Sampling protein form and function with the atomic force microscope

Molecular and Cellular Proteomics

Volumn 9, Issue 8, 2010, Pages 1678-1688

  Baclayon, Marian ^a   Roos, Wouter H ^a   Wuite, Gijs J L ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; BIOTIN; CALMODULIN; CONNECTIN; DNA; FIBRINOGEN; GREEN FLUORESCENT PROTEIN; RNA; STREPTAVIDIN; VIRUS DNA; YELLOW FLUORESCENT PROTEIN; PROTEIN;

ATOMIC FORCE MICROSCOPY; BIOMECHANICS; BLASTOCHLORIS VIRIDIS; BLOOD CLOT; CHEMICAL BOND; COWPEA; FORCE; HEPATITIS B VIRUS; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; OSCILLATION; PIEZOELECTRICITY; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SPECTROSCOPY; STRUCTURAL BIOINFORMATICS; TRICHOVIRUS; VIRUS GENOME; ANIMAL; CHEMISTRY; DEVICES; METABOLISM;

ANIMALS; MICROSCOPY, ATOMIC FORCE; PROTEINS;

EID: 77955362122     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.R110.001461     Document Type: Review

References (175)

1. Heck, A. J. (2008) Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 5, 927-933
2. Binnig, G., Quate, C. F., and Gerber, C. (1986) Atomic force microscope. Phys. Rev. Lett. 56, 930-933
3. Fechner, P., Boudier, T., Mangenot, S., Jaroslawski, S., Sturgis, J. N., and Scheuring, S. (2009) Structural information, resolution, and noise in high-resolution atomic force microscopy topographs. Biophys. J. 96, 3822-3831
4. Scheuring, S., and Sturgis, J. N. (2005) Chromatic adaptation of photosynthetic membranes. Science 309, 484-487
5. Henderson, E. (1992) Imaging and nanodissection of individual supercoiled plasmids by atomic force microscopy. Nucleic Acids Res. 20, 445-447
6. Engel, A., and Müller, D. J. (2000) Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7, 715-718
7. Baclayon, M., Wuite, G. J., and Roos, W. H. (2010) Imaging and manipulation of single viruses by atomic force microscopy. Soft Matter, doi:10.1039/b923992h
8. Scheuring, S., Fotiadis, D., Moller, C., Muller, S. A., Engel, A., and Muller, D. J. (2001) Single proteins observed by atomic force microscopy. Single Mol. 2, 59-67
9. King, G. M., Carter, A. R., Churnside, A. B., Eberle, L. S., and Perkins, T. T. (2009) Ultrastable atomic force microscopy: atomic-scale stability and registration in ambient conditions. Nano Lett. 9, 1451-1456
10. Junker, J. P., Ziegler, F., and Rief, M. (2009) Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science 323, 633-637
11. Hafner, J. H., Cheung, C. L., Woolley, A. T., and Lieber, C. M. (2001) Structural and functional imaging with carbon nanotube AFM probes. Prog. Biophys. Mol. Biol. 77, 73-110
12. Cheung, C. L., Hafner, J. H., and Lieber, C. M. (2000) Carbon nanotube atomic force microscopy tips: direct growth by chemical vapor deposition and application to high-resolution imaging. Proc. Natl. Acad. Sci. U.S.A. 97, 3809-3813
13. Ebner, A., Wildling, L., Zhu, R., Rankl, C., Haselgrubler, T., Hinterdorfer, P., and Gruber, H. J. (2008) Functionalization of probe tips and supports for single-molecule recognition force microscopy, in STM and AFM Studies On (Bio)Molecular Systems: Unravelling the Nanoworld, pp. 29-76, Springer-Verlag, Berlin
14. Ebner, A., Hinterdorfer, P., and Gruber, H. J. (2007) Comparison of different aminofunctionalization strategies for attachment of single antibodies to AFM cantilevers. Ultramicroscopy 107, 922-927
15. Hinterdorfer, P., Baumgartner, W., Gruber, H. J., Schilcher, K., and Schindler, H. (1996) Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 93, 3477-3481
16. Wong, S. S., Joselevich, E., Woolley, A. T., Cheung, C. L., and Lieber, C. M. (1998) Covalently functionalized nanotubes as nanometre-sized probes in chemistry and biology. Nature 394, 52-55
17. Hinterdorfer, P., and Dufrêne, Y. F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3, 347-355
18. Ebner, A., Wildling, L., Kamruzzahan, A. S., Rankl, C., Wruss, J., Hahn, C. D., Hölzl, M., Zhu, R., Kienberger, F., Blaas, D., Hinterdorfer, P., and Gruber, H. J. (2007) A new, simple method for linking of antibodies to atomic force microscopy tips. Bioconjug. Chem. 18, 1176-1184
