Interaction forces between F-actin and titin PEVK domain measured with optical tweezers

Biophysical Journal

Volumn 93, Issue 6, 2007, Pages 2102-2109

  Bianco, Pasquale ^a,b   Nagy, Attila ^c   Kengyel, András ^c   Szatmári, Dávid ^c   Mártonfalvi, Zsolt ^c   Huber, Tamás ^c   Kellermayer, Miklós S Z ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b DBAG   (Italy)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; CONNECTIN; F ACTIN; PEPTIDE; PROLYLGLUTAMYLVALLYLLYSINE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DEVICE; DISSOCIATION; ELASTICITY; FORCE; MEASUREMENT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MUSCLE CONTRACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTICAL TWEEZERS; OPTICS; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SARCOMERE; SKELETAL MUSCLE; SPECTROSCOPY; THIXOTROPY; VISCOELASTICITY;

EID: 34548783879     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.106153     Document Type: Article

References (45)

1. 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.
2. Tskhovrebova, L., and J. Trinick. 2003. Titin: properties and family relationships. Nat. Rev. Mol. Cell Biol. 4:679-689.
3. Labeit, S., and B. Kolmerer. 1995. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science. 270:293-296.
4. Freiburg, A., K. Trombitas, W. Hell, O. Cazorla, F. Fougerousse, T. Centner, B. Kolmerer, C. Witt, J. S. Beckmann, C. C. Gregorio, H. Granzier, and S. Labeit. 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.
5. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27:527-533.
6. Trombitás, K., M. Greaser, S. Labeit, J. P. 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.
7. Ma, K., L. Kan, and K. Wang. 2001. Polyproline II helix is a key structural motif of the elastic PEVK segment of titin. Biochemistry. 40:3427-3438.
8. Greaser, M. 2001. Identification of new repeating motifs in titin. Proteins. 43:145-149.
9. Gutierrez-Cruz, G., A. H. Van Herdeen, and K. Wang. 2001. Modular motif, structural folds and affinity profiles of the PEVK segment of human fetal skeletal muscle titin. J. Biol. Chem. 276:7442-7449.
10. Ma, K., and K. Wang. 2003. Malleable conformation of the elastic PEVK segment of titin: non-cooperative interconversion of polyproline II helix, beta turn and unordered structures. Biochem. J. 374:687-695.
11. Kulke, M., S. Fujita-Becker, E. Rostkova, C. Neagoe, D. Labeit, D. J. Manstein, M. Gautel, and W. A. Linke. 2001. Interaction between PEVK-titin and actin filaments: origin of a viscous force component in cardiac myofibrils. Circ. Res. 89:874-881.
12. 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.
13. Yamasaki, R., M. Berri, Y. Wu, K. Trombitas, M. McNabb, M. S. Kellermayer, C. Witt, D. Labeit, S. Labeit, M. Greaser, and H. Granzier. 2001. Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys. J. 81:2297-2313.
14. Nagy, A., P. Cacciafesta, L. Grama, A. Kengyel, A. Malnasi-Csizmadia, and M. S. Kellermayer. 2004. Differential actin binding along the PEVK domain of skeletal muscle titin. J. Cell Sci. 117:5781-5789.
15. Niederlander, N., F. Raynaud, C. Astier, and P. Chaussepied. 2004. Regulation of the actin-myosin interaction by titin. Eur. J. Biochem. 271:4572-4581.
16. Raynaud, F., C. Astier, and Y. Benyamin. 2004. Evidence for a direct but sequential binding of titin to tropomyosin and actin filaments. Biochim. Biophys. Acta. 1700:171-178.
17. Pardee, J. D., and J. A. Spudich. 1982. Purification of muscle actin. Methods Enzymol. 85:164-182.
18. Margossian, S. S., and S. Lowey. 1982. Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol. 85:55-72.
19. Kron, S. J., Y. Y. Toyoshima, T. Q. Uyeda, and J. A. Spudich. 1991. Assays for actin sliding movement over myosin-coated surfaces. Methods Enzymol. 196:399-416.
20. Howard, J., A. J. Hudspeth, and R. D. Vale. 1989. Movement of microtubules by single kinesin molecules. Nature. 342:154-158.
