Protein Nanomechanics

Comprehensive Nanoscience and Technology

Volumn 1-5, Issue , 2011, Pages 227-261

  Li, H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Atomic force microscopy; Elastomeric proteins; Folding and unfolding; Force spectroscopy; Protein nanomechanics; Single molecule studies

Indexed keywords

EID: 85042774432     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-374396-1.00087-8     Document Type: Chapter

References (151)

1. Howard J. Mechanics of Motor Proteins and the Cytoskeleton 2001, Sinauer Associates, Sunderland.
2. Tatham A.S., Shewry P.R. Elastomeric proteins: Biological roles, structures and mechanisms. Trends in Biochemical Sciences 2000, 25:567-571.
3. Schwartz M.A. Cell biology. The force is with us. Science 2009, 323:588-589.
4. del Rio A., Perez-Jimenez R., Liu R., Roca-Cusachs P., Fernandez J.M., Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 2009, 323:638-641.
5. Ingber D.E. Cellular mechanotransduction: Putting all the pieces together again. FASEB Journal 2006, 20:811-827.
6. Vogel V. Mechanotransduction involving multimodular proteins: Converting force into biochemical signals. Annual Review of Biophysics and Biomolecular Structure 2006, 35:459-488.
7. Bustamante C., Chemla Y.R., Forde N.R., Izhaky D. Mechanical processes in biochemistry. Annual Review of Biochemistry 2004, 73:705-748.
8. Gosline J., Lillie M., Carrington E., Guerette P., Ortlepp C., Savage K. Elastic proteins: Biological roles and mechanical properties. Philosophical Transactions of the Royal Society of London, Series B-Biological Sciences 2002, 357:121-132.
9. Clausen-Schaumann H., Seitz M., Krautbauer R., Gaub H.E. Force spectroscopy with single bio-molecules. Current Opinion in Chemical Biology 2000, 4:524-530.
10. Bustamante C., Macosko J.C., Wuite G.J. Grabbing the cat by the tail: Manipulating molecules one by one. Nature Reviews Molecular Cell Biology 2000, 1:130-136.
11. Evans E. Probing the relation between force-lifetime-chemistry in single molecular bonds. Annual Review of Biophysics and Biomolecular Structure 2001, 30:105-128.
12. Fisher T.E., Oberhauser A.F., Carrion-Vazquez M., Marszalek P.E., Fernandez J.M. The study of protein mechanics with the atomic force microscope. Trends in Biochemical Sciences 1999, 24:379-384.
13. Carrion-Vazquez M., Oberhauser A.F., Fisher T.E., Marszalek P.E., Li H., Fernandez J.M. Mechanical design of proteins studied by single-molecule force spectroscopy and protein engineering. Progress in Biophysics and Molecular biology 2000, 74:63-91.
14. Borgia A., Williams P.M., Clarke J. Single-molecule studies of protein folding. Annual Review of Biochemistry 2008, 77:101-125.
15. Forman J.R., Clarke J. Mechanical unfolding of proteins: Insights into biology, structure and folding. Current Opinion in Structural Biology 2007, 17:58-66.
16. Brockwell D.J. Probing the mechanical stability of proteins using the atomic force microscope. Biochemical Society Transactions 2007, 35:1564-1568.
17. Oberhauser A.F., Carrion-Vazquez M. Mechanical biochemistry of proteins one molecule at a time. Journal of Biological Chemistry 2008, 283:6617-6621.
18. Engel A., Gaub H.E. Structure and mechanics of membrane proteins. Annual Review of Biochemistry 2008, 77:127-148.
19. Muller D.J. AFM: A nanotool in membrane biology. Biochemistry 2008, 47:7986-7998.
20. Muller D.J., Sapra K.T., Scheuring S., et al. Single-molecule studies of membrane proteins. Current Opinion in Structural Biology 2006, 16:489-495.
