Nanovisualization of Proteins in Action Using High-Speed AFM

Part of the Biophysics for the Life Sciences book series (BIOPHYS, volume 2)


Direct and real-time visualization of single protein molecules is a powerful approach to understanding how they operate to function. Recent advances in high-speed atomic force microscopy (HS-AFM) provide a new opportunity to visualize dynamic events of label-free proteins in action under physiological conditions, at subsecond temporal and submolecular resolution. In this chapter, we first overview HS-AFM techniques used for fast and low-invasive imaging of proteins. Then, we highlight recent imaging studies on myosin V walking on an actin filament, rotary catalysis of rotorless F1-ATPase, and processive run of cellulase hydrolyzing cellulose fibers.


Atomic Force Microscopy Actin Filament Crystalline Cellulose Cellulose Surface Highly Order Pyrolytic Graphite 
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.



The authors thank Daisuke Yamamoto, Hayato Yamashita, Mikihiro Shibata, Ryota Iino, Hiroyuki Noji, Kiyohiko Igarashi, Hideki Kandori, and many present and past students in Ando lab for collaborations or contributions to the work described in this chapter. Long-term financial support by NEDO, JST (CREST project), JSPS (Grant-in-Aid for Basic Research (S)), Knowledge Cluster Initiative, and the Mitsubishi Foundation is gratefully acknowledged.


  1. Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondri. Nature 370:621–628PubMedGoogle Scholar
  2. Abuja PM, Pilz I, Claeyssens M, Tomme P (1988a) Domain structure of cellobiohydrolase II as studied by small angle X-ray scattering: close resemblance to cellobiohydrolase I. Biochem Biophys Res Commun 156:180–185PubMedGoogle Scholar
  3. Abuja PM, Schmuck M, Pilz I, Tomme P, Claeyssens M, Esterbauer H (1988b) Structural and functional domains of cellobiohydrolase I from trichoderma reesei. Eur Biophys J 15:339–342Google Scholar
  4. Abuja PM, Pilz I, Tomme P, Claeyssens M (1989) Structural changes in cellobiohydrolase I upon binding of a macromolecular ligand as evident by SAXS investigations. Biochem Biophys Res Commun 165:615–623PubMedGoogle Scholar
  5. Adachi K, Oiwa K, Nishizaka T, Furuike S, Noji H, Itoh H, Yoshida M, Kinosita K (2007) Coupling of rotation and catalysis in F1-ATPase revealed by single-molecule imaging and manipulation. Cell 130:309–321PubMedGoogle Scholar
  6. Aloise P, Kagawa Y, Coleman PS (1991) Comparative Mg2+-dependent sequential covalent binding stoichiometries of 3’-O-(4-benzoyl)benzoyl adenosine 5'-diphosphate of MF1, TF1, and the alpha 3 beta 3 core complex of TF1. The binding change motif is independent of the F1 gamma delta epsilon sub. J Biol Chem 266:10368–10376PubMedGoogle Scholar
  7. Ando T (2012) High-speed atomic force microscopy coming of age. Nanotechnology 23:062001 (27 pp)PubMedGoogle Scholar
  8. Ando T, Kodera N, Maruyama D, Takai E, Saito K, Toda A (2002) A high-speed atomic force microscope for studying biological macromolecules in action. Jpn J Appl Phys 41:4851–4856Google Scholar
  9. Ando T, Kodera N, Takai E, Maruyama D, Saito K, Toda A (2001) A high-speed atomic force microscope for studying biological macromolecules in action. Proc Natl Acad Sci USA 98:12468–12472PubMedGoogle Scholar
  10. Ando T, Kodera N, Uchihashi T, Miyagi A, Nakakita R, Namashita H, Matada K (2005) High-speed atomic force microscopy for capturing dynamic behavior of protein molecules at work. e-J Surf Sci Nanotech 3:384–392Google Scholar
  11. Ando T, Uchihashi T, Fukuma T (2008) High-speed atomic force microscopy for nano-visualization of dynamic biomolecular processes. Prog Surf Sci 83:337–437Google Scholar
