Changing the mechanical unfolding pathway of FnIII10 by tuning the pulling strength

Biophysical Journal

Volumn 96, Issue 2, 2009, Pages 429-441

  Mitternacht, Simon ^a,d   Luccioli, Stefano ^b   Torcini, Alessandro ^b   Imparato, Alberto ^c   Irbäck, Anders ^a  

^a LUND UNIVERSITY   (Sweden)

^b ISTITUTO DEI SISTEMI COMPLESSI   (Italy)

^c ISI FOUNDATION   (Italy)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 58849130229     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.09.043     Document Type: Article

References (53)

1. Geiger, B., A. Bershadsky, R. Pankov, and K. M. Yamada. 2001. Transmembrane crosstalk between the extracellular matrix and the cytoskeleton. Nat. Rev. Mol. Cell Biol. 2:793-805.
2. Vogel, V. 2006. Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 35:459-488.
3. Ruoslahti, E., and M. D. Pierschbacher. 1987. New perspectives in cell adhesion: RGD and integrins. Science. 238:491-497.
4. Aota, S. -I., M. Nomizu, and K. M. Yamada. 2004. The short amino acid sequence Pro-His-Ser-Arg-Asn in human fibronectin enhances cell-adhesive function. J. Biol. Chem. 269:24756-24761.
5. Krammer, A., H. Lu, B. Isralewitz, K. Schulten, and V. Vogel. 1999. Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc. Natl. Acad. Sci. USA. 96:1351-1356.
6. Ohashi, T., D. P. Kiehart, and H. P. Erickson. 1999. Dynamics and elasticity of the fibronectin matrix in living cell culture visualized by fibronectin-green fluorescent protein. Proc. Natl. Acad. Sci. USA. 96:2153-2158.
7. Abu-Lail, N. I., T. Ohashi, R. L. Clark, H. P. Erickson, and S. Zauscher. 2006. Understanding the elasticity of fibronectin fibrils: unfolding strengths of FN-III and GFP domains measured by single molecule force spectroscopy. Matrix Biol. 25:175-184.
8. Baneyx, G., L. Baugh, and V. Vogel. 2002. Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc. Natl. Acad. Sci. USA. 99:5139-5143.
9. Smith, M. L., D. Gourdon, W. C. Little, K. E. Kubow, R. Andresen Eguiluz, S. Luna-Morris, and V. Vogel. 2007. Force-induced unfolding of fibronectin in the extracellular matrix of living cells. PLoS Biol. 5:e268.
10. Plaxco, K. W., C. Spitzfaden, I. D. Campbell, and C. M. Dobson. 1997. A comparison of the folding kinetics and thermodynamics of two homologous fibronection type III modules. J. Mol. Biol. 270:763-770.
11. Oberhauser, A. F., C. Badilla-Fernandez, M. Carrion-Vazquez, and J. M. Fernandez. 2002. The mechanical hierarchies of fibronectin observed by single-molecule AFM. J. Mol. Biol. 319:433-447.
12. Li, L., H. H. -L. Huang, C. L. Badilla, and J. M. Fernandez. 2005. Mechanical unfolding intermediates observed by single-molecule force spectroscopy in a fibronectin type III module. J. Mol. Biol. 345:817-826.
13. Ng, S. P., and J. Clarke. 2007. Experiments suggest that simulations may overestimate electrostatic contributions to the mechanical stability of a fibronectin type III domain. J. Mol. Biol. 371:851-854.
14. Cota, E., and J. Clarke. 2000. Folding of β-sandwich proteins: three-state transition of a fibronectin type III module. Protein Sci. 9:112-120.
15. Paci, E., and M. Karplus. 1999. Forced unfolding of fibronectin type 3 modules: an analysis by biased molecular dynamics simulations. J. Mol. Biol. 288:441-459.
16. Klimov, D. K., and D. Thirumalai. 2000. Native topology determines force-induced unfolding pathways in globular proteins. Proc. Natl. Acad. Sci. USA. 97:7254-7259.
17. 10 by steered molecular dynamics. J. Mol. Biol. 323:939-950.
18. Craig, D., M. Gao, K. Schulten, and V. Vogel. 2004. Tuning the mechanical stability of fibronectin type III modules through sequence variations. Structure. 12:21-30.
19. Sułkowska, J. I., and M. Cieplak. 2007. Mechanical stretching of proteins: a theoretical survey of the Protein Data Bank. J. Phys. Condens. Matter. 19:283201.
20. Li, M. S. 2007. Secondary structure, mechanical stability, and location of transition state of proteins. Biophys. J. 93:2644-2654.
21. Irbäck, A., B. Samuelsson, F. Sjunnesson, and S. Wallin. 2003. Thermodynamics of α- and β-structure formation in proteins. Biophys. J. 85:1466-1473.
22. Irbäck, A., and S. Mohanty. 2005. Folding thermodynamics of peptides. Biophys. J. 88:1560-1569.
23. Lu, H., and K. Schulten. 2000. The key event in force-induced unfolding of titin's immunoglobulin domains. Biophys. J. 79:51-65.
24. Jarzynski, C. 1997. Nonequilibrium equality for free energy differences. Phys. Rev. Lett. 78:2690-2693.
