Structure and stability of an immunoglobulin superfamily domain from twitchin, a muscle protein of the nematode caenorhabditis elegrans

Journal of Molecular Biology

Volumn 264, Issue 3, 1996, Pages 624-639

  Fong, Sun ^a   Hamill, Stefan J ^a   Proctor, Mark ^a   Freund, Stefan M V ^a   Benian, Guy M ^b   Chothia, Cyrus ^c   Bycroft, Mark ^a   Clarke, Jane ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

I set; Immunoglobulin; NMR structure; Protein folding; Structure prediction

Indexed keywords

CONNECTIN; IMMUNOGLOBULIN; MUSCLE PROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; IMMUNOGLOBULIN STRUCTURE; KINETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; THERMODYNAMICS;

EID: 0030573054     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0665     Document Type: Article

References (50)

1. Axe, D. D., Foster, N. W. & Fersht, A. R. (1996). Active barnase variants with completely random hydrophobic cores. Proc. Natl Acad. Sci. USA, 93, 2172-2175.
2. Bateman, A., Eddy, S. R. & Chothia, C. (1996). Members of the immunoglobulin superfamily in bacteria. Protein Sci. 5, 1936-1942.
3. Bax, A. & Davis, D. G. (1985). MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360.
4. 13C-enriched proteins. J. Magn. Reson. 88, 425-431.
5. Benian, G. M., Kiff, J. E., Neckelmann, N., Moerman, D. G. & Waterson, R. H. (1989). Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature, 342, 45-50.
6. Benian, G. M., L'Hernault, S. W. & Morris, M. E. (1993). Additional sequence complexity in the muscle gene unc-22 and its encoded protein twitchin of Caenorhabditis elegans. Genetics, 134, 1097-1104.
7. Bodenhausen, G. & Ruben, D. L. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters, 69, 185-188.
8. Bork, P., Holm, L. & Sander, C. (1994). The immunoglobulin fold. J. Mol. Biol. 242, 309-320.
9. Chothia, C. & Lesk, A. M. (1987). Canonical structures for the hypervariable regions of immunoglobulins. J. Mol. Biol. 196, 901-917.
10. Chothia, C., Lesk, A. M., Tramontano, A., Levitt, M., Smith-Gill, S. J., Air, G., Sheriff, S., Padlan, E. A., Davies, D., Tulip, W. R., Colman, P. M., Spinelli, S., Alzari, P. M. & Poljak, R. J. (1989). Conformations of immunoglobulin hypervariable regions. Nature, 342, 877-883.
11. Clarke, J. & Fersht, A. R. (1993). Engineering disulfide bonds as probes of the folding pathway of barnase: increasing the stability of proteins against the rate of denaturation. Biochemistry, 32, 4322-4329.
12. Erickson, H. P. (1994). Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl Acad. Sci. USA, 91, 10114-10118.
13. Eriksson, A. E., Baase, W. A., Zhang, X. J., Heinz, D. W., Blaber, M., Baldwin, E. P. & Matthews, B. W. (1992). Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science, 255, 178-183.
14. Grzesiek, S. & Bax, A. (1992a). Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR. J. Am. Chem. Soc. 114, 6291-6293.
15. Grzesiek, S. & Bax, A. (1992b). Improved 3D triple-resonance NMR techniques applied to a 31 kDa protein. J. Magn. Reson. 96, 432-440.
16. Harpaz, Y. & Chothia, C. (1994). Many of the immunoglobulin superfamily domains in cell adhesion molecules and surface receptors belong to a new structural set which is close to that containing variable domains. J. Mol. Biol. 238, 528-539.
17. Heierhorst, J., Probst, W. C., Kohanski, R. A., Buku, A. & Weiss, K. R. (1995). Phosphorylation of myosin regulatory light chains by the molluscan twitchin kinase. Eur. J. Biochem. 233, 426-431.
18. 2+/S100 regulation of giant protein kinases. Nature, 380, 636-639.
19. Holden, H. M., Ito, M., Hartshorne, D. J. & Rayment, I. (1992). X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase, at 2.8 Å resolution. J. Mol. Biol. 227, 840-851.
20. Hu, S.-H., Parker, M. W., Lei, J. Y., Wilce, M. C. J., Benian, G. M. & Kemp, B. E. (1994). Insights into autoregulation from the crystal structure of twitchin kinase. Nature, 369, 581-584.
21. Improta, S., Politou, A. & Pastore, A. (1996). Immunoglobulin-like modules from titin I-band: extensible components of muscle elasticity. Structure, 4, 323-337.
22. Jones, E. Y., Harlos, K., Bottomley, M. J., Robinson, R. C., Driscoll, P. C., Edwards, R. M., Clements, J. M., Dudgeon, T. J. & Stuart, D. I. (1995). Crystal-structure of an integrin-binding fragment of vascular cell-adhesion molecule-1 at 1.8 angstrom resolution. Nature, 373, 539-544.