  12. Bezanilla M, Drake B, Nudler E, Kashlev M, Hansma PK, Hansma HG (1994) Motion and enzymatic degradation of DNA in the atomic force microscope. Biophys J 67:2454–2459PubMedGoogle Scholar
  13. Binnig G (1992) Force microscopy. Ultramicroscopy 42–44:7–15Google Scholar
  14. Binnig G, Quate C, Gerber C (1986) Phys Rev Lett 56:930–933PubMedGoogle Scholar
  15. Boisset C, Fraschini C, Schulein M, Henrissat B, Chanzy H (2000) Imaging the enzymatic digestion of bacterial cellulose ribbons reveals the endo character of the cellobiohydrolase Cel6A from humicola insolens and its mode of synergy with cellobiohydrolase Cel7A. Appl Environ Microbiol 66:1444–1452PubMedGoogle Scholar
  16. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781PubMedGoogle Scholar
  17. Boyer PD (1993) The binding change mechanism for ATP synthase–some probabilities and possibilities. Biochim Biophys Acta 1140:215–250PubMedGoogle Scholar
  18. Boyer PD (1997) The ATP synthase–a splendid molecular machine. Annu Rev Biochem 66:717–749PubMedGoogle Scholar
  19. Burgess S, Walker M, Wang F, Sellers JR, White HD, Knight PJ, Trinick J (2002) The prepower stroke conformation of myosin V. J Cell Biol 159:983–991PubMedGoogle Scholar
  20. Capaldi RA (1998) Unisite Catalysis without Rotation of the γ - ε Domain in Escherichia coli F 1 -ATPase. Biochemistry 273:15940–15945Google Scholar
  21. Casuso I, Kodera N, Le Grimellec C, Ando T, Scheuring S (2009) High-resolution high-speed contact mode atomic force microscopy movies of purple membrane. Biophys J 97:1354–1361PubMedGoogle Scholar
  22. Casuso I, Sens P, Rico F, Scheuring S (2010) Experimental evidence for membrane-mediated protein-protein interaction. Biophys J 99:L47–L49PubMedGoogle Scholar
  23. Chanzy H, Henrissat B (1985) Unidirectional degradation of Valonia cellulose microcrystals subjected to cellulase action. FEBS Lett 184:285–288Google Scholar
  24. Crampton N, Yokokawa M, Dryden DTF, Edwardson JM, Rao DN, Takeyasu K, Yoshimura SH, Henderson RM (2007) Fast-scan atomic force microscopy reveals that the type III restriction enzyme EcoP15I is capable of DNA translocation and looping. Proc Natl Acad Sci USA 104:12755–12760PubMedGoogle Scholar
  25. Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859PubMedGoogle Scholar
  26. Divne C, Stahlberg J, Reinikainen T, Ruohonen L, Pettersson G, Knowles J, Teeri T, Jones T (1994) The three-dimensional crystal structure of the catalytic core of cellobiohydrolase I from Trichoderma reesei. Science 265:524–528PubMedGoogle Scholar
  27. Divne C, Ståhlberg J, Teeri TT, Jones TA (1998) High-resolution crystal structures reveal how a cellulose chain is bound in the 50 A long tunnel of cellobiohydrolase I from Trichoderma reesei. J Mol Biol 275:309–325PubMedGoogle Scholar
  28. Drake B, Prater C, Weisenhorn A, Gould S, Albrecht T, Quate C, Cannell D, Hansma H, Hansma P (1989) Imaging crystals, polymers, and processes in water with the atomic force microscope. Science 243:1586–1589PubMedGoogle Scholar
  29. Endo M, Sugiyama H (2009) Three-dimensional DNA nanostructures constructed by folding of multiple rectangles. Nucleic Acids Symp Ser 53:81–82Google Scholar
  30. Endo M, Hidaka K, Kato T, Namba K, Sugiyama H (2009) DNA prism structures constructed by folding of multiple rectangular arms. J Am Chem Soc 131:15570–15571PubMedGoogle Scholar
  31. Endo M, Hidaka K, Sugiyama H (2011) Direct AFM observation of an opening event of a DNA cuboid constructed via a prism structure. Org Biomol Chem 9:2075–2077PubMedGoogle Scholar
