Force-induced remodelling of proteins and their complexes

Current Opinion in Structural Biology

Volumn 30, Issue , 2015, Pages 89-99

  Chen, Yun ^a   Radford, Sheena E ^a   Brockwell, David J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEIN; MULTIPROTEIN COMPLEX;

ATOMIC FORCE MICROSCOPY; BINDING SITE; BIOSENSOR; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; FORCE; MOLECULAR INTERACTION; OPTICAL TWEEZERS; PATCH CLAMP TECHNIQUE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN UNFOLDING; REVIEW; BIOLOGICAL MODEL; BIOMECHANICS; BIOPHYSICS; CHEMISTRY; MOLECULAR MODEL; PROCEDURES; PROTEIN FOLDING;

BIOMECHANICAL PHENOMENA; BIOPHYSICS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; OPTICAL TWEEZERS; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 84923084610     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.02.001     Document Type: Review

References (103)

1. Crampton N., Brockwell D.J. Unravelling the design principles for single protein mechanical strength. Curr Opin Struct Biol 2010, 20:508-517.
2. Woodside M.T., Block S.M. Reconstructing folding energy landscapes by single-molecule force spectroscopy. Ann Rev Biophys 2014, 43:19-39.
3. Hinterdorfer P., Dufrene Y.F. Detection and localization of single molecular recognition events using atomic force microscopy. Nat Methods 2006, 3:347-355.
4. Churnside A.B., Sullan R.M., Nguyen D.M., Case S.O., Bull M.S., King G.M., Perkins T.T. Routine and timely subpicoNewton force stability and precision for biological applications of atomic force microscopy. Nano Lett 2012, 12:3557-3561.
5. Bull M.S., Sullan R.M., Li H., Perkins T.T. Improved single molecule force spectroscopy using micromachined cantilevers. ACS Nano 2014, 8:4984-4995.
6. Perkins T.T. Angstrom-precision optical traps and applications. Ann Rev Biophys 2014, 43:279-302.
7. De Vlaminck I., Dekker C. Recent advances in magnetic tweezers. Ann Rev Biophys 2012, 41:453-472.
8. Sellers J.R., Veigel C. Direct observation of the myosin-Va power stroke and its reversal. Nat Struct Mol Biol 2010, 17:590-595.
9. Clancy B.E., Behnke-Parks W.M., Andreasson J.O., Rosenfeld S.S., Block S.M. A universal pathway for kinesin stepping. Nat Struct Mol Biol 2011, 18:1020-1027.
10. Maillard R.A., Chistol G., Sen M., Righini M., Tan J., Kaiser C.M., Hodges C., Martin A., Bustamante C. ClpX(P) generates mechanical force to unfold and translocate its protein substrates. Cell 2011, 145:459-469.
11. Aubin-Tam M.-E., Olivares A.O., Sauer R.T., Baker T.A., Lang M.J. Single-molecule protein unfolding and translocation by an ATP-fueled proteolytic machine. Cell 2011, 145:257-267.
12. Klaue D., Kobbe D., Kemmerich F., Kozikowska A., Puchta H., Seidel R. Fork sensing and strand switching control antagonistic activities of RecQ helicases. Nat Commun 2013, 4:2024.
13. Stigler J., Ziegler F., Gieseke A., Gebhardt J.C., Rief M. The complex folding network of single calmodulin molecules. Science 2011, 334:512-516.
14. Andersen O.S., Koeppe R.E. Molecular determinants of channel function. Physiol Rev 1992, 72:S89-S158.
15. Zhou R., Schlierf M., Ha T. Force fluorescence spectroscopy at the single-molecule level. Methods Enzymol 2010, 475:405-426.
16. del Rio A., Perez-Jimenez R., Liu R.C., Roca-Cusachs P., Fernandez J.M., Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 2009, 323:638-641.
17. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys J 1997, 72:1541-1555.
18. Evans E. Probing the relation between force - lifetime - and chemistry in single molecular bonds. Ann Rev Biophys Biomol Struct 2001, 30:105-128.
19. Hummer G., Szabo A. Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J 2003, 85:5-15.
20. Dudko O.K., Hummer G., Szabo A. Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proc Natl Acad Sci USA 2008, 105:15755-15760.
21. Friddle R.W., Noy A., De Yoreo J.J. Interpreting the widespread nonlinear force spectra of intermolecular bonds. Proc Natl Acad Sci USA 2012, 109:13573-13578.
22. Smith D.E., Tans S.J., Smith S.B., Grimes S., Anderson D.L., Bustamante C. The bacteriophage phi 29 portal motor can package DNA against a large internal force. Nature 2001, 413:748-752.
23. Wang X., Ha T. Defining single molecular forces required to activate integrin and notch signaling. Science 2013, 340:991-994.
24. Natkanski E., Lee W.-Y., Mistry B., Casal A., Molloy J.E., Tolar P. B cells use mechanical energy to discriminate antigen affinities. Science 2013, 340:1587-1590.
25. Schwesinger F., Ros R., Strunz T., Anselmetti D., Guntherodt H.J., Honegger A., Jermutus L., Tiefenauer L., Pluckthun A. Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates. Proc Natl Acad Sci USA 2000, 97:9972-9977.
26. Preiner J., Kodera N., Tang J., Ebner A., Brameshuber M., Blaas D., Gelbmann N., Gruber H.J., Ando T., Hinterdorfer P. IgGs are made for walking on bacterial and viral surfaces. Nat Commun 2014, 5:4394.
27. Lv C., Gao X., Li W., Xue B., Qin M., Burtnick L.D., Zhou H., Cao Y., Robinson R.C., Wang W. Single-molecule force spectroscopy reveals force-enhanced binding of calcium ions by gelsolin. Nat Commun 2014, 5:4623.
28. Choi B., Zocchi G. Mimicking cAMP-dependent allosteric control of protein kinase a through mechanical tension. J Am Chem Soc 2006, 128:8541-8548.
29. Tseng C.-Y., Zocchi G. Mechanical control of renilla luciferase. J Am Chem Soc 2013, 135:11879-11886.
30. Bustamante C., Chemla Y.R., Forde N.R., Izhaky D. Mechanical processes in biochemistry. Ann Rev Biochem 2004, 73:705-748.
31. Beyer M.K., Clausen-Schaumann H. Mechanochemistry: the mechanical activation of covalent bonds. Chem Rev 2005, 105:2921-2948.
32. Yang Q.-Z., Huang Z., Kucharski T.J., Khvostichenko D., Chen J., Boulatov R. A molecular force probe. Nat Nanotechnol 2009, 4:302-306.
33. Wiita A.P., Perez-Jimenez R., Walther K.A., Graeter F., Berne B.J., Holmgren A., Sanchez-Ruiz J.M., Fernandez J.M. Probing the chemistry of thioredoxin catalysis with force. Nature 2007, 450:124-127.
34. Perez-Jimenez R., Ingles-Prieto A., Zhao Z.-M., Sanchez-Romero I., Alegre-Cebollada J., Kosuri P., Garcia-Manyes S., Kappock T.J., Tanokura M., Holmgren A., et al. Single-molecule paleoenzymology probes the chemistry of resurrected enzymes. Nat Struct Mol Biol 2011, 18:592-596.
35. Puchner E.M., Alexandrovich A., Kho A.L., Hensen U., Schafer L.V., Brandmeier B., Grater F., Grubmuller H., Gaub H.E., Gautel M. Mechanoenzymatics of titin kinase. Proc Natl Acad Sci USA 2008, 105:13385-13390.
36. Ehrlicher A.J., Nakamura F., Hartwig J.H., Weitz D.A., Stossel T.P. Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A. Nature 2011, 478:260-263.
37. Rognoni L., Stigler J., Pelz B., Ylaenne J., Rief M. Dynamic force sensing of filamin revealed in single-molecule experiments. Proc Natl Acad Sci USA 2012, 109:19679-19684.
38. Rognoni L., Moest T., Zoldak G., Rief M. Force-dependent isomerization kinetics of a highly conserved proline switch modulates the mechanosensing region of filamin. Proc Natl Acad Sci USA 2014, 111:5568-5573.
39. 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.
40. 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. Proc Natl Acad Sci USA 2001, 98:1565-1570.
41. Pinotsis N., Chatziefthimiou S.D., Berkemeier F., Beuron F., Mavridis I.M., Konarev P.V., Svergun D.I., Morris E., Rief M., Wilmanns M. Superhelical architecture of the myosin filament-linking protein myomesin with unusual elastic properties. PLoS Biol 2012, 10:e1001261.
42. Pinotsis N., Lange S., Perriard J.-C., Svergun D.I., Wilmanns M. Molecular basis of the C-terminal tail-to-tail assembly of the sarcomeric filament protein myomesin. EMBO J 2008, 27:253-264.
43. Berkemeier F., Bertz M., Xiao S., Pinotsis N., Wilmanns M., Graeter F., Rief M. Fast-folding alpha-helices as reversible strain absorbers in the muscle protein myomesin. Proc Natl Acad Sci USA 2011, 108:14139-14144.
44. Forero M., Yakovenko O., Sokurenko E.V., Thomas W.E., Vogel V. Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds. PLoS Biol 2006, 4:1509-1516.
45. Miller E., Garcia T., Hultgren S., Oberhauser A.F. The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophys J 2006, 91:3848-3856.
46. Lugmaier R.A., Schedin S., Kuehner F., Benoit M. Dynamic restacking of Escherichia coli P-pili. Eur Biophys J 2008, 37:111-120.
47. Beaussart A., Baker A.E., Kuchma S.L., El-Kirat-Chatel S., O'Toole G.A., Dufrene Y.F. Nanoscale adhesion forces of Pseudomonas aeruginosa type IV pili. ACS Nano 2014, 8:10723-10733.
48. Perez-Jimenez R., Alonso-Caballero A., Berkovich R., Franco D., Chen M.-W., Richard P., Badilla C.L., Fernandez J.M. Probing the effect of force on HIV-1 receptor CD4. ACS Nano 2014, 8:10313-10320.
49. Freeman M.M., Seaman M.S., Rits-Volloch S., Hong X., Kao C.-Y., Ho D.D., Chen B. Crystal structure of HIV-1 primary receptor CD4 in complex with a potent antiviral antibody. Structure 2010, 18:1632-1641.
50. 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.
51. Lu H., Schulten K. Steered molecular dynamics simulations of force-induced protein domain unfolding. Proteins 1999, 35:453-463.
52. Paci E., Karplus M. Unfolding proteins by external forces and temperature: the importance of topology and energetics. Proc Natl Acad Sci USA 2000, 97:6521-6526.
53. Klimov D.K., Thirumalai D. Native topology determines force-induced unfolding pathways in globular proteins. Proc Natl Acad Sci USA 2000, 97:7254-7259.
54. Hoffmann T., Tych K.M., Hughes M.L., Brockwell D.J., Dougan L. Towards design principles for determining the mechanical stability of proteins. Phys Chem Chem Phys 2013, 15:15767-15780.
55. Yao M., Qiu W., Liu R., Efremov A.K., Cong P., Seddiki R., Payre M., Lim C.T., Ladoux B., Mege R.-M., et al. Force-dependent conformational switch of alpha-catenin controls vinculin binding. Nat Commun 2014, 5:4525.
56. Remaut H., Waksman G. Protein-protein interaction through beta-strand addition. Trends Biochem Sci 2006, 31:436-444.
57. Waksman G., Hultgren S.J. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 2009, 7:765-774.
58. Shultis D.D., Purdy M.D., Banchs C.N., Wiener M.C. Outer membrane active transport: structure of the BtuB: TonB complex. Science 2006, 312:1396-1399.
59. Fang J., Mehlich A., Koga N., Huang J., Koga R., Gao X., Hu C., Jin C., Rief M., Kast J., et al. Forced protein unfolding leads to highly elastic and tough protein hydrogels. Nat Commun 2013, 4:2974.
60. Brockwell D.J., Beddard G.S., Paci E., West D.K., Olmsted P.D., Smith D.A., Radford S.E. Mechanically unfolding the small, topologically simple protein L. Biophys J 2005, 89:506-519.
61. Sadler D.P., Petrik E., Taniguchi Y., Pullen J.R., Kawakami M., Radford S.E., Brockwell D.J. Identification of a mechanical rheostat in the hydrophobic core of protein L. J Mol Biol 2009, 393:237-248.
62. Brockwell D.J., Paci E., Zinober R.C., Beddard G.S., Olmsted P.D., Smith D.A., Perham R.N., Radford S.E. Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nat Struct Biol 2003, 10:731-737.
63. Carrion-Vazquez M., Li H.B., Lu H., Marszalek P.E., Oberhauser A.F., Fernandez J.M. The mechanical stability of ubiquitin is linkage dependent. Nat Struct Biol 2003, 10:738-743.
64. Dietz H., Berkemeier F., Bertz M., Rief M. Anisotropic deformation response of single protein molecules. Proc Natl Acad Sci USA 2006, 103:12724-12728.
65. Jagannathan B., Elms P.J., Bustamante C., Marqusee S. Direct observation of a force-induced switch in the anisotropic mechanical unfolding pathway of a protein. Proc Natl Acad Sci USA 2012, 109:17820-17825.
66. Li Y.D., Lamour G., Gsponer J., Zheng P., Li H. The molecular mechanism underlying mechanical anisotropy of the protein GB1. Biophys J 2012, 103:2361-2368.
67. Lee W., Zeng X., Rotolo K., Yang M., Schofield C.J., Bennett V., Yang W., Marszalek P.E. Mechanical anisotropy of ankyrin repeats. Biophys J 2012, 102:1118-1126.
68. Junker J.P., Rief M. Evidence for a broad transition-state ensemble in calmodulin folding from single-molecule force spectroscopy. Angew Chem Int Ed Engl 2010, 49:3306-3309.
69. Gao X., Qin M., Yin P., Liang J., Wang J., Cao Y., Wang W. Single-molecule experiments reveal the flexibility of a Per-ARNT-Sim domain and the kinetic partitioning in the unfolding pathway under force. Biophys J 2012, 102:2149-2157.
70. Popa I., Berkovich R., Alegre-Cebollada J., Badilla C.L., Rivas-Pardo J.A., Taniguchi Y., Kawakami M., Fernandez J.M. Nanomechanics of HaloTag tethers. J Am Chem Soc 2013, 135:12762-12771.
71. 4 metal center in rubredoxin. J Am Chem Soc 2013, 135:17783-17792.
72. Bertz M., Wilmanns M., Rief M. The titin-telethonin complex is a directed, superstable molecular bond in the muscle Z-disk. Proc Natl Acad Sci USA 2009, 106:13307-13310.
73. Farrance O.E., Hann E., Kaminska R., Housden N.G., Derrington S.R., Kleanthous C., Radford S.E., Brockwell D.J. A force-activated trip switch triggers rapid dissociation of a colicin from its immunity protein. PLoS Biol 2013, 11:e1001489.
74. Buckley C.D., Tan J., Anderson K.L., Hanein D., Volkmann N., Weis W.I., Nelson W.J., Dunn A.R. Cell adhesion: the minimal cadherin-catenin complex binds to actin filaments under force. Science 2014, 346:1254211.
75. Dembo M., Torney D.C., Saxman K., Hammer D. The reaction-limited kinetics of membrane-to-surface adhesion and detachment. Proc R Soc Lond B Biol Sci 1988, 234:55-83.
76. Thomas W.E., Trintchina E., Forero M., Vogel V., Sokurenko E.V. Bacterial adhesion to target cells enhanced by shear force. Cell 2002, 109:913-923.
77. Marshall B.T., Long M., Piper J.W., Yago T., McEver R.P., Zhu C. Direct observation of catch bonds involving cell-adhesion molecules. Nature 2003, 423:190-193.
78. Lou J., Yago T., Klopocki A.G., Mehta P., Chen W., Zarnitsyna V.I., Bovin N.V., Zhu C., McEver R.P. Flow-enhanced adhesion regulated by a selectin interdomain hinge. J Cell Biol 2006, 174:1107-1117.
79. Manibog K., Li H., Rakshit S., Sivasankar S. Resolving the molecular mechanism of cadherin catch bond formation. Nat Commun 2014, 5:3941.
80. Chakrabarti S., Hinczewski M., Thirumalai D. Plasticity of hydrogen bond networks regulates mechanochemistry of cell adhesion complexes. Proc Natl Acad Sci USA 2014, 111:9048-9053.
81. Kim J., Zhang C.Z., Zhang X.H., Springer T.A. A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 2010, 466:992-995.
