The assembly of immunoglobulin-like modules in titin: Implications for muscle elasticity

Journal of Molecular Biology

Volumn 284, Issue 3, 1998, Pages 761-777

  Improta, Sabina ^a,d   Krueger, Joanna K ^f   Gautel, Mathias ^a   Atkinson, R Andrew ^c,e   Lefèvre, Jean François ^c   Moulton, Stewart ^a   Trewhella, Jill ^f   Pastore, Annalisa ^a,b,e  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITÉ DE ROUEN   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d SANOFI   (France)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f NONE

Author keywords

Connectin; Elasticity; Ig superfamily; Muscle; NMR

Indexed keywords

CONNECTIN; DNA FRAGMENT; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; MUSCLE PROTEIN; NITROGEN 15;

ARTICLE; CHROMOSOME BAND; DNA CONFORMATION; DNA RECOMBINATION; ELASTICITY; FLEXOR REFLEX; HUMAN; LEISURE; MUSCLE CONTRACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN DOMAIN; RADIATION SCATTERING; SARCOMERE; TANDEM REPEAT;

EID: 0032484034     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2028     Document Type: Article

References (79)

1. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry, 31, 5269-5278.
2. 13C enriched proteins. J. Biomol. NMR, 1, 99-104.
3. Bodenhausen, G. & Ruben, D. J. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters, 69, 185-188.
4. Bodian, D. L., Jones, E. Y., Harlos, K., Stuart, D. I. & Davis, S. J. (1994). Crystal structure of the extracellular region of the human cell adhesion molecule CD2 at 2.5 Å resolution. Structure, 2, 755-766.
5. Bork, P., Downing, K. A., Kieffer, B. & Campbell, I. D. (1996). Structure and distribution of modules in extracellular proteins. Quart. Rev. Biophys. 29, 119-167.
6. Cantor, C. R. & Schimmel, P. R. (1980). Biophysical Chemistry. Part III. The Behaviour of Biological macromolecules, San Francisco.
7. Copié, V., Tomita, Y., Akiyama, S. K., Aota, S., Yamada, K. M., Venable, R. M., Pastor, R. W. & Krueger, S. (1998). Torchia DA solution structure and dynamics of linked cell attachment modules of mouse fibronectin containing the RGD and synergy regions: comparison with the human fibronectin crystal structure. J. Mol. Biol. 277(3), 663-682.
8. Dayie, K. T., Wagner, G. & Lefèvre, J. F. (1996). Theory and practice of nuclear spin relaxation in proteins. Annu. Rev. Phys. Chem. 47, 243-282.
9. Farrow, N. A., Zhang, O., Szabo, A., Torchia, D. A. & Kay, L. E. (1995). Spectral density function mapping using 15N relaxation data exclusively. J. Biomol. NMR, 6, 162-163.
10. Fesik, S. W. & Zuiderweg, E. R. P. (1988). Heteronuclear three-dimensional NMR spectroscopy: a strategy for the simplification of homonuclear two-dimensional NMR spectra. J. Magn. Reson. 78, 588-593.
11. Freund, C., Ross, A., Plückthun, A. & Holak, T. A. (1994). Structural and dynamic properties of the Fv fragment and the single-chain Fv fragment of an antibody in solution investigated by heteronuclear three-dimensional NMR spectroscopy. Biochemistry, 33, 3296-3303.
12. Funatsu, T. (1993). Elastic filaments in situ in cardiac muscles: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. J. Cell Biol. 120, 711-724.
13. Fürst, D. O., Osborn, M., Nave, R. & Wever, K. (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.
14. Gautel, M. & Goulding, D. (1996). A molecular map of titin/connectin elasticity reveals two different mechanisms acting in series. FEBS Letters, 385, 11-14.