  32. Endo M, Katsuda Y, Hidaka K, Sugiyama H (2010a) Regulation of DNA methylation using different tensions of double strands constructed in a defined DNA nanostructure. J Am Chem Soc 132:1592–1597PubMedGoogle Scholar
  33. Endo M, Sugita T, Katsuda Y, Hidaka K, Sugiyama H (2010b) Programmed-assembly system using DNA jigsaw pieces. Chem Eur J 16:5362–5368PubMedGoogle Scholar
  34. Eriksson T, Karlsson J, Tjerneld F (2002) A model explaining declining rate in hydrolysis of lignocellulose substrates with cellobiohydrolase I (Cel7A) and endoglucanase I (Cel7B) of Trichoderma reesei. Appl Biochem Biotechnol 101:41–60PubMedGoogle Scholar
  35. Fantner GE, Barbero RJ, Gray DS, Belcher AM (2010) Kinetics of antimicrobial peptide activity measured on individual bacterial cells using high-speed atomic force microscopy. Nat Nanotechnol 5:280–285PubMedGoogle Scholar
  36. Forgacs E, Cartwright S, Sakamoto T, Sellers JR, Corrie JET, Webb MR, White HD (2008) Kinetics of ADP dissociation from the trail and lead heads of actomyosin V following the power stroke. J Biol Chem 283:766–773PubMedGoogle Scholar
  37. Forkey JN, Quinlan ME, Shaw MA, Corrie JET, Goldman YE (2003) Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization. Nature 422:399–404PubMedGoogle Scholar
  38. Fukuma T, Okazaki Y, Kodera N, Uchihashi T, Ando T (2008) High resonance frequency force microscope scanner using inertia balance support. Appl Phys Lett 92:243119 (3 pp)Google Scholar
  39. Furuike S, Hossain MD, Maki Y, Adachi K, Suzuki T, Kohori A, Itoh H, Yoshida M, Kinosita K (2008) Axle-less F1-ATPase rotates in the correct direction. Science 319:955–958PubMedGoogle Scholar
  40. Geeves MA, Holmes KC (1999) Structura mechanism of muscle contraction. Annu Rev Biochem 68:687–728PubMedGoogle Scholar
  41. Gilmore JL, Suzuki Y, Tamulaitis G, Siksnys V, Takeyasu K, Lyubchenko YL (2009) Single-molecule dynamics of the DNA-EcoRII protein complexes revealed with high-speed atomic force microscopy. Biochemistry 48:10492–10498PubMedGoogle Scholar
  42. Giocondi M-C, Yamamoto D, Lesniewska E, Milhiet P-E, Ando T, Le Grimellec C (2010) Surface topography of membrane domains. Biochim Biophys Acta—Biomembranes 1798:703–718Google Scholar
  43. Goldman YE (1987) Kinetics of the actomyosin ATPase in muscle fibers. Annu Rev Physiol 49:637–654PubMedGoogle Scholar
  44. Guthold M, Bezanilla M, Erie DA, Jenkins B, Hansma HG, Bustamante C (1994) Following the assembly of RNA polymerase-DNA complexes in aqueous solutions with the scanning force microscope. Proc Natl Acad Sci USA 91:12927–12931PubMedGoogle Scholar
  45. Häberle W, Hörber JKH, Ohnesorge F, Smith DPE, Binnig G (1992) In situ investigations of single living cells infected by viruses. Ultramicroscopy 42–44:1161–1167PubMedGoogle Scholar
  46. Hansma HG, Bezanilla M, Zenhausern F, Adrian M, Sinsheimer RL (1993) Atomic force microscopy of DNA in aqueous solutions. Nucleic Acids Res 21:505–512PubMedGoogle Scholar
  47. Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316PubMedGoogle Scholar
  48. Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:781–788Google Scholar
  49. Henrissat B, Driguez H, Viet C, Schülein M (1985) Synergism of cellulases from Trichoderma reesei in the degradation of cellulose. Nat Biotechnol 3:722–726Google Scholar
  50. Henrissat B, Teeri TT, Warren RA (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett 425:352–354PubMedGoogle Scholar
  51. Hon DNS (1994) Cellulose: a random walk along its historical path. Cellulose 1:1–25Google Scholar
  52. Hossain MD, Furuike S, Maki Y, Adachi K, Ali MY, Huq M, Itoh H, Yoshida M, Kinosita K (2006) The rotor tip inside a bearing of a thermophilic F1-ATPase is dispensable for torque generation. Biophys J 90:4195–4203PubMedGoogle Scholar
  53. Hossain MD, Furuike S, Maki Y, Adachi K, Suzuki T, Kohori A, Itoh H, Yoshida M, Kinosita K (2008) Neither helix in the coiled coil region of the axle of F1-ATPase plays a significant role in torque production. Biophys J 95:4837–4844PubMedGoogle Scholar
  54. Hua W, Chung J, Gelles J (2002) Distinguishing inchworm and hand-over-hand processive kinesin movement by neck rotation measurements. Science 295:844–848PubMedGoogle Scholar
  55. Huxley HE (1969) The mechanism of muscular contraction. Science 164:1356–1366PubMedGoogle Scholar
  56. Igarashi K, Koivula A, Wada M, Kimura S, Penttilä M, Samejima M (2009) High speed atomic force microscopy visualizes processive movement of Trichoderma reesei cellobiohydrolase I on crystalline cellulose. J Biol Chem 284:36186–36190PubMedGoogle Scholar
  57. Igarashi K, Uchihashi T, Koivula A, Wada M, Kimura S, Okamoto T, Penttila M, Ando T, Samejima M (2011) Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333:1279–1282PubMedGoogle Scholar
  58. Igarashi K, Wada M, Samejima M (2007) Activation of crystalline cellulose to cellulose III(I) results in efficient hydrolysis by cellobiohydrolase. FEBS J 274:1785–1792PubMedGoogle Scholar
  59. Iko Y, Tabata KV, Sakakihara S, Nakashima T, Noji H (2009) Acceleration of the ATP-binding rate of F1-ATPase by forcible forward rotation. FEBS Lett 583:3187–3191PubMedGoogle Scholar
  60. Imai T, Boisset C, Samejima M, Igarashi K, Sugiyama J (1998) Unidirectional processive action of cellobiohydrolase Cel7A on Valonia cellulose microcrystals. FEBS Lett 432:113–116PubMedGoogle Scholar
  61. Inoue S, Uchihashi T, Yamamoto D, Ando T (2011) Direct observation of surfactant aggregate behavior on a mica surface using high-speed atomic force microscopy. Chem Commun 47:4974–4976Google Scholar
  62. Itoh H, Takahashi A, Adachi K, Noji H, Yasuda R, Yoshida M, Kinosita K (2004) Mechanically driven ATP synthesis by F1-ATPase. J Jpn Biochem Soc 427:42–45Google Scholar
  63. Johansson G, Stahlberg J, Lindeberg G, Engstrom A, Pettersson G (1989) Isolated fungal cellulose terminal domains and a synthetic minimum analogue bind to cellulose. FEBS Lett 243:389–393Google Scholar
  64. Joo C, Balci H, Ishitsuka Y, Buranachai C, Ha T (2008) Advances in single-molecule fluorescence methods for molecular biology. Annu Rev Biochem 77:51–76PubMedGoogle Scholar
  65. Kaibara C, Matsui T, Hisabori T, Yoshida M (1996) Structural asymmetry of F1-ATPase caused by the gamma subunit generates a high affinity nucleotide binding site. J Biol Chem 271:2433–2438PubMedGoogle Scholar
  66. Kasas S, Thomson NH, Smith BL, Hansma HG, Zhu X, Guthold M, Bustamante C, Kool ET, Kashlev M, Hansma PK (1997) Escherichia coli RNA polymerase activity observed using atomic force microscopy. Biochemistry 36:461–468PubMedGoogle Scholar
  67. Kitazawa M, Shiotani K, Toda A (2003) Batch fabrication of sharpened silicon nitride tips. Jpn J Appl Phys 42:4844–4847Google Scholar
  68. Kodera N, Sakashita M, Ando T (2006) Dynamic proportional-integral-differential controller for high-speed atomic force microscopy. Rev Sci Instrum 77:083704 (7 pp)Google Scholar
  69. Kodera N, Yamamoto D, Ishikawa R, Ando T (2010) Video imaging of walking myosin V by high-speed atomic force microscopy. Nature 468:72–76PubMedGoogle Scholar
  70. Kodera N, Yamashita H, Ando T (2005) Active damping of the scanner for high-speed atomic force microscopy. Rev Sci Instrum 76:053708 (5 pp)Google Scholar
