Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 2001 Jun;80(6):3009–3018. doi: 10.1016/S0006-3495(01)76266-2

From images to interactions: high-resolution phase imaging in tapping-mode atomic force microscopy.

M Stark 1, C Möller 1, D J Müller 1, R Guckenberger 1
PMCID: PMC1301484  PMID: 11371473

Abstract

In tapping-mode atomic force microscopy, the phase shift between excitation and response of the cantilever is used as a material-dependent signal complementary to topography. The localization of information in the phase signal is demonstrated with 1.4-nm lateral resolution on purple membrane of Halobacterium salinarum in buffer solution. In a first-order approximation, the phase signal is found to correlate with modulations of the tip oscillation amplitude, induced by topography. Extending the analysis to contributions of the tip-sample interaction area as a second-order approximation, a method is proposed to extract information about the interaction from the phase signal for surfaces with a roughness in the order of the tip radius.

Full Text

The Full Text of this article is available as a PDF (269.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anczykowski B, Krüger D, Fuchs H. Cantilever dynamics in quasinoncontact force microscopy: Spectroscopic aspects. Phys Rev B Condens Matter. 1996 Jun 15;53(23):15485–15488. doi: 10.1103/physrevb.53.15485. [DOI] [PubMed] [Google Scholar]
  2. Belrhali H., Nollert P., Royant A., Menzel C., Rosenbusch J. P., Landau E. M., Pebay-Peyroula E. Protein, lipid and water organization in bacteriorhodopsin crystals: a molecular view of the purple membrane at 1.9 A resolution. Structure. 1999 Aug 15;7(8):909–917. doi: 10.1016/s0969-2126(99)80118-x. [DOI] [PubMed] [Google Scholar]
  3. Binnig G, Quate CF, Gerber C. Atomic force microscope. Phys Rev Lett. 1986 Mar 3;56(9):930–933. doi: 10.1103/PhysRevLett.56.930. [DOI] [PubMed] [Google Scholar]
  4. Blaurock A. E., Stoeckenius W. Structure of the purple membrane. Nat New Biol. 1971 Sep 29;233(39):152–155. doi: 10.1038/newbio233152a0. [DOI] [PubMed] [Google Scholar]
  5. Czajkowsky D. M., Allen M. J., Elings V., Shao Z. Direct visualization of surface charge in aqueous solution. Ultramicroscopy. 1998 Jul;74(1-2):1–5. doi: 10.1016/s0304-3991(98)00024-2. [DOI] [PubMed] [Google Scholar]
  6. Czajkowsky D. M., Shao Z. Submolecular resolution of single macromolecules with atomic force microscopy. FEBS Lett. 1998 Jun 23;430(1-2):51–54. doi: 10.1016/s0014-5793(98)00461-x. [DOI] [PubMed] [Google Scholar]
  7. Dorn I. T., Eschrich R., Seemüller E., Guckenberger R., Tampé R. High-resolution AFM-imaging and mechanistic analysis of the 20 S proteasome. J Mol Biol. 1999 May 21;288(5):1027–1036. doi: 10.1006/jmbi.1999.2714. [DOI] [PubMed] [Google Scholar]
  8. Drake B., Prater C. B., Weisenhorn A. L., Gould S. A., Albrecht T. R., Quate C. F., Cannell D. S., Hansma H. G., Hansma P. K. Imaging crystals, polymers, and processes in water with the atomic force microscope. Science. 1989 Mar 24;243(4898):1586–1589. doi: 10.1126/science.2928794. [DOI] [PubMed] [Google Scholar]
  9. Essen L., Siegert R., Lehmann W. D., Oesterhelt D. Lipid patches in membrane protein oligomers: crystal structure of the bacteriorhodopsin-lipid complex. Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11673–11678. doi: 10.1073/pnas.95.20.11673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grandbois M., Clausen-Schaumann H., Gaub H. Atomic force microscope imaging of phospholipid bilayer degradation by phospholipase A2. Biophys J. 1998 May;74(5):2398–2404. doi: 10.1016/S0006-3495(98)77948-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grigorieff N., Ceska T. A., Downing K. H., Baldwin J. M., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J Mol Biol. 1996 Jun 14;259(3):393–421. doi: 10.1006/jmbi.1996.0328. [DOI] [PubMed] [Google Scholar]
