Secondary and tertiary structure elasticity of titin Z1Z2 and a titin chain model

Biophysical Journal

Volumn 93, Issue 5, 2007, Pages 1719-1735

  Lee, Eric H ^a   Hsin, Jen ^b   Mayans, Olga ^c   Schulten, Klaus ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; IMMUNOGLOBULIN; TITIN Z1Z2; UNCLASSIFIED DRUG;

ARTICLE; ELASTICITY; ENERGY TRANSFER; ENTROPY; MOLECULAR DYNAMICS; MUSCLE CELL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIMULATION; STOCHASTIC MODEL;

EID: 34548645722     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.105528     Document Type: Article

References (107)

1. Wang, K. 1996. Titin/connectin and nebulin: giant protein ruler of muscle structure and function. Adv. Biophys. 33:123-134.
2. Erickson, H. 1997. Stretching single protein modules: titin is a weird spring. Science. 276:1090-1093.
3. Maruyama, K. 1997. Connectin/titin, a giant elastic protein of muscle. FASEB J. 11:341-345.
4. Linke, W. 2000. Stretching molecular springs: elasticity of titin filaments in vertebrate striated muscle. Histol. Histopath. 15:799-811.
5. Tskhovrebova, L., and J. Trinick. 2003. Titin: properties and family relationships. Nat. Rev. Mol. Cell Biol. 4:679-689.
6. Granzier, H. L., and S. Labeit. 2004. The giant protein titin a major player in myocardial mechanics, signaling and disease. Circ. Res. 94:284-295.
7. Granzier, H. L., and S. Labeit. 2006. The giant muscle protein titin is an adjustable molecular spring. Exerc. Sport Sci. Rev. 34:50-53.
8. Bang, M. L., T. Centner, F. Fornoff, A. J. Geach, M. Gotthardt, M. McNabb, C. C. Witt, D. Labeit, C. C. Gregorio, H. Granzier, and S. Labeit. 2001. The complete gene sequence of titin, expression of an unusual approximate to 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 89:1065-1072.
9. Gautel, M., D. Goulding, B. Bullard, K. Weber, and D. O. Furst. 1996. The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J. Cell Sci. 109:2747-2754.
10. Mues, A., P. F. M. van der Ven, P. Young, D. O. Furst, and M. Gautel. 1998. Two immunoglobulin-like domains of the z-disc portion of titin interact in a conformation-dependent way with telethonin. FEBS Lett. 428:111-114.
11. Pyle, W. G., and R. J. Solaro. 2004. At the crossroads of myocardial signaling - the role of Z-discs in intracellular signaling and cardiac function. Circ. Res. 94:296-305.
12. Furst, D., M. Osborn, R. Nave, and K. Weber. 1988. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immuno-electron microscopy - a map of 10 non-repetitive epitopes starting at the Z-line extends to the M-line. J. Cell Biol. 106:1563-1572.
13. Obermann, W., M. Gautel, K. Weber, and D. Furst. 1997. Molecular structure of the sarcomeric M-band: mapping of titin and myosin binding domains in myomesin and the identification of potential regulatory phosphorylation site in myomesin. EMBO J. 16:211-220.
14. Whiting, A., J. Wardale, and J. Trinick. 1992. The protein-ruler model of titin control of thick-filament assembly. J. Mol. Biol. 205:262-268.
15. van der Ven, P. F., E. Ehler, J. C. Perriard, and D. O. Furst. 1999. Thick filament assembly occurs after formation of a cytoskeletal scaffold. J. Muscle Res. Cell Mot. 20:569-579.
16. Gräter, F., J. Shen, H. Jiang, M. Gautel, and H. Grubmüller. 2005. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88:790-804.
17. Lange, S., F. Xiang, A. Yakovenko, A. Vihola, P. Hackman, E. Rostkova, J. Kristensen, B. Brandmeier, G. Franzen, B. Hedberg, L. Gunnarsson, S. Hughes, S. Marchand, T. Sejersen, I. Richard, L. Edström, B. Udd, and M. Gautel. 2005. The kinase domain of titin controls muscle gene expression and protein turnover. Science. 308:1599-1603.
18. Gregorio, C. C., K. Trombitas, T. Centner, B. Kolmerer, G. Stier, K. Kunke, K. Suzuki, F. Obermayr, B. Herrmann, H. Granzier, H. Sorimachi, and S. Labeit. 1998. The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kDa ligand (T-cap) is required for sarcomeric integrity. J. Cell Biol. 143:1013-1027.