21. Samori B., Zuccheri G., Baschieri R. Protein unfolding and refolding under force: Methodologies for nanomechanics. ChemPhysChem 2005, 6:29-34.
22. Zhuang X.W., Rief M. Single-molecule folding. Current Opinion in Structural Biology 2003, 13:88-97.
23. Carrion-Vazquez M., Oberhauser A.F., Diez H., et al. Protein nanomechanics - as studied by AFM single-molecule force spectroscopy. Advanced Techniques in Biophysics 2006, 163-235. Springer, Berlin. J.L.R. Arrondo, A. Alonso (Eds.).
24. Brockwell D.J. Force denaturation of proteins - an unfolding story. Current Nanoscience 2007, 3:3-15.
25. Li H. Engineering proteins with tailored nanomechanical properties: A single molecule approach. Organic and Biomolecular Chemistry 2007, 5:3399-3406.
26. Li H.B. Mechanical engineering' of elastomeric proteins: Toward designing new protein building blocks for biomaterials. Advanced Functional Materials 2008, 18:2643-2657.
27. Fersht A.R. Structure and Mechanism in Protein Science 1999, W. H. Freeman, New York.
28. Fersht A.R. From the first protein structures to our current knowledge of protein folding: Delights and scepticisms. Nature Reviews Molecular Cell Biology 2008, 9:650-654.
29. Fersht A.R., Daggett V. Protein folding and unfolding at atomic resolution. Cell 2002, 108:573-582.
30. Prakash S., Matouschek A. Protein unfolding in the cell. Trends in Biochemical Sciences 2004, 29:593-600.
31. Kenniston J.A., Baker T.A., Fernandez J.M., Sauer R.T. Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 2003, 114:511-520.
32. Bell G.I. Models for the specific adhesion of cells to cells. Science 1978, 200:618-627.
33. Hinterdorfer P., Dufrene Y.F. Detection and localization of single molecular recognition events using atomic force microscopy. Nature Methods 2006, 3:347-355.
34. Merkel R., Nassoy P., Leung A., Ritchie K., Evans E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 1999, 397:50-53.
35. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophysical Journal 1997, 72:1541-1555.
36. Izrailev S., Stepaniants S., Balsera M., Oono Y., Schulten K. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophysical Journal 1997, 72:1568-1581.
37. Rief M., Gautel M., Oesterhelt F., Fernandez J.M., Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 1997, 276:1109-1112.
38. Kellermayer M.S., Smith S.B., Granzier H.L., Bustamante C. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 1997, 276:1112-1116.
39. Tskhovrebova L., Trinick J., Sleep J.A., Simmons R.M. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 1997, 387:308-312.
40. Cecconi C., Shank E.A., Bustamante C., Marqusee S. Direct observation of the three-state folding of a single protein molecule. Science 2005, 309:2057-2060.
41. Kellermayer M.S., Smith S., Bustamante C., Granzier H.L. Mechanical manipulation of single titin molecules with laser tweezers. Advances in Experimental Medicine and Biology 2000, 481:111-126. discussion 127-128.
42. Kellermayer M.S., Smith S.B., Bustamante C., Granzier H.L. Mechanical fatigue in repetitively stretched single molecules of titin. Biophysics Journal 2001, 80:852-863.
43. Oberhauser A.F., Marszalek P.E., Erickson H.P., Fernandez J.M. The molecular elasticity of the extracellular matrix protein tenascin. Nature 1998, 393:181-185.
44. Fernandez J.M. Fingerprinting single molecules in vivo. Biophysics Journal 2005, 89:3676-3677.
45. Carrion-Vazquez M., Oberhauser A.F., Fowler S.B., et al. Mechanical and chemical unfolding of a single protein: A comparison. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:3694-3699.
46. Garcia-Manyes S., Brujic J., Badilla C.L., Fernandez J.M. Force-clamp spectroscopy of single-protein monomers reveals the individual unfolding and folding pathways of I27 and ubiquitin. Biophysics Journal 2007, 93:2436-2446.
