Malleable conformation of the elastic PEVK segment of titin: Non-co-operative interconversion of polyproline II helix, β-turn and unordered structures

Biochemical Journal

Volumn 374, Issue 3, 2003, Pages 687-695

  Ma, Kan ^a   Wang, Kuan ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

Circular dichroism (CD); Elastic protein; Nuclear magnetic resonance (NMR); Polyproline II helix coil (PhC) motif; Titin; Trans to cis proline isomerization

Indexed keywords

ELASTICITY; HIGH TEMPERATURE EFFECTS; LOW TEMPERATURE EFFECTS; NUCLEAR MAGNETIC RESONANCE; STRUCTURE (COMPOSITION);

SIDE CHAINS;

PROTEINS;

CONNECTIN; PEPTIDE; PROLINE; PROLYLGLUTAMYLVALYLLYSINE; UNCLASSIFIED DRUG; GLUTAMIC ACID; INORGANIC SALT; LYSINE; MUSCLE PROTEIN; PROTEIN KINASE; TRIFLUOROETHANOL; UREA; VALINE;

ARTICLE; CIRCULAR DICHROISM; IONIC STRENGTH; ISOMERISM; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; POLARIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN MOTIF; ROOM TEMPERATURE; TEMPERATURE DEPENDENCE; AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMISTRY; DRUG EFFECT; ELASTICITY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; OSMOLARITY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STEREOISOMERISM;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; ELASTICITY; GLUTAMIC ACID; HUMANS; LYSINE; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OSMOLAR CONCENTRATION; PEPTIDES; PROLINE; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SALTS; STEREOISOMERISM; TRIFLUOROETHANOL; UREA; VALINE;

EID: 0141567671     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20030702     Document Type: Article

References (50)

1. Wang, K., McClure, J. and Tu, A. (1979) Titin: major myofibrillar components of striated muscle. Proc. Natl. Acad. Sci. U.S.A. 76, 3698-3702
2. Maruyama, K., Kimura, S., Ohashi, K. and Kuwano, Y. (1981) Connectin, an elastic protein of muscle: identification of "titin" with connectin. J. Biochem. (Tokyo) 89, 701-709
3. Bang, M. L., Centner, T., Fornoff, F., Geach, A. J., Gotthardt, M., McNabb, M., Witt, C. C., Labeit, D., Gregorio, C. C., Granzier, H. and Labeit, S. (2001) The complete gene sequence of titin, expression of an unusual 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circ. Res. 89, 1065-1072
4. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A. et al. (2001) The sequence of the human genome. Science 291, 1304-1351
5. Horowits, R. (1999) The physiological role of titin in striated muscle. Rev. Physiol. Biochem. Pharmacol. 138, 57-96
6. Wang, K., Forbes, J. G. and Jin, A. J. (2001) Single molecule measurements of titin elasticity. Prog. Biophys. Mol. Biol. 77, 1-44
7. Young, P., Ferguson, C., Bauelos, S. and Gautel, M. (1998) Molecular structure of the sarcomeric Z-disk: two types of titin interactions lead to an asymmetrical sorting of α-actinin. EMBO J. 17, 1614-1624
8. Labeit, S. and Kolmerer, B. (1995) Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270, 293-296
9. Linke, W. A., Ivemeyer, M., Mundel, P., Stockmeier, M. R. and Kolmerer, B. (1998) Nature of PEVK-titin elasticity in skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 95, 8052-8057
10. Freiburg, A., Trombitas, K., Wolfgang, H., Cazorla, O., Fougerousse, F., Centner, T., Kolmerer, B., Witt, C., Beckmann, J. S., Gregorio et al. (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
11. Gutierrez-Cruz, G., Van Heerden, A. and Wang, K. (2001) Modular motif, structural folds and affinity profiles of PEVK segment of human fetal skeletal muscle titin. J. Biol. Chem. 276, 7442-7449
12. Yamasaki, R., Berri, M., Wu, Y., Trombitas, K., McNabb, M., Kellermayer, M. S., Witt, C., Labeit, D., Labeit, S., Greaser, M. and Granzier, H. (2001) Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys. J. 81, 2297-2313
13. Ma, K. and Wang, K. (2002) Interaction of nebulin SH3 domain with titin PEVK and myopalladin: implications for the signaling and assembly role of titin and nebulin. FEBS Lett. 532, 273-278
14. Politou, A. S., Spadaccini, R., Joseph, C., Brannetti, B., Guerrini, R., Helmer-Citterich, M., Salvadori, S., Temussi, P. A. and Pastore, A. (2002) The SH3 domain of nebulin binds selectively to type II peptides: theoretical prediction and experimental validation. J. Mol. Biol. 16, 305-315
15. Labeit, S., Kolmerer, B. and Linke, W. A. (1997) The giant protein titin: emerging roles in physiology and pathophysiology. Circ. Res. 80, 290-294
16. Bustamante, C., Marko, J. F., Siggia, E. D. and Smith, S. (1994) Entropic elasticity of λ-phage DNA. Science 265, 1599-1600
17. Greaser, M. (2001) Identification of new repeating motifs in titin. Proteins 43, 145-149
18. Wang, M. D., Yin, H., Landick, R., Gelles, J. and Block, S. M. (1997) Stretching DNA with optical tweezers. Biophys. J. 72, 1335-1346
19. Machado, C. and Andrew, D. J. (2000) D-titin: a giant protein with dual roles in chromosomes and muscles. J. Cell Biol. 151, 639-651
20. Fukuzawa, A., Shimamura, J., Takemori, S., Kanzawa, N., Yamaguchi, M., Sun, P., Maruyama, K. and Kimura, S. (2001) Invertebrate connectin spans as much as 3.5 μm in the giant sarcomeres of crayfish claw muscle. EMBO J. 20, 4826-4835
21. Flaherty, D. B., Gernert, K. M., Shmeleva, N., Tang, X., Mercer, K. B., Borodovsky, M. and Benian, G. M. (2002) Titins in C. elegans with unusual features: coiled-coil domains, novel regulation of kinase activity and two new possible elastic regions. J. Mol. Biol. 323, 533-549
22. Champagne, M. B., Edwards, K. A., Erickson, H. P. and Kiehart, D. P. (2000) Drosophila stretchin-MLCK is a novel member of the titin/myosin light chain kinase family. J. Mol. Biol. 300, 759-777
23. Ma, K., Kan, L. and Wang, K. (2001) Polyproline II helix is a key structural motif of the elastic PEVK segment of titin. Biochemistry 40, 3427-3438
24. Perczel, A., Hollosi, M., Tusnady, G. and Fasman, G. D. (1991) Convex constraint analysis: a natural deconvolution of circular dichroism curves of proteins. Protein Eng. 4, 669-679
25. Perczel, A., Park, K. and Fasman, G. D. (1992) Analysis of the circular dichroism spectrum of proteins using the convex constraint algorithm: a practical guide. Anal. Biochem. 203, 83-93
26. Greenfield, N. J. (1996) Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal. Biochem. 235, 1-10
27. Sreerama, N. and Woody, R. W. (1994) Poly(pro)ll helices in globular proteins: identification and circular dichroic analysis. Biochemistry 33, 10022-10025
28. Sreerama, N. and Woody, R. W. (1994) Protein secondary structure from circular dichroism spectroscopy: combining variable selection principle and cluster analysis with neural network, ridge regression and self-consistent methods. J. Mol. Biol. 242, 497-507
29. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
30. Bax, A. and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360
31. Bax, A. and Davis, D. G. (1985) Practical aspects of two-dimensional transverse NOE spectroscopy. J. Magn. Reson. 63, 207-215
32. Ronish, E. W. and Krimm, S. (1974) The calculated circular dichroism of polyproline II in the polarizability approximation. Biopolymers 13, 1635-51
33. Rabanal, F., Ludevid, M. D., Pons, M. and Giralt, E. (1993) CD of proline-rich polypeptides: application to the study of the repetitive domain of maize glutelin-2. Biopolymers 33, 1019-1028
34. Woody, R. W. (1996) In Circular Dichroism and the Conformational Analysis of Biomolecules (Fasman, G. D., ed.), pp. 25-68, Plenum Press, New York
35. 2 cyclic hexapeptides, preferred β-turn conformers and implications for β turns in proteins. Biochemistry 20, 4730-4738
36. Buck, M. (1998) Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 31, 297-355
37. Hutchinson, E. G. and Thornton, J. M. (1994) A revised set of potentials for β-turn formation in proteins. Protein Sci. 3, 2207-2216
38. Nagpal, S., Gupta, V., Kaur, K. J. and Salunke, D. M. (1999) Structure-function analysis of tritrypticin, an antibacterial peptide of innate immune origin. J. Biol. Chem. 274, 23296-23304
39. Bienkiewicz, E. A., Moon Woody, A. and Woody, R. W. (2000) Conformation of the RNA polymerase II C-terminal domain: circular dichroism of long and short fragments. J. Mol. Biol. 297, 119-133
40. Matsushima, N., Creutz, C. E. and Kretsinger, R. H. (1990) Polyproline, β-turn helices: novel secondary structures proposed for the tandem repeats within rhodopsin, synaptophysin, synexin, gliadin, RNA polymerase II, hordein, and gluten. Proteins 7, 125-185
41. 1H NMR conformations and evidence for a KG/PG multiple turn repeat motif in the all-trans proline state. Biochemistry 30, 8251-8267
42. Gothel, S. F. and Marahiel, M. A. (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell. Mol. Life Sci. 55, 423-436
43. 1H-NMR. Biopolymers 34, 1221-1230
44. Ma, K. and Wang, K. (2003) Binding of copper(II) ions to the polyproline II helices of PEVK modules of the giant elastic protein titin as revealed by ESI-MS, CD and NMR. Biopolymers, in the press
45. Blanch, E. W., Morozova-Roche, L. A., Cochran, D. A., Doig, A. J., Hecht, L. and Barron, L. D. (2000) Is polyproline II helix the killer conformation? A Raman optical activity study of the amyloidogenic prefibrillar intermediate of human lysozyme. J. Mol. Biol. 301, 553-563
46. Uversky, V. N. (2002) What does it mean to be natively unfolded? Eur. J. Biochem. 269, 2-12
47. Creamer, T. P. and Campbell, M. N. (2002) Determinants of the polyproline II helix from modeling studies. Adv. Protein Chem. 62, 263-282
48. Shi, Z., Woody, R. W. and Kallenbach, N. R. (2002) Is polyproline II a major backbone conformation in unfolded proteins? Adv. Protein Chem. 62, 163-240
49. Cox, C. and Lectka, T. (2000) Synthetic catalysis of amide isomerization. Acc. Chem. Res. 33, 849-858
50. Forbes, J. G., Jin, A. J., Ma, K. and Wang, K. (2003) Elasticity of the PEVK segment of titin is dominated by sequence-specific charge pairing interactions. Biophys. J. 84, 140a