  71. Kokavecz J, Tóth Z, Horváth ZL, Heszler P, Mechler Á (2006) Novel amplitude and frequency demodulation algorithm for a virtual dynamic atomic force microscope. Nanotechnology 17:S173–S177PubMedGoogle Scholar
  72. De La Cruz EM, Wells AL, Rosenfeld SS, Ostap EM, Sweeney HL (1999) The kinetic mechanism of myosin V. Proc Natl Acad Sci USA 96:13726–13731Google Scholar
  73. Lin H, Clegg DO, Lal R (1999) Imaging real-time proteolysis of single collagen I molecules with an atomic force microscope. Biochemistry 38:9956–9963PubMedGoogle Scholar
  74. Linder M (1997) The roles and function of cellulose-binding domains. J Biotechnol 57:15–28Google Scholar
  75. Lindsay SM, Nagahara LA, Thundat T, Knipping U, Rill RL, Drake B, Prater CB, Weisenhorn AL, Gould SA, Hansma PK (1989) STM and AFM images of nucleosome DNA under water. J Biomol Struct Dyn 7:279–287PubMedGoogle Scholar
  76. Matsui T, Yoshida M (1995) Expression of the wild-type and the Cys-/Trp-less alpha 3 beta 3 gamma complex of thermophilic F1-ATPase in Escherichia coli. Biochim Biophys 1231:139–146Google Scholar
  77. Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS, Cheney RE (1999) Myosin-V is a processive actin-based motor. Nature 400:590–593PubMedGoogle Scholar
  78. Menz RI, Walker JE, Leslie AG (2001) Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106:331–341PubMedGoogle Scholar
  79. Milhiet P-E, Yamamoto D, Berthoumieu O, Dosset P, Le Grimellec C, Verdier J-M, Marchal S, Ando T (2010) Deciphering the structure, growth and assembly of amyloid-like fibrils using high-speed atomic force microscopy. PLoS One 5:e13240 (8 pp)PubMedGoogle Scholar
  80. Miyagi A, Tsunaka Y, Uchihashi T, Mayanagi K, Hirose S, Morikawa K, Ando T (2008) Visualization of intrinsically disordered regions of proteins by high-speed atomic force microscopy. Chemphyschem 9:1859–1866PubMedGoogle Scholar
  81. Müller DJ, Büldt G, Engel A (1995) Force-induced conformational change of bacteriorhodopsin. J Mol Biol 249:239–243PubMedGoogle Scholar
  82. Müller DJ, Engel A (1999) Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy. J Mol Biol 285:1347–1351PubMedGoogle Scholar
  83. Nakamoto RK, Ketchum CJ, Al-Shawi MK (1999) Rotational coupling in the F0F1 ATP synthase. Annu Rev Biophys Biomol Struct 28:205–234PubMedGoogle Scholar
  84. Nidetzky B, Steiner W, Hayn M, Claeyssens M (1994) Cellulose hydrolysis by the cellulases from Trichoderma reesei: a new model for synergistic interaction. Biochem J 298:705–710PubMedGoogle Scholar
  85. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose I(alpha) from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125:14300–14306PubMedGoogle Scholar
  86. Noji H, Yasuda R, Yoshida M, Kinosita K (1997) Direct observation of the rotation of F1-ATPase. Nature 386:299–302PubMedGoogle Scholar
  87. Oberleithner H, Schillers H, Wilhelmi M, Butzke D, Danker T (2000) Nuclear pores collapse in response to CO2 imaged with atomic force microscopy. Pflugers Arch Eur J Physiol 439:251–255Google Scholar
  88. Oguchi Y, Mikhailenko SV, Ohki T, Olivares AO, De La Cruz EM, Ishiwata S (2008) Load-dependent ADP binding to myosins V and VI: implications for subunit coordination and function. Proc Natl Acad Sci USA 105:7714–7719PubMedGoogle Scholar
  89. Ohnesorge F, Heckl WM, Häberle W, Pum D, Sara M, Schindler H, Schilcher K, Kiener A, Smith DP, Sleytr UB (1992) Scanning force microscopy studies of the S-layers from Bacillus coagulans E38-66, Bacillus sphaericus CCM2177 and of an antibody binding process. Ultramicroscopy 42–44:1236–1242PubMedGoogle Scholar
  90. Okada T, Tanaka H, Iwane AH, Kitamura K, Ikebe M, Yanagida T (2007) The diffusive search mechanism of processive myosin class-V motor involves directional steps along actin subunits. Biochem Biophys Res Commun 354:379–384PubMedGoogle Scholar
