Introduction to Atomic Force Microscopy (AFM) in Biology
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Abstract
The atomic force microscope (AFM) has the unique capability of imaging biological samples with molecular resolution in buffer solution. In addition to providing topographical images of surfaces with nanometer? to angstrom?scale resolution, forces between single molecules and mechanical properties of biological samples can be investigated from the nanoscale to the microscale. Importantly, the measurements are made in buffer solutions, allowing biological samples to ?stay alive? within a physiological?like environment while temporal changes in structure are measured?e.g., before and after addition of chemical reagents. These qualities distinguish AFM from conventional imaging techniques of comparable resolution, e.g., electron microscopy (EM). This unit provides an introduction to AFM on biological systems and describes specific examples of AFM on proteins, cells, and tissues. The physical principles of the technique and methodological aspects of its practical use and applications are also described. Curr. Protoc. Protein Sci. 58:17.7.1?17.7.19. © 2009 by John Wiley & Sons, Inc.
Keywords: topography; force spectroscopy; manipulation; fluorescence microscopy
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PDF or HTML at Wiley Online LibraryTable of Contents
- Introduction
- Experimental Setup
- Applications
- Image Interpretation: Troubleshooting and Instrumental Effects
- Summary
- Acknowledgements
- Literature Cited
- Figures
- Tables
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Figure 17.7.1 Scheme showing how AFM produces images of surfaces. (A ) The sample surface is scanned with a fine tip. The interaction force between the tip and the surface causes the cantilever to bend. (B ) The sample is mounted in the AFM under a transparent cantilever holder (fluid cell). A laser beam is focused on the end of the cantilever. The deflection of the laser spot, induced by the bending of the cantilever, is measured by a photodiode detector and a feedback loop corrects the vertical distance by adjusting the piezo position. (C ) The AFM thereby produces a topographical image of the sample (surface of “constant force”). This figure was obtained from the M.E.Mueller‐Institute for Structural Biology, Basel, Switzerland, publication “Imaging, measuring and manipulating native biomolecular systems with the atomic force microscope” prepared by Daniel J. Müller, Ueli Aebi, and Andreas Engel. View Image -
Figure 17.7.2 Force versus distance curve. The deflection ( y ‐axis) of the free end of the cantilever is measured as the fixed end of the cantilever is brought vertically towards and then away from the sample surface. (1 ) The tip is initially not touching the surface—no cantilever deflection occurs. (2 ) As the tip approaches the surface, attractive forces cause it to “jump” into contact with the sample (note: this adhesive force is less pronounced when acquiring images under physiological conditions, i.e., in liquid, as compared to air). (3 ) Cantilever deflection becomes maximal when the tip is in contact with the sample (relates linearly to further approach to the sample as the tip is already in contact). If the tip indents the surface, elasticity forces related to the sample can be measured from the force curve. (4 ) As the tip retracts from the sample, adhesion or specific receptor‐ligand binding forces can cause the cantilever to stay attached to the sample some distance past the original point of contact. The point on the force curve where the tip eventually jumps off the surface can thus provide information about bond rupturing forces. Adapted from Digital Instruments. View Image -
Figure 17.7.3 (A ) Substrate with five cantilevers attached. (B ) Integration of a fine tip on the end of a cantilever. Images are from Veeco Probes: https://www.veecoprobes.com. View Image -