47. Li H., Oberhauser A.F., Redick S.D., Carrion-Vazquez M., Erickson H.P., Fernandez J.M. Multiple conformations of PEVK proteins detected by single-molecule techniques. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:10682-10686.
48. Li H., Linke W.A., Oberhauser A.F., et al. Reverse engineering of the giant muscle protein titin. Nature 2002, 418:998-1002.
49. Best R.B., Li B., Steward A., Daggett V., Clarke J. Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophysics Journal 2001, 81:2344-2356.
50. Sharma D., Feng G., Khor D., Genchev G.Z., Lu H., Li H. Stabilization provided by neighboring strands is critical for the mechanical stability of proteins. Biophysics Journal 2008, 95:3935-3942.
51. Dietz H., Rief M. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16192-16197.
52. Peng Q., Li H. Atomic force microscopy reveals parallel mechanical unfolding pathways of T4 lysozyme: Evidence for a kinetic partitioning mechanism. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:1885-1890.
53. Perez-Jimenez R., Garcia-Manyes S., Ainavarapu S.R., Fernandez J.M. Mechanical unfolding pathways of the enhanced yellow fluorescent protein revealed by single molecule force spectroscopy. Journal of Biological Chemistry 2006, 281:40010-40014.
54. Sandal M., Valle F., Tessari I., et al. Conformational equilibria in monomeric alpha-synuclein at the single-molecule level. PLoS Biology 2008, 6:e6.
55. Dietz H., Bertz M., Schlierf M., et al. Cysteine engineering of polyproteins for single-molecule force spectroscopy. Nature Protocols 2006, 1:80-84.
56. Dietz H., Berkemeier F., Bertz M., Rief M. Anisotropic deformation response of single protein molecules. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:12724-12728.
57. Lee G., Abdi K., Jiang Y., Michaely P., Bennett V., Marszalek P.E. Nanospring behaviour of ankyrin repeats. Nature 2006, 440:246-249.
58. Li L., Wetzel S., Pluckthun A., Fernandez J.M. Stepwise unfolding of ankyrin repeats in a single protein revealed by atomic force microscopy. Biophysics Journal 2006, 90:L30-L32.
59. Carrion-Vazquez M., Marszalek P.E., Oberhauser A.F., Fernandez J.M. Atomic force microscopy captures length phenotypes in single proteins. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:11288-11292.
60. Dietz H., Rief M. Protein structure by mechanical triangulation. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:1244-1247.
61. Rief M., Fernandez J.M., Gaub H.E. Elastically coupled two-level systems as a model for biopolymer extensibility. Physical Review Letters 1998, 81:4764-4767.
62. Urry D.W., Hugel T., Seitz M., et al. Elastin: A representative ideal protein elastomer. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2002, 357:169-184.
63. Schwaiger I., Sattler C., Hostetter D.R., Rief M. The myosin coiled-coil is a truly elastic protein structure. Nature Materials 2002, 1:232-235.
64. Li L., Huang H.H., Badilla C.L., Fernandez J.M. Mechanical unfolding intermediates observed by single-molecule force spectroscopy in a fibronectin type III module. Journal of Molecular Biology 2005, 345:817-826.
65. Schwaiger I., Kardinal A., Schleicher M., Noegel A.A., Rief M. A mechanical unfolding intermediate in an actin-crosslinking protein. Nature Structural and Molecular Biology 2004, 11:81-85.
66. Bertz M., Rief M. Mechanical unfoldons as building blocks of maltose-binding protein. Journal of Molecular Biology 2008, 378:447-458.
67. Marszalek P.E., Lu H., Li H., et al. Mechanical unfolding intermediates in titin modules. Nature 1999, 402:100-103.
68. Zinober R.C., Brockwell D.J., Beddard G.S., et al. Mechanically unfolding proteins: The effect of unfolding history and the supramolecular scaffold. Protein Science 2002, 11:2759-2765.
