Mechanical unfolding of TNfn3: The unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation

Journal of Molecular Biology

Volumn 350, Issue 4, 2005, Pages 776-789

  Ng, Sean P ^a   Rounsevell, Ross W S ^a   Steward, Annette ^a   Geierhaas, Christian D ^a   Williams, Philip M ^b   Paci, Emanuele ^c   Clarke, Jane ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

AFM; MD simulation; Phi value analysis; Tenascin; Titin

Indexed keywords

IMMUNOGLOBULIN; TENASCIN;

AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BETA SHEET; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PROBE; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SIMULATION;

EID: 20544465799     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.04.070     Document Type: Article

References (61)

1. K. Maruyama Connectin/titin, giant elastic protein of muscle FASEB J. 11 1997 341 345
2. S. Labeit, and B. Kolmerer Titins: giant proteins in charge of muscle ultrastructure and elasticity Science 270 1995 293 296
3. K. Wang, R. McCarter, J. Wright, J. Beverly, and R. Ramirez-Mitchell Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension Proc. Natl Acad. Sci. USA 88 1991 7101 7105
4. K. Wang, J. McClure, and A. Tu Titin: major myofibrillar components of striated muscle Proc. Natl Acad. Sci. USA 76 1979 3698 3702
5. N.L. Halliday, and J.J. Tomasek Mechanical properties of the extracellular matrix influence fibronectin fibril assembly in vitro Expt. Cell Res. 217 1995 109 117
6. R.O. Hynes The dynamic dialogue between cells and matrices: implications of fibronectin's elasticity Proc. Natl Acad. Sci. USA 96 1999 2588 2590
7. A. Sharma, J.A. Askari, M.J. Humphries, E.Y. Jones, and D.I. Stuart Crystal structure of a heparin- and integrin-binding segment of human fibronectin EMBO J. 18 1999 1468 1479
8. J.L. Sechler, H. Rao, A.M. Cumiskey, I. Vega-Colon, M.S. Smith, T. Murata, and J.E. Schwarzbauer A novel fibronectin binding site required for fibronectin fibril growth during matrix assembly J. Cell Biol. 154 2001 1081 1088
9. H.P. Erickson Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions Curr. Opin. Cell Biol. 5 1993 869 876
10. P. Joshi, C.Y. Chung, I. Aukhil, and H.P. Erickson Endothelial cells adhere to the RGD domain and the fibrinogen-like terminal knob of tenascin J. Cell Sci. 106 1993 389 400
11. D.J. Leahy, W.A. Hendrickson, I. Aukhil, and 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
12. M. Rief, M. Gautel, F. Oesterhelt, J.M. Fernandez, and H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112
13. M. Rief, M. Gautel, A. Schemmel, and H.E. Gaub The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by atomic force microscopy Biophys. J. 75 1998 3008 3014
14. A.F. Oberhauser, P.E. Marszalek, H.P. Erickson, and J.M. Fernandez The molecular elasticity of the extracellular matrix protein tenascin Nature 393 1998 181 185
15. Y. Oberdorfer, H. Fuchs, and A. Janshoff Conformational analysis of native fibronectin by means of force microscopy Langmuir 16 2000 9955 9958
16. H. Li, W.A. Linke, A.F. Oberhauser, M. Carrion-Vazquez, J.G. Kerkvliet, and H. Lu Reverse engineering of the giant muscle protein titin Nature 418 2002 998 1002
17. A.F. Oberhauser, C. Badilla-Fernandez, M. Carrion-Vazquez, and J.M. Fernandez The mechanical hierarchies of fibronectin observed with single-molecule AFM J. Mol. Biol. 319 2002 433 447
18. R.B. Best, S.B. Fowler, J.L. Herrera, A. Steward, E. Paci, and 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
19. M.S. Kellermayer, C. Bustamante, and H.L. Granzier Mechanics and structure of titin oligomers explored with atomic force microscopy Biochim. Biophys. Acta 1604 2003 105 114
20. P.M. Williams, S.B. Fowler, R.B. Best, J.L. Toca-Herrera, K.A. Scott, A. Steward, and J. Clarke Hidden complexity in the mechanical properties of titin Nature 422 2003 446 449
21. K.C. Ingham, S.A. Brew, and H.P. Erickson Localization of a cryptic binding site for tenascin on fibronectin J. Biol. Chem. 279 2004 28132 28135
22. D.C. Hocking, J. Sottile, and P.J. McKeown-Longo Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin J. Biol. Chem. 269 1994 19183 19187
23. K.C. Ingham, S.A. Brew, S. Huff, and S.V. Litvinovich Cryptic self-association sites in type III modules of fibronectin J. Biol. Chem. 272 1997 1718 1724
24. C. Zhong, M. Chrzanowska-Wodnicka, J. Brown, A. Shaub, A.M. Belkin, and K. Burridge Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly J. Cell Biol. 141 1998 539 551
25. L. Li, H.H. Huang, C.L. Badilla, and 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
26. H. Li, M. Carrion-Vazquez, A.F. Oberhauser, P.E. Marszalek, and J.M. Fernandez Point mutations alter the mechanical stability of immunoglobulin modules Nature Struct. Biol. 7 2000 1117 1120
27. M. Carrion-Vazquez, A.F. Oberhauser, S.B. Fowler, P.E. Marszalek, S.E. Broedel, J. Clarke, and J.M. Fernandez Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl Acad. Sci. USA 96 1999 3694 3699
28. P.E. Marszalek, H. Lu, H. Li, M. Carrion-Vazquez, A.F. Oberhauser, K. Schulten, and J.M. Fernandez Mechanical unfolding intermediates in titin modules Nature 402 1999 100 103