Figure 17.7.4 Adsorption density of purple membrane to mica as a function of the electrolyte concentration. Two micrograms of protein was incubated for 5 min at room temperature on 6‐mm‐diameter supports in buffer containing different amounts of (A ) monovalent or (B ) divalent ions. Adapted from Müller et al. (). View Image -
Figure 17.7.5 Force‐distance curves recorded on the extracellular surface of purple membrane. Force‐distance curves were recorded during the approach of sample and AFM tip under different electrolyte concentrations at constant pH (7.6). The dotted lines represent force‐distance curves recorded on purple membrane without electrostatic repulsion. Conditions: scan frequency: 1.97 Hz, scan range: 50 nm (512 pixels). Arrows (1 ) mark the onset of measurable electrostatic repulsion, whereas arrows (2 ) indicate the point of contact between tip and sample. Adapted from Müller et al. (). View Image -
Figure 17.7.6 High‐resolution topograph of a two‐dimensional crystal of the membrane protein aquaporin Z (AqpZ) using contact‐mode AFM recorded in buffer solution. Adapted from Scheuring et al. (). View Image -
Figure 17.7.7 Time‐lapse imaging: watching proteins at work. (A ) Movement of a single DNA molecule through an RNA polymerase complex (adapted from Kasas et al., ). (B ) Structural change induced in the nuclear basket of individual native nuclear pore complexes (NPCs) with addition of calcium ions. The same specimen area was imaged in two distinct conformational states. Three corresponding NPCs are marked by arrowheads. For a more quantitative comparison of the “closed” and “open” states, 30 corresponding NPCs were aligned and averaged, and their average radial height profiles computed. Scale bar, 100 nm (adapted from Stolz et al., ), (C ) Growth of an individual Aβ amyloid fibril adhering to a mica support (Goldsbury et al., ). View Image -
Figure 17.7.8 Image before (A ) and after (B ) unzipping of a full hexameric core of the Corynebacterium glutamicum S‐layer. (C ) Force‐distance curve corresponding to the change of the surface structure as shown in (A) and (B). The hexameric core is unzipped in a sequence of three dimer‐like rupture events (Scheuring et al., ,b). View Image -
Figure 17.7.9 (A ) Images after nanomanipulation of single desmin intermediate filaments. (B ) Typical lateral force versus displacement curve recorded during one nanomanipulation (adapted from Kreplak et al., ). View Image
Videos
Literature Cited
| 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 42‐44:1095‐1100. | |
| Allen, S., Davies, J., Dawkes, A.C., Davies, M.C., Edwards, J.C., Parker, M.C., Roberts, C.J., Sefton, J., Tendler, S.J.B., and Williams, P.M. 1996. In situ observation of streptavidin‐biotin binding on an immunoassay well surface using an atomic force microscope. FEBS Lett. 390:161‐164. | |
| Allison, D.P., Hinterdorfer, P., and Han, W. 2002. Biomolecular force measurements and the atomic force microscope. Curr. Opin. Biotechnol. 13:47‐51. | |
| Binnig, G., Quate, C.F., and Gerber, C. 1986. Atomic force microscope. Phys. Rev. Lett. 56:930‐933. | |
| Bustamante, C., Rivetti, C., and Keller, D.J. 1997. Scanning force microscopy under aqueous solutions. Curr. Opin. Struct. Biol. 7:709‐716. | |
| Bustamante, C., Guthold, M., Zhu, X., and Yang, G. 1999. Facilitated target location on DNA by individual Escherichia coli RNA polymerase molecules observed with the scanning force microscope operating in liquid. J. Biol. Chem. 274:16665‐16668. | |
| Carrion‐Vazquez, M., Oberhauser, A.F., Fowler, S.B., Marszalek, P.E., Broedel, S.E., Clarke, J., and Fernandez, J.M. 1999. Mechanical and chemical unfolding of a single protein: A comparison. Proc. Natl. Acad. Sci. U.S.A. 96:3694‐3699. | |
