Biol. 290:581-593.
8. Freiburg, A., K. Trombitas, W. Hell, O. Cazorla, F. Fougerousse, T. Centner, B. Kolmerer, C. Witt, J. S. Beckmann, C. C. Gregorio, H. Granzier, and S. Labeit. 2000. Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ. Res. 86:1114-1121.
9. Fürst, D. O., M. Osbom, R. 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.
10. Gautel, M., E. Lehtonen, and F. Pietruschka. 1996a. Assembly of the cardiac I-band region of titin/connectin: expression of the cardiac-specific regions and their relation to the elastic segments. J. Muscle Res. Cell Motil. 17:449-461.
11. 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.
12. Gautel, M., D. Goulding, B. Bullard, K. Weber, and D. O. Fürst. 1996b. The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J. Cell Sci. 109:2747-2754.
13. Goll, C. M., A. Pastore, and M. Nilges. 1998. The three-dimensional structure of a type I module from titin: a prototype of intracellular fibronectin type III domains. Structure, 6:1291-1302.
14. Grantham, R. 1974. Amino acid difference formula to help explain protein evolution. Science. 185:862-864.
15. Granzier, H., M. Helmes, and K. Trombitas. 1996. Nonuniform elasticity of titin in cardiac myocytes: a study using immunoelectron microscopy and cellular mechanics. Biophys. J. 70:430-442.
16. Granzier, H. L., and T. C. Irving. 1995. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J. 68:1027-1044.
17. Greaser, M. L. 2001. Identification of new repeating motifs in titin. Proteins. 43:145-149.
18. Higuchi, H., Y. Nakauchi, K. Maruyama, and S. Fujime. 1993. Characterization of beta-connectin (titin 2) from striated muscle by dynamic light scattering. Biophys. J. 65:1906-1915.
19. Kellermayer, M. S., S. B. Smith, C. Bustamante, and H. L. Granzier. 1998. Complete unfolding of the titin molecule under external force. J. Struct. Biol. 122:197-205.
20. Kellermayer, M. S., S. B. Smith, C. Bustamante, and H. L. Granzier. 2001. Mechanical fatigue in repetitively stretched single molecules of titin. Biophys. J. 80:852-863.
21. Kellermayer, M. S., S. B. Smith, H. L. Granzier, and C. Bustamante. 1997. Folding-unfolding transitions in single titin molecules characterized with laser-tweezers. Science. 276:1112-1116.
22. Kuo, S. C. 1998. A simple assay for local heating by optical tweezers. Meth. Cell Biol. 55:43-45.
23. Labeit, S., M. Gautel, A. Lakey, and J. Trinick. 1992. Towards a molecular understanding of titin. EMBO J. 11:1711-1716.
24. Labeit, S., and B. Kolmerer. 1995. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science. 270:293-296.
25. Labeit, D., K. Watanabe, C. Witt, H. Fujita, Y. Wu, S. Lahmers, T. Funck, S. Labeit, and H. Granzier. 2003. Calcium-dependent molecular spring elements in the giant protein titin. Proc. Natl. Acad. Sci. USA. 100: 13716-13721.
26. Leake, M. C., D. Wilson, B. Bullard, and R. M. Simmons. 2003. The elasticity of single kettin molecules using a two-bead laser-tweezers assay. FEBS Lett. 535:55-60.
27. Li, H., W. A. Linke, A. F. Oberhauser, M. Carrion-Vazquez, J. G. Kerkvliet, H. Lu, P. E. Marszalek, and J. M. Fernandez. 2002. Reverse engineering of the giant muscle protein titin. Nature. 418:998-1002.
28. Li, H., A. F. Oberhauser, S. D. Redick, M. Carrion-Vazquez, H. P. Erickson, and J. M. Fernandez. 2001. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc. Natl. Acad. Sci. USA. 98:10682-10686.
