Protein unfolding under force: Crack propagation in a network

Biophysical Journal

Volumn 101, Issue 3, 2011, Pages 736-744

  De Graff, Adam M R ^a   Shannon, Gareth ^b   Farrell, Daniel W ^a   Williams, Philip M ^b   Thorpe, M F ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

ARTICLE; BIOMECHANICS; CHEMISTRY; ELASTICITY; HYDROGEN BOND; MECHANICAL STRESS; MECHANICS; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTEIN UNFOLDING;

BIOMECHANICS; ELASTICITY; HYDROGEN BONDING; MECHANICAL PROCESSES; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN UNFOLDING; PROTEINS; STRESS, MECHANICAL;

EID: 80052495568     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.05.072     Document Type: Article

References (53)

1. X.H. Zhang, and K. Halvorsen T.A. Springer Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor Science 324 2009 1330 1334
2. M. Auton, M.A. Cruz, and J. Moake Conformational stability and domain unfolding of the Von Willebrand factor A domains J. Mol. Biol. 366 2007 986 1000 (Pubitemid 46175860)
3. W. Chen, J.Z. Lou, and C. Zhu Molecular dynamics simulated unfolding of von Willebrand factor A domains by force Cell. Mol. Bioeng. 2 2009 75 86
4. C. Baldauf, and R. Schneppenheim F. Gräter Shear-induced unfolding activates von Willebrand factor A2 domain for proteolysis J. Thromb. Haemost. 7 2009 2096 2105
5. V. Vogel Mechanotransduction involving multimodular proteins: converting force into biochemical signals Annu. Rev. Biophys. Biomol. Struct. 35 2006 459 488 (Pubitemid 43877387)
6. J.R. Forman, and J. Clarke Mechanical unfolding of proteins: insights into biology, structure and folding Curr. Opin. Struct. Biol. 17 2007 58 66 (Pubitemid 46240817)
7. C. Cecconi, and E.A. Shank S. Marqusee Direct observation of the three-state folding of a single protein molecule Science 309 2005 2057 2060 (Pubitemid 41362324)
8. S.B. Fowler, and R.B. Best J. Clarke Mechanical unfolding of a titin Ig domain: structure of unfolding intermediate revealed by combining AFM, molecular dynamics simulations, NMR and protein engineering J. Mol. Biol. 322 2002 841 849
9. S.P. Ng, and R.W.S. Rounsevell J. Clarke Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation J. Mol. Biol. 350 2005 776 789 (Pubitemid 40848674)
10. R.B. Best, and S.B. Fowler J. Clarke Mechanical unfolding of a titin Ig domain: structure of transition state revealed by combining atomic force microscopy, protein engineering and molecular dynamics simulations J. Mol. Biol. 330 2003 867 877
11. M. Gao, and D. Craig K. Schulten Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics J. Mol. Biol. 323 2002 939 950 (Pubitemid 35341066)
12. H. Lu, and B. Isralewitz K. Schulten Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation Biophys. J. 75 1998 662 671 (Pubitemid 28357508)
13. D.K. West, and D.J. Brockwell E. Paci Mechanical resistance of proteins explained using simple molecular models Biophys. J. 90 2006 287 297
14. S. Mitternacht, and S. Luccioli A. Irbäck Changing the mechanical unfolding pathway of FnIII10 by tuning the pulling strength Biophys. J. 96 2009 429 441
15. E. Eyal, and I. Bahar Toward a molecular understanding of the anisotropic response of proteins to external forces: insights from elastic network models Biophys. J. 94 2008 3424 3435
16. H. Dietz, and M. Rief Elastic bond network model for protein unfolding mechanics Phys. Rev. Lett. 100 2008 098101
17. D.W. Farrell, K. Speranskiy, and M.F. Thorpe Generating stereochemically acceptable protein pathways Proteins 78 2010 2908 2921
18. D.J. Jacobs, and A.J. Rader M.F. Thorpe Protein flexibility predictions using graph theory Proteins 44 2001 150 165
19. B.K. Ho, A. Thomas, and R. Brasseur Revisiting the Ramachandran plot: hard-sphere repulsion, electrostatics, and H-bonding in the alpha-helix Protein Sci. 12 2003 2508 2522 (Pubitemid 37310791)
20. B.I. Dahiyat, D.B. Gordon, and S.L. Mayo Automated design of the surface positions of protein helices Protein Sci. 6 1997 1333 1337 (Pubitemid 27260167)
21. B.M. Hespenheide, and A.J. Rader L.A. Kuhn Identifying protein folding cores from the evolution of flexible regions during unfolding J. Mol. Graph. Model. 21 2002 195 207 (Pubitemid 35279850)
22. Reference deleted in proof.
23. P. Maragakis, A. van der Vaart, and M. Karplus Gaussian-mixture umbrella sampling J. Phys. Chem. B 113 2009 4664 4673
24. M.A. Murcko, H. Castejon, and K.B. Wiberg Carbon-carbon rotational barriers in butane, 1-butene, and 1,3-butadiene J. Phys. Chem. 100 1996 16162 16168 (Pubitemid 126799356)
25. A. Fernández, and R.S. Berry Extent of hydrogen-bond protection in folded proteins: a constraint on packing architectures Biophys. J. 83 2002 2475 2481 (Pubitemid 35265741)