| Chen, C.H., Clegg, D.O., and Hansma, H.G. 1998. Structures and dynamic motion of laminin‐1 as observed by atomic force microscopy. Biochemistry 37:8262‐8267. | |
| 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. | |
| Czajkowsky, D.M. and Shao, Z. 1998. Submolecular resolution of single macromolecules with atomic force microscopy. FEBS Lett. 430:51‐54. | |
| Czajkowsky, D.M., Iwamoto, H., Cover, T.L., and Shao, Z. 1999. The vacuolating toxin from Helicobacter pylori forms hexameric pores in lipid bilayers at low pH. Proc. Natl. Acad. Sci. U.S.A. 96:2001‐2006. | |
| Clausen‐Schaumann, H., Seitz, M., Krautbauer, R., and Gaub, H.E. 2000. Force spectroscopy with single bio‐molecules. Curr. Opin. Chem. Biol. 4:524‐530. | |
| Dammer, U., Hegner, M., Anselmetti, D., Wagner, P., Dreier, M., Huber, W., and Guntherodt, H.J. 1996. Specific antigen/antibody interactions measured by force microscopy. Biophys. J. 70:2437‐2441. | |
| Domke, J., Parak, W.J., George, M., Gaub, H.E., and Radmacher, M. 1999. Mapping the mechanical pulse of single cardiomyocytes with the atomic force microscope. Eur. Biophys. J. 28:179‐186. | |
| Dorn, I.T., Eschrich, R., Seemuller, E., Guckenberger, R., and Tampe, R. 1999. High‐resolution AFM‐imaging and mechanistic analysis of the 20 S proteasome. J. Mol. Biol. 288:1027‐1036. | |
| Dorobantu, L.S., Bhattacharjee, S., Foght, J.M., and Gray, M.R. 2008. Atomic force microscopy measurement of heterogeneity in bacterial surface hydrophobicity. Langmuir 24:4944‐4951. | |
| Efimov, A.E., Tonevitsky, A.G., Dittrich, M., and Matsko, N.B. 2007. Atomic force microscope (AFM) combined with the ultramicrotome: A novel device for the serial section tomography and AFM/TEM complementary structural analysis of biological and polymer samples. J. Microsc. 226:207‐217. | |
| Engel, A. and Müller, D.J. 2000. Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7:715‐718. | |
| Engel, A., Gaub, H.E., and Müller, D.J. 1999. Atomic force microscopy: A forceful way with single molecules. Curr. Biol. 9:R133‐R136. | |
| Falvo, M.R., Taylor, R.M., Helser, A., Chi, V., Brooks, F.P., Washburn, S., and Superfine, R. 1999. Nanometre‐scale rolling of carbon nanotubes. Nature 397:236‐238. | |
| Fisher, T.E., Marszalek, P.E., Oberhauser, A.F., Carrion‐Vazquez, M., and Fernandez, J.M. 1999a. The micro‐mechanics of single molecules studied with atomic force microscopy. J. Physiol. (Lond). 520:5‐14. | |
| Fisher, T.E., Oberhauser, A.F., Carrion‐Vazquez, M., Marszalek, P.E., and Fernandez, J.M. 1999b. The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24:379‐384. | |
| 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. | |
| Florin, E.‐L., Moy, V.T., and Gaub, H.E. 1994. Adhesion forces between individual ligand‐receptor pairs. Science 264:415‐417. | |
| Fotiadis, D., Müller, D.J., Tsiotis, G., Hasler, L., Tittmann, P., Mini, T., Jeno, P., Gross, H., and Engel, A. 1998. Surface analysis of the photosystem I complex by electron and atomic force microscopy. J. Mol. Biol. 283:83‐94. | |
| Fotiadis, D., Hasler, L., Müller, D.J., Stahlberg, H., Kistler, J., and Engel, A. 2000. Surface tongue‐and‐groove contours on lens MIP facilitate cell‐to‐cell adherence. J. Mol. Biol. 300:779‐789. | |
| Fritz, J., Katopodis, A.G., Kolbinger, F., and Anselmetti, D. 1998. Force‐mediated kinetics of single P‐selectin/ligand complexes observed by atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 95:12283‐12288. | |
| Fritz, J., Baller, M.K., Lang, H.P., Rothuizen, H., Vettiger, P., Meyer, E., Guntherodt, H.‐J., Gerber, C., and Gimzewski, J.K. 2000. Translating biomolecular recognition into nanomechanics. Science 288:316‐318. | |
| Goldsbury, C., Kistler, J., Aebi, U., Arvinte, T., and Cooper, G.J. 1999. Watching amyloid fibrils grow by time‐lapse atomic force microscopy. J. Mol. Biol. 285:33‐39. | |
| Goldsbury, C., Aebi, U., and Frey, P. 2001. Visualizing the growth of Alzheimer's β amyloid‐like fibrils. Trends Mol. Med. 7:582. | |