69. Oberhauser A.F., Hansma P.K., Carrion-Vazquez M., Fernandez J.M. Stepwise unfolding of titin under force-clamp atomic force microscopy. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:468-472.
70. Schlierf M., Li H., Fernandez J.M. The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:7299-7304.
71. Fernandez J.M., Li H. Force-clamp spectroscopy monitors the folding trajectory of a single protein. Science 2004, 303:1674-1678.
72. Cao Y., Kuske R., Li H. Direct observation of Markovian behavior of the mechanical unfolding of individual proteins. Biophysics Journal 2008, 95:782-788.
73. Wang M.J., Cao Y., Li H.B. The unfolding and folding dynamics of TNfnALL probed by single molecule force-ramp spectroscopy. Polymer 2006, 47:2548-2554.
74. Brujic J., Hermans R.I., Garcia-Manyes S., Walther K.A., Fernandez J.M. Dwell-time distribution analysis of polyprotein unfolding using force-clamp spectroscopy. Biophysics Journal 2007, 92:2896-2903.
75. Walther K.A., Grater F., Dougan L., Badilla C.L., Berne B.J., Fernandez J.M. Signatures of hydrophobic collapse in extended proteins captured with force spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7916-7921.
76. Schwaiger I., Schleicher M., Noegel A.A., Rief M. The folding pathway of a fast-folding immunoglobulin domain revealed by single-molecule mechanical experiments. EMBO Rep 2005, 6:46-51.
77. Oberhauser A.F., Marszalek P.E., Carrion-Vazquez M., Fernandez J.M. Single protein misfolding events captured by atomic force microscopy. Natural Structural Biology 1999, 6:1025-1028.
78. Hyeon C., Dima R.I., thirumalai D. Pathways and kinetic barriers in mechanical unfolding and refolding of RNA and proteins. Structure 2006, 14:1633-1645.
79. Junker J.P., Ziegler F., Rief M. Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science 2009, 323:633-637.
80. Li H., Oberhauser A.F., Fowler S.B., Clarke J., Fernandez J.M. Atomic force microscopy reveals the mechanical design of a modular protein. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:6527-6531.
81. Brockwell D.J., Beddard G.S., Clarkson J., et al. The effect of core destabilization on the mechanical resistance of I27. Biophysics Journal 2002, 83:458-472.
82. Cao Y., Li H. Polyprotein of GB1 is an ideal artificial elastomeric protein. Nature Materials 2007, 6:109-114.
83. Williams P.M., Fowler S.B., Best R.B., et al. Hidden complexity in the mechanical properties of titin. Nature 2003, 422:446-449.
84. Carrion-Vazquez M., Li H., Lu H., Marszalek P.E., Oberhauser A.F., Fernandez J.M. The mechanical stability of ubiquitin is linkage dependent. Natural Structural Biology 2003, 10:738-743.
85. Brockwell D.J., Paci E., Zinober R.C., et al. Pulling geometry defines the mechanical resistance of a beta-sheet protein. Natural Structural Biology 2003, 10:731-737.
86. Dietz H., Rief M. Elastic bond network model for protein unfolding mechanics. Physical Review Letters 2008, 100:098101.
87. Rief M., Gautel M., Schemmel A., Gaub H.E. The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by atomic force microscopy. Biophysics Journal 1998, 75:3008-3014.
88. Jollymore A., Lethias C., Peng Q., Cao Y., Li H. Nanomechanical properties of tenascin-X revealed by single-molecule force spectroscopy. Journal of Molecular Biology 2009, 385:1277-1286.
89. Oberhauser A.F., Badilla-Fernandez C., Carrion-Vazquez M., Fernandez J.M. The mechanical hierarchies of fibronectin observed with single-molecule AFM. Journal of Molecular Biology 2002, 319:433-447.