19. Hards, A., Zhou, C., Seitz, M., Bräuchle, C., and Zumbusch, A. (2005) Simultaneous AFM manipulation and fluorescence imaging of single DNA strands. ChemPhysChem 6, 534-540
20. Kufer, S. K., Puchner, E. M., Gumpp, H., Liedl, T., and Gaub, H. E. (2008) Single-molecule cut-and-paste surface assembly. Science 319, 594-596
21. Kassies, R., van der Werf, K. O., Lenferink, A., Hunter, C. N., Olsen, J. D., Subramaniam, V., and Otto, C. (2005) Combined AFM and confocal fluorescence microscope for applications in bio-nanotechnology. J. Microsc. 217, 109-116
22. Ando, T., Kodera, N., Takai, E., Maruyama, D., Saito, K., and Toda, A. (2001) A high-speed atomic force microscope for studying biological macromolecules. Proc. Natl. Acad. Sci. U.S.A. 98, 12468-12472
23. Sulchek, T., Hsieh, R., Adams, J. D., Minne, S. C., Quate, C. F., and Adderton, D. M. (2000) High-speed atomic force microscopy in liquid. Rev. Sci. Instrum. 71, 2097-2099
24. Casuso, I., Kodera, N., Le Grimellec, C., Ando, T., and Scheuring, S. (2009) Contact-mode high-resolution high-speed atomic force microscopy movies of the purple membrane. Biophys. J. 97, 1354-1361
25. Fantner, G. E., Barbero, R. J., Gray, D. S., and Belcher, A. M. (2010) Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nat. Nanotechnol. 5, 280-285
26. Hansma, P. K., Schitter, G., Fantner, G. E., and Prater, C. (2006) Applied physics - high-speed atomic force microscopy. Science 314, 601-602
27. Dufrêne, Y. F. (2009) Atomic force microscopy: a powerful molecular toolkit in nanoproteomics. Proteomics 9, 5400-5405
28. Yu, X., Xu, D., and Cheng, Q. (2006) Label-free detection methods for protein microarrays. Proteomics 6, 5493-5503
29. Archakov, A. I., Ivanov, Y. D., Lisitsa, A. V., and Zgoda, V. G. (2007) AFM fishing nanotechnology is the way to reverse the Avogadro number in proteomics. Proteomics 7, 4-9
30. Rief, M., and Grubmüller, H. (2002) Force spectroscopy of single biomolecules. ChemPhysChem 3, 255-261
31. Zeng, G., Chen, J., Zhong, L., Wang, R., Jiang, L., Cai, J., Yan, L., Huang, D., Chen, C. Y., and Chen, Z. W. (2009) NSOM- and AFM-based nanotechnology elucidates nano-structural and atomic-force features of a Y-pestis V immunogen-containing particle vaccine capable of eliciting robust response. Proteomics 9, 1538-1547
32. Roos, W. H., and Wuite, G. L. (2009) Nanoindentation studies reveal material properties of viruses. Adv. Mater. 21, 1187-1192
33. Kasas, S., and Dietler, G. (2008) Probing nanomechanical properties from biomolecules to living cells. Pflugers Arch. 456, 13-27
34. Binnig, G., Gerber, C., Stoll, E., Albrecht, T. R., and Quate, C. F. (1987) Atomic resolution with atomic force microscope. Europhys. Lett. 3, 1281-1286
35. Giessibl, F. J., and Binnig, G. (1992) Investigation of the (001) cleavage plane of potassium-bromide with an atomic force microscope at 4.2-k in ultra-high vacuum. Ultramicroscopy 42, 281-289
36. Parot, P., Dufrêne, Y. F., Hinterdorfer, P., Le Grimellec, C., Navajas, D., Pellequer, J. L., and Scheuring, S. (2007) Past, present and future of atomic force microscopy in life sciences and medicine. J. Mol. Recognit. 20, 418-431
37. Zlatanova, J., and Leuba, S. H. (2002) Stretching and imaging single DNA molecules and chromatin. J. Muscle Res. Cell Motil. 23, 377-395
38. Hansma, H. G., and Hoh, J. H. (1994) Biomolecular imaging with the atomic-force microscope. Annu. Rev. Biophys. Biomol. Struct. 23, 115-139
39. Giessibl, F. J. (2003) Advances in atomic force microscopy. Rev. Mod. Phys. 75, 949-983
40. Jalili, N., and Laxminarayana, K. (2004) A review of atomic force microscopy imaging systems: application to molecular metrology and biological sciences. Mechatronics 14, 907-945
41. Morris, V. J., Kirby, A. R., and Gunning, A. P. (2010) Atomic Force Microscopy for Biologists, 2nd Ed., Chapter 3, Imperial College Press, London
42. Garcia, R., and Perez, R. (2002) Dynamic atomic force microscopy methods. Surf. Sci. Rep. 47, 197-301
43. Braga, P. C., and Ricci, D. (2004) Atomic Force Microscopy: Biomedical Methods and Applications, Humana Press, Totowa, NJ
44. de Pablo, P. J., Colchero, J., Gomez-Herrero, J., and Baro, A. M. (1998) Jumping mode scanning force microscopy. Appl. Phys. Lett. 73, 3300-3302
