Forced unfolding of fibronectin type 3 modules: An analysis by biased molecular dynamics simulations

Journal of Molecular Biology

Volumn 288, Issue 3, 1999, Pages 441-459

  Paci, Emanuele ^a,b   Karplus, Martin ^a,c  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c HARVARD UNIVERSITY   (United States)

Author keywords

Atomic force microscopy; Muscle proteins; Protein denaturation; Protein structure; Titin

Indexed keywords

FIBRONECTIN;

ARTICLE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SIMULATION; SOLVATION;

VERTEBRATA;

EID: 0033531973     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2670     Document Type: Article

References (49)

1. Bork P., Downing A. K., Kieffer B., Campbell I. D. Structure and distribution of modules in extracellular proteins. Quart. Rev. Biophys. 29:1996;119-167.
2. Braxenthaler M., Unger R., Auerbach D., Given J. A., Moult J. Chaos in protein dynamics. Proteins: Struct. Funct. Genet. 29:1997;417-425.
3. Brooks B. R., Bruccoleri R. E., Olafson B. D., States D. J., Swaminathan S., Karplus M. CHARMM: a program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4:1983;187-217.
4. Caflisch A., Karplus M. Acid and thermal denaturation of barnase investigated by molecular dynamics simulations. J. Mol. Biol. 252:1995;672-708.
5. Chandler D., Weeks J. D., Andersen H. C. van der Waals picture of liquids, solids, and phase transformations. Science. 220:1983;787-794.
6. Cluzel P., Lebrun A., Heller C., Lavry R., Viovy J.-L., Chatenay D., Caron F. DNA: an extensible molecule. Science. 271:1996;792-794.
7. Copié V., Tomita Y., Akiyama S. K., Ichi Aoto S., Yamada K. M., Venable R. M., Pastor R. W., Krueger S., Torchia D. A. 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. 277:1998;663-682.
8. Creighton T. E. Proteins. Structures and Molecular Properties. 1993;Freeman, London.
9. Duan Y., Kollman P. A. Pathways to a protein folding intermediate observed in a 1-microsecond simulation in aqueous solution. Science. 282:1998;740-744.
10. Erickson H. P. Stretching single protein molecules: Titin is a weird spring. Science. 276:1997;1090.
11. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1997;1541-1555.
12. Grubmüller H., Heymann B., Tavan P. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science. 271:1996;997-999.
13. Harvey S. C., Gabb H. A. Conformational transition using molecular dynamics with minimum biasing. Biopolymers. 33:1993;1167-1172.
14. Herschbach D. R. Molecular dynamics of elementary chemical reactions (Nobel lecture). Angew. Chem. Int. Ed. 26:1987;1221-1243.
15. Hünenberger P. H., Mark A. E., van Gunsteren W. F. Computational approaches to study protein unfolding: Hen egg white lysozyme as a case study. Proteins: Struct. Funct. Genet. 21:1995;196-213.
16. Hoover W. G. Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. ser. A. 31:1985;1695-1697.
17. Isralewitz B., Izrailev S., Schulten K. Binding pathway of retinal to bacterio-opsin: a prediction by molecular dynamics simulations. Biophys. J. 73:1997;2972-2979.
18. Izrailev S., Stepaniatis S., Balsra M., Oono Y., Schulten K. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72:1997;1568-1581.
19. Kabsch w., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometric features. Biopolymers. 22:1983;2577-2637.
20. Keller T. C. S. Structure and function of titin and nebulin. Curr. Opin. Cell Biol. 7:1995;32-38.
21. Keller T. C. S. Molecular bungees. Nature. 387:1997;233-235.
22. Kellermayer M. S., Smith S. B., Granzier H. L., Bustamante C. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science. 276:1997;1112-1116.
23. Koradi R., Billeter M., Wüthrich K. Molmol: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
24. Labeit S., Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science. 270:1995;293-296.