19. Mayans, O., P. F. M. van der Ven, M. Wilm, A. Mues, P. Young, D. O. Furst, M. Wilmanns, and M. Gautel. 1998. Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature. 395:863-869.
20. Zou, P. J., N. Pinotsis, M. Marino, S. Lange, A. Popov, I. Mavridis, M. Gautel, O. M. Mayans, and M. Wilmanns. 2006. Palindromic assembly of the giant muscle protein in the sarcomeric Z-disk. Nature. 439:229-233.
21. Lee, E. H., M. Gao, N. Pinotsis, M. Wilmanns, and K. Schulten. 2006. Mechanical strength of the titin Z1Z2/telethonin complex. Structure. 14:497-509.
22. Leake, M., D. Wilson, M. Gautel, and R. Simmons. 2004. The elasticity of single titin molecules using a two-bead optical tweezers assay. Biophys. J. 87:1112-1135.
23. Nagy, A., L. Grama, T. Huber, P. Bianco, K. Trombitas, H. L. Granzier, and M. S. Z. Kellermayer. 2005. Hierarchical extensibility in the PEVK domain of skeletal-muscle titin. Biophys. J. 89:329-336.
24. Sarkar, A., S. Caamano, and J. Fernandez. 2005. The elasticity of individual titin PEVK exons measured by single molecular atomic force microscopy. J. Biol. Chem. 280:6261-6264.
25. Duan, Y., J. DeKeyser, S. Damodaran, and M. Greaser. 2006. Studies on titin PEVK peptides and their interaction. Arch. Biochem. Biophys. 454:16-25.
26. Li, H., W. 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.
27. Tskhovrebova, L., J. Trinick, J. Sleep, and R. Simmons. 1997. Elasticity and unfolding of single molecules of the giant protein titin. Nature. 387:308-312.
28. 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.
29. Rief, M., M. Gautel, A. Schemmel, and H. Gaub. 1998. The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by AFM. Biophys. J. 75:3008-3014.
30. Linke, W. A., M. R. Stockmeier, M. Ivermeyer, H. Hosser, and P. Mundel. 1998. Characterizing titin's I-band Ig domain region as an entropic spring. J. Cell Sci. 111:1567-1574.
31. Marszalek, P. E., H. Lu, H. Li, M. Carrion-Vazquez, A. F. Oberhauser, K. Schulten, and J. M. Fernandez. 1999. Mechanical unfolding intermediates in titin modules. Nature. 402:100-103.
32. Carrion-Vazquez, M., A. Oberhauser, S. Fowler, P. Marszalek, S. Broedel, J. Clarke, and J. Fernandez. 1999. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA. 96:3694-3699.
33. 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.
34. Fowler, S. B., R. B. Best, J. L. T. Herrera, T. J. Rutherford, A. Steward, E. Paci, M. Karplus, and J. Clarke. 2002. Mechanical unfolding of a titin Ig domain: structure of unfolding intermediate revealed by combining AFM, molecular dynamics simulations, NMR and protein engineering. J. Mol. Biol. 322:841-849.
35. III domains in single and multiple titin molecules. Biophys. J. 80:597-605.
36. Linke, W. A., M. Kulke, H. Li, S. Fujita-Becker, C. Neagoe, D. J. Manstein, M. Gautel, and J. M. Fernandez. 2002. PEVK domain of titin: an entropic spring with actin-binding properties. J. Struct. Biol. 137:194-205.
37. Li, H. B., and J. M. Fernandez. 2003. Mechanical design of the first proximal Ig domain of human cardiac titin revealed by single molecule force spectroscopy. J. Mol. Biol. 334:75-86.
38. Williams, P. M., S. B. Fowler, R. B. Best, J. L. Toca-Herrera, K. A. Scott, A. Steward, and J. Clarke. 2003. Hidden complexity in the mechanical properties of titin. Nature. 422:446-449.
39. Kellermayer, M., S. Smith, H. Granzier, and C. Bustamante. 1997. Folding-unfolding transition in single titin modules characterized with laser tweezers. Science. 276:1112-1116.
40. Lu, H., B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:662-671.
41. Lu, H., and K. Schulten. 1999. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins: Struct., Func. Gen. 35:453-463.
42. Paci, E., and M. Karplus. 2000. Unfolding proteins by external forces and temperature: the importance of topology and energetics. Proc. Natl. Acad. Sci. USA. 97:6521-6526.