45. Zhong, Q., Inniss, D., Kjoller, K., and Elings, V. B. (1993) Fractured polymer silica fiber surface studied by tapping mode atomic force microscopy. Surf. Sci. 290, L688-L692
46. Cappella, B., and Dietler, G. (1999) Force-distance curves by atomic force microscopy. Surf. Sci. Rep. 34, 1-104
47. Butt, H. J., Cappella, B., and Kappl, M. (2005) Force measurements with the atomic force microscope: technique, interpretation and applications. Surf. Sci. Rep. 59, 1-152
48. de Pablo, P. J., Schaap, I. A., MacKintosh, F. C., and Schmidt, C. F. (2003) Deformation and collapse of microtubules on the nanometer scale. Phys. Rev. Lett. 91, 098101
49. Chilkoti, A., Boland, T., Ratner, B. D., and Stayton, P. S. (1995) The relationship between ligand-binding thermodynamics and protein-ligand interaction forces measured by atomic force microscopy. Biophys. J. 69, 2125-2130
50. Takano, H., Kenseth, J. R., Wong, S. S., O'Brien, J. C., and Porter, M. D. (1999) Chemical and biochemical analysis using scanning force microscopy. Chem. Rev. 99, 2845-2890
51. Leckband, D. (2000) Measuring the forces that control protein interactions. Annu. Rev. Biophys. Biomol. Struct. 29, 1-26
52. Zlatanova, J., Lindsay, S. M., and Leuba, S. H. (2000) Single molecule force spectroscopy in biology using the atomic force microscope. Prog. Biophys. Mol. Biol. 74, 37-61
53. Oberhauser, A. F., Hansma, P. K., Carrion-Vazquez, M., and Fernandez, J. M. (2001) Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 98, 468-472
54. Linke, W. A., and Grützner, A. (2008) Pulling single molecules of titin by AFM - recent advances and physiological implications. Pflugers Arch. 456, 101-115
55. Fernandez, J. M., and Li, H. B. (2004) Force-clamp spectroscopy monitors the folding trajectory of a single protein. Science 303, 1674-1678
56. Schlierf, M., Li, H., and Fernandez, J. M. (2004) The unfolding kinetics of ubiquitin captured with single-molecule force-clamp techniques. Proc. Natl. Acad. Sci. U.S.A. 101, 7299-7304
57. Oesterhelt, F., Oesterhelt, D., Pfeiffer, M., Engel, A., Gaub, H. E., and Müller, D. J. (2000) Unfolding pathways of individual bacteriorhodopsins. Science 288, 143-146
58. Kedrov, A., Janovjak, H., Sapra, K. T., and Müller, D. J. (2007) Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy. Annu. Rev. Biophys. Biomol. Struct. 36, 233-260
59. Fisher, T. E., Marszalek, P. E., and Fernandez, J. M. (2000) Stretching single molecules into novel conformations using the atomic force microscope. Nat. Struct. Biol. 7, 719-724
60. Vinckier, A., Gervasoni, P., Zaugg, F., Ziegler, U., Lindner, P., Groscurth, P., Plückthun, A., and Semenza, G. (1998) Atomic force microscopy detects changes in the interaction forces between GroEL and substrate proteins. Biophys. J. 74, 3256-3263
61. Willemsen, O. H., Snel, M. M., Cambi, A., Greve, J., De Grooth, B. G., and Figdor, C. G. (2000) Biomolecular interactions measured by atomic force microscopy. Biophys. J. 79, 3267-3281
62. Senden, T. J., and Ducker, W. A. (1994) Experimental determination of spring constants in atomic force microscopy. Langmuir 10, 1003-1004
63. Clifford, C. A., and Seah, M. P. (2005) The determination of atomic force microscope cantilever spring constants via dimensional methods for nanomechanical analysis. Nanotechnology 16, 1666-1680
64. Chen, G. Y., Warmack, R. J., Thundat, T., Allison, D. P., and Huang, A. (1994) Resonance response of scanning force microscopy cantilevers. Rev. Sci. Instrum. 65, 2532-2537
65. Albrecht, T. R., Akamine, S., Carver, T. E., and Quate, C. F. (1990) Microfabrication of cantilever styli for the atomic force microscope. J. Vac. Sci. Technol. A 8, 3386-3396
66. Hutter, J. L., and Bechhoefer, J. (1993) Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868-1873
67. Sader, J. E., Larson, I., Mulvaney, P., and White, L. R. (1995) Method for the calibration of atomic force microscope cantilevers. Rev. Sci. Instrum. 66, 3789-3798
68. Sader, J. E., Chon, J. W., and Mulvaney, P. (1999) Calibration of rectangular atomic force microscope cantilevers. Rev. Sci. Instrum. 70, 3967-3969