90. Rief M., Pascual J., Saraste M., Gaub H.E. Single molecule force spectroscopy of spectrin repeats: Low unfolding forces in helix bundles. Journal of Molecular Biology 1999, 286:553-561.
91. Law R., Liao G., Harper S., Yang G., Speicher D.W., Discher D.E. Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains. Biophysics Journal 2003, 85:3286-3293.
92. Lenne P.F., Raae A.J., Altmann S.M., Saraste M., Horber J.K. States and transitions during forced unfolding of a single spectrin repeat. FEBS Letters 2000, 476:124-128.
93. Fuson K.L., Ma L., Sutton R.B., Oberhauser A.F. The c2 domains of human synaptotagmin 1 have distinct mechanical properties. Biophysics Journal 2009, 96:1083-1090.
94. Ainavarapu S.R., Li L., Badilla C.L., Fernandez J.M. Ligand binding modulates the mechanical stability of dihydrofolate reductase. Biophysics Journal 2005, 89:3337-3344.
95. Junker J.P., Hell K., Schlierf M., Neupert W., Rief M. Influence of substrate binding on the mechanical stability of mouse dihydrofolate reductase. Biophysics Journal 2005, 89:L46-L48.
96. Brown A.E., Litvinov R.I., Discher D.E., Weisel J.W. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophysics Journal 2007, 92:L39-L41.
97. Cao Y., Lam C., Wang M., Li H. Nonmechanical protein can have significant mechanical stability. Angewandte Chemie International Edition English 2006, 45:642-645.
98. Bornschlogl T., Rief M. Single molecule unzipping of coiled coils: Sequence resolved stability profiles. Physical Review Letters 2006, 96:118102.
99. Hann E., Kirkpatrick N., Kleanthous C., Smith D.A., Radford S.E., Brockwell D.J. The effect of protein complexation on the mechanical stability of im9. Biophysics Journal 2007, 92:L79-L81.
100. Bullard B., Garcia T., Benes V., Leake M.C., Linke W.A., Oberhauser A.F. The molecular elasticity of the insect flight muscle proteins projectin and kettin. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:4451-4456.
101. Bornschlogl T., Woehlke G., Rief M. Single molecule mechanics of the kinesin neck. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:6992-6997.
102. Carl P., Kwok C.H., Manderson G., Speicher D.W., Discher D.E. Forced unfolding modulated by disulfide bonds in the Ig domains of a cell adhesion molecule. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:1565-1570.
103. Schoenauer R., Bertoncini P., Machaidze G., et al. Myomesin is a molecular spring with adaptable elasticity. Journal of Molecular Biology 2005, 349:367-379.
104. Zhao J.M., Lee H., Nome R.A., Majid S., Scherer N.F., Hoff W.D. Single-molecule detection of structural changes during Per-Arnt-Sim (PAS) domain activation. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:11561-11566.
105. Bornschlogl T., Anstrom D.M., Mey E., Dzubiella J., Rief M., Forest K.T. Tightening the knot in phytochrome by single-molecule atomic force microscopy. Biophysics Journal 2009, 96:1508-1514.
106. Miller E., Garcia T., Hultgren S., Oberhauser A.F. The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophysics Journal 2006, 91:3848-3856.
107. Forman J.R., Qamar S., Paci E., Sandford R.N., Clarke J. The remarkable mechanical strength of polycystin-1 supports a direct role in mechanotransduction. Journal of Molecular Biology 2005, 349:861-871.
108. Brockwell D.J., Beddard G.S., Paci E., et al. Mechanically unfolding the small, topologically simple protein L. Biophysics Journal 2005, 89:506-519.
109. Altmann S.M., Grunberg R.G., Lenne P.F., et al. Pathways and intermediates in forced unfolding of spectrin repeats. Structure 2002, 10:1085-1096.
110. Randles L.G., Rounsevell R.W., Clarke J. Spectrin domains lose cooperativity in forced unfolding. Biophysics Journal 2007, 92:571-577.