82. Hong H.D., Tamm L.K. Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc Natl Acad Sci USA 2004, 101:4065-4070.
83. Lee G., Abdi K., Jiang Y., Michaely P., Bennett V., Marszalek P.E. Nanospring behaviour of ankyrin repeats. Nature 2006, 440:246-249.
84. Howard J., Bechstedt S. Hypothesis: a helix of ankyrin repeats of the NOMPIC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol 2004, 14:R224-R226.
85. Corey D.P., Garcia-Anoveros J., Holt J.R., Kwan K.Y., Lin S.Y., Vollrath M.A., Amalfitano A., Cheung E.L., Derfler B.H., Duggan A., et al. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 2004, 432:723-730.
86. Sotomayor M., Corey D.P., Schulten K. In search of the hair-cell gating spring: elastic properties of ankyrin and cadherin repeats. Structure 2005, 13:669-682.
87. Dupres V., Alsteens D., Wilk S., Hansen B., Heinisch J.J., Dufrene Y.F. The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo. Nat Chem Biol 2009, 5:857-862.
88. Muller D.J. AFM: a nanotool in membrane biology. Biochemistry 2008, 47:7986-7998.
89. Kessler M., Gottschalk K.E., Janovjak H., Muller D.J., Gaub H.E. Bacteriorhodopsin folds into the membrane against an external force. J Mol Biol 2006, 357:644-654.
90. Anishkin A., Loukin S.H., Teng J., Kung C. Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci USA 2014, 111:7898-7905.
91. Sukharev S.I., Blount P., Martinac B., Blattner F.R., Kung C. A large-conductance mechanosensitive channel in E. coli encoded by MscL alone. Nature 1994, 368:265-268.
92. Nomura T., Cranfield C.G., Deplazes E., Owen D.M., Macmillan A., Battle A.R., Constantine M., Sokabe M., Martinac B. Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS. Proc Natl Acad Sci USA 2012, 109:8770-8775.
93. Berrier C., Pozza A., De lavalette A.D.L., Chardonnet S., Mesneau A., Jaxel C., Le Maire M., Ghazi A. The purified mechanosensitive channel TREK-1 is directly sensitive to membrane tension. J Biol Chem 2013, 288:27307-27314.
94. + channels. Proc Natl Acad Sci USA 2014, 111:3614-3619.
95. Guo M., Ehrlicher A.J., Jensen M.H., Renz M., Moore J.R., Goldman R.D., Lippincott-Schwartz J., Mackintosh F.C., Weitz D.A. Probing the stochastic, motor-driven properties of the cytoplasm using force spectrum microscopy. Cell 2014, 158:822-832.
96. Grashoff C., Hoffman B.D., Brenner M.D., Zhou R., Parsons M., Yang M.T., McLean M.A., Sligar S.G., Chen C.S., Ha T., et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 2010, 466:263-266.
97. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF chimera - a visualization system for exploratory research and analysis. J Comput Chem 2004, 25:1605-1612.
98. Lad Y., Kiema T., Jiang P., Pentikaeinen O.T., Coles C.H., Campbell I.D., Calderwood D.A., Ylaenne J. Structure of three tandem filamin domains reveals auto-inhibition of ligand binding. EMBO J 2007, 26:3993-4004.
99. Kiema T., Lad Y., Jiang P.J., Oxley C.L., Baldassarre M., Wegener K.L., Campbell I.D., Ylanne J., Calderwood D.A. The molecular basis of filamin binding to integrins and competition with talin. Mol Cell 2006, 21:337-347.
100. Le Trong I., Aprikian P., Kidd B.A., Forero-Shelton M., Tchesnokova V., Rajagopal P., Rodriguez V., Interlandi G., Klevit R., Vogel V., et al. Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting. Cell 2010, 141:645-655.
101. Rangarajan E.S., Izard T. Dimer asymmetry defines alpha-catenin interactions. Nat Struct Mol Biol 2013, 20:188-193.
102. Rangarajan E.S., Izard T. The cytoskeletal protein alpha-catenin unfurls upon binding to vinculin. J Biol Chem 2012, 287:18492-18499.
103. Fillingham I., Gingras A.R., Papagrigoriou E., Patel B., Emsley J., Critchley D.R., Roberts G.C.K., Barsukov I.L. A vinculin binding domain from the talin rod unfolds to form a complex with the vinculin head. Structure 2005, 13:65-74.