69. Ogletree, D. F., Carpick, R. W., and Salmeron, M. (1996) Calibration of frictional forces in atomic force microscopy. Rev. Sci. Instrum. 67, 3298-3306
70. Staii, C., Wood, D. W., and Scoles, G. (2008) Verification of biochemical activity for proteins nanografted on gold surfaces. J. Am. Chem. Soc. 130, 640-646
71. Gladnikoff, M., Shimoni, E., Gov, N. S., and Rousso, I. (2009) Retroviral Assembly and Budding Occur through an Actin-Driven Mechanism. Biophys. J. 97, 2419-2428
72. Melcher, J., Carrasco, C., Xu, X., Carrascosa, J. L., Gómez-Herrero, J., Joséde Pablo, P., and Raman, A. (2009) Origins of phase contrast in the atomic force microscope in liquids. Proc. Natl. Acad. Sci. U.S.A. 106, 13655-13660
73. Magonov, S. N., Elings, V., and Whangbo, M. H. (1997) Phase imaging and stiffness in tapping-mode atomic force microscopy. Surf. Sci. 375, L385-L391
74. Worcester, D. L., Miller, R. G., and Bryant, P. J. (1988) Atomic force microscopy of purple membranes. J. Microsc. 152, 817-821
75. Lyubchenko, Y. L., Gall, A. A., Shlyakhtenko, L. S., Harrington, R. E., Jacobs, B. L., Oden, P. I., and Lindsay, S. M. (1992) Atomic force microscopy imaging of double-stranded DNA and RNA. J. Biomol. Struct. Dyn. 10, 589-606
76. Hansma, H. G., Bezanilla, M., Zenhausern, F., Adrian, M., and Sinsheimer, R. L. (1993) Atomic force microscopy of DNA in aqueous solutions. Nucleic Acids Res. 21, 505-512 (Pubitemid 23155538)
77. Müller, D. J., Janovjak, H., Lehto, T., Kuerschner, L., and Anderson, K. (2002) Observing structure, function and assembly of single proteins by AFM. Prog. Biophys. Mol. Biol. 79, 1-43
78. Kasas, S., Thomson, N. H., Smith, B. L., Hansma, P. K., Miklossy, J., and Hansma, H. G. (1997) Biological applications of the AFM: from single molecules to organs. Int. J. Imaging Syst. Technol. 8, 151-161
79. Drake, B., Prater, C. B., Weisenhorn, A. L., Gould, S. A., Albrecht, T. R., Quate, C. F., Cannell, D. S., Hansma, H. G., and Hansma, P. K. (1989) Imaging crystals, polymers, and processes in water with the atomic force microscope. Science 243, 1586-1589
80. Thundat, T., Zheng, X. Y., Sharp, S. L., Allison, D. P., Warmack, R. J., Joy, D. C., and Ferrell, T. L. (1992) Calibration of atomic force microscope tips using biomolecules. Scanning Microsc. 6, 903-910
81. Häberle, W., Hörber, J. K., Ohnesorge, F., Smith, D. P., and Binnig, G. (1992) In situ investigations of single living cells infected by viruses. Ultramicroscopy 42, 1161-1167
82. Kuznetsov, Y. G., Malkin, A. J., Lucas, R. W., Plomp, M., and McPherson, A. (2001) Imaging of viruses by atomic force microscopy. J. Gen. Virol. 82, 2025-2034
83. Allen, M. J., Hud, N. V., Balooch, M., Tench, R. J., Siekhaus, W. J., and Balhorn, R. (1992) Tip-radius-induced artifacts in AFM images of protamine-complexed DNA fibers. Ultramicroscopy 42, 1095-1100
84. Prasad, B. V., Rothnagel, R., Jiang, X., and Estes, M. K. (1994) 3-Dimensional structure of Baculovirus-expressed Norwalk virus capsids. J. Virol. 68, 5117-5125
85. Prasad, B. V., Hardy, M. E., Dokland, T., Bella, J., Rossmann, M. G., and Estes, M. K. (1999) X-ray crystallographic structure of the Norwalk virus capsid. Science 286, 287-290
86. Shoemaker, G. K., van Duijn, E., Crawford, S. E., Uetrecht, C., Baclayon, M., Roos, W. H., Wuite, G. J., Estes, M. K., Prasad, B. V., and Heck, A. J. (April 22, 2010) Norwalk virus assembly and stability monitored by mass spectrometry. Mol. Cell. Proteomics 10.1074/mcp.M900620-MCP200
87. Valle, M., Valpuesta, J. M., Carrascosa, J. L., Tamayo, J., and Garcia, R. (1996) The interaction of DNA with bacteriophage phi 29 connector: a study by AFM and TEM. J. Struct. Biol. 116, 390-398
88. Müller, D. J., Engel, A., Carrascosa, J. L., and Vélez, M. (1997) The bacteriophage phi 29 head-tail connector imaged at high resolution with the atomic force microscope in buffer solution. EMBO J. 16, 2547-2553
89. Roos, W. H., Radtke, K., Kniesmeijer, E., Geertsema, H., Sodeik, B., and Wuite, G. J. L. (2009) Scaffold expulsion and genome packaging trigger stabilization of herpes simplex virus capsids. Proc. Natl. Acad. Sci. U.S.A. 106, 9673-9678
90. Gladnikoff, M., and Rousso, I. (2008) Directly monitoring individual retrovirus budding events using atomic force microscopy. Biophys. J. 94, 320-326
91. Ohnesorge, F. M., Hörber, J. K., Häberle, W., Czerny, C. P., Smith, D. P., and Binnig, G. (1997) AFM review study on pox viruses and living cells. Biophys. J. 73, 2183-2194
92. Kolbe, W. F., Ogletree, D. F., and Salmeron, M. B. (1992) Atomic force microscopy imaging of T4 bacteriophages on silicon substrates. Ultramicroscopy 42, 1113-1117
93. Kuznetsov, Y. G., Daijogo, S., Zhou, J., Semler, B. L., and McPherson, A. (2005) Atomic force microscopy analysis of icosahedral virus RNA. J. Mol. Biol. 347, 41-52
94. Kienberger, F., Zhu, R., Moser, R., Blaas, D., and Hinterdorfer, P. (2004) Monitoring RNA release from human rhinovirus by dynamic force microscopy. J. Virol. 78, 3203-3209
95. Müller, D. J., Sapra, K. T., Scheuring, S., Kedrov, A., Frederix, P. L., Fotiadis, D., and Engel, A. (2006) Single-molecule studies of membrane proteins. Curr. Opin. Struct. Biol. 16, 489-495
96. Engel, A., and Gaub, H. E. (2008) Structure and mechanics of membrane proteins. Annu. Rev. Biochem. 77, 127-148
97. Butt, H. J., Downing, K. H., and Hansma, P. K. (1990) Imaging the membrane-protein bacteriorhodopsin with the atomic force microscope. Biophys. J. 58, 1473-1480
98. Scheuring, S., Seguin, J., Marco, S., Lévy, D., Robert, B., and Rigaud, J. L. (2003) Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM. Proc. Natl. Acad. Sci. U.S.A. 100, 1690-1693
99. Moukhtar, J., Fontaine, E., Faivre-Moskalenko, C., and Arneodo, A. (2007) Probing persistence in DNA curvature properties with atomic force microscopy. Phys. Rev. Lett. 98, 178101
100. Lyubchenko, Y. L., and Shlyakhtenko, L. S. (1997) Visualization of supercoiled DNA with atomic force microscopy in situ. Proc. Natl. Acad. Sci. U.S.A. 94, 496-501
101. Hansma, H. G., Kim, K. J., Laney, D. E., Garcia, R. A., Argaman, M., Allen, M. J., and Parsons, S. M. (1997) Properties of biomolecules measured from atomic force microscope images: a review. J. Struct. Biol. 119, 99-108
102. Hansma, H. G., Vesenka, J., Siegerist, C., Kelderman, G., Morrett, H., Sinsheimer, R. L., Elings, V., Bustamante, C., and Hansma, P. K. (1992) Reproducible imaging and dissection of plasmid DNA under liquid with the atomic force microscope. Science 256, 1180-1184
103. Dufrêne, Y. F., and Lee, G. U. (2000) Advances in the characterization of supported lipid films with the atomic force microscope. Biochim. Biophys. Acta 1509, 14-41
104. Domke, J., Dannöhl, S., Parak, W. J., Müller, O., Aicher, W. K., and Radmacher, M. (2000) Substrate dependent differences in morphology and elasticity of living osteoblasts investigated by atomic force microscopy. Colloids Surf. B Biointerfaces 19, 367-379
105. Kroeze, R. J., Helder, M. N., Roos, W. H., Wuite, G. J., Bank, R. A., and Smit, T. H. (2010) The effect of ethylene oxide, glow discharge and electron beam on the surface characteristics of poly(L-lactide-co-caprolactone) and the corresponding cellular response of adipose stem cells. Acta Biomater. 6, 2060-2065
106. Bonomini, M., Pavone, B., Sirolli, V., Del Buono, F., Di Cesare, M., Del Boccio, P., Amoroso, L., Di Ilio, C., Sacchetta, P., Federici, G., and Urbani, A. (2006) Proteomics characterization of protein adsorption onto hemodialysis membranes. J. Proteome Res. 5, 2666-2674
107. Thomson, N. H., Fritz, M., Radmacher, M., Cleveland, J. P., Schmidt, C. F., and Hansma, P. K. (1996) Protein tracking and detection of protein motion using atomic force microscopy. Biophys. J. 70, 2421-2431
108. Müller, D. J., Engel, A., Matthey, U., Meier, T., Dimroth, P., and Suda, K. (2003) Observing membrane protein diffusion at subnanometer resolution. J. Mol. Biol. 327, 925-930
109. Viani, M. B., Pietrasanta, L. I., Thompson, J. B., Chand, A., Gebeshuber, I. C., Kindt, J. H., Richter, M., Hansma, H. G., and Hansma, P. K. (2000) Probing protein-protein interactions in real time. Nat. Struct. Biol. 7, 644-647
110. Yokokawa, M., Wada, C., Ando, T., Sakai, N., Yagi, A., Yoshimura, S. H., and Takeyasu, K. (2006) Fast-scanning atomic force microscopy reveals the ATP/ADP-dependent conformational changes of GroEL. EMBO J. 25, 4567-4576 (Pubitemid 44498130)
111. Thomson, N. H., Kasas, S., Riederer, B. M., Catsicas, S., Dietler, G., Kulik, A. J., and Forró, L. (2003) Large fluctuations in the disassembly rate of microtubules revealed by atomic force microscopy. Ultramicroscopy 97, 239-247
112. Guthold, M., Zhu, X., Rivetti, C., Yang, G., Thomson, N. H., Kasas, S., Hansma, H. G., Smith, B., Hansma, P. K., and Bustamante, C. (1999) Direct observation of one-dimensional diffusion and transcription by Escherichia coli RNA polymerase. Biophys. J. 77, 2284-2294
113. Kasas, S., Thomson, N. H., Smith, B. L., Hansma, H. G., Zhu, X., Guthold, M., Bustamante, C., Kool, E. T., Kashlev, M., and Hansma, P. K. (1997) Escherichia coli RNA polymerase activity observed using atomic force microscopy. Biochemistry 36, 461-468
114. Puchner, E. M., and Gaub, H. E. (2009) Force and function: probing proteins with AFM-based force spectroscopy. Curr. Opin. Struct. Biol. 19, 605-614
115. Rotsch, C., Jacobson, K., and Radmacher, M. (1999) Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 96, 921-926
116. Mahaffy, R. E., Shih, C. K., MacKintosh, F. C., and Käs, J. (2000) Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys. Rev. Lett. 85, 880-883
117. Li, Q. S., Lee, G. Y., Ong, C. N., and Lim, C. T. (2008) AFM indentation study of breast cancer cells. Biochem. Biophys. Res. Commun. 374, 609-613
118. Radmacher, M., Fritz, M., Kacher, C. M., Cleveland, J. P., and Hansma, P. K. (1996) Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys. J. 70, 556-567
119. Vinckier, A., Dumortier, C., Engelborghs, Y., and Hellemans, L. (1996) Dynamical and mechanical study of immobilized microtubules with atomic force microscopy. J. Vac. Sci. Technol. B Microelectron. Nanometer Struct. Process. Meas. Phenom. 14, 1427-1431
120. Kis, A., Kasas, S., Babiæ, B., Kulik, A. J., Benoît, W., Briggs, G. A., Schönenberger, C., Catsicas, S., and Forró, L. (2002) Nanomechanics of microtubules. Phys. Rev. Lett. 89, 248101
121. Ivanovska, I. L., de Pablo, P. J., Ibarra, B., Sgalari, G., MacKintosh, F. C., Carrascosa, J. L., Schmidt, C. F., and Wuite, G. J. L. (2004) Bacteriophage capsids: tough nanoshells with complex elastic properties. Proc. Natl. Acad. Sci. U.S.A. 101, 7600-7605
122. Radmacher, M., Fritz, M., Cleveland, J. P., Walters, D. A., and Hansma, P. K. (1994) Imaging adhesion forces and elasticity of lysozyme adsorbed on mica with the atomic-force microscope. Langmuir 10, 3809-3814
123. Ikai, A., Afrin, R., and Sekiguchi, H. (2007) Pulling and pushing protein molecules by AFM. Curr. Nanosci. 3, 17-29
124. Florin, E. L., Moy, V. T., and Gaub, H. E. (1994) Adhesion forces between individual ligand-receptor pairs. Science 264, 415-417
125. Merkel, R., Nassoy, P., Leung, A., Ritchie, K., and Evans, E. (1999) Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397, 50-53
126. Lee, G. U., Kidwell, D. A., and Colton, R. J. (1994) Sensing discrete streptavidin biotin interactions with atomic-force microscopy. Langmuir 10, 354-357
127. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M., and Gaub, H. E. (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109-1112
128. Fotiadis, D., Scheuring, S., Müller, S. A., Engel, A., and Müller, D. J. (2002) Imaging and manipulation of biological structures with the AFM. Micron 33, 385-397
129. Lee, G. U., Chrisey, L. A., and Colton, R. J. (1994) Direct measurement of the forces between complementary strands of DNA. Science 266, 771-773
130. Colton, R. J. (2004) Nanoscale measurements and manipulation. J. Vac. Sci. Technol. B Microelectron. Nanometer Struct. Process. Meas. Phenom. 22, 1609-1635
131. Costa, K. D., and Yin, F. C. (1999) Analysis of indentation: implications for measuring mechanical properties with atomic force microscopy. J. Biomech. Eng. 121, 462-471
132. Roos, W. H., Ivanovska, I. L., Evilevitch, A., and Wuite, G. J. L. (2007) Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell. Mol. Life Sci. 64, 1484-1497
133. Gelbart, W. M., and Knobler, C. M. (2009) Pressurized viruses. Science 323, 1682-1683