| Green, J.D., Kreplak, L., Goldsbury, C., Li‐Blatter, X., Stolz, M., Cooper, G.S., Seelig, A., Kistler, J., and Aebi, U. 2004. Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide. J. Mol. Biol. 342:877‐887. | |
| 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. | |
| Heinz, W.F. and Hoh, J.H. 1999. Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope. Trends Biotechnol. 17:143‐150. | |
| Hofmann, U.G., Rotsch, C., Parak, W.J., and Radmacher, M. 1997. Investigating the cytoskeleton of chicken cardiocytes with the atomic force microscope. J. Struct. Biol. 119:84‐91. | |
| Hoh, J.H. and Schoenenberger, C.A. 1994. Surface morphology and mechanical properties of MDCK monolayers by atomic force microscopy. J. Cell Sci. 107:1105‐1114. | |
| Horber, J.K., Mosbacher, J., Haberle, W., Ruppersberg, J.P., and Sakmann, B. 1995. A look at membrane patches with a scanning force microscope. Biophys. J. 68:1687‐1693. | |
| Hutter, J.L. and Bechhoefer, J. 1993. Calibration of atomic force microscope tips. Rev. Sci. Instr. 64:1868‐1873. | |
| Ilic, B., Czaplewski, D., Craighead, H.G., Neuzil, P., Campagnolo, C., and Batt, C. 2000. Mechanical resonant immunospecific biological detector. Appl. Phys. Lett. 77:450‐452. | |
| Karrasch, S., Dolder, M., Schabert, F., Ramsden, J., and Engel, A. 1993. Covalent binding of biological samples to solid supports for scanning probe microscopy in buffer solution. Biophys. J. 65:2437‐2446. | |
| Karrasch, S., Hegerl, R., Hoh, J., Baumeister, W., and Engel, A. 1994. Atomic force microscopy produces faithful high‐resolution images of protein surfaces in an aqueous environment. Proc. Natl. Acad. Sci. U.S.A. 91:836‐838. | |
| 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. | |
| Kreplak, L., Wang, H., Aebi, U., and Kong, X.P. 2007. Atomic force microscopy of mammalian urothelial surface. J. Mol. Biol. 374:365‐373. | |
| Kreplak, L., Herrmann, H., and Aebi, U. 2008. Tensile properties of single desmin intermediate filaments. Biophys. J. 94:2790‐2799. | |
| Lal, R. and John, S.A. 1994. Biological applications of atomic force microscopy. Am. J. Physiol. 266:C1‐C21. | |
| Lamontagne, C‐A., Cuerrier, C.M., and Grandbois, M. 2008. AFM as a tool to probe and manipulate cellular processes. Pflugers Arch. 456:61‐70. | |
| Lee, K.‐B., Park, S.‐J., Mirkin, C., Smith, J., and Mrksich, M. 2002. Protein nanoarrays generated by dip‐pen nanolithography. Science 295:1702‐1705. | |
| Levadny, V.G., Belaya, M.L., Pink, D.A., and Jericho, M.H. 1996. Theory of electrostatic effects in soft biological interfaces using atomic force microscopy. Biophys. J. 70:1745‐1752. | |
| Ludwig, T., Kirmse, R., Poole, K., and Schwarz, U.S. 2008. Probing cellular microenvironments and tissue remodeling by atomic force microscopy. Pflugers Arch. 456:29‐49. | |
| Markiewicz, P. 1988. Orientational dependency of AFM images revealed by Alzheimer paired helical filaments. Ph.D. thesis. Department of Chemistry, University of Toronto. | |
| McPherson, A., Malkin, A.J., and Kuznetsov, Y.G. 2000. Atomic force microscopy in the study of macromolecular crystal growth. Annu. Rev. Biophys. Biomol. Struct. 29:361‐410. | |
| McPherson, A., Malkin, A.J., Kuznetsov, Y.G., and Plomp, M. 2001. Atomic force microscopy applications in macromolecular crystallography. Acta Crystallogr. D. Biol. Crystallogr. 57:1053‐1060. | |
| Mitsui, K., Hara, M., and Ikai, A. 1996. Mechanical unfolding of alpha(2)‐macroglobulin molecules with atomic force microscope. FEBS Lett. 385:29‐33. | |
| Möller, C., Allen, M., Elings, V., Engel, A., and Müller, D.J. 1999. Tapping‐mode atomic force microscopy produces faithful high‐resolution images of protein surfaces. Biophys. J. 77:1150‐1158. | |
| Mou, J.X., Yang, J., and Shao, Z.F. 1995. Atomic force microscopy of cholera toxin B‐oligomers bound to bilayers of biologically relevant lipids. J. Mol. Biol. 248:507‐512. | |