23. Karpusas, M., Baase, W. A., Matsumura, M. & Matthews, B. W. (1989). Hydrophobic packing in T4 lysozyme probed by cavity-filling mutants. Proc. Natl Acad. Sci. USA, 86, 8237-8241.
24. Kay, L. E., Keifer, P. & Saarinen, T. (1992). Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
25. Kellis, J. T., Nyberg, K., Sali, D. & Fersht, A. R. (1988). Contribution of hydrophobic interactions to protein stability. Nature, 333, 784-786.
26. Kraulis, P. (1991). MolScript, a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
27. Labeit, S. & Kolmerer, B. (1995). Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science, 270, 293-296.
28. Labeit, S., Gautel, M., Lakey, A. & Trinick, J. (1992). Towards a molecular understanding of titin. EMBO J. 11, 1711-1716.
29. Lei, J., Tang, X., Chambers, T. C., Pohl, J. & Benian, G. M. (1994). Protein kinase domain of twitchin has protein kinase activity and an autoinhibitory region. J. Biol. Chem. 269, 21078-21085.
30. Lesk, A. M. & Chothia, C. (1982). Evolution of proteins formed by β-sheets II. The core of the immunoglobulin domains. J. Mol. Biol. 160, 325-342.
31. Lim, W. A. & Sauer, R. T. (1991). The role of internal packing interactions in determining the structure and stability of a protein. J. Mol. Biol. 219, 359-376.
32. 13C assignments of barstar using nuclear magnetic resonance spectroscopy. Biochemistry, 33, 8866-8877.
33. 15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy. Application to interleukin 1β. Biochemistry, 28, 6150-6156.
34. Milla, M. E. & Sauer, R. T. (1995). Critical side-chain interactions at a subunit interface in the arc repressor dimer. Biochemistry, 34, 3344-3351.
35. 2O. J. Magn. Reson. ser. B, 102, 317-321.
36. Okagaki, T., Weber, F. E., Fischman, D. A., Vaughan, K. T., Mikawa, T. & Reinach, F. C. (1993). The major myosin-binding domain of skeletal muscle MyBP-C (C protein) in the COOH-terminal, immunoglobulin C2 motif. J. Cell. Biol. 123, 619-626.
37. Pace, C. N. (1986). Determination and analysis of urea and guanidinium denaturation curves. Methods Enzymol. 131, 266-279.
38. Pfuhl, M. & Pastore, A. (1995). Tertiary structure of an immunoglobulin-like domain from the giant muscle protein titin: a new member of the I set. Structure, 3, 391-401.
39. Piotto, M., Saudek, V. & Sklenar, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
40. Politou, A. S., Gautel, M., Joseph, C. & Pastore, A. (1994a). Immunoglobulin-type domains of titin are stabilized by amino-terminal extension. FEBS Letters, 352, 27-31.
41. Politou, A. S., Gautel, M., Pfuhl, M., Labeit, S. & Pastore, A. (1994b). Immunoglobulin-type domains of titin: same fold, different stability? Biochemistry, 33, 4730-4737.
42. Politou, A. S., Gautel, M., Improta, S., Vangelista, L. & Pastore, A. (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.
43. Probst, W. C., Cropper, E. C., Heierhorst, J., Hooper, S. L., Jaffe, H., Vilim, F., Beushausen, S., Kupfermann, I. & Weiss, K. R. (1994). cAMP-dependent phosphorylation of Aplysia twitchin may mediate modulation of muscle contractions by neuropeptide cotransmitters. Proc. Natl Acad. Sci. USA, 91, 8487-8491.
44. Serrano, L., Kellis, J. T., Jr, Cann, P., Matouschek, A. & Fersht, A. R. (1992). The folding of an enzyme II. Substructure of barnase and the contribution of different interactions to protein stability. J. Mol. Biol. 224, 783-804.
45. Shirinsky, V. P., Vorotnikov, A. V., Birukov, K. G., Nanaev, A. K., Collinge, M., Lukas, T. J., Sellers, J. R. & Watterson, D. M. (1993). A kinase-related protein stabilizes unphosphorylated smooth muscle myosin minifilaments in the presence of ATP. J. Biol. Chem. 268, 16578-16583.
46. Stonehouse, J. & Keeler, J. (1995). A convenient and accurate method for the measurement of the values of spin-spin coupling constants. J. Magn. Reson. ser. A, 112, 43-57.
47. 13C-labelling. J. Biol. NMR, 2, 323-334.
48. Thomsen, N. K., Soroka, V., Jensen, P. H., Berezin, V., Kiselyov, V. V., Bock, E. & Poulsen, F. M. (1996). The three-dimensional structure of the first domain of neural cell adhesion molecule. Nature Struct. Biol. 3, 581-585.
49. Williams, A. F. & Barclay, A. N. (1988). The immunoglobulin superfamily - domains for cell surface recognition. Annu. Rev. Immunol. 6, 381-405.
50. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. John Wiley & Sons, New York.