134. Arkhipov, A., Roos, W. H., Wuite, G. J., and Schulten, K. (2009) Elucidating the mechanism behind irreversible deformation of viral capsids. Biophys. J. 97, 2061-2069
135. Uetrecht, C., Versluis, C., Watts, N. R., Roos, W. H., Wuite, G. J., Wingfield, P. T., Steven, A. C., and Heck, A. J. R. (2008) High-resolution mass spectrometry of viral assemblies: molecular composition and stability of dimorphic hepatitis B virus capsids. Proc. Natl. Acad. Sci. U.S.A. 105, 9216-9220
136. Michel, J. P., Ivanovska, I. L., Gibbons, M. M., Klug, W. S., Knobler, C. M., Wuite, G. J., and Schmidt, C. F. (2006) Nanoindentation studies of full and empty viral capsids and the effects of capsid protein mutations on elasticity and strength. Proc. Natl. Acad. Sci. U.S.A. 103, 6184-6189
137. Ivanovska, I., Wuite, G., Jönsson, B., and Evilevitch, A. (2007) Internal DNA pressure modifies stability of WT phage. Proc. Natl. Acad. Sci. U.S.A. 104, 9603-9608
138. Carrasco, C., Carreira, A., Schaap, I. A., Serena, P. A., Gómez-Herrero, J., Mateu, M. G., and de Pablo, P. J. (2006) DNA-mediated anisotropic mechanical reinforcement of a virus. Proc. Natl. Acad. Sci. U.S.A. 103, 13706-13711
139. Liashkovich, I., Hafezi, W., Kühn, J. E., Oberleithner, H., Kramer, A., and Shahin, V. (2008) Exceptional mechanical and structural stability of HSV-1 unveiled with fluid atomic force microscopy. J. Cell Sci. 121, 2287-2292
140. Gibbons, M. M., and Klug, W. S. (2007) Mechanical modeling of viral capsids. J. Mater. Sci. 42, 8995-9004
141. Buenemann, M., and Lenz, P. (2007) Mechanical limits of viral capsids. Proc. Natl. Acad. Sci. U.S.A. 104, 9925-9930
142. Klug, W. S., Bruinsma, R. F., Michel, J. P., Knobler, C. M., Ivanovska, I. L., Schmidt, C. F., and Wuite, G. J. (2006) Failure of viral shells. Phys. Rev. Lett. 97, 228101
143. Gibbons, M. M., and Klug, W. S. (2008) Influence of nonuniform geometry on nanoindentation of viral capsids. Biophys. J. 95, 3640-3649
144. Roos, W. H., Gibbons, M. M., Arkhipov, A., Uetrecht, C., Watts, N. R., Wingfield, P. T., Steven, A. C., Heck, A. J., Schulten, K., Klug, W. S., and Wuite, G. J. (2010) Squeezing protein shells: how continuum elastic models, molecular dynamics simulations and experiments coalesce at the nanoscale. Biophys. J., doi: 10.1016/j.bpj.2010.05.033
145. Kol, N., Gladnikoff, M., Barlam, D., Shneck, R. Z., Rein, A., and Rousso, I. (2006) Mechanical properties of murine leukemia virus particles: effect of maturation. Biophys. J. 91, 767-774
146. Kol, N., Shi, Y., Tsvitov, M., Barlam, D., Shneck, R. Z., Kay, M. S., and Rousso, I. (2007) A stiffness switch in human immunodeficiency virus. Biophys. J. 92, 1777-1783
147. Zhao, Y., Ge, Z., and Fang, J. (2008) Elastic modulus of viral nanotubes. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 78, 031914
148. Munson, K. M., Mulugeta, P. G., and Donhauser, Z. J. (2007) Enhanced mechanical stability of microtubules polymerized with a slowly hydrolyzable nucleotide analogue. J. Phys. Chem. B 111, 5053-5057
149. Schaap, I. A., Hoffmann, B., Carrasco, C., Merkel, R., and Schmidt, C. F. (2007) Tau protein binding forms a 1 nmthick layer along protofilaments without affecting the radial elasticity of microtubules. J. Struct. Biol. 158, 282-292
150. Kasas, S., Kis, A., Riederer, B. M., Forró, L., Dietler, G., and Catsicas, S. (2004) Mechanical properties of microtubules explored using the finite elements method. ChemPhysChem 5, 252-257
151. Guzmán, C., Jeney, S., Kreplak, L., Kasas, S., Kulik, A. J., Aebi, U., and Forró, L. (2006) Exploring the mechanical properties of single vimentin intermediate filaments by atomic force microscopy. J. Mol. Biol. 360, 623-630
152. Koenders, M. M., Yang, L., Wismans, R. G., van der Werf, K. O., Reinhardt, D. P., Daamen, W., Bennink, M. L., Dijkstra, P. J., van Kuppevelt, T. H., and Feijen, J. (2009) Microscale mechanical properties of single elastic fibers: the role of fibrillin-microfibrils. Biomaterials 30, 2425-2432
