The effect of different force applications on the protein-protein complex Barnase-Barstar

Biophysical Journal

Volumn 97, Issue 6, 2009, Pages 1687-1699

  Neumann, Jan ^a   Gottschalk, Kay Eberhard ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BARNASE; BARSTAR;

ARTICLE; BINDING SITE; COMPLEX FORMATION; FORCE; GEOMETRY; MATHEMATICAL COMPUTING; MOLECULAR DYNAMICS; MOLECULAR STABILITY; NONHUMAN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; SIMULATION; TENSION; VELOCITY;

EID: 70350023195     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.01.052     Document Type: Article

References (70)

1. Huang, S., S. Murphy, and A. Matouschek. 2000. Effect of the protein import machinery at the mitochondrial surface on precursor stability. Proc. Natl. Acad. Sci. USA. 97:12991-12996.
2. Sukharev, M., Betanzos, C. S. Chiang, and H. Guy. 2001. The gating mechanism of the large mechanosensitive channel MscL. Nature. 409:720-724. (Pubitemid 32144517)
3. Bershadsky, A. D., N. Q. Balaban, and B. Geiger. 2003. Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19:677-695.
4. Evans, E., A. Leung, V. Heinrich, and C. Zhu. 2004. Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl. Acad. Sci. USA. 101:11281-11286.
5. Gumbart, J., M. C. Wiener, and E. Tajkhorshid. 2007. Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys. J. 93:496-504. (Pubitemid 47057815)
6. Nevo, R., V. Brumfeld, R. Kapon, P. Hinterdorfer, and Z. Reich. 2005. Direct measurement of protein energy landscape roughness. EMBO Rep. 6:482-486. (Pubitemid 40767083)
7. Barsegov, V., and D. Thirumalai. 2005. Probing protein-protein interactions by dynamic force correlation spectroscopy. Phys. Rev. Lett. 95:168302.
8. Kessler, M., K. E. Gottschalk, H. Janovjak, D. J. Muller, and H. E. Gaub. 2006. Bacteriorhodopsin folds into the membrane against an external force. J. Mol. Biol. 357:644-654.
9. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555. (Pubitemid 27133095)
10. Huang, S., K. S. Ratliff, M. P. Schwartz, J. M. Spenner, and A. Matouschek. 1999. Mitochondria unfold precursor proteins by unraveling them from their N-termini. Nat. Struct. Biol. 6:1132-1138.
11. Best, R. B., B. Li, A. Steward, V. Daggett, and J. Clarke. 2001. Can non-mechanical proteins withstand force? Stretching Barnase by atomic force microscopy and molecular dynamics simulation. Biophys. J. 81:2344-2356.
12. Evans, E., K. Ritchie, and R. Merkel. 1995. Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys. J. 68:2580-2587.
13. Grubmüller, H., B. Heymann, and P. Tavan. 1996. Ligand binding: molecular mechanics calculation of the streptavidin-biotin rupture force. Science. 271:997-999. (Pubitemid 26066398)
14. Rief, M., M. Gautel, F. Oesterhelt, J. M. Fernandez, and H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112. (Pubitemid 27218118)
15. Lu, H., and K. Schulten. 1999. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins. 35:453-463. (Pubitemid 29264842)
16. Oesterhelt, F., D. Oesterhelt, M. Pfeiffer, A. Engel, H. E. Gaub, et al. 2000. Unfolding pathways of individual bacteriorhodopsins. Science. 288:143-146.
17. Gao, M., D. Craig, V. Vogel, and K. Schulten. 2002. Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics. J. Mol. Biol. 323:939-950.
18. Grubmüller, H. 2005. Force probe molecular dynamics simulations. Methods Mol. Biol. 305:493-515.
19. Gao, S., M. Sotomayor, E. Villa, E. H. Lee, and K. Schulten. 2006. Molecular mechanisms of cellular mechanics. Phys. Chem. Chem. Phys. 8:3692-3706.
20. Kessler, M., and H. E. Gaub. 2006. Unfolding barriers in bacteriorhodopsin probed from the cytoplasmic and the extracellular side by AFM. Structure. 14:521-527. (Pubitemid 43363485)
21. Vogel, V. 2006. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35:459-488.
22. Sotomayor, M., and K. Schulten. 2007. Single-molecule experiments in vitro and in silico. Science. 316:1144-1148.