  12. Heinz W. F., Hoh J. H. Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope. Trends Biotechnol. 1999 Apr;17(4):143–150. doi: 10.1016/s0167-7799(99)01304-9. [DOI] [PubMed] [Google Scholar]
  13. Heymann J. B., Müller D. J., Landau E. M., Rosenbusch J. P., Pebay-Peyroula E., Büldt G., Engel A. Charting the surfaces of the purple membrane. J Struct Biol. 1999 Dec 30;128(3):243–249. doi: 10.1006/jsbi.1999.4180. [DOI] [PubMed] [Google Scholar]
  14. Hoh J. H., Sosinsky G. E., Revel J. P., Hansma P. K. Structure of the extracellular surface of the gap junction by atomic force microscopy. Biophys J. 1993 Jul;65(1):149–163. doi: 10.1016/S0006-3495(93)81074-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kuznetsov YuG, Malkin A. J., Land T. A., DeYoreo J. J., Barba A. P., Konnert J., McPherson A. Molecular resolution imaging of macromolecular crystals by atomic force microscopy. Biophys J. 1997 May;72(5):2357–2364. doi: 10.1016/S0006-3495(97)78880-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lanyi J. K. Bacteriorhodopsin as a model for proton pumps. Nature. 1995 Jun 8;375(6531):461–463. doi: 10.1038/375461a0. [DOI] [PubMed] [Google Scholar]
  17. Luecke H., Richter H. T., Lanyi J. K. Proton transfer pathways in bacteriorhodopsin at 2.3 angstrom resolution. Science. 1998 Jun 19;280(5371):1934–1937. doi: 10.1126/science.280.5371.1934. [DOI] [PubMed] [Google Scholar]
  18. McMaster T. J., Berry M., Corfield A. P., Miles M. J. Atomic force microscopy of the submolecular architecture of hydrated ocular mucins. Biophys J. 1999 Jul;77(1):533–541. doi: 10.1016/S0006-3495(99)76910-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Möller C., Allen M., Elings V., Engel A., Müller D. J. Tapping-mode atomic force microscopy produces faithful high-resolution images of protein surfaces. Biophys J. 1999 Aug;77(2):1150–1158. doi: 10.1016/S0006-3495(99)76966-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Möller C., Büldt G., Dencher N. A., Engel A., Müller D. J. Reversible loss of crystallinity on photobleaching purple membrane in the presence of hydroxylamine. J Mol Biol. 2000 Aug 25;301(4):869–879. doi: 10.1006/jmbi.2000.3995. [DOI] [PubMed] [Google Scholar]
  21. Müller D. J., Büldt G., Engel A. Force-induced conformational change of bacteriorhodopsin. J Mol Biol. 1995 Jun 2;249(2):239–243. doi: 10.1006/jmbi.1995.0292. [DOI] [PubMed] [Google Scholar]
  22. Müller D. J., Engel A. Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J Mol Biol. 1999 Jan 29;285(4):1347–1351. doi: 10.1006/jmbi.1998.2359. [DOI] [PubMed] [Google Scholar]
  23. Müller D. J., Fotiadis D., Scheuring S., Müller S. A., Engel A. Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscope. Biophys J. 1999 Feb;76(2):1101–1111. doi: 10.1016/S0006-3495(99)77275-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Müller D. J., Sass H. J., Müller S. A., Büldt G., Engel A. Surface structures of native bacteriorhodopsin depend on the molecular packing arrangement in the membrane. J Mol Biol. 1999 Feb 5;285(5):1903–1909. doi: 10.1006/jmbi.1998.2441. [DOI] [PubMed] [Google Scholar]