25. Crooks, G. E. 1999. Entropy production fluctuation theorem and the nonequilibrium work relation for free energy differences. Phys. Rev. E. 60:2721-2726.
26. Hummer, G., and A. Szabo. 2001. Free energy reconstruction from nonequilibrium single-molecule pulling experiments. Proc. Natl. Acad. Sci. USA. 98:3658-3661.
27. West, D. K., P. D. Olmsted, and E. Paci. 2006. Free energy for protein folding from nonequilibrium simulations using the Jarzynski equality. J. Chem. Phys. 125:204910.
28. Imparato, A., A. Pelizzola, and M. Zamparo. 2007. Ising-like model for protein mechanical unfolding. Phys. Rev. Lett. 98:148102.
29. Imparato, A., A. Pelizzola, and M. Zamparo. 2007. Protein mechanical unfolding: a model with binary variables. J. Chem. Phys. 127:145105.
30. Imparato, A., S. Luccioli, and A. Torcini. 2007. Reconstructing the free-energy landscape of a mechanically unfolded model protein. Phys. Rev. Lett. 99:168101.
31. Harris, N. C., Y. Song, and C. -H. Kiang. 2007. Experimental free energy surface reconstruction from single-molecule force spectroscopy using Jarzynski's equality. Phys. Rev. Lett. 99:068101.
32. Imparato, A., F. Sbrana, and M. Vassalli. 2008. Reconstructing the free-energy landscape of a polyprotein by single-molecule experiments. Europhys. Lett. 82:58006.
33. Irbäck, A., S. Mitternacht, and S. Mohanty. 2005. Dissecting the mechanical unfolding of ubiquitin. Proc. Natl. Acad. Sci. USA. 102:13427-13432.
34. Irbäck, A., and S. Mitternacht. 2006. Thermal versus mechanical unfolding of ubiquitin. Proteins. 65:759-766.
35. Schlierf, M., H. Li, and J. M. Fernandez. 2004. The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques. Proc. Natl. Acad. Sci. USA. 101:7299-7304.
36. Li, M. S., M. Kouza, and C. K. Hu. 2007. Refolding upon force quench and pathways of mechaincal and thermal unfolding of ubiquitin. Biophys. J. 92:547-561.
37. Kleiner, A., and E. Shakhnovich. 2007. The mechanical unfolding of ubiquitin through all-atom Monte Carlo simulation with a Gō-type potential. Biophys. J. 92:2054-2061.
38. Imparato, A., and A. Pelizzola. 2008. Mechanical unfolding and refolding pathways of ubiquitin. 2008. Phys. Rev. Lett. 100:158104.
39. Favrin, G., A. Irbäck, and F. Sjunnesson. 2001. Monte Carlo update for chain molecules: biased Gaussian steps in torsional space. J. Chem. Phys. 114:8154-8158.
40. Irbäck, A., and S. Mohanty. 2006. PROFASI: a Monte Carlo simulation package for protein folding and aggregation. J. Comput. Chem. 27:1548-1555.
41. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
42. Imparato, A., and L. Peliti. 2006. Evaluation of free energy landscapes from manipulation experiments. J. Stat. Mech. P03005.
43. Ferrenberg, A. M., and R. H. Swendsen. 1989. Optimized Monte Carlo analysis. Phys. Rev. Lett. 63:1195-1198.
44. Evans, E., and K. Ritchie. 1997. Dynamic strength of molecular adhesion bonds. Biophys. J. 72:1541-1555.
45. Marko, J. F., and E. D. Siggia. 1995. Stretching DNA. Macromolecules. 28:8759-8770.
46. Li, P. -C., and D. E. Makarov. 2003. Theoretical studies of the mechanical unfolding of the muscle protein titin: bridging the time-scale gap between simulation and experiment. J. Chem. Phys. 119:9260-9268.
47. Hyeon, C., and D. Thirumalai. 2006. Forced-unfolding and force-quench refolding of RNA hairpins. Biophys. J. 90:3410-3427.
48. West, D. K., E. Paci, and P. D. Olmsted. 2006. Internal protein dynamics shifts the distance to the mechanical transition state. Phys. Rev. E. 74:061912.
49. Dudko, O. K., J. Mathé, A. Szabo, A. Meller, and G. Hummer. 2007. Extracting kinetics from single-molecule force spectroscopy: nanopore unzipping of DNA hairpins. Biophys. J. 92:4186-4195.
50. Bell, G. I. 1978. Models for specific adhesion of cells to cells. Science. 200:618-627.
51. Li, H., W. A. Linke, A. F. Oberhauser, M. Carrion-Vazquez, J. G. Kerkvliet, H. Lu, P. E. Marszalek, and J. M. Fernandez. 2002. Reverse engineering of the giant muscle protein titin. Nature. 418:998-1002.
52. Erickson, H. P. 1994. Reversible unfolding of fibronectin type III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc. Natl. Acad. Sci. USA. 91:10114-10118.
53. Main, A. L., T. S. Harvey, M. Baron, J. Boyd, and I. D. Campbell. 1992. The three-dimensional structure of the tenth type III module of fibronectin: an insight into RGD-mediated interactions. Cell. 71:671-678.