21. Sakakibara, H., H. Kojima, Y. Sakai, E. Katayama, and K. Oiwa. 1999. Inner-arm dynein c of Chlamydomonas flagella is a single-headed processive motor. Nature. 400:586-590.
22. Svoboda, K., and S. M. Block. 1994. Force and velocity measured for single kinesin molecules. Cell. 77:773-784.
23. Kellermayer, M. S. Z., S. B. Smith, H. L. Granzier, and C. Bustamante. 1997. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science. 276:1112-1116.
24. Smith, S. B., Y. Cui, and C. Bustamante. 1996. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science. 271:795-799.
25. Smith, S. B., Y. Cui, and C. Bustamante. 2003. Optical-trap force transducer that operates by direct measurement of light momentum. Methods Enzymol. 361:134-162.
26. Bell, G. I. 1978. Models for the specific adhesion of cells to cells. Science. 200:618-627.
27. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
28. Bustamante, C., J. F. Marko, E. D. Siggia, and S. Smith. 1994. Entropic elasticity of lambda-phage DNA. Science. 265:1599-1600.
29. Nishizaka, T., R. Seo, H. Tadakuma, K. Kinosita, Jr., and S. Ishiwata. 2000. Characterization of single actomyosin rigor bonds: Load dependence of lifetime and mecahnical properties. Biophys. J. 79:962-974.
30. Tsuda, Y., H. Yasutake, A. Ishijima, and T. Yanagida. 1996. Torsional rigidity of single actin filaments and actin-actin bond breaking force under torsion measured directly by in vitro micromanipulation. Proc. Natl. Acad. Sci. USA. 93:12937-12942.
31. Forbes, J. G., A. J. Jin, G. Gutierrez-Cruz, W. L. Tsai, and K. Wang. 2005. Titin PEVK segment: charge-driven elasticity of the open and flexible polyampholyte. J. Muscle Res. Cell Motil. 26:291-301.
32. Nagy, A., L. Grama, T. Huber, P. Bianco, K. Trombitás, H. L. Granzier, and M. S. Z. Kellermayer. 2005. Hierarchical extensibility in the PEVK domain of skeletal-muscle titin. Biophys. J. 89:329-336.
33. Merkel, R., P. Nassoy, A. Leung, K. Ritchie, and E. Evans. 1999. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 397:50-53.
34. Li, H., A. F. Oberhauser, S. D. Redick, M. Carrion-Vazquez, H. P. Erickson, and J. M. Fernandez. 2001. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc. Natl. Acad. Sci. USA. 98:10682-10686.
35. Watanabe, K., P. Nair, D. Labeit, M. S. Kellermayer, M. Greaser, S. Labeit, and H. Granzier. 2002. Molecular mechanics of cardiac titin's PEVK and N2B spring elements. J. Biol. Chem. 277:11549-11558.
36. Gittes, F., B. Mickey, J. Nettleton, and J. Howard. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923-934.
37. Van Troys, M., J. Vandekerckhove, and C. Ampe. 1999. Structural modules in actin-binding proteins: towards a new classification. Biochim. Biophys. Acta. 1448:323-348.
38. 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.
39. Trombitas, K., Y. Wu, M. McNabb, M. Greaser, M. S. Kellermayer, S. Labeit, and H. Granzier. 2003. Molecular basis of passive stress relaxation in human soleus fibers: assessment of the role of immunoglobulin-like domain unfolding. Biophys. J. 85:3142-3153.
40. Liversage, A. D., D. Holmes, P. J. Knight, L. Tskhovrebova, and J. Trinick. 2001. Titin and the sarcomere symmetry paradox. J. Mol. Biol. 305:401-409.
41. Piazzesi, G., L. Lucii, and V. Lombardi. 2002. The size and speed of the working sktroke for myosin and its dependence on the force. J. Physiol. 545:145-151.
42. Takagi, Y., E. Homsher, Y. E. Goldman, and H. Shuman. 2006. Force generation in single conventional actomyosin complexes under high dynamic load. Biophys. J. 90:1295-1307.
43. Suzuki, M., H. Fujita, and S. Ishiwata. 2005. A new muscle contractile system composed of a thick-filament lattice and a single actin filament. Biophys. J. 89:321-328.
44. Mutungi, G., and K. W. Ranatunga. 1996. The viscous, viscoelastic and elastic characteristics of resting fast and slow mammalian (rat) muscle fibres. J. Physiol. 496:827-836.
45. Whitehead, N. P., J. E. Gregory, D. L. Morgan, and U. Proske. 2001. Passive mechanical properties of the medial gastrocnemius muscle of the cat. J. Physiol. 536:893-903.