29. H. Lu, and K. Schulten Steered molecular dynamics simulation of conformational changes of immunoglobulin domain I27 interpret atomic force microscopy observations Chem. Phys. 247 1999 141 153
30. H. Lu, and K. Schulten The key event in force-induced unfolding of Titin's immunoglobulin domains Biophys. J. 79 2000 51 65
31. H. Lu, B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation Biophys. J. 75 1998 662 671
32. S.B. Fowler, R.B. Best, J.L. Toca Herrera, T.J. Rutherford, A. Steward, and E. Paci 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
33. D.J. Brockwell, G.S. Beddard, J. Clarkson, R.C. Zinober, A.W. Blake, and J. Trinick The effect of core destabilization on the mechanical resistance of I27 Biophys. J. 83 2002 458 472
34. 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
35. A.R. Fersht, A. Matouschek, and L. Serrano The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding J. Mol. Biol. 224 1992 771 782
36. H. Lu, and K. Schulten Steered molecular dynamics simulations of force-induced protein domain unfolding Proteins: Struct. Funct. Genet. 35 1999 453 463
37. A. Krammer, H. Lu, B. Isralewitz, K. Schulten, and V. Vogel Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch Proc. Natl Acad. Sci. USA 96 1999 1351 1356
38. E. Paci, and M. Karplus Forced unfolding of fibronectin type 3 modules: an analysis by biased molecular dynamics simulations J. Mol. Biol. 288 1999 441 459
39. 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
40. D. Craig, A. Krammer, K. Schulten, and V. Vogel Comparison of the early stages of forced unfolding for fibronectin type III modules Proc. Natl Acad. Sci. USA 98 2001 5590 5595
41. M. Gao, D. Craig, V. Vogel, and K. Schulten Identifying unfolding intermediates of FN-III(10) by steered molecular dynamics J. Mol. Biol. 323 2002 939 950
42. 1 intermediates Proc. Natl Acad. Sci. USA 100 2003 14784 14789
43. D. Craig, M. Gao, K. Schulten, and V. Vogel Tuning the mechanical stability of fibronectin type III modules through sequence variations Structure 12 2004 21 30
44. C.R. Ruegg, R. Chiquet-Ehrismann, and S.S. Alkan Tenascin, an extracellular matrix protein, exerts immunomodulatory activities Proc. Natl Acad. Sci. USA 86 1989 7437 7441
45. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
46. J. Clarke, E. Cota, S.B. Fowler, and S.J. Hamill Folding studies of immunoglobulin-like beta-sandwich proteins suggest that they share a common folding pathway Struct. Fold. Des. 7 1999 1145 1153
47. S.J. Hamill, A. Steward, and J. Clarke The folding of an immunoglobulin-like Greek key protein is defined by a common-core nucleus and regions constrained by topology J. Mol. Biol. 297 2000 165 178
48. E. Cota, S.J. Hamill, S.B. Fowler, and J. Clarke Two proteins with the same structure respond very differently to mutation: the role of plasticity in protein stability J. Mol. Biol. 302 2000 713 725
49. R.W.S. Rounsevell, A. Steward, and J. Clarke Biophysical investigations of engineered polyproteins: implications for force data Biophys. J. 88 2005 2022 2029
50. J.L. Hutter, and J. Bechhoefer Calibration of atomic force microscope tips Rev. Sci. Instrum. 64 1993 1868 1873
51. W.H. Press, S.A. Teukolsky, W.T. Vetterling, and B.P. Flannery Numerical Recipes in C: The Art of Scientific Computing 2nd edit. 1992 Cambridge University Press USA
52. R.B. Best, D.J. Brockwell, J.L. Toca-Herrera, A.W. Blake, D.A. Smith, S.E. Radford, and J. Clarke Force mode atomic force microscopy as a tool for protein folding studies Anal. Chim. Acta 479 2003 87 105
53. J. Clarke, and P.M. Williams Unfolding induced by mechanical force J. Buchner T. Kiefaber Protein Folding Handbook 2005 Wiley Weinheim part 1
54. A.E. Meekhof, S.J. Hamill, V.L. Arcus, J. Clarke, and S.M. Freund The dependence of chemical exchange on boundary selection in a fibronectin type III domain from human tenascin J. Mol. Biol. 282 1998 181 194
55. S.J. Hamill, A.E. Meekhof, and J. Clarke The effect of boundary selection on the stability and folding of the third fibronectin type III domain from human tenascin Biochemistry 37 1998 8071 8079
56. E. Paci, J. Clarke, A. Steward, M. Vendruscolo, and M. Karplus Self-consistent determination of the transition state for protein folding. Application to a fibronectin type III domain Proc. Natl Acad. Sci. USA 100 2003 394 399
57. A. Steward, J.L. Toca-Herrera, and J. Clarke Versatile cloning system for construction of multimeric proteins for use in atomic force microscopy Protein Sci. 11 2002 2179 2183
58. S.B. Fowler, and J. Clarke Mapping the folding pathway of an immunoglobulin domain: structural detail from phi value analysis and movement of the transition state Structure 9 2001 355 366
59. R.B. Best, B. Li, A. Steward, V. Daggett, and J. Clarke Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation Biophys. J. 81 2001 2344 2356
60. E. Evans, and P.M. Williams Dynamic force spectroscopy I:Single bonds Les Houches-Ecole d'Ete de Physique Theorique 2002 Springer Berlin
61. T. Lazaridis, and M. Karplus Effective energy function for proteins in solution Proteins: Struct. Funct. Genet. 35 1999 133 152