43. 10 by steered molecular dynamics. J. Mol. Biol. 323:939-950.
44. Gao, M., D. Craig, O. Lequin, I. D. Campbell, V. Vogel, and K. Schulten. 2003. Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc. Natl. Acad. Sci. USA. 100:14784-14789.
45. Craig, D., M. Gao, K. Schulten, and V. Vogel. 2004. Tuning the mechanical stability of fibronectin type III modules through sequence variation. Structure. 12:21-30.
46. Gao, M., M. Sotomayor, E. Villa, E. Lee, and K. Schulten. 2006. Molecular mechanisms of cellular mechanics. Phys. Chem. Chem. Phys. 8:3692-3706.
47. Best, R. B., S. B. Fowler, J. L. T. Herrera, A. Steward, E. Paci, and J. Clarke. 2003. Mechanical unfolding of a titin Ig domain: structure of transition state revealed by combining atomic force microscopy, protein engineering and molecular dynamics simulations. J. Mol. Biol. 330:867-877.
48. Li, P., and D. Makarov. 2003. Theoretical studies of the mechanical unfolding of the muscle protein titin: bridging the timescale gap between simulation and experiment. J. Chem. Phys. 119:9260-9268.
49. Cieplak, M., T. Hoang, and M. Robbins. 2004. Thermal effects in stretching of Gō-like models of titin and secondary structures. Proteins. 56:285-297.
50. Duff, N., N. Duong, and D. Lacks. 2006. Stretching the immunoglobulin 27 domain of the titin protein: the dynamic energy landscape. Biophys. J. 91:3446-3455.
51. Geierhaas, C., R. Best, E. Paci, M. Vendruscolo, and J. Clarke. 2006. Structural comparison of two alternative transition states for folding of titin I27. Biophys. J. 91:263-275.
52. Li, M., C. Hu, D. Klimov, and D. Thirumalai. 2006. Multiple stepwise refolding of immunoglobulin domain I27 upon force quench depends on initial conditions. Proc. Natl. Acad. Sci. USA. 103:93-98.
53. Pabon, G., and L. Amzel. 2006. Mechanism of titin unfolding by force: insight from quasi-equilibrium molecular dynamics simulations. Biophys. J. 91:467-472.
54. 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.
55. Mayans, O., J. Wuerges, S. Canela, M. Gautel, and M. Wilmanns. 2001. Structural evidence for a possible role of reversible disulphide bridge formation in the elasticity of the muscle protein titin. Structure. 9:331-340.
56. Improta, S., A. Politou, and A. Pastore. 1996. Immunoglobulin-like modules from titin I-band: extensible components of muscle elasticity. Structure. 4:323-337.
57. Trombitas, K., M. Greaser, S. Labeit, J. Jin, M. Kellermayer, M. Helmes, and H. Granzier. 1998. Titin extensibility in situ: entropic elasticity of permanently folded and permanently unfolded molecular segments. J. Cell Biol. 140:853-859.
58. Marino, M., P. Zou, D. I. Svergun, P. Garcia, C. Edlich, B. Simon, M. Wilmanns, C. Muhle-Goll, and O. Mayans. 2006. The Ig doublet Z1Z2: A model system for hybrid analysis of conformational dynamics in Ig tandems from titin. Structure. 14:1437-1447.
59. Mrosek, M., D. Labeit, S. Witt, H. Heerklotz, E. von Castelmur, S. Labeit, and O. Mayans. 2007. Molecular determinants for the recruitment of the ubiquitin-ligase MuRF-1 onto M-line titin. FASEB J. Epub ahead of publication.
60. Isralewitz, B., M. Gao, and K. Schulten. 2001. Steered molecular dynamics and mechanical functions of proteins. Curr. Opin. Struct. Biol. 11:224-230.
61. Darve, E., and A. Pohorille. 2001. Calculating free energies using average force. J. Chem. Phys. 115:9169-9183.
62. Darve, E., D. Wilson, and A. Pohorille. 2002. Calculating free energies using a scaled-force molecular dynamics algorithm. Mol. Sim. 28:113-144.
63. Rodriguez-Gomez, D., E. Darve, and A. Pohorille. 2004. Assessing the efficiency of free energy calculation methods. J. Chem. Phys. 120:3563-3578.
64. Hénin, J., and C. Chipot. 2004. Overcoming free energy barriers using unconstrained molecular dynamics simulations. J. Chem. Phys. 121:2904-2914.