  91. Oke OA, Burgess SA, Forgacs E, Knight PJ, Sakamoto T, Sellers JR, White H, Trinick J (2010) Influence of lever structure on myosin 5a walking. Proc Natl Acad Sci USA 107:2509–2514PubMedGoogle Scholar
  92. Peterman EJG, Sosa H, Moerner WE (2004) Single-molecule fluorescence spectroscopy and microscopy of biomolecular motors. Annu Rev Phys Chem 55:79–96PubMedGoogle Scholar
  93. Purcell TJ, Sweeney HL, Spudich JA (2005) A force-dependent state controls the coordination of processive myosin V. Proc Natl Acad Sci USA 102:13873–13878PubMedGoogle Scholar
  94. Putman CAJ, Van Der Werf KO, De Grooth BG, Van Hulst NF, Greve J (1994) Tapping mode atomic force microscopy in liquid. Appl Phys Lett 64:2454–2456Google Scholar
  95. Rajendran A, Endo M, Katsuda Y, Hidaka K, Sugiyama H (2011) Programmed two-dimensional self-assembly of multiple DNA origami jigsaw pieces. ACS Nano 5:665–671PubMedGoogle Scholar
  96. Reverbel-Leroy C, Pages S, Belaich A, Belaich JP, Tardif C (1997) The processive endocellulase CelF, a major component of the Clostridium cellulolyticum cellulosome: purification and characterization of the recombinant form. J Bacteriol 179:46–52PubMedGoogle Scholar
  97. Rondelez Y, Tresset G, Nakashima T, Kato-Yamada Y, Fujita H, Takeuchi S, Noji H (2005) Highly coupled ATP synthesis by F1-ATPase single molecules. Nature 433:773–777PubMedGoogle Scholar
  98. Rosenfeld SS, Sweeney HL (2004) A model of myosin V processivity. J Biol Chem 279:40100–40111PubMedGoogle Scholar
  99. Rouvinen J, Bergfors T, Teeri T, Knowles JK, Jones TA (1990) Three-dimensional structure of cellobiohydrolase II from Trichoderma reesei. Science 249:380–386PubMedGoogle Scholar
  100. Roy R, Hohng S, Ha T (2008) A practical guide to single-molecule FRET. Nat Methods 5:507–516PubMedGoogle Scholar
  101. Ryu DDY, Mandels M (1980) Cellulases: biosynthesis and applications. Enzyme Microb Technol 2:91–102Google Scholar
  102. Sakamoto T, Amitani I, Yokota E, Ando T (2000) Direct observation of processive movement by individual myosin V molecules. Biochem Biophys Res Commun 272:586–590PubMedGoogle Scholar
  103. Sakamoto T, Webb MR, Forgacs E, White HD, Sellers JR (2008) Direct observation of the mechanochemical coupling in myosin Va during processive movement. Nature 455:128–132PubMedGoogle Scholar
  104. Sannohe Y, Endo M, Katsuda Y, Hidaka K, Sugiyama H (2010) Visualization of dynamic conformational switching of the G-quadruplex in a DNA nanostructure. J Am Chem Soc 132:16311–16313PubMedGoogle Scholar
  105. Schabert FA, Engel A (1994) Reproducible acquisition of Escherichia coli porin surface topographs by atomic force microscopy. Biophys J 67:2394–2403PubMedGoogle Scholar
  106. Schäffer TE, Cleveland JP, Ohnesorge F, Walters DA, Hansma PK (1996) Studies of vibrating atomic force microscope cantilevers in liquid. J Appl Phys 80:3622–3627Google Scholar
  107. Sellers JR, Weisman LS (2008) Myosins: a superfamily of molecular motors. In: Coluccio LM (ed) Proteins and cell regulation. Springer, Netherland, pp 289–324Google Scholar
  108. Shao Z, Yang J (1995) Progress in high resolution atomic force microscopy in biology. Q Rev Biophys 28:195–251PubMedGoogle Scholar
  109. Shibata M, Uchihashi T, Yamashita H, Kandori H, Ando T (2011) Structural changes in bacteriorhodopsin in response to alternate illumination observed by high-speed atomic force microscopy. Angew Chem Int Ed 50:4410–4413Google Scholar