| Mou, J., Sheng, S., Ho, R., and Shao, Z. 1996a. Chaperonins GroEL and GroES: Views from atomic force microscopy. Biophys. J. 71:2213‐2221. | |
| Mou, J., Czajkowsky, D.M., Sheng, S., Ho, R., and Shao, Z. 1996b. High resolution surface structure of E. coli GroES oligomer by atomic force microscopy. FEBS Lett. 381:161‐164. | |
| Mucke, N., Kreplak, L., Kirmse, R., Wedig, T., Herrmann, H., Aebi, U. and Langowski, J. 2004. Assessing the flexibility of intermediate filaments with atomic force microscopy. J. Mol. Biol. 335:1241‐1250. | |
| Müller, D.J. and Engel, A. 1997. The height of biomolecules measured with the atomic force microscope depends on electrostatic interactions. Biophys. J. 73:1633‐1644. | |
| Müller, D.J., Engel, A., and Amrein, M. 1997a. Preparation techniques for the observation of native biological systems with the atomic force microscope. Biosens. Bioelectron. 12:867‐877. | |
| Müller, D.J., Engel, A., Carrascosa, J., and Velez, M. 1997b. The bacteriophage o29 head‐tail connector imaged at high resolution with atomic force microscopy in buffer solution. EMBO J. 16:101‐107. | |
| Müller, D.J., Amrein, M., and Engel, A. 1997c. Adsorption of biological molecules to a solid support for scanning probe microscopy. J. Struct. Biol. 119:172‐188. | |
| Müller, D.J., Fotiadis, D., and Engel, A. 1998. Mapping flexible protein domains at subnanometer resolution with the atomic force microscope. FEBS Lett. 430:105‐111. | |
| Müller, D.J., Baumeister, W., and Engel, A. 1999a. Controlled unzipping of a bacterial surface layer with atomic force microscopy. Proc. Natl. Acad. Sci. U.S.A. 96:13170‐13174. | |
| Müller, D.J., Fotiadis, D., Scheuring, S., Müller, S.A., and Engel, A. 1999b. Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscopy. Biophys. J. 76:1101‐1111. | |
| Neumeister, J.M. and Ducker, W.A. 1994. Lateral, normal and longitudinal spring constants of atomic force microscopy cantilevers. Rev. Sci. Instrum. 65:2527‐2531. | |
| 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. | |
| Pesen, D., and Hoh, J.H. 2005. Micromechanical architecture of the endothelial cell cortex. Biophys. J. 88:670‐679. | |
| Raab, A., Han, W., Badt, D., Smith‐Gill, S., Lindsay, S., Schindler, H., and Hinterdorfer, P. 1999. Antibody recognition imaging by atomic force microscopy. Nature Biotech. 17:902‐905. | |
| Radmacher, M., Fritz, M., Hansma, H.G., and Hansma, P.K. 1994. Direct observation of enzyme activity with the atomic force microscopy. Science 265:1577‐1579. | |
| Radmacher, M., Fritz, M., and Hansma, P.K. 1995. Imaging soft samples with the atomic force microscope: Gelatin in water and propanol. Biophys. J. 69:264‐270. | |
| Radmacher, M. 1997. Measuring the elastic properties of biological samples with the atomic force microscope. IEEE Medicine and Engineering Biology 16:47‐57. | |
| Reviakine, I., Bergsma‐Schutter, W., and Brisson, A. 1998. Growth of protein 2‐D con supported planar lipid bilayers imaged in situ by AFM. J. Struct. Biol. 121:356‐361. | |
| Rief, M., Oesterhelt, F., Heymann, B., and Gaub, H.E. 1997a. Single molecule force spectroscopy on polysaccharides by AFM. Science 275:1295‐1298. | |
| Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J.M., and Gaub, H.E. 1997b. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276:1109‐1112. | |
| Rief, M., Gautel, M., and Gaub, H.E. 2000. Unfolding forces of titin and fibronectin domains directly measured by AFM. Adv. Exp. Med. Biol. 481:129‐136. | |
| Rinia, H.A., Kik, R.A., Demel, R.A., Snel, M.M., Killian, J.A., van Der Eerden, J.P., and de Kruijff, B. 2000. Visualization of highly ordered striated domains induced by transmembrane peptides in supported phosphatidylcholine bilayers. Biochemistry 39:5852‐5858. | |
| Sader, J.E., Chon, J.W.M., and Mulvaney, P. 1999. Calibration of rectangular atomic force microscope cantilevers. Rev. Sci. Inst. 70:3967‐3969. | |