26. S. Improta, A.S. Politou, and A. Pastore Immunoglobulin-like modules from titin I-band: extensible components of muscle elasticity Structure 4 1996 323 337
27. D.J. Leahy, I. Aukhil, and H.P. Erickson 2.0 crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region Cell 84 1996 155 164
28. D.J. Leahy, and W.A. Hendrickson H.P. Erickson Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein Science 258 1992 987 991
29. H. Jing, and J. Takagi T.A. Springer Archaeal surface layer proteins contain beta propeller, PKD, and beta helix domains and are related to metazoan cell surface proteins Structure 10 2002 1453 1464 (Pubitemid 35232388)
30. P. Fucini, and C. Renner T.A. Holak The repeating segments of the F-actin cross-linking gelation factor (ABP-120) have an immunoglobulin-like fold Nat. Struct. Biol. 4 1997 223 230 (Pubitemid 27111169)
31. S. Vijay-Kumar, C.E. Bugg, and W.J. Cook Structure of ubiquitin refined at 1.8 A resolution J. Mol. Biol. 194 1987 531 544
32. J.W. O'Neill, and D.E. Kim K.Y. Zhang Structures of the B1 domain of protein L from Peptostreptococcus magnus with a tyrosine to tryptophan substitution Acta Crystallogr. D Biol. Crystallogr. 57 2001 480 487 (Pubitemid 32296024)
33. K. Katayanagi, and M. Miyagawa K. Morikawa Structural details of ribonuclease H from Escherichia coli as refined to an atomic resolution J. Mol. Biol. 223 1992 1029 1052
34. Q. Zhang, and Y.F. Zhou T.A. Springer Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor Proc. Natl. Acad. Sci. USA 106 2009 9226 9231
35. A.M. Buckle, K. Henrick, and A.R. Fersht Crystal structural analysis of mutations in the hydrophobic cores of barnase J. Mol. Biol. 234 1993 847 860 (Pubitemid 24007805)
36. J. Pascual, and M. Pfuhl M. Nilges Solution structure of the spectrin repeat: a left-handed antiparallel triple-helical coiled-coil J. Mol. Biol. 273 1997 740 751 (Pubitemid 27488814)
37. K.V. Andersen, and F.M. Poulsen The three-dimensional structure of acyl-coenzyme A binding protein from bovine liver: structural refinement using heteronuclear multidimensional NMR spectroscopy J. Biomol. NMR 3 1993 271 284
38. B.R. Brooks, and C.L. Brooks 3rd M. Karplus CHARMM: the biomolecular simulation program J. Comput. Chem. 30 2009 1545 1614
39. T. Lazaridis, and M. Karplus Effective energy function for proteins in solution Proteins 35 1999 133 152 (Pubitemid 29165128)
40. E. Neria, S. Fischer, and M. Karplus Simulation of activation free energies in molecular systems J. Chem. Phys. 105 1996 1902 1921 (Pubitemid 126612899)
41. E. Paci, and M. Karplus Unfolding proteins by external forces and temperature: the importance of topology and energetics Proc. Natl. Acad. Sci. USA 97 2000 6521 6526 (Pubitemid 30412746)
42. R.B. Best, and B. Li J. Clarke Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation Biophys. J. 81 2001 2344 2356 (Pubitemid 32917181)
43. M. Rief, and M. Gautel H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112 (Pubitemid 27218118)
44. P.M. Williams, and S.B. Fowler J. Clarke Hidden complexity in the mechanical properties of titin Nature 422 2003 446 449 (Pubitemid 36411399)
45. D.K. Klimov, and D. Thirumalai Native topology determines force-induced unfolding pathways in globular proteins Proc. Natl. Acad. Sci. USA 97 2000 7254 7259 (Pubitemid 30431450)
46. P.E. Marszalek, and H. Lu J.M. Fernandez Mechanical unfolding intermediates in titin modules Nature 402 1999 100 103
47. L.W. Li, and H.H.L. Huang J.M. Fernandez Mechanical unfolding intermediates observed by single-molecule force spectroscopy in a fibronectin type III module J. Mol. Biol. 345 2005 817 826 (Pubitemid 39600935)
48. D. Craig, and A. Krammer V. Vogel Comparison of the early stages of forced unfolding for fibronectin type III modules Proc. Natl. Acad. Sci. USA 98 2001 5590 5595 (Pubitemid 32435686)
49. I. Schwaiger, and A. Kardinal M. Rief A mechanical unfolding intermediate in an actin-crosslinking protein Nat. Struct. Mol. Biol. 11 2004 81 85 (Pubitemid 38173445)
50. M. Schlierf, H.B. Li, and J.M. Fernandez The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques Proc. Natl. Acad. Sci. USA 101 2004 7299 7304 (Pubitemid 38638027)
51. T.M. Raschke, and S. Marqusee The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions Nat. Struct. Biol. 4 1997 298 304 (Pubitemid 27157202)
52. A.K. Chamberlain, T.M. Handel, and S. Marqusee Detection of rare partially folded molecules in equilibrium with the native conformation of RNaseH Nat. Struct. Biol. 3 1996 782 787 (Pubitemid 26303404)
53. A.K. Faradjian, and R. Elber Computing time scales from reaction coordinates by milestoning J. Chem. Phys. 120 2004 10880 10889