29. Linke, W. A., M. Ivemeyer, S. Labeit, H. Hinssen, J. C. Ruegg, and M. Gautel. 1997. Actin-titin interaction in cardiac myofibrils: probing a physiological role. Biophys. J. 73:905-919.
30. Linke, W. A., M. Ivemeyer, P. Mundel, M. R. Stockmeier, and B. Kolmerer. 1998a. Nature of PEVK-titin elasticity in skeletal muscle. Proc. Natl. Acad. Sci. USA. 95:8052-8057.
31. Linke, W. A., M. Ivemeyer, N. Olivieri, B. Kolmerer, J. C. Ruegg, and S. Labeit. 1996. Towards a molecular understanding of the elasticity of titin. J. Mol. Biol. 261:62-71.
32. Linke, W. A., M. R. Stockmeier, M. Ivemeyer, H. Hosser, and P. Mundel. 1998b. Characterizing titin's I-band Ig domain region as an entropic spring. J. Cell Sci. 111:1567-1574.
33. Ma, K., L. S. Kan, and K. Wang. 2001. Polyproline II helix is a key structural motif of the elastic PEVK segment of titin. Biochemistry. 40:3427-3438.
34. Marko, J. F., and E. Siggia. 1995. Stretching DNA. Macromolecules. 28:209-212.
35. Minajeva, A., M. Kulke, J. M. Fernandez, and W. A. Linke. 2001. Unfolding of titin domains explains the viscoelastic behavior of skeletal myofibrils. Biophys. J. 80:1442-1451.
36. Nave, R., D. O. Fürst, and K. Weber. 1989. Visualization of the polarity of isolated titin molecules; a single globular head on a long thin rod as the M-band anchoring domain? J. Cell Biol. 109:2177-2188.
37. Neagoe, C., C. A. Opitz, I. Makarenko, and W. A. Linke. 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.
38. Nelder, J. A., and R. Mead. 1965. A simplex method for function minimization. Comput. J. 7:308-313.
39. Opitz, C. A., M. Kulke, M. C. Leake, C. Neagoe, H. Hinssen, R. J. Hajjar, and W. A. Linke. 2003. Damped elastic recoil of the titin spring in myofibrils of human myocardium. Proc. Natl. Acad. Sci. USA. 100:12688-12693.
40. Pauling, L. 1960. The Nature of the Chemical Bond, 3rd ed. Cornell University Press, Ithaca, NY.
41. Peckham, M., P. Young, and M. Gautel. 1997. Constitutive and variable regions of Z-disk titin/connectin in myofibril formation: a dominant-negative screen. Cell Struct. Funct. 22:95-101.
42. Pfuhl, M., M. Gautel, A. S. Politou, C. Joseph, and A. Pastore. 1995. Secondary structure determination by NMR spectroscopy of an immunoglobulin-like domain from the giant muscle protein titin. J. Biomol. NMR. 6:48-58.
43. Privalov, P. L., and G. I. Makhatadze. 1993. Contribution of hydration to protein folding thermodynamics. 11. The entropy and Gibbs energy of hydration. J. Mol. Biol. 232:660-679.
44. Rief, M., M. Gautel, F. Oesterhelt, J. M. Fernandez, and H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112.
45. Rief, M., M. Gautel, A. Schemmel, and H. E. Gaub. 1998. The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by atomic force microscopy. Biophys. J. 75:3008-3014.
46. Schimmel, P. R., and P. J. Flory. 1968. Conformational energies and configurational statistics of copolypeptides containing L-proline. J. Mol. Biol. 34:105-120.
47. Schwesinger, F., R. Ros, T. Strunz, D. Anselmetti, H. J. Guntherodt, A. Honegger, L. Jermutus, L. Tiefenauer, and A. Pluckthun. 2000. Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates. Proc. Natl. Acad. Sci. USA. 97:9972-9977.
48. Simmons, R. M., J. T. Finer, S. Chu, and J. A. Spudich. 1996. Quantitative measurements of force and displacement using an optical trap. Biophys. J. 70:1813-1822.
49. Svoboda, K., and S. M. Block. 1994. Biological applications of optical forces. Annu. Rev. Biophys. Biomol. Struct. 23:247-285.
50. Tonelli, A. E. 1974. Conformational characteristics of polypeptides containing isolated L-proline residues with cis peptide bonds. J. Mol. Biol. 86:627-635.
51. Trinick, J., P. Knight, and A. Whiting. 1984. Purification and properties of native titin. J. Mol. Biol. 180:331-356.
52. Trombitas, K., P. H. Baatsen, M. S. Kellermayer, and G. H. Pollack. 1991. Nature and origin of gap filaments in striated muscle. J. Cell Sci. 100:809-814.
53. Trombitas, K., M. Greaser, G. French, and H. Granzier. 1998. PEVK extension of human soleus muscle titin revealed by immunolabeling with the anti-titin antibody 9D10. J. Struct. Biol. 122:188-196.
54. Trombitas, K., G. H. Pollack, J. Wright, and K. Wang. 1993. Elastic properties of titin filaments demonstrated using a "freeze-break" technique. Cell Motil. Cytoskeleton. 24:274-283.
55. Trombitas, K., Y. Wu, M. McNabb, M. Greaser, M. S. Kellermayer, S. Labeit, and H. Granzier. 2003. Molecular basis of passive stress relaxation in human soleus fibers: assessment of the role of immunoglobulin-like domain unfolding. Biophys. J. 85:3142-3153.
56. Tskhovrebova, L., and J. Trinick. 1997. Direct visualization of extensibility in isolated titin molecules. J. Mol. Biol. 265:100-106.
57. Tskhovrebova, L., and J. Trinick. 2000. Extensibility in the titin molecule and its relation to muscle elasticity. Adv. Exp. Med. Biol. 481:163-178.
58. Tskhovrebova, L., and J. Trinick. 2001. Flexibility and extensibility in the titin molecule: analysis of electron microscope data and its relation to muscle elasticity. J. Mol. Biol. 301:755-771.
59. Tskhovrebova, L., and J. Trinick. 2002. Role of titin in vertebrate striated muscle. Phil. Trans. R. Soc. Lond. B. 357:199-206.
60. Tskhovrebova, L., J. Trinick, J. A. Sleep, and R. M. Simmons. 1997. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature. 387:308-312.
61. Wang, S. M., and M. L. 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.
62. Wang, K., J. McClure, and A. Tu. 1979. Titin: major myofibrillar components of striated muscle. Proc. Natl. Acad. Sci. USA. 76:3698-3702.
63. Watanabe, K., P. Nair, D. Labeit, M. S. Z. Kellermayer, M. Greaser, S. Labeit, and H. Granzier. 2002. Molecular mechanics of cardiac titin's PEVK and N2B spring elements. J. Biol. Chem. 277:11549-11558.
64. Whiting, A., J. Wardale, and J. Trinick. 1989. Does titin regulate the length of muscle thick filaments? J. Mol. Biol. 205:263-268.
65. Williams, P. M., S. B. Fowler, R. B. Best, J. L. Toca-Herrera, K. Scott, A. Steward, and J. Clarke. 2003. Hidden complexity in the mechanical properties of titin. Nature. 422:446-449.
66. Wuthrich, K., and C. Grathwohl. 1974. A novel approach for studies of the molecular conformations in flexible polypeptides. FEBS Lett. 43:337-340.
67. Yamasaki, R., M. Berri, Y. Wu, K. Trombitas, M. McNabb, M. S. Kellermayer, C. Witt, D. Labeit, S. Labeit, M. Greaser, and H. Granzier. 2001. Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys. J. 81:2297-2313.
68. Young, P., C. Ferguson, S. Banuelos, and M. Gautel. 1998. Molecular structure of the sarcomeric Z-disk: two types of titin interactions lead to an asymmetrical sorting of alpha-actinin. EMBO J. 17:1614-1624.