25. Lazaridis T., Karplus M. "New View" of protein folding reconciled with the old through multiple unfolding simulations. Science. 278:1997;1928-1931.
26. Lazaridis T., Karplus M. Effective energy function for protein dynamics and thermodynamics. Proteins Struct. Funct. Genet. 1999.
27. Lazaridis T., Archontis G., Karplus M. Enthalpic contribution to protein stability: Insights from atom-based calculation statistical mechanics. Advan. Protein Chem. 47:1995;231-306.
28. Leahy D. J., Aukhil I., Erickson H. P. 2.0 Å crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell. 84:1996;155-164.
29. Leger J.-F., Robert J., Bourdieu L., Chatenay D., Marko J. RecA binding to a single double-stranded DNA molecule: a possible role of DNA conformational fluctuations. Proc. Natl Acad. Sci. USA. 95:1998;12295-12299.
30. Li A., Daggett V. Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J. Mol. Biol. 257:1996;412-429.
31. Li A., Fenselau C., Kaltashov I. A. Stability of secondary structural elements in a solvent-free environment. II. The β-pleated sheets. Proteins: Struct. Funct. Genet. 2:1998;22-27.
32. Lu H., Isralewitz B., Krammer A., Vogel V., Schulten K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:1998;662-671.
33. Mu ñ V., Thompson P. A., Hofrichter J., Eaton W. A. Folding dynamics and mechanism of β-hairpin formation. Nature. 390:1998;196-199.
34. Neria E., Fischer S., Karplus M. Simulation of activation free energies in molecular dynamics system. J. Chem. Phys. 105:1996;1902-1921.
35. Northrup S. H., Pear M. R., Lee C.-Y., McCammon J. A., Karplus M. Dynamical theory of activated processes in globular proteins. Proc. Natl Acad. Sci. USA. 79:1982;4035-4039.
36. Nosé S. A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys. 52:1984;255-268.
37. Noy A., Vezenov D. V., Lieber C. M. Chemical force microscopy. Annu. Rev. Mater. Sci. 27:1997;381-421.
38. Oberhauser A. F., Marszalek P. E., Erickson H. P., Fernandez J. M. The molecular elasticity of extracellular matrix protein tenascin. Nature. 393:1998;181-185.
39. Plaxco K. W., Spitzfaden C., Campbell I. D., Dobson C. M. A comparison of the folding kinetics and thermodynamics of two homologous fibronectin type III modules. J. Mol. Biol. 270:1997;763-770.
40. Prévost M., Ortmans I. Refolding simulations of an isolated fragment of barnase into a native-like beta hairpin: evidence for compactness and hydrogen bonding as concurrent stabilizing factors. Proteins: Struct. Funct. Genet. 29:1997;212-227.
41. Richards F. M. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6:1977;151-176.
42. Rief M., Gautel M., Oesterhelt F., Fernandez J. M., Gaub H. E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1997;1109-1112.
43. Schaefer M., Bartels C., Karplus M. The solution conformation and thermodynamics of structured peptides: Molecular dynamics simulation with and implicit solvation model. J. Mol. Biol. 284:1998;835-847.
44. Schlitter J., Engles M., Kruger P., Jacoby E., Wollmer A. Targeted molecular dynamics simulation of conformational change. Application to the T⇔R transition in insulin. Mol. Simulat. 10:1993;291-308.
45. Spitzfaden C., Grant R. P., Mardon H. J., Campbell I. D. Module-module interactions in the cellbinding region of fibronectin: stability, flexibility and specificity. J. Mol. biol. 265:1997;565-579.
46. Tobias D. J., Sneddon S. F., Brooks C. L. Stability of a model β-sheet in water. J. Mol. biol. 227:1992;1244-1252.
47. Tskhovrebova L., Trinick J., Sleep J. A., Simmons R. M. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature. 387:1007;308-312.
48. Yang A. S., Hitz B., Honig B. Free energy determinants of secondary structure formation: II. Antiparallel β-sheets. J. Mol. Biol. 252:1995;366-376.
49. Zocchi G. Proteins unfold in steps. Proc. Natl Acad. Sci. USA. 94:1997;10647-10651.