23. Rohs, R., C. Etchebest, and R. Lavery. 1999. Unraveling proteins: a molecular mechanics study. Biophys. J. 76:2760-2768. (Pubitemid 29264636)
24. Bryant, Z., V. S. Pande, and D. S. Rokhsar. 2000. Mechanical unfolding of a β-hairpin using molecular dynamics. Biophys. J. 78:584-589. (Pubitemid 30211818)
25. Brockwell, D. J., E. Paci, R. C. Zinober, G. S. Beddard, P. D. Olmsted, et al. 2003. Pulling geometry defines the mechanical resistance of a β-sheet protein. Nat. Struct. Biol. 10:731-737.
26. Carrion-Vazquez, M., H. Li, H. Lu, P. E. Marszalek, A. F. Oberhauser, et al. 2003. The mechanical stability of ubiquitin is linkage dependent. Nat. Struct. Biol. 10:738-743.
27. Li, P.-C., and D. E. Makarov. 2004. Simulation of the mechanical unfolding of ubiquitin: probing different unfolding reaction coordinates by changing the pulling geometry. J. Chem. Phys. 121:4826-4832.
28. Eyal, E., and I. Bahar. 2008. Toward a molecular understanding of the anisotropic response of proteins to external forces: insights from elastic network models. Biophys. J. 94:3424-3435.
29. Gee, E. P. S., D. E. Ingber, and C. M. Stultz. 2008. Fibronectin unfolding revisited: modeling cell traction-mediated unfolding of the tenth type-III repeat. PLoS ONE. 3:e2373.
30. Dietz, H., and M. Rief. 2004. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. USA. 101:16192-161971.
31. Dietz, H., and M. Rief. 2008. Elastic bond network model for protein unfolding mechanics. Phys. Rev. Lett. 100:098101.
32. Gräter, F., J. H. Shen, H. L. Jiang, M. Gautel, and H. Grubmüller. 2005. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88:790-804. (Pubitemid 40975919)
33. Puchner, E. M., A. Alexandrovich, A. L. Kho, U. Hensen, L. V. Schäfer, et al. 2008. Mechanoenzymatics of titin kinase. Proc. Natl. Acad. Sci. USA. 105:13385-13390.
34. Gräter, F., and H. Grubmüller. 2007. Fluctuations of primary ubiquitin folding intermediates in a force clamp. J. Struct. Biol. 157:557-569.
35. Autenrieth, F., E. Tajkhorshid, K. Schulten, and Z. Luthey-Schulten. 2004. Role of water in transient cytochrome c2 docking. J. Phys. Chem. B. 108:20376-20387.
36. Morfill, J., J. Neumann, K. Blank, U. Steinbach, E. M. Puchner, et al. 2008. Force-based analysis of multidimensional energy landscapes: application of dynamic force spectroscopy and steered molecular dynamics simulations to an antibody fragment-peptide complex. J. Mol. Biol. 381:1253-1266.
37. Cuendet, M. A., and O. Michielin. 2008. Protein-protein interaction investigated by steered molecular dynamics: the TCR-pMHC complex. Biophys. J. 95:3575-3590.
38. Hartley, R. W. 1989. Barnase and Barstar: two small proteins to fold and fit together. Trends Biochem. Sci. 14:450-454.
39. Schreiber, G., and A. R. Fersht. 1995. Energetics of protein-protein interactions: analysis of the Barnase-Barstar interface by single mutations and double mutant cycles. J. Mol. Biol. 248:478-486.
40. Schreiber, G., C. Frisch, and A. R. Fersht. 1997. The role of Glu-73 of Barnase in catalysis and the binding of Barstar. J. Mol. Biol. 270:111-122.
41. Frisch, C., A. R. Fersht, and G. Schreiber. 2001. Experimental assignment of the structure of the transition state for the association of Barnase and Barstar. J. Mol. Biol. 308:69-77.
42. Matouschek, A. 2003. Protein unfolding-an important process in vivo? Curr. Opin. Struct. Biol. 13:98-109.
43. Schreiber, G., A. M. Buckle, and A. R. Fersht. 1994. Stability and function: two constraints in the evolution of Barstar and other proteins. Structure. 2:945-951. (Pubitemid 2154305)
44. Schreiber, G., and A. R. Fersht. 1996. Rapid, electrostatically assisted association of proteins. Nat. Struct. Biol. 3:427-431.
45. Vijayakumar, M., K. Y. Wong, G. Schreiber, A. R. Fersht, A. Szabo, et al. 1998. Electrostatic enhancement of diffusion-controlled proteinprotein association: comparison of theory and experiment on Barnase and Barstar. J. Mol. Biol. 278:1015-1024.