| Schabert, F.A. and Engel, A. 1994. Reproducible acquisition of Escherichia coli porin surface topographs by atomic force microscopy. Biophys. J. 67:2394‐2403. | |
| Schabert, F.A., Henn, C., and Engel, A. 1995. Native Escherichia coli OmpF porin surfaces probed by atomic force microscopy. Science 268:92‐94. | |
| Scheuring, S., Müller, D.J., Ringler, P., Heymann, J.B., and Engel, A. 1999a. Imaging streptavidin 2D crystals on biotinylated lipid monolayers at high resolution with the atomic force microscopy. J. Microsc. 193:28‐35. | |
| Scheuring, S., Ringler, P., Borgina, M., Stahlberg, H., Müller, D.J., Agre, P., and Engel, A. 1999b. High resolution topographs of the Escherichia coli waterchannel aquaporin Z. EMBO J. 18:4981‐4987. | |
| Scheuring, S., Freiss‐Husson, F., Engel, A., Rigaud, J., and Ranck, J. 2001a. High resolution topographs of the Rubrivivax gelatinosus light‐harvesting complex 2. EMBO J. 20:3029‐3035. | |
| Scheuring, S., Fotiadis, D., Möller, C., Müller, S.A., Engel, A., and Müller, D.J. 2001b. Single proteins observed by atomic force microscopy. Single Mol. 2:59‐67. | |
| Scheuring, S., Stahlberg, H., Chami, M., Houssin, C., Rigaud, J., and Engel, A. 2002a. Charting and unzipping the surface‐layer of Corynebacterium glutamicum with the atomic force microscope. Mol. Microbiol. 44:675‐684. | |
| Scheuring, S., Müller, D.J., Stahlberg, H., Engel, H.‐A., and Engel, A. 2002b. Sampling the conformational space of membrane protein surfaces with the AFM. Eur. Biophys. J. 31:172‐178. | |
| Schoenenberger, C.A. and Hoh, J.H. 1994. Slow cellular dynamics in MDCK and R5 cells monitored by time‐lapse atomic force microscopy. Biophys. J. 67:929‐936. | |
| Seelert, H., Poetsch, A., Dencher, N.A., Engel, A., Stahlberg, H., and Müller, D.J. 2000. Proton powered turbine of a plant motor. Nature 405:418‐419. | |
| Severin, N., Barner, J., Kalachev, A.A., and Rabe, J.P. 2004. Manipulation and overstretching of genes on solid substrates. Nano Letters 4:577‐579. | |
| Shi, D., Somlyo, A.V., Somlyo, A.P., and Shao, Z. 2001. Visualizing filamentous actin on lipid bilayers by atomic force microscopy in solution. J. Microsc. 201:377‐382. | |
| Sotres, J., Lostao, A., Ebner, A., Gomez‐Moreno, C., Gruber, H.J., Hinterdorfer, P., and Baro, A.M. 2008. Unbinding molecular recognition force maps of localized single receptor molecules by atomic force microscopy. Chemphyschem. 9:590‐599. | |
| Stahlberg, H., Müller, D.J., Suda, K., Fotiadis, D., Engel, A., Matthey, U., Meier, T., and Dimroth, P. 2001. Bacterial ATP synthase has an undacemeric rotor. EMBO Rep. 2:229‐235. | |
| Stolz, M., Stoffler, D., Aebi, U., and Goldsbury, C. 2000. Monitoring biomolecular interactions by time‐lapse atomic force microscopy. J. Struct. Biol. 131:171‐180. | |
| Stolz, M., Raiteri, R., Daniels, A.U., VanLandingham, M.R., Baschong, W., and Aebi, U. 2004. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation‐type atomic force microscopy. Biophys. J. 86:3269‐3283. | |
| 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. | |
| Viani, M.B., Schafer, T.E., Chand, A., Rief, M., Gaub, H.E., and Hansma, P.K., 1999. Small cantilevers for force spectroscopy of single molecules. J. Appl. Phys. 86:2258‐2262. | |
| 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. | |
| Wagner, P. 1998. Immobilization strategies for biological scanning probe microscopy. FEBS Lett. 430:112‐115. | |
| 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. | |
| Wu, G., Datar, R.H., Hansen, K.M., Thundat, T., Cote, R.J., and Majumdar, A. 2001. Bioassay of prostate‐specific antigen (PSA) using microcantilevers. Nat. Biotechnol. 19:856‐860. | |
| Xu, S.H. and Arnsdorf, M.F. 1995. Electrostatic force microscope for probing surface charges in aqueous solutions. Proc. Natl. Acad. Sci. U.S.A. 92:10384‐10388. | |
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