15. Gautel, M., Leehtonen, E. & Pietruschka, F. (1996). Assembly of the cardiac I-band region of titin/connectin: expression of the cardiac-specific regions and their structural relation to the elastic segments. J. Muscle Res. Cell Motil. 17(4), 449-461.
16. Grzesiek, S. & Bax, A. (1992). Improved 3D triple resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson, 96, 432-440.
17. Guinier, A. (1939). La diffraction des rayon X aux tres petit angles; application à l'étude de phǹom'enes ultramicroscopiques. Ann. Phys. (Paris), 12, 161.
18. Heidorn, D. B. & Trewhella, J. (1988). Comparison of the crystal and solution structures of calmodulin and troponin C. Biochemistry, 27, 909-915.
19. Higuchi, H., Nakauchi, Y., Maruyama, K. & Fujime, S. (1993). Characterization of β-connectin (titin 2) from striated muscle by dynamic light scattering. Biophys. J. 65, 1906-1915.
20. 15N]glycine benzyl ester. J. Am. Chem. Soc. 110, 2378-2383.
21. Horowits, R. (1992). Passive force generation and titin isoforms in mammalian skeletal muscle. Biophys. J. 61, 392-398.
22. Horowits, R., Maruyama, K. & Podolsky, R. J. (1989). Elastic behavior of connectin filaments during thick filament movement in activated skeletal muscle. J. Cell Biol. 109, 2169-2176.
23. Huber, A. H., Wang, Y. M., Bieber, A. J. & Bjorkman, P. J. (1994). Crystal structure of tandem type-III fibronectin domains from Drosophila neuroglian at 2.0 A. Neuron, 12, 717-731.
24. Improta, S., Politou, A. S. & Pastore, A. (1996). Immunoglobulin-like modules from titin I-band: extensible components of muscle elasticity. Structure, 4, 323-337.
25. Ishima, R. & Nagayama, K. (1995). Quasi-spectral-density function analysis for nitrogen-15 nuclei in proteins. J. Magn. Reson. Ser. B, 108, 73-76.
26. Jacrot, B. & Zaccai, G. (1981). Determination of molecular weight by neutron scattering. Biopolymers, 20, 2413-2426.
27. Kadkhodaei, M., Hwang, T. & Shaka, A. J. (1993). A simple windowless mixing sequence to suppress cross relaxation in TOCSY experiments. J. Magn. Reson. ser. A, 105, 104-107.
28. Kay, L. E., Ilura, M., Tschudn, R. & Bax, A. (1990). Three-dimensional triple-resonance NMR spectroscopy of isotopically enriched proteins. J. Magn. Reson. 89, 496-514.
29. Keller, T. C. S. (1995). Structure and function of titin and nebulin. Curr. Opin. Cell Biol. 7, 32-38.
30. Kellermayer, M. S. Z., Smith, S. B., Granzier, H. L. & Bustamante, C. (1997). Folding-unfolding transitions in single titin molecules characterized with forcemeasuring laser tweezers. Science, 276, 1112-1116.
31. Krigbaum, W. R. & Kugler, F. R. (1970). Molecular conformation of egg-white lysozyme and bovine alphalactalbumin in solution. Biochemistry, 9, 1216-1223.
32. Labeit, S. & Kolmerer, B. (1995). Titins, giant proteins in charge of muscle ultrastructure and elasticity. Science, 270, 293-296.
33. Labeit, S. (1990). A regular pattern of two types of 100-residue motif in the sequence of titin. Nature, 345, 273-276.
34. Lai, C. S., Wolff, C. E., Novello, D., Griffone, L., Cuiberti, C., Molina, F. & Rocco, M. (1993). Solution structure of human plasma fibronectin under different solvent conditions. J. Mol. Biol. 230, 625-640.
35. Lefèvre, J. F., Dayie, K. T., Peng, J. W. & Wagner, G. (1996). Internal mobility in the partially folded DNA binding and dimerization domains of GAL4: NMR analysis of the N-H spectral density functions. Biochemistry, 35, 2674-2686.