153. Yang, L., van der Werf, K. O., Koopman, B. F., Subramaniam, V., Bennink, M. L., Dijkstra, P. J., and Feijen, J. (2007) Micromechanical bending of single collagen fibrils using atomic force microscopy. J. Biomed. Mater. Res. A 82, 160-168
154. Yang, L., van der Werf, K. O., Fitié, C. F., Bennink, M. L., Dijkstra, P. J., and Feijen, J. (2008) Mechanical properties of native and cross-linked type I collagen fibrils. Biophys. J. 94, 2204-2211
155. Schaap, I. A., Carrasco, C., de Pablo, P. J., MacKintosh, F. C., and Schmidt, C. F. (2006) Elastic response, buckling, and instability of microtubules under radial indentation. Biophys. J. 91, 1521-1531
156. Sept, D., and MacKintosh, F. C. (2010) Microtubule elasticity: connecting all-atom simulations with continuum mechanics. Phys. Rev. Lett. 104, 018101
157. Afrin, R., Alam, M. T., and Ikai, A. (2005) Pretransition and progressive softening of bovine carbonic anhydrase II as probed by single molecule atomic force microscopy. Protein Sci. 14, 1447-1457
158. Kodama, T., Ohtani, H., Arakawa, H., and Ikai, A. (2005) Mechanical perturbation-induced fluorescence change of green fluorescent protein. Appl. Phys. Lett. 86, 043901
159. Kodama, T., Ohtani, H., Arakawa, H., and Ikai, A. (2005) Observation of the destruction of biomolecules under compression force. Ultramicroscopy 105, 189-195
160. Lin, S., Chen, J. L., Huang, L. S., and Lin, H. W. (2005) Measurements of the forces in protein interactions with atomic force microscopy. Curr. Proteomics 2, 55-81
161. Browning-Kelley, M. E., Wadu-Mesthrige, K., Hari, V., and Liu, G. Y. (1997) Atomic force microscopic study of specific antigen/antibody binding. Langmuir 13, 343-350
162. Moy, V. T., Florin, E. L., and Gaub, H. E. (1994) Intermolecular forces and energies between ligands and receptors. Science 266, 257-259
163. Grubmüller, H., Heymann, B., and Tavan, P. (1996) Ligand binding: molecular mechanics calculation of the streptavidin biotin rupture force. Science 271, 997-999
164. Izrailev, S., Stepaniants, S., Balsera, M., Oono, Y., and Schulten, K. (1997) Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72, 1568-1581
165. Evans, E., and Ritchie, K. (1997) Dynamic strength of molecular adhesion bonds. Biophys. J. 72, 1541-1555
166. Willemsen, O. H., Snel, M. M., van der Werf, K. O., de Grooth, B. G., Greve, J., Hinterdorfer, P., Gruber, H. J., Schindler, H., van Kooyk, Y., and Figdor, C. G. (1998) Simultaneous height and adhesion imaging of antibody-antigen interactions by atomic force microscopy. Biophys. J. 75, 2220-2228
167. Nakajima, H., Kunioka, Y., Nakano, K., Shimizu, K., Seto, M., and Ando, T. (1997) Scanning force microscopy of the interaction events between a single molecule of heavy meromyosin and actin. Biochem. Biophys. Res. Commun. 234, 178-182
168. Puchner, E. M., Alexandrovich, A., Kho, A. L., Hensen, U., Schäfer, L. V., Brandmeier, B., Gräter, F., Grubmüller, H., Gaub, H. E., and Gautel, M. (2008) Mechanoenzymatics of titin kinase. Proc. Natl. Acad. Sci. U.S.A. 105, 13385-13390
169. Perez-Jimenez, R., Garcia-Manyes, S., Ainavarapu, S. R., and Fernandez, J. M. (2006) Mechanical unfolding pathways of the enhanced yellow fluorescent protein revealed by single molecule force spectroscopy. J. Biol. Chem. 281, 40010-40014
170. Dietz, H., and Rief, M. (2004) Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc. Natl. Acad. Sci. U.S.A. 101, 16192-16197
171. Bornschlögl, T., Woehlke, G., and Rief, M. (2009) Single molecule mechanics of the kinesin neck. Proc. Natl. Acad. Sci. U.S.A. 106, 6992-6997
172. Lu, H., Isralewitz, B., Krammer, A., Vogel, V., and Schulten, K. (1998) Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75, 662-671
173. Marszalek, P. E., Lu, H., Li, H., Carrion-Vazquez, M., Oberhauser, A. F., Schulten, K., and Fernandez, J. M. (1999) Mechanical unfolding intermediates in titin modules. Nature 402, 100-103
174. Gräter, F., Shen, J., Jiang, H., Gautel, M., and Grubmüller, H. (2005) Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88, 790-804
175. Hisatomi, Y., Katagiri, D., Neya, S., Hara, M., and Hoshino, T. (2008) Analysis of the unfolding process of green fluorescent protein by molecular dynamics simulation. J. Phys. Chem. B 112, 8672-8680