Structural and Functional Studies of Titin's fn3 Modules Reveal Conserved Surface Patterns and Binding to Myosin S1 - A Possible Role in the Frank-Starling Mechanism of the Heart

Journal of Molecular Biology

Volumn 313, Issue 2, 2001, Pages 431-447

  Muhle Goll, Claudia ^a,c   Habeck, Michael ^a,d   Cazorla, Olivier ^b   Nilges, Michael ^a,d   Labeit, Siegfried ^b,c   Granzier, Henk ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d INSTITUT PASTEUR   (France)

Author keywords

Fibronectin type III; Molecular modeling; Muscle contraction; Striated muscle; Titin

Indexed keywords

STURNUS VULGARIS;

CALCIUM; CONNECTIN; FIBRONECTIN; IMMUNOGLOBULIN; MUSCLE PROTEIN; MYOSIN SUBFRAGMENT; PEPTIDE FRAGMENT; PROTEIN KINASE; SOLVENT;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; HEART CONTRACTION; HEART MUSCLE; HEART VENTRICLE; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; RABBIT; SARCOMERE; SEQUENCE ALIGNMENT; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CONSERVED SEQUENCE; FIBRONECTINS; HEART VENTRICLES; HUMANS; IMMUNOGLOBULINS; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOSIN SUBFRAGMENTS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RABBITS; SARCOMERES; SEQUENCE ALIGNMENT; SOLVENTS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0035914471     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.2001.5017     Document Type: Article

References (35)

1. Maruyama K., Matsubara S., Natori R., Nonomura Y., Kimura S., Ohashi K. et al. Connectin, an elastic protein of muscle: characterization and function. J. Biochem. (Tokyo). 82:1977;317-337.
2. Wang K., Ramirez-Mitchell R. Titin, a huge protein from vertebrate skeletal muscle. J. Cell Biol. 83:1979;389.
3. Trinick J. Titin and nebulin: protein rulers in muscle? Trends Biochem. Sci. 19:1994;405-409.
4. Gregorio C. G., Granzier H., Sorimachi H., Labeit S. Muscle assembly: a titanic achievement? Curr. Opin. Cell Biol. 11:1999;18-25.
5. Labeit S., Kolmerer B. Titins: giant poteins in charge of muscle ultrastructure and elasticity. Science. 270:1995;293-296.
6. Fürst D. O., Vinkemeier U., Weber K. Mammalian skeletal muscle C-protein: purification from bovine muscle, binding to titin and the characterization of a full-length human c-DNA. J. Cell Sci. 102:1992;769-778.
7. Soteriou A., Gamage M., Trinick J. A survey of interactions made by the giant muscle protein titin. J. Cell Sci. 104:1993;119-123.
8. Houmeida A., Holt J., Tskhovrebova L., Trinick J. Studies of the interaction between Titin and Myosin. J. Cell Biol. 131:1995;1471-1481.
9. Craig R., Offer G. The location of C-Protein in rabbit skeletal muscle. Proc. Roy. Soc. London B. 192:1976;451-461.
10. Labeit S., Gautel M., Lakey A., Trinick J. Towards a molecular understanding of titin. EMBO J. 11:1992;1711-1716.
11. Freiburg A., Gautel M. A molecular map of the interactions between titin and myosin-binding protein C. Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy. Eur. J. Biochem. 235:1996;317-323.
12. Muhle-Goll C., Pastore A., Nilges M. The three-dimensional structure of a type I module from titin: a prototype of intracellular fibronectin type III domains. Structure. 6:1998;1291-1302.
13. Fraternali F., Pastore A. Modularity and homology: modeling of the type II module family from titin. J. Mol. Biol. 290:1999;581-593.
14. Allen D. G., Kentish J. The cellular basis of the length-tension relation in cardiac muscle. J. Mol. Cell. Cardiol. 17:1985;821-840.
15. Schneider T. D., Stephens R. M. Sequence logos: a new way to display consensus sequences. Nucl. Acids Res. 18:1990;6097-6100.
16. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
17. Šali A., Blundell T. L. Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234:1993;778-815.
18. Sippl M. J. Recognition of errors in three-dimensional structures of proteins. Proteins: Struct. Funct. Genet. 17:1993;355-362.
19. Vriend G., Sander C. Quality control of protein models: directional atomic contact analysis. J. Appl. Crystallog. sect. A. 26:1993;47-60.
20. Schultz J., Milpetz F., Bork P., Ponting C. P. SMART, a simple modular architecture research tool: identification of signalling domains. Proc. Natl Acad. Sci. USA. 95:1998;5857-5864.
21. Ayme-Southgate A., Southgate R., McEliece M. K. Drosophila projectin: a look at protein structure and sarcomeric assembly. Adv. Exp. Med. Biol. 481:2000;262-264.
22. Ayme-Southgate A., Vigoreaux J., Benian G., Pardue M. L. Drosophila has a twitchin/titin related gene that appears to encode projectin. Proc. Natl Acad. Sci. USA. 88:1991;7973-7977.
23. Benian G. M., Kiff J. E., Neckelmann N., Moerman D. G., Waterston R. H. Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature. 342:1989;45-50.
24. Squire J., Cantino M., Chew M., Denny R., Harford J., Hudson L., Luther P. Myosin rod-packing schemes in vertebrate muscle thick filaments. J. Struct. Biol. 122:1998;128-138.
25. Liversage A. D., Holmes D., Knight P. J., Tskhovrebova L., Trinick J. Titin and the sarcomere symmetry paradox. J. Mol. Biol. 305:2001;401-409.
26. Cazorla O., Freiburg A., Helmes M., Centner T., McNabb M., Trombitás K. et al. Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ. Res. 86:2000;59-67.
27. Li Q., Jin J. P., Granzier H. L. The effect of genetically expressed cardiac titin fragments on in vitro actin motility. Biophys. J. 69:1995;1508-1518.
28. Trombitas K., Greaser M. L., Pollack G. H. Interaction between titin and thin filaments in intact cardiac muscle. J. Musc. Cell Motil. 18:1997;345-351.
29. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24:1997;4876-4882.
30. Saiki R. K., Scharf S., Faloona F., Mullis K., Horn G., Ehrlich H. A., Arnheim N. Enzymatic amplification of β-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 230:1985;1350-1354.
31. Studier F. W., Rosenberg A. H., Dubendorf J. W. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:1990;60-89.
32. Melcher K. A modular set of prokaryotic and eukaryotic expression vectors. Anal. Biochem. 277:2000;109-120.
33. Cazorla O., Wu Y., Irving T., Granzier H. Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ. Res. 88:2001;1028-1035.
34. Fabiato A. Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157:1988;378-416.
35. Granzier H. L., Irving T. C. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys. J. 68:1995;1027-1044.