111. Yang G., Cecconi C., Baase W.A., et al. Solid-state synthesis and mechanical unfolding of polymers of T4 lysozyme. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:139-144.
112. Ng S.P., Rounsevell R.W., Steward A., et al. Mechanical unfolding of TNfn3: The unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation. Journal of Molecular Biology 2005, 350:776-789.
113. Watanabe K., Muhle-Goll C., Kellermayer M.S., Labeit S., Granzier H. Different molecular mechanics displayed by titin's constitutively and differentially expressed tandem Ig segments. Journal of Structural Biology 2002, 137:248-258.
114. Puchner E.M., Alexandrovich A., Kho A.L., et al. Mechanoenzymatics of titin kinase. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:13385-13390.
115. Greene D.N., Garcia T., Sutton R.B., Gernert K.M., Benian G.M., Oberhauser A.F. Single-molecule force spectroscopy reveals a stepwise unfolding of Caenorhabditis elegans giant protein kinase domains. Biophysics Journal 2008, 95:1360-1370.
116. Li H., Fernandez J.M. Mechanical design of the first proximal Ig domain of human cardiac titin revealed by single molecule force spectroscopy. Journal of Molecular Biology 2003, 334:75-86.
117. Sharma D., Perisic O., Peng Q., et al. Single-molecule force spectroscopy reveals a mechanically stable protein fold and the rational tuning of its mechanical stability. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:9278-9283.
118. Chyan C.L., Lin F.C., Peng H., et al. Reversible mechanical unfolding of single ubiquitin molecules. Biophysics Journal 2004, 87:3995-4006.
119. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP: A structural classification of proteins database for the investigation of sequences and structures. Journal of Molecular Biology 1995, 247:536-540. http://scop.mrc-lmb.cam.ac.uk.
120. Kuhlman B., Dantas G., Ireton G.C., Varani G., Stoddard B.L., Baker D. Design of a novel globular protein fold with atomic-level accuracy. Science 2003, 302:1364-1368.
121. Sulkowska J.I., Cieplak M. Mechanical stretching of proteins - a theoretical survey of the Protein Data Bank. Journal of Physics-Condensed Matter 2007, 19:1-60.
122. Li P.C., Makarov D.E. Ubiquitin-like protein domains show high resistance to mechanical unfolding similar to that of the 127 domain in titin: Evidence from simulations. Journal of Physical Chemistry B 2004, 108:745-749.
123. Labeit S., Kolmerer B. Titins: Giant proteins in charge of muscle ultrastructure and elasticity. Science 1995, 270:293-296.
124. Wang K., McClure J., Tu A. Titin: Major myofibrillar components of striated muscle. Proceedings of the National Academy of Sciences of the United States of America 1979, 76:3698-3702.
125. Maruyama K. Connectin, an elastic filamentous protein of striated muscle. International Review of Cytology 1986, 104:81-114.
126. Lu H., Isralewitz B., Krammer A., Vogel V., Schulten K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophysics Journal 1998, 75:662-671.
127. Lu H., Schulten K. The key event in force-induced unfolding of Titin's immunoglobulin domains. Biophysics Journal 2000, 79:51-65.
128. Paci E., Karplus M. Unfolding proteins by external forces and temperature: The importance of topology and energetics. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:6521-6526.
129. Li H., Carrion-Vazquez M., Oberhauser A.F., Marszalek P.E., Fernandez J.M. Point mutations alter the mechanical stability of immunoglobulin modules. Natural Structural Biology 2000, 7:1117-1120.
130. Best R.B., Fowler S.B., Herrera J.L., Steward A., Paci E., Clarke J. Mechanical unfolding of a titin Ig domain: Structure of transition state revealed by combining atomic force microscopy, protein engineering and molecular dynamics simulations. Journal of Molecular Biology 2003, 330:867-877.
131. Linke W.A., Rudy D.E., Centner T., et al. I-band titin in cardiac muscle is a three-element molecular spring and is critical for maintaining thin filament structure. Journal of Cell Biology 1999, 146:631-644.
132. Cao Y., Li H.B. Engineered elastomeric proteins with dual elasticity can be controlled by a molecular regulator. Nature Nanotechnology 2008, 3:512-516.
133. Klimov D.K., Thirumalai D. Stretching single-domain proteins: Phase diagram and kinetics of force-induced unfolding. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:6166-6170.
134. Paci E., Karplus M. Forced unfolding of fibronectin type 3 modules: An analysis by biased molecular dynamics simulations. Journal of Molecular Biology 1999, 288:441-459.
135. Li P.C., Makarov D.E. Simulation of the mechanical unfolding of ubiquitin: Probing different unfolding reaction coordinates by changing the pulling geometry. Journal of Chemical Physics 2004, 121:4826-4832.
136. Li P.C., Makarov D.E. Theoretical studies of the mechanical unfolding of the muscle protein titin: Bridging the time-scale gap between simulation and experiment. Journal of Chemical Physics 2003, 119:9260-9268.
137. Best R.B., Fowler S.B., Toca-Herrera J.L., Clarke J. A simple method for probing the mechanical unfolding pathway of proteins in detail. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:12143-12148.
138. Deechongkit S., Dawson P.E., Kelly J.W. Toward assessing the position-dependent contributions of backbone hydrogen bonding to beta-sheet folding thermodynamics employing amide-to-ester perturbations. Journal of the American Chemical Society 2004, 126:16762-16771.
139. Deechongkit S., Nguyen H., Powers E.T., Dawson P.E., Gruebele M., Kelly J.W. Context-dependent contributions of backbone hydrogen bonding to beta-sheet folding energetics. Nature 2004, 430:101-105.
140. Wilcox A.J., Choy J., Bustamante C., Matouschek A. Effect of protein structure on mitochondrial import. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:15435-15440.
141. Cao Y., Balamurali M.M., Sharma D., Li H. A functional single-molecule binding assay via force spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15677-15681.
142. Cao Y., Yoo T., Zhuang S., Li H. Protein-protein interaction regulates proteins' mechanical stability. Journal of Molecular Biology 2008, 378:1132-1141.
143. Cao Y., Yoo T., Li H. Single molecule force spectroscopy reveals engineered metal chelation is a general approach to enhance mechanical stability of proteins. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:11152-11157.
144. Schlierf M., Rief M. Temperature softening of a protein in single-molecule experiments. Journal of Molecular Biology 2005, 354:497-503.
145. Cao Y., Li H. How do chemical denaturants affect the mechanical folding and unfolding of proteins?. Journal of Molecular Biology 2008, 375:316-324.
146. Dougan L., Feng G., Lu H., Fernandez J.M. Solvent molecules bridge the mechanical unfolding transition state of a protein. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:3185-3190.
147. Yuan J.M., Chyan C.L., Zhou H.X., et al. The effects of macromolecular crowding on the mechanical stability of protein molecules. Protein Science 2008, 17:2156-2166.
148. Maruyama K., Matsubara S., Natori R., Nonomura Y., Kimura S. Connectin, an elastic protein of muscle. Characterization and function. Journal of Biochemistry (Tokyo) 1977, 82:317-337.
149. Minajeva A., Kulke M., Fernandez J.M., Linke W.A. Unfolding of titin domains explains the viscoelastic behavior of skeletal myofibrils. Biophysics Journal 2001, 80:1442-1451.
150. Dugdale T.M., Dagastine R., Chiovitti A., Mulvaney P., Wetherbee R. Single adhesive nanofibers from a live diatom have the signature fingerprint of modular proteins. Biophysics Journal 2005, 89:4252-4260.
151. Sarkar A., Caamano S., Fernandez J.M. The mechanical fingerprint of a parallel polyprotein dimer. Biophysics Journal 2007, 92:L36-L38.