  25. Oesterhelt D., Stoeckenius W. Functions of a new photoreceptor membrane. Proc Natl Acad Sci U S A. 1973 Oct;70(10):2853–2857. doi: 10.1073/pnas.70.10.2853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Oesterhelt D., Stoeckenius W. Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 1974;31:667–678. doi: 10.1016/0076-6879(74)31072-5. [DOI] [PubMed] [Google Scholar]
  27. Oesterhelt D. The structure and mechanism of the family of retinal proteins from halophilic archaea. Curr Opin Struct Biol. 1998 Aug;8(4):489–500. doi: 10.1016/s0959-440x(98)80128-0. [DOI] [PubMed] [Google Scholar]
  28. Oesterhelt F., Oesterhelt D., Pfeiffer M., Engel A., Gaub H. E., Müller D. J. Unfolding pathways of individual bacteriorhodopsins. Science. 2000 Apr 7;288(5463):143–146. doi: 10.1126/science.288.5463.143. [DOI] [PubMed] [Google Scholar]
  29. Pebay-Peyroula E., Rummel G., Rosenbusch J. P., Landau E. M. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science. 1997 Sep 12;277(5332):1676–1681. doi: 10.1126/science.277.5332.1676. [DOI] [PubMed] [Google Scholar]
  30. San Paulo A., García R. High-resolution imaging of antibodies by tapping-mode atomic force microscopy: attractive and repulsive tip-sample interaction regimes. Biophys J. 2000 Mar;78(3):1599–1605. doi: 10.1016/S0006-3495(00)76712-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Saxton W. O., Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J Microsc. 1982 Aug;127(Pt 2):127–138. doi: 10.1111/j.1365-2818.1982.tb00405.x. [DOI] [PubMed] [Google Scholar]
  32. Schabert F. A., Engel A. Reproducible acquisition of Escherichia coli porin surface topographs by atomic force microscopy. Biophys J. 1994 Dec;67(6):2394–2403. doi: 10.1016/S0006-3495(94)80726-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schabert F. A., Henn C., Engel A. Native Escherichia coli OmpF porin surfaces probed by atomic force microscopy. Science. 1995 Apr 7;268(5207):92–94. doi: 10.1126/science.7701347. [DOI] [PubMed] [Google Scholar]
  34. Unser M., Trus B. L., Steven A. C. A new resolution criterion based on spectral signal-to-noise ratios. Ultramicroscopy. 1987;23(1):39–51. doi: 10.1016/0304-3991(87)90225-7. [DOI] [PubMed] [Google Scholar]
  35. Viani M. B., Pietrasanta L. I., Thompson J. B., Chand A., Gebeshuber I. C., Kindt J. H., Richter M., Hansma H. G., Hansma P. K. Probing protein-protein interactions in real time. Nat Struct Biol. 2000 Aug;7(8):644–647. doi: 10.1038/77936. [DOI] [PubMed] [Google Scholar]
  36. Vinckier A., Gervasoni P., Zaugg F., Ziegler U., Lindner P., Groscurth P., Plückthun A., Semenza G. Atomic force microscopy detects changes in the interaction forces between GroEL and substrate proteins. Biophys J. 1998 Jun;74(6):3256–3263. doi: 10.1016/S0006-3495(98)78032-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Winkler RG, Spatz JP, Sheiko S, Möller M, Reineker P, Marti O. Imaging material properties by resonant tapping-force microscopy: A model investigation. Phys Rev B Condens Matter. 1996 Sep 15;54(12):8908–8912. doi: 10.1103/physrevb.54.8908. [DOI] [PubMed] [Google Scholar]
  38. Yang J., Mou J., Shao Z. Molecular resolution atomic force microscopy of soluble proteins in solution. Biochim Biophys Acta. 1994 Mar 2;1199(2):105–114. doi: 10.1016/0304-4165(94)90104-x. [DOI] [PubMed] [Google Scholar]
  39. Yip C. M., DeFelippis M. R., Frank B. H., Brader M. L., Ward M. D. Structural and morphological characterization of ultralente insulin crystals by atomic force microscopy: evidence of hydrophobically driven assembly. Biophys J. 1998 Sep;75(3):1172–1179. doi: 10.1016/S0006-3495(98)74036-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES