Atomic Force Microscopy of Isolated Nanostructures: Biomolecular Imaging in Hydrated Environments – Status and Future Prospects

  • Sergio Santos
  • Neil H. Thomson
Chapter
Part of the NanoScience and Technology book series (NANO)

Abstract

The use of the atomic force microscope (AFM) in ambient conditions has some key advantages for characterising isolated nanostructures over other operating environments. The lack of a bulk liquid environment minimises motion of the sample to maximise resolution, while humidity control allows retention of surface water, keeping biomolecules sufficiently hydrated. The use of relatively stiff cantilevers in air (k > 10 N/m) prevents significant energy being transferred to higher modes or frequencies. This enables reliable modelling of the cantilever dynamics with relatively straightforward point mass and spring models. We show herein that combining modelling with experiment leads to robust interpretation of dynamic AFM in air. This understanding has led to new ways of operation, including a true non-contact mode in ambient and small amplitude small set-point (SASS) modes. These modes will be important to gain quantitative information about structure and processes on the nanoscale. We also discuss interpretation of height information obtained from AFM on the nanoscale and summarise a framework for recovery of apparent height loss for nanostructures. A combination of these methods will lead to a new era of quantitative AFM for nanoscience and nanotechnology.

Keywords

Atomic Force Microscope Amplitude Modulation Scanning Tunnelling Microscope Atomic Force Microscope Technique Force Regime 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We would like to acknowledge Matteo Chiesa and Marco Stefancich (Masdar Institute of Science and Technology) for their comments when developing this work and Maritsa Kissamitaki for helping with the artwork. We would also like to thank Dr. David Adams, Dr. Simon Connell and Dr. Toby Kurk for their contribution to this work (Oscillatoria A2 cyanobacterium, Fig. 5.12).

References

  1. 1.
    G. Binnig, C.F. Quate, C. Gerber, Atomic force microscope. Phys. Rev. Lett. 56, 930–933 (1986)Google Scholar
  2. 2.
    R. Garcia, R. Perez, Dynamic atomic force microscopy methods. Surf. Sci. Rep. 47, 197–301 (2002)Google Scholar
  3. 3.
    A. Alessandrini, P. Facci, AFM: A versatile tool in biophysics. Meas. Sci. Technol. 16, R65–R92 (2005)Google Scholar
  4. 4.
    H.G. Hansma, J.H. Hoh, Biomolecular imaging with the atomic force microscope. Ann. Rev. Biophys. Biomol. Struct. 23, 115–140 (1994)Google Scholar
  5. 5.
    N.H. Thomson et al., Protein tracking and detection of protein motion using atomic force microscopy. Biophys. J. 70, 2421–2431 (1996)Google Scholar
  6. 6.
    B. Drake et al., Imaging crystals, polymers, and processes in water with the atomic force microscope. Science 243, 1586 (1989)Google Scholar
  7. 7.
    P.K. Hansma et al., Tapping mode atomic force microscopy in liquids. Appl. Phys. Lett. 64, 1738–1740 (1994)Google Scholar
  8. 8.
    L. Gross, F. Mohn, N. Moll, P. Liljeroth, G. Meyer, The chemical structure of a molecule resolved by atomic force microscopy. Science 325, 1110–1114 (2009)Google Scholar
  9. 9.
    T. Ushiki, J. Hitomi, S. Ogura, T. Umemoto, M. Shigeno, Atomic force microscopy in histology and cytology. Arch. Histol. Cytol. 59, 421–431 (1996)Google Scholar
  10. 10.
    C.F. Quate, The AFM as a tool for surface imaging. Surf. Sci. 299–300, 980–995 (1994)Google Scholar
  11. 11.
    N. Kodera, D. Yamamoto, R. Ishikawa, T. Ando, Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468, 72–76 (2010)Google Scholar
  12. 12.
    C. Bustamante, D. Keller, Scanning force microscopy in biology. Phys. Today 48, 33–38 (1995)Google Scholar
  13. 13.
    P. Parot et al., Past, present and future of atomic force microscopy in life sciences and medicine. J. Mol. Recognit. 20, 418–431 (2007)Google Scholar
  14. 14.
    S. Santos, N.H. Thomson, High Resolution Imaging of Immunoglobulin G (IgG) Antibodies and Other Biomolecules Using Amplitude Modulation Atomic Force Microscopy in Air (Humana Press, New York, 2011), pp. 61–79Google Scholar
  15. 15.
    L.W. Francis, P.D. Lewis, C.J. Wright, R.S. Conlan, Atomic force microscopy comes of age. Biol. Cell 102, 133–143 (2010)Google Scholar
  16. 16.
    C. Gerber, H.P. Lang, How the doors to the nanoworld were opened. Nat. Nanotechnol. 1, 3–5 (2006)Google Scholar
  17. 17.
    R. Garcia, R. Magerele, R. Perez, Nanoscale compositional mapping with gentle forces. Nat. Mater. 6, 405–411 (2007)Google Scholar
  18. 18.
    G. Binnig, H. Rohrer, Scanning Tunneling Microscopy (European Physical Society, The Hague, 1984), pp. 38–46Google Scholar
  19. 19.
    S. Gould et al., Molecular resolution images of amino acid crystals with the atomic force microscope. Nature 332, 332–334 (1988)Google Scholar
  20. 20.
    C. Clemmer, T.P.J. Beebe, Graphite: A mimic for DNA and other biomolecules in scanning tunneling microscope studies. Science 251, 640–642 (1991)Google Scholar
  21. 21.
    S.-M. Lim, A. Trache, Integrated microscopy for real-time imaging of mechanotransduction studies in live cells. J. Biomed. Opt. 14, 034024 (2009)Google Scholar
  22. 22.
    R. Merkel, P. Nassoy, A. Leung, K. Ritchie, E. Evans, Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy. Nature 397, 50–53 (1999)Google Scholar
  23. 23.
    K.C. Neuman, A. Nagy, Single-molecule force spectroscopy: Optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5, 491–505 (2008)Google Scholar
  24. 24.
    A. French, Vibrations and Waves (Thomas Nelson and Sons Ltd, New York, 1981)Google Scholar
  25. 25.
    R. Stark, W. Heckl, Higher harmonics imaging in tapping-mode atomic-force microscopy. Rev. Sci. Instrum. 74, 5111–5114 (2003)Google Scholar
  26. 26.
    S. Santos, Dynamic atomic force microscopy and applications in biomolecular imaging. Ph.D. thesis, University of Leeds, 2011Google Scholar
  27. 27.
    T.R. Albrecht, P. Grutter, D. Horne, D. Rugar, Frequency modulation detection using high-Q cantilevers for enhanced force microscope sensitivity. J. Appl. Phys. 69, 668–673 (1991)Google Scholar
  28. 28.
    Y. Martin, C.C. Williams, H.K. Wickramasinghe, Atomic force microscope-force mapping and profiling on a sub 100-Å scale. J. Appl. Phys. 61, 4723–4729 (1987)Google Scholar
  29. 29.
    Q. Zhong, D. Innlss, K. Kjoller, V.B. Elings, Fractured polymer/silica fiber surface studied by tapping mode atomic force microscopy. Surf. Sci. Lett. 290, L688–L692 (1993)Google Scholar
  30. 30.
    J. Tamayo, R. Garcia, Deformation, contact time, and phase contrast in tapping mode scanning force microscopy. Langmuir 12, 4430–4435 (1996)Google Scholar
  31. 31.
    A.L. Weisenhorn, P.K. Hansma, T.R. Albrecht, C.F. Quate, Forces in atomic force microscopy in air and water. Appl. Phys. Lett. 54, 2651–2653 (1989)Google Scholar
  32. 32.
    T. Fukuma, K. Kobayashi, K. Matsushige, H. Yamada, True molecular resolution in liquid by frequency modulation atomic force microscopy. Appl. Phys. Lett. 86, 193108–193110 (2005)Google Scholar
  33. 33.
    F.J. Giessibl, Advances in atomic force microscopy. Rev. Mod. Phys. 75, 949–983 (2003)Google Scholar
  34. 34.
    L. Gross et al., Organic structure determination using atomic-resolution scanning probe microscopy. Nat. Chem. 2, 821–825 (2010)Google Scholar
  35. 35.
    D. Anselmetti et al., Attractive-mode imaging of biological materials with dynamic force microscopy. Nanotechnology 5, 87–94 (1994)Google Scholar
  36. 36.
    R. Pérez, I. Štich, M.C. Payne, K. Terakura, Surface-tip interactions in noncontact atomic-force microscopy on reactive surfaces: Si(111). Phys. Rev. B 58, 10835–10849 (1998)Google Scholar
  37. 37.
    R. Boisgard., D. Michel, J.P. Aime, Hysteresis generated by attractive interaction: Oscillating behavior of a vibrating tip-microlever system near a surface. Surf. Sci. 401, 199–205 (1998)Google Scholar
  38. 38.
    R. Garcia, A. San Paulo, Attractive and repulsive tip-sample interaction regimes in tapping mode atomic force microscopy. Phys. Rev. B 60, 4961–4967 (1999)Google Scholar
  39. 39.
    X. Chen et al., Optimizing phase imaging via dynamic force curves. Surf. Sci. 460, 292–300 (2000)Google Scholar
  40. 40.
    B. Anczykowski, D. Krüger, H. Fuchs, Cantilever dynamics in quasinoncontact force microscopy: Spectroscopic aspects. Phys. Rev. B 53, 15485–15488 (1996)Google Scholar
  41. 41.
    A. San Paulo, R. Garcia, High-resolution imaging of antibodies by tapping-mode atomic force microscopy: Attractive and repulsive tip-sample interaction regimes. Biophys. J. 78, 1599–1605 (2000)Google Scholar
  42. 42.
    R. Stark, G. Schitter, A. Stemmer, Tuning the interactions forces in tapping mode atomic force microscopy. Phys. Rev. B 68, 0854011–0854015 (2003)Google Scholar
  43. 43.
    F. Ostendorf et al., Evidence for potassium carbonate crystallites on air-cleaved mica surfaces. Langmuir 25, 10764–10767 (2009)Google Scholar
  44. 44.
    S. Santos, D.J. Billingsley, W.A. Bonass, N.H. Thomson, The double-helix of single DNA molecules. Unpublished (2010)Google Scholar
  45. 45.
    A. Ikai, Nanobiomechanics of proteins and biomembrane. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 2163–2171 (2008)Google Scholar
  46. 46.
    R.D. Turner, J. Kirkham, D. Devine, N.H. Thomson, Second harmonic atomic force microscopy of living Staphylococcus aureus bacteria. Appl. Phys. Lett. 94, 043901 (2009)Google Scholar
  47. 47.
    R.W. Stark, Spectroscopy of higher harmonics in dynamic atomic force microscopy. Nanotechnology 15, 347–351 (2004)Google Scholar
  48. 48.
    S. Patil, N.F. Martinez, J.R. Lozano, R. Garcia, Force microscopy imaging of individual protein molecules with sub-pico Newton force sensitivity. J. Mol. Recognit. 20, 516–523 (2007)Google Scholar
  49. 49.
    R. Proksch, Multi-frequency, repulsive mode amplitude modulated atomic force microscopy. Appl. Phys. Lett. 89, 113121–113123 (2006)Google Scholar
  50. 50.
    X. Xu, J. Melcher, S. Basak, R. Reifenberger, A. Raman, Compositional contrast of biological materials in liquids using the momentary excitation of higher eigenmodes in dynamic atomic force microscopy. Phys. Rev. Lett. 102, 060801–060804 (2009)Google Scholar
  51. 51.
    J. Melcher et al., Origins of phase contrast in the atomic force microscope in liquids. PNAS 106, 13655–13660 (2009)Google Scholar
  52. 52.
    D. Kiracofe, A. Raman, On eigenmodes, stiffness, and sensitivity of atomic force microscope cantilevers in air versus liquids. J. Appl. Phys. 107, 033506–033515 (2010)Google Scholar
  53. 53.
    X. Xu, J. Melcher, A. Raman, Accurate force spectroscopy in tapping mode atomic force microscopy in liquids. Phys. Rev. B 81, 035407–035414 (2010)Google Scholar
  54. 54.
    G. Bar, Y. Thomann, R. Brandsch, H.J. Cantow, Factors affecting the height and phase images in tapping mode atomic force microscopy. Study of phase-separated polymer blends of poly(ethene-costyrene) and poly(2,6-dimethyl-1,4-phenylene oxide). Langmuir 13, 3807–3812 (1997)Google Scholar
  55. 55.
    J. Tamayo, R. Garcia, Effects of elastic and inelastic interactions on phase contrast images in tapping-mode scanning force microscopy. Appl. Phys. Lett. 71, 2394–2396 (1997)Google Scholar
  56. 56.
    J.P. Cleveland, B. Anczykowski, A.E. Schmid, V.B. Elings,. Energy dissipation in tapping-mode atomic force microscopy. Appl. Phys. Lett. 72, 2613–2615 (1998)Google Scholar
  57. 57.
    N. Martinez, R. Garcia, Measuring phase shifts and energy dissipation with amplitude modulation atomic force microscopy. Nanotechnology 17, S167–S172 (2006)Google Scholar
  58. 58.
    R. Garcia et al., Identification of nanoscale dissipation processes by dynamic atomic force microscopy. Phys. Rev. Lett. 97, 016103–016104 (2006)Google Scholar
  59. 59.
    C.J. Gomez, R. Garcia, Determination and simulation of nanoscale energy dissipation processes in amplitude modulation AFM. Ultramicroscopy 110, 626–633 (2010)Google Scholar
  60. 60.
    O. Sahin, S. Magonov, C. Su, C.F. Quate, O. Solgaard, An atomic force microscope tip designed to measure time-varying nanomechanical forces. Nat. Nanotechnol. 2, 507–514 (2007)Google Scholar
  61. 61.
    Y. Gan, Atomic and subnanometer resolution in ambient conditions by atomic force microscopy. Surf. Sci. Rep. 64, 99–121 (2009)Google Scholar
  62. 62.
    K. Voïtchovsky, J.J. Kuna, S. Antoranz Contera, E. Tosatti, F. Stellacci, Direct mapping of the solid–liquid adhesion energy with subnanometre resolution. Nat. Nanotechnol. 5, 401–405 (2010)Google Scholar
  63. 63.
    S. Santos, V. Barcons, H.K. Christenson, N.H. Thomson, J. Font, The intrinsic resolution limit in the atomic force microscope: Implications for heights of nano-scale features. PLoS ONE 6, e23821 (2011)Google Scholar
  64. 64.
    S. Santos, M. Stefancich, M. Chiesa, H.N. Thomson, The hydrophilicity of a single DNA molecule. Submitted (2011)Google Scholar
  65. 65.
    S. Santos et al., How localised are energy dissipation processes in the nanoscale? Nanotechnology 22, 345401–345407 (2011)Google Scholar
  66. 66.
    S. Santos, N.H. Thomson, Energy dissipation in a dynamic nanoscale contact. Appl. Phys. Lett. 98, 013101–013103 (2011)Google Scholar
  67. 67.
    J.M. Drake, J. Klafter, Dynamics of confined molecular systems. Phys. Today 43, 43–45 (1990)Google Scholar
  68. 68.
    E. Meyer et al., Molecular-resolution images of Langmuir-Blodgett films using atomic force microscopy. Nature 349, 398–400 (1991)Google Scholar
  69. 69.
    M. Radmacher, R.W. Tillamnn, M. Fritz, H.E. Gaub, From molecules to cells: Imaging soft samples with the atomic force microscope. Science 257, 1900–1905 (1992)Google Scholar
  70. 70.
    F.J. Giessibl, Atomic resolution of the silicon (111)-(7 ×7) surface by atomic force microscopy. Science 267, 68–71 (1995)Google Scholar
  71. 71.
    S. Yasuhiro, M. Ohta, H. Ueyama, S. Morita, Defect motion on an InP(110) surface observed with noncontact atomic force microscopy. Science 270, 1646–1648 (1995)Google Scholar
  72. 72.
    L. Nony, R. Boisgard, J.P. Aimé, DNA properties investigated by dynamic force microscopy. Biomacromolecules 2, 827–835 (2001)Google Scholar
  73. 73.
    P. Hinterdorfer, Y.F. Dufrene, Detection and localization of single molecular recognition events using atomic force microscopy. Nat. Methods 3, 347–355 (2006)Google Scholar
  74. 74.
    R.W. Stark, Bistability, higher harmonics, and chaos in AFM. Mater. Today 13, 24–32 (2010)Google Scholar
  75. 75.
    S. Santos, V. Barcons, J. Font, N.H. Thomson, Cantilever dynamics in amplitude modulation AFM: Continuous and discontinuous transitions. J. Phys. D Appl. Phys. 43, 275401–275407 (2010)Google Scholar
  76. 76.
    S. Santos, V. Barcons, J. Font, N.H. Thomson, Bi-stability of amplitude modulation AFM in air: Deterministic and stochastic outcomes for imaging biomolecular systems. Nanotechnology 21, 225710–225720 (2010)Google Scholar
  77. 77.
    R. Garcia, Amplitude Modulation Atomic Force Microscopy (Wiley, Weinheim, 2010)Google Scholar
  78. 78.
    N. Hashemi, H. Dankowicz, M.R. Paul, The nonlinear dynamics of tapping mode atomic force microscopy with capillary force interaction. J. Appl. Phys. 103, 093512–093518 (2008)Google Scholar
  79. 79.
    S. Basak, A. Raman, Dynamics of tapping mode atomic force microscopy in liquids: Theory and experiments. Appl. Phys. Lett. 91, 064107–064109 (2007)Google Scholar
  80. 80.
    A.S. Paulo, R. Garcia, Unifying theory of tapping-mode atomic force microscopy. Phys. Rev. B 66, 0414061–0414064 (2002)Google Scholar
  81. 81.
    R. Garcia, A. San Paulo, Dynamics of a vibrating tip near or in intermittent contact with a surface. Phys. Rev. B 61, R13381–R13384 (2000)Google Scholar
  82. 82.
    L. Wang, The role of damping in phase imaging in tapping mode atomic force microscopy. Surf. Sci. 429, 178–185 (1999)Google Scholar
  83. 83.
    L. Nony, R. Boisgard, J.P. Aime, Nonlinear dynamical properties of an oscillating tip–cantilever system in the tapping mode. J. Chem. Phys. 111, 1615–1627 (1999)Google Scholar
  84. 84.
    M. Marth, D. Maier, J. Honerkamp, A unifying view on some experimental effects in tapping-mode atomic force microscopy. J. Appl. Phys. 85, 7030–7036 (1999)Google Scholar
  85. 85.
    H. Hölscher, U.D. Schwarz, R. Wiesendanger, Calculation of the frequency shift in dynamic force microscopy. Appl. Surf. Sci. 140, 344–351 (1999)Google Scholar
  86. 86.
    B. Gotsmann, C. Seidel, B. Anczykowski, H. Fuchs, Conservative and dissipative tip-sample interaction forces probed with dynamic AFM. Phys. Rev. B 60, 11051–11061 (1999)Google Scholar
  87. 87.
    J.P. Aimé, R. Boisgard, L. Nony, G. Couturier, Nonlinear dynamic behavior of an oscillating tip-microlever system and contrast at the atomic scale. Phys. Rev. Lett. 82, 3388–3391 (1999)Google Scholar
  88. 88.
    F.J. Giessibl, Forces and frequency shifts in atomic-resolution dynamic-force microscopy. Phys. Rev. B 56, 16010–16015 (1997)Google Scholar
  89. 89.
    T. Rodriguez, R. Garcia, Compositional mapping of surfaces in atomic force microscopy by excitation of the second normal mode of the microcantilever. Appl. Phys. Lett. 84, 449–551 (2004)Google Scholar
  90. 90.
    R. García, N.F. Martínez, C.J. Gómez, A. García-Martín, in Fundamentals of Friction and Wear, vol. 4, ed. by E. Gnecco, E. Meyer (Springer, New York, 2007), pp. 361–371Google Scholar
  91. 91.
    M.H. Whangbo, R. Brandsch, G. Bar, Description of phase imaging in tapping mode atomic force microscopy by harmonic approximation. Surf. Sci. 411, L794–L801 (1998)Google Scholar
  92. 92.
    M. Gauthier, R. Pérez, T. Arai, M. Tomitori, M. Tsukada, Interplay between nonlinearity, scan speed, damping, and electronics in frequency modulation atomic-force microscopy. Phys. Rev. Lett. 89, 146104 (2002)Google Scholar
  93. 93.
    F. Ostendorf et al., How flat is an air-cleaved mica surface? Nanotechnology 19, 305705 (2008)Google Scholar
  94. 94.
    M. Bezanilla, S. Manne, D.E. Laney, Y.L. Lyubchenko, H.G. Hansma, Adsorption of DNA to mica, silylated mica, and minerals: Characterization by atomic force microscopy. Langmuir 11, 655–659 (1995)Google Scholar
  95. 95.
    H. Hansma, D. Laney, DNA binding to mica correlates with cationic radius: Assay by atomic force microscopy. Biophys. J. 70, 1933–1939 (1996)Google Scholar
  96. 96.
    S.M. Richardson, J.W. Richardson, Crystal structure of a pink muscoyite from Archer’s Post, Kenya: Implications for reverse pleochroism in dioctahedral micas. Am. Miner. 67, 69–75 (1982)Google Scholar
  97. 97.
    J. Vesenka et al., Substrate preparation for reliable imaging of DNA molecules with the scanning force microscope. Ultramicroscopy 42–44, 1243–1249 (1992)Google Scholar
  98. 98.
    S. Santos, N.H. Thomson, High Resolution Imaging of Immunoglobulin G (IgG) Antibodies and Other Biomolecules Using Amplitude Modulation Atomic Force Microscopy in Air (Humana Press, New York, 2010)Google Scholar
  99. 99.
    J. Israelachvili, Intermolecular & Surface Forces, 2nd edn. (Academic, San Diego, 1991)Google Scholar
  100. 100.
    D. Voet, J. Voet, Biochemistry, 2nd edn. (Wiley, New York, 1995)Google Scholar
  101. 101.
    D.V. Klinov et al., High resolution atomic force microscopy of DNA. Biochemistry (Moscow) 74, 1150–1154 (2009)Google Scholar
  102. 102.
    M. Maaloum, A close encounter with DNA. Eur. Biophys. J. 32, 585–587 (2003)Google Scholar
  103. 103.
    T. Uchihashi et al., Identification of B-form DNA in an ultrahigh vacuum by noncontact-mode atomic force microscopy. Langmuir 16, 1349–1353 (2000)Google Scholar
  104. 104.
    Y. Maeda, T. Matsumoto, T. Kawai, Observation of single- and double-stranded DNA using non-contact atomic force microscopy. Appl. Surf. Sci. 140, 400–405 (1999)Google Scholar
  105. 105.
    H.G. Hansma et al., Progress in sequencing deoxyribonucleic acid with an atomic force microscope. J. Vac. Sci. Technol. B 9, 1227–1230 (1991)Google Scholar
  106. 106.
    F. Kienbergera et al., Dynamic force microscopy imaging of plasmid DNA and viral RNA. Biomaterials 28, 2403–2411 (2007)Google Scholar
  107. 107.
    Y. Wu, J. Cai, L. Cheng, C. Wang, Y. Chen, Chromosome imaging by atomic force microscopy: influencing factors and comparative evaluation. J. Genet. 85, 141–145 (2006)Google Scholar
  108. 108.
    J. Tamayo, Structure of human chromosomes studied by atomic force microscopy. J. Struct. Biol. 141, 198–207 (2003)Google Scholar
  109. 109.
    D.J. Billingsley, J. Kirkham, W.A. Bonass, N.H. Thomson, Atomic force microscopy of DNA at high humidity: Irreversible conformational switching of supercoiled molecules. Phys. Chem. Chem. Phys. 12, 14727–14734 (2010)Google Scholar
  110. 110.
    D. Beaglehole, H.K. Christenson, Vapor adsorption on mica and silicon: Entropy effects, layering, and surface forces. J. Phys. Chem. 96, 3395–3403 (1992)Google Scholar
  111. 111.
    N.H. Thomson, Imaging the substructure of antibodies with tapping-mode AFM in air: The importance of a water layer on mica. J. Microsc. 217, 193–199 (2005)Google Scholar
  112. 112.
    W. Doster et al., in Protein-Water Interactions, vol. 1804, eds. by W. Doster, T. Gutberlet (Elsevier, Burlington 2010), pp. 1–242Google Scholar
  113. 113.
    L.A. Lipscomb et al., Water ring structure at DNA interfaces: Hydration and dynamics of DNA-anthracycline complexes. Biochemistry 33, 3649–3659 (1994)Google Scholar
  114. 114.
    M.S. Cheung, A.E. García, J.N. Onuchic, Protein folding mediated by solvation: Water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc. Natl. Acad. Sci. 22, 685–690 (2002)Google Scholar
  115. 115.
    M.U. Hammer, T.H. Anderson, A. Chaimovich, M.S. Shell, J. Israelachvili, The search for the hydrophobic force law. Farad. Discuss. 146, 299–308 (2010)Google Scholar
  116. 116.
    S.C. Ha, K. Lowenhaupt, A. Rich, Y.G. Kim, K. Kim, Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases. Nature 437, 1183–1186 (2005)Google Scholar
  117. 117.
    A.D. Bates, A. Maxwell, DNA Topology. (Oxford University Press, Oxford, 2005)Google Scholar
  118. 118.
    A. Rich, S. Zhang, Timeline: Z-DNA: The long road to biological function. Nat. Rev. Genet. 4, 566–572 (2003)Google Scholar
  119. 119.
    J.G. Heddle, S. Mitelheiser, A. Maxwell, N.H. Thomson, Nucleotide binding to DNA gyrase causes loss of DNA wrap. J. Mol. Biol. 337, 597–610 (2004)Google Scholar
  120. 120.
    J. Martinez et al., Length control and sharpening of atomic force microscope carbon nanotube tips assisted by an electron beam. Nanotechnology 16, 2493–2496 (2005)Google Scholar
  121. 121.
    R.J. Driscoll, G.M. Youngquist, D.J. Baldeschwieler, Atomic-scale imaging of DNA using scanning tunnelling microscopy. Nature 346, 294–296 (1990)Google Scholar
  122. 122.
    M. Amrein, R. Durr, A. Stasiak, H. Gross, G. Travaglini, Scanning tunneling microscopy of uncoated recA-DNA complexes. Science 243, 1708–1711 (1998)Google Scholar
  123. 123.
    R. Guckenberger et al., Imaging of uncoated purple membrane by scanning tunneling microscopy. J. Vac. Sci. Technol. B 9, 1227–1230 (1991)Google Scholar
  124. 124.
    J. Tamayo, R. Garcia, Relationship between phase shift and energy dissipation in tapping-mode scanning force microscopy. Appl. Phys. Lett. 73, 2926–2928 (1998)Google Scholar
  125. 125.
    Y. Chen, W. Huang, Automatic glitch elimination of scanning probe microscopy images. Anal. Sci. 27, 153 (2011)Google Scholar
  126. 126.
    P. Gleyzes, P.K. Kuo, A.C. Boccara, Bistable behavior of a vibrating tip near a solid surface. Appl. Phys. Lett. 58, 2989–2991 (1991)Google Scholar
  127. 127.
    L. Zitzler, S. Herminghaus, F. Mugele, Capillary forces in tapping mode atomic force microscopy. Phys. Rev. B 66, 155436–155438 (2002)Google Scholar
  128. 128.
    J. Tamayo, Energy dissipation in tapping-mode scanning force microscopy with low quality factors. Appl. Phys. Lett. 75, 3569–3571 (1999)Google Scholar
  129. 129.
    T.R. Rodríguez, R. García, Tip motion in amplitude modulation tapping-mode atomic-force microscopy: Comparison between continuous and point-mass models. Appl. Phys. Lett. 80, 1646–1648 (2002)Google Scholar
  130. 130.
    R. Garcia, A. San Paulo, Amplitude curves and operating regimes in dynamic atomic force microscopy. Ultramicroscopy 82, 79–83 (2000)Google Scholar
  131. 131.
    A.S. Paulo, R. Garcia, Tip-surface, amplitude, and energy dissipation in amplitude-modulation (tapping mode) force microscopy. Phys. Rev. B 64, 193411–193414 (2001)Google Scholar
  132. 132.
    N.H. Thomson, The substructure of immunoglobulin G resolved to 25 kDA using amplitude modulation in air. Ultramicroscopy 105, 103–110 (2005)Google Scholar
  133. 133.
    S. Santos, A. Verdaguer, T. Souier, N.H. Thomson, M. Chiesa, Measuring the true height of water layers in the nanoscale. Nanotechnology, Under review (2011)Google Scholar
  134. 134.
    A. Verdaguer, G.M. Sacha, H. Bluhm, M. Salmeron, The molecular structure of water at interfaces: Wetting at the nanometer scale. Chem. Rev. 106, 1478–1510 (2006)Google Scholar
  135. 135.
    H.K. Christenson, Adhesion and surface energy of mica in air and water. J. Phys. Chem. 97, 12034–12041 (1993)Google Scholar
  136. 136.
    A. Round, M. Miles, Exploring the consequences of attractive and repulsive interaction regimes in tapping mode atomic force microscopy of DNA. Nanotechnology 15, S176–183 (2004)Google Scholar
  137. 137.
    R.H. Abou-Saleh et al., Nanoscale probing reveals that reduced stiffness of clots from fibrinogen lacking 42 N-terminal Bβ-chain residues is due to the formation of abnormal oligomers. Biophys. J. 96, 2415–2427 (2009)Google Scholar
  138. 138.
    C.-W. Yang, I.-S. Hwang, Soft-contact imaging in liquid with frequency-modulation torsion resonance mode atomic force microscopy. Nanotechnology 21, 065710–065716 (2010)Google Scholar
  139. 139.
    B.V. Derjaguin, V. Muller, Y. Toporov, Effect of contact deformations on the adhesion of particles. J. Colloid Interface Sci. 53, 314–326 (1975)Google Scholar
  140. 140.
    T. Tatsuyama-Kurk, Visualising the surface of filamentous cyanobacteria with atomic force microscopy. Ph.D. thesis, University of Leeds, 2010Google Scholar
  141. 141.
    R.M. Brydson et al., Nanoscale Science and Technology (Wiley, Chichester, 2005)Google Scholar
  142. 142.
    L. Zhang, T.J. Webster, Nanotechnology and nanomaterials: Promises for improved tissue regeneration. Nano Today 4, 66–80 (2009)Google Scholar
  143. 143.
    F.C. Simmel, W.U. Dittmer, DNA nanodevices. Small 1, 284–299 (2005)Google Scholar
  144. 144.
    R. Feynman, The Pleasure of Finding Things Out, New edn. (Penguin Books Ltd, London, 2001)Google Scholar
  145. 145.
    R. Feynman, R. Leighton, M. Sands, The Feynman Lectures on Physics, 2nd edn. Vol. 1 (Addison Wesley, Boston, 2005)Google Scholar
  146. 146.
    D.J. Müller, A. Engel, The height of biomolecules measured with the atomic force microscope depends on electrostatic interactions. Biophys. J. 73, 1633–1644 (1997)Google Scholar
  147. 147.
    F. Moreno-Herrero, J. Colchero, A. Baro, DNA height in atomic force microscopy. Ultramicroscopy 96, 167–174 (2003)Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Sergio Santos
    • 1
  • Neil H. Thomson
    • 1
  1. 1.Molecular and Nanoscale Physics Group, School of Physics and AstronomyUniversity of LeedsLeedsUK

Personalised recommendations