65. Henin, J., K. Schulten, and C. Chipot. 2006. Conformational equilibrium in alanine-rich peptides probed by reversible stretching simulations. J. Phys. Chem. B. 110:16718-16723.
66. Reference deleted in proof.
67. Gao, M., M. Wilmanns, and K. Schulten. 2002. Steered molecular dynamics studies of titin I1 domain unfolding. Biophys. J. 83:3435-3445.
68. Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale, and K. Schulten. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802.
69. MacKerell, A. D., Jr., D. Bashford, M. Bellott, R. L. Dunbrack, Jr., J. Evanseck, M. J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph, L. Kuchnir, K. Kuczera, F. T. K. Lau, C. Mattos, S. Michnick, T. Ngo, D. T. Nguyen, B. Prodhom, I. W. E. Reiher, B. Roux, M. Schlenkrich, J. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiorkiewicz-Kuczera, D. Yin, and M. Karplus. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B. 102:3586-3616.
70. Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935.
71. Grubmüller, H., H. Heller, A. Windemuth, and K. Schulten. 1991. Generalized Verlet algorithm for efficient molecular dynamics simulations with long-range interactions. Mol. Sim. 6:121-142.
72. Schlick, T., R. Skeel, A. Brünger, L. Kalé, J. A. Board, Jr., J. Hermans, and K. Schulten. 1999. Algorithmic challenges in computational molecular biophysics. J. Comput. Phys. 151:9-48.
73. Izrailev, S., S. Stepaniants, B. Isralewitz, D. Kosztin, H. Lu, F. Molnar, W. Wriggers, and K. Schulten. 1998. Steered molecular dynamics. In Computational Molecular Dynamics: Challenges, Methods, Ideas, Vol. 4 of Lecture Notes in Computational Science and Engineering. P. Deuflhard, J. Hermans, B. Leimkuhler, A. E. Mark, S. Reich, and R. D. Skeel, editors. Springer-Verlag, Berlin.
74. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD - visual molecular dynamics. J. Mol. Graph. 14:33-38.
75. Schulten, K., Z. Schulten, and A. Szabo. 1980. Reactions governed by a binomial redistribution process. The Ehrenfest urn problem. Phys. 100A:599-614.
76. Risken, H. 1989. The Fokker-Planck Equation: Methods of Solution and Applications, 2nd Ed. Springer, New York.
77. Schulten, K. 1982. Magnetic field effects in chemistry and biology. In Festkörperprobleme, Vol. 22. J. Treusch, editor. Vieweg, Braunschweig, Germany.
78. Kac, M. 1947. Random walk and the theory of Brownian motion. Am. Math. Mon. 54:369-391.
79. Chandrasekhar, S. 1943. Stochastic problems in physics and astronomy. Rev. Mod. Phys. 15:1-89.
80. Flory, P. J. 2003. Statistical Mechanics of Polymer Chains. Hanser Publishers, Cincinnati.
81. Bird, R. B., C. F. Curtiss, R. C. Armstrong, and O. Hassager. 1987. Dynamics of Polymer Liquids. Wiley InterScience, New York.
82. Kellermayer, M., and H. Granzier. 1996. Elastic properties of single titin molecules made visible through fluorescent F-actin binding. Biochem. Biophys. Res. Commun. 221:491-497.
83. Politou, A. S., M. Gautel, S. Improta, L. Vangelista, and A. Pastore. 1996. The elastic I-band region of titin is assembled in a "modular" fashion by weakly interacting Ig-like domains. J. Mol. Biol. 255:604-616.
84. Improta, S., J. K. Krueger, M. Gautel, R. A. Atkinson, J.-F. Lefevre, S. Moulton, J. Trewhella, and A. Pastore. 1998. The assembly of immunoglobulin-like modules in titin: implications for muscle elasticity. J. Mol. Biol. 284:761-777.
85. Scott, K. A., A. Steward, S. B. Fowler, and J. Clarke. 2002. Titin; a multidomain protein that behaves as the sum of its parts. J. Mol. Biol. 315:819-829.
86. Kawakami, M., K. Byrne, D. J. Brockwell, S. E. Radford, and D. A. Smith. 2006. Viscoelastic study of the mechanical unfolding of a protein by AFM. Biophys. J. 11:1710-1716.
87. Vazina, A. A., N. F. Lanina, D. G. Alexeev, W. Bras, and I. P. Dolbnya. 2006. The structural principles of multidomain organization of the giant polypeptide chain of the muscle titin protein: SAXS/WAXS studies during the stretching of oriented titin fibers. J. Struct. Biol. 155:251-262.
88. Kellemayer, M., S. Smith, C. Bustamante, and H. Granzier. 2001. Mechanical fatigue in repetitively stretched single molecules of titin. Biophys. J. 80:852-863.
89. Gullingsrud, J., R. Braun, and K. Schulten. 1999. Reconstructing potentials of mean force through time series analysis of steered molecular dynamics simulations. J. Comp. Phys. 151:190-211.
90. Park, S., F. Khalili-Araghi, E. Tajkhorshid, and K. Schulten. 2003. Free energy calculation from steered molecular dynamics simulations using Jarzynski's equality. J. Chem. Phys. 119:3559-3566.
91. Park, S., and K. Schulten. 2004. Calculating potentials of mean force from steered molecular dynamics simulations. J. Chem. Phys. 120:5946-5961.
92. Wang, Y., K. Schulten, and E. Tajkhorshid. 2005. What makes an aquaporin a glycerol channel: a comparative study of AqpZ and GlpF. Structure. 13:1107-1118.
93. Yin, Y., M. Ø. Jensen, E. Tajkhorshid, and K. Schulten. 2006. Sugar binding and protein conformational changes in lactose permease. Biophys. J. In press.
94. Lu, H., and K. Schulten. 2000. The key event in force-induced unfolding of titin's immunoglobulin domains. Biophys. J. 79:51-65.
95. Gao, M., H. Lu, and K. Schulten. 2002. Unfolding of titin domains studied by molecular dynamics simulations. J. Muscle Res. Cell Mot. 23:513-521.
96. Marino, M., D. I. Svergun, L. Kreplak, P. V. Konarev, B. Maco, D. Labeit, and O. Mayans. 2005. Poly-Ig tandems from I-band titin share extended domain arrangements irrespective of the distinct features of their modular constituents. J. Muscle Res. Cell Mot. 26:355-365.
97. Oberhauser, A., C. Badilla-Fernandez, M. Carrion-Vazquez, and J. Fernandez. 2002. The mechanical hierarchies of fibronectin observed with single molecule AFM. J. Mol. Biol. 319:433-447.
98. Higgins, M., J. Sadler, and S. Jarvis. 2006. Frequency modulation AFM reveals individual intermediates associated with each unfolding I27 titin domain. Biophys. J. 90:640-647.
99. Sarkar, A., S. Caamano, and J. Fernandez. 2007. The mechanical fingerprint of a parallel polyprotein dimer. Biophys. J. 92:36-38.
100. Lu, H., A. Krammer, B. Isralewitz, V. Vogel, and K. Schulten. 2000. Computer modeling of force-induced titin domain unfolding. In Elastic Filaments of the Cell, Chapt. 1. J. Pollack and H. Granzier, editors. Kluwer Academic/Plenum Publishers, New York.
101. Gao, M., H. Lu, and K. Schulten. 2001. Simulated refolding of stretched titin immunoglobulin domains. Biophys. J. 81:2268-2277.
102. Mosavi, L. K., T. J. Cammett, D. C. Desrosiers, and Z. Peng. 2004. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 13:1435-1448.
103. Michaely, P., D. R. Tomchick, M. Machius, and R. G. W. Anderson. 2002. Crystal structure of a 12 ANK repeat stack from human ankyrin-R. EMBO J. 21:6387-6396.
104. Sotomayor, M., D. P. Corey, and K. Schulten. 2005. In search of the hair-cell gating spring: elastic properties of ankyrin and cadherin repeats. Structure. 13:669-682.
105. Lee, G., K. Abdi, Y. Jiang, P. Michaely, V. Bennett, and P. E. Marszalek. 2006. Nanospring behavior of ankyrin repeats. Nature. 440:246-249.
106. Boggon, T. J., J. Murray, S. Chappuis-Flament, E. Wong, B. M. Gumbiner, and L. Shapiro. 2002. C- cadherin ectodomain structure and implications for cell adhesion mechanisms. Science. 296:1308-1313.
107. Haussinger, D., T. Ahrens, H. J. Sass, O. Pertz, J. Engel, and S. Grzeslek. 2002. Calcium-dependent homoassociation of E-cadherin by NMR spectroscopy: changes in mobility, conformation, and mapping of contact regions. J. Mol. Biol. 324:823-839.