46. Schreiber, G., Y. Shaul, and K. E. Gottschalk. 2006. Electrostatic design of protein-protein association rates. Methods Mol. Biol. 340:235-249.
47. Dong, F., M. Vijayakumar, and H.-X. Zhou. 2003. Comparison of calculation and experiment implicates significant electrostatic contributions to the binding stability of Barnase and Barstar. Biophys. J. 85:49-60. (Pubitemid 36753615)
48. Gabdoulline, R. R., and R. C. Wade. 1997. Simulation of the diffusional association of Barnase and Barstar. Biophys. J. 72:1917-1929.
49. Gabdoulline, R. R., and R. C. Wade. 2001. Protein-protein association: investigation of factors influencing association rates by Brownian dynamics simulations. J. Mol. Biol. 306:1139-1155.
50. Camacho, C. J., Z. Weng, S. Vajda, and C. DeLisi. 1999. Free energy landscapes of encounter complexes in protein-protein association. Biophys. J. 76:1166-1178.
51. Spaar, A., C. Dammer, R. R. Gabdoulline, R. C. Wade, and V. Helms. 2006. Diffusional encounter of Barnase and Barstar. Biophys. J. 90:1913-1924.
52. Buckle, A. M., G. Schreiber, and A. R. Fersht. 1994. Protein-protein recognition: crystal structural analysis of a Barnase-Barstar complex at 2.0-Å resolution. Biochemistry. 33:8878-8889. (Pubitemid 24257995)
53. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
54. van der Spoel, D., E. Lindahl, B. Hess, G. Groenhof, A. E. Mark, et al. 2005. GROMACS: fast, flexible, and free. J. Comput. Chem. 26:1701-1718.
55. Berendsen, H. J. C., J. R. Grigera, and T. P. Straatsma. 1987. The missing term in effective pair potentials. J. Phys. Chem. 91:6269-6271.
56. Jorgensen, W. L., D. S. Maxwell, and J. Tirado-Rives. 1996. Development and testing of the OplS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118:11225-11236.
57. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comp. Chem. 18:1463-1472.
58. Berendsen, H., J. Postma, W. van Gunsteren, A. Dinola, and J. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
59. Ewald, P. P. 1921. Die Berechnung optischer und elektrostatischer Gitterpotentiale. Ann. Phys. 64:253-287.
60. Shariff, K., S. Ghosal, and A. Matouschek. 2004. The force exerted by the membrane potential during protein import into the mitochondrial matrix. Biophys. J. 86:3647-3652. (Pubitemid 38780243)
61. Friedsam, C., A. K. Wiehle, F. Kuhner, and H. E. Gaub. 2003. Dynamic single-molecule force spectroscopy: bond rupture analysis with variable spacer length. J. Phys. Cond. Mat. 15:S1709-S1723.
62. Gao, M., M. Wilmanns, and K. Schulten. 2002. Steered molecular dynamics studies of titin I1 domain unfolding. Biophys. J. 83:3435-3445. (Pubitemid 36041960)
63. Pabón, G., and L. M. Amzel. 2006. Mechanism of titin unfolding by force: insight from quasi-equilibrium molecular dynamics calculations. Biophys. J. 91:467-472.
64. Lu, H., B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:662-671. (Pubitemid 28357508)
65. Sharma, D., G. Feng, D. Khor, G. Z. Genchev, H. Lu, et al. 2008. Stabilization provided by neighboring strands is critical for the mechanical stability of proteins. Biophys. J. 95:3935-3942.
66. Selzer, T., and G. Schreiber. 1999. Predicting the rate enhancement of protein complex formation from the electrostatic energy of interaction. J. Mol. Biol. 287:409-419.
67. Selzer, T., S. Albeck, and G. Schreiber. 2000. Rational design of faster associating and tighter binding protein complexes. Nat. Struct. Biol. 7:537-541.
68. Chernyak, V., M. Chertkov, and C. Jarzynski. 2005. Dynamical generalization of nonequilibrium work relation. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 71:025102.
69. Park, S., and K. Schulten. 2004. Calculating potentials of mean force from steered molecular dynamics simulations. J. Chem. Phys. 120: 5946-5961.
70. Izrailev, S., S. Stepaniants, M. Balsera, Y. Oono, and K. Schulten. 1997. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72:1568-1581. (Pubitemid 27133097)