36. Linke, W. A., Ivemeyer, M., Olivieri, M., Kolmerer, B., Ruegg, C. & Labeit, S. (1996). Towards a molecular understanding of the elasticity of titin. J. Mol. Biol. 261, 62-71.
37. Linke, W. A., Ivemeyer, M., Mundel, P., Stockmeier, M. R. & Kolmerer, B. (1998a). Nature of PEVK-titin elasticity in skeletal muscle. Proc. Natl Acad. Sci. USA, 95(14), 8052-8057.
38. Linke, W. A., Stockmeier, M. R., Ivemeyer, M., Hosser, H. & Mündel, P. (1998b). Characterizing titin's I-band Ig domain region as an entropic spring. J. Cell. Sci. 111, 1567-1574.
39. Lipari, G. & Szabo, A. (1982a). Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Analysis of experimental results. J. Am. Chem. Soc. 104, 4546-4559.
40. Lipari, G. & Szabo, A. (1982b). Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Theory and range of validity. J. Am. Chem. Soc. 104, 4559-4570.
41. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 113, 967-974.
42. Marion, D., Ikura, M., Tschudin, R. & Bax, A. (1989a). Rapid recording of 2D NMR spectra without phase-cycling: application to the study of hydrogen exchange in proteins. J. Magn. Reson. 85, 393-399.
43. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple. Biochemistry, 28, 6150-6156.
44. Maruyama, K. (1994). Connectin, an elastic protein of striated muscle. Biophys. Chem. 50, 73-85.
45. Maruyama, K. (1997). Connectin/titin, giant elastic protein of muscle. FASEB J. 11, 341-345.
46. McEvoy, M. M., de la Cruz, A. F. & Dahlquist, F. W. (1997). Large modular proteins by NMR. Nature Struct. Biol. 4, 1.
47. Moore, P. B. (1980). Small-angle scattering. Information content and error analysis. J. Appl. Crystallog. 13, 168.
48. Moreau, M., de Cock, E., Fortier, P. L., Garcia, C., Albaret, C., Blanquet, S., Lallemand, J. Y. & Dardel, F. (1997). Heteronuclear NMR studies of E. coli translation initiation factor IF3. Evidence that the inter-domain region is disordered in solution. J. Mol. Biol. 266, 15-22.
49. Nave, R., Fürst, D. O. & Weber, K. (1989). Visualization of the polarity of isolated titin molecule: a single globular head on a long thin rod as the M-band anchoring domain? J. Cell. Biol. 109, 2177-2187.
50. Neidig, P. (1995). AURELIA, a program for computer-aided analysis of multidimensional NMR spectra. J. Biomol. NMR, 6, 255-270.
51. Peng, J. W. & Wagner, G. (1995). Frequency spectrum of NH bonds in eglin c from spectral density mapping at multiple fields. Biochemistry, 34, 16733-16752.
52. Pfuhl, M., Improta, S., Politou, A. S. & Pastore, A. (1997). When a module is also a domain: the role of the N terminus in the stability and the dynamics of immunoglobulin domains from titin. J. Mol. Biol. 265, 242-256.
53. Phan, I. Q. H., Boyd, J. & Campbell, I. D. (1997). Dynamic studies of a fibronectin type I module pair at three frequencies: anisotropic modelling and direct determination of conformational exchange. J. Biomol. NMR, 8, 369-378.
54. Pilz, I. (1982). Small Angle X-ray Scattering (Glatter, O. & Kratky, O., eds), pp. 244-246, Academic Press, New York.
55. Piotto, M., Saudek, V. & Sklenar, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
56. Politou, A. S., Gautel, M., Pfuhl, M., Labeit, S. & Pastore, A. (1994a). Immunoglobulin-type domains of titin: same fold, different stability? Biochemistry, 33, 4730-4737.
57. Politou, A. S., Gautel, M., Joseph, C. & Pastore, A. (1994b). Immunoglobulin-like domains of titin are stabilized by amino-terminal extension. FEBS Letters, 352, 27-31.
58. Politou, A. S., Thomas, D. J. & Pastore, A. (1995). The folding and stability of titin immunoglobulin-like modules, with implications for the mechanism of elasticity. Biophys. J. 69, 2601-2610.
59. Politou, A. S., Gautel, M., Improta, S., Bangelista, L. & Pastore, A. (1996). The elastic I-band region of titin is assembled by weakly interacting Ig-like domains. J. Mol. Biol. 255, 604-616.
60. Porod, G. (1982). Small Angle X-ray Scattering (Glatter, O. & Kratky, O., eds), pp. 17-51, Academic Press, New York.
61. Rief, M., Gautel, M., Oestehelt, F., Fernandez, J. M. & Gaub, H. E. (1997). Reversible unfolding of individual titin Ig-domains by AFM. Science, 276, 1109-1112.
62. Shaka, A. J., Barker, P. B. & Freeman, R. (1985). Computer-optimized decoupling scheme for wideband applications and low-level operation. J. Magn. Reson. 64, 547-552.
63. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson. ser. A, 102, 241-245.
64. Spitzfaden, C., Grant, R. P., Mardon, H. J. & Campbell, I. D. (1997). Module-module interactions in the cell binding region of fibronectin: stability, flexibility and specificity. J. Mol. Biol. 265, 565-579.
65. 2+ binding to the first EGF domain. A combined NMR small-angle X-ray scattering study. Biochemistry, 35, 11547-11559.
66. Svergun, D. I., Semenyuk, A. V. & Feigen, L. A. (1988). Small-angle scattering data treatment by the regularization method. Acta Crystallog. sect. A, 44, 244.
67. Treloar, L. R. G. (1975). The Physics of Rubber Elasticity, Clarendon Press, Oxford.
68. Trewhella, J. (1994). Conformational flexibility in biochemical regulation. In Structural Biology: State of the Art 1993 (Sarma, H. & Sarma, M. H., eds), vol. I, pp. 43-47, Proceedings of the Eighth Conversations, Adenine Press.
69. Trewhella, J. (1997). Insights into biomolecular function from small-Angle scattering. Curr. Opin. Struct. Biol. 7, 702-708.
70. Trinick, J. (1994). Titin and nebulin: protein rulers in muscle? Trends Biochem. Sci. 19, 405-408.
71. Trinick, J. (1996). Cytoskeleton: titin as a scaffold and spring. Curr. Biol. 6, 258-260.
72. Trombitas, P. H. W. W., Baatsen, M. S. Z., Kellermayer, & Pollack, G. H. (1991). Nature and origin of gap filaments in striated muscle. J. Cell. Sci. 100, 809-814.
73. Tskhovrebov, L., Trinick, J., Sleep, J. A. & Simmons, R. M. (1997). Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature, 387, 308-312.
74. 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.
75. Witt, C. C., Olivieri, N., Centner, T., Kolmerer, B., Millevoi, S., Morell, J., Labeit, D., Labeit, S., Jockusch, H. & Pastore, A. A. (1998). Survey of the primary structure and the interspecies conservation of I-band Titin's elastic elements in vertebrates. J. Struct. Biol. 122, 206-215.
76. Woessner, D. E. (1962). Nuclear spin relaxation in ellipsoids undergoind Brownian motion. J. Chem. Phys. 37, 647-654.
77. Wyss, D. F., Dayie, K. T. & Wagner, G. (1997). The counterreceptor binding site of human CD2 exhibits an extended surface patch with multiple conformations fluctuating with millisecond to microsecond motions. Protein Sci. 6, 534-542.
78. 15N NMR relaxation. Biochemistry, 34, 5212-5223.
79. Zhou, H., McEvoy, M. M., Lowry, D. F., Swanson, R. V., Simon, M. I. & Dalquist, F. W. (1996). Phosphotransfer and CheY-binding domains of the histidine autokinase CheA are joined by a flexible linker. Biochemistry, 35, 433-443.