  110. Shibata M, Yamashita H, Uchihashi T, Kandori H, Ando T (2010) High-speed atomic force microscopy shows dynamic molecular processes in photoactivated bacteriorhodopsin. Nat Nanotechnol 5:208–212PubMedGoogle Scholar
  111. Shinozaki Y, Sumitomo K, Tsuda M, Koizumi S, Inoue K, Torimitsu K (2009) Direct observation of ATP-induced conformational changes in single P2X4 receptors. PLoS Biol 7:e1000103 (12 pp)PubMedGoogle Scholar
  112. Shirakihara Y, Leslie AG, Abrahams JP, Walker JE, Ueda T, Sekimoto Y, Kambara M, Saika K, Kagawa Y, Yoshida M (1997) The crystal structure of the nucleotide-free alpha 3 beta 3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer. Structure 5:825–836PubMedGoogle Scholar
  113. Ståhlberg J, Johansson G, Pettersson G (1991) A new model for enzymatic hydrolysis of cellulose based on the two-domain structure of cellobiohydrolase I. Bio/Technology 9:286–290Google Scholar
  114. Sugimoto S, Yamanaka K, Nishikori S, Miyagi A, Ando T, Ogura T (2010) AAA+ chaperone ClpX regulates dynamics of prokaryotic cytoskeletal protein FtsZ. J Biol Chem 285:6648–6657PubMedGoogle Scholar
  115. Suzuki Y, Higuchi Y, Hizume K, Yokokawa M, Yoshimura SH, Yoshikawa K, Takeyasu K (2010) Molecular dynamics of DNA and nucleosomes in solution studied by fast-scanning atomic force microscopy. Ultramicroscopy 110:682–688PubMedGoogle Scholar
  116. Teeri TT (1997) Crystalline cellulose degradation: new insight into the function of cellobiohydrolases. Trends Biotechnol 15:160–167Google Scholar
  117. Teeri TT, Koivula A, Linder M, Wohlfahrt G, Divne C, Jones TA (1998) Trichoderma reesei cellobiohydrolases: why so efficient on crystalline cellulose? Biochem Soc Trans 26:173–178PubMedGoogle Scholar
  118. Todd RD, Griesenbeck TA, Douglas MG (1980) The yeast mitochondrial adenosine triphosphatase complex Subunit stoichiometry and physical characterization. J Biol Chem 255:5461–5467PubMedGoogle Scholar
  119. Uchihashi T, Iino R, Ando T, Noji H (2011) High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333:755–758PubMedGoogle Scholar
  120. Veigel C, Schmitz S, Wang F, Sellers JR (2005) Load-dependent kinetics of myosin-V can explain its high processivity. Nat Cell Biol 7:861–869PubMedGoogle Scholar
  121. Vianni MB, Pietrasanta LI, Thompson JB, Chand A, Gebeshuber IC, Kindt JH, Richter M, Hansma HG, Hansma PK (2000) Probing protein-proein interactions in real time. Nature Struct Biol 7:644–647Google Scholar
  122. Wada M, Chanzy H, Nishiyama Y, Langan P (2004) Cellulose III I crystal structure and hydrogen bonding by synchrotron X-ray and neutron fiber diffraction. Macromolecules 37:8548–8555Google Scholar
  123. Walker JE, Fearnley IM, Gay NJ, Gibson BW, Northrop FD, Powell SJ, Runswick MJ, Saraste M, Tybulewicz VL (1985) Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J Mol Biol 184:677–701PubMedGoogle Scholar
  124. Walker ML, Burgess SA, Sellers JR, Wang F, Hammer JA, Trinick J, Knight PJ (2000) Two-headed binding of a processive myosin to F-actin. Nature 405:804–807PubMedGoogle Scholar
  125. Walz T, Tittmann P, Fuchs KH, Müller DJ, Smith BL, Agre P, Gross H, Engel A (1996) Surface topographies at subnanometer-resolution reveal asymmetry and sidedness of aquaporin-1. J Mol Biol 264:907–918PubMedGoogle Scholar
  126. Wang H, Oster G (1998) Energy transduction in the F1 motor of ATP synthase. Nature 396:279–282PubMedGoogle Scholar
  127. Watanabe R, Iino R, Noji H (2010) Phosphate release in F1-ATPase catalytic cycle follows ADP release. Nat Chem Biol 6:814–820PubMedGoogle Scholar
  128. Weisenhorn AL, Hansma PK, Albrecht TR, Quate CF (1989) Forces in atomic force microscopy in air and water. Appl Phys Lett 54:2651 (3 pp)Google Scholar
  129. Wendel M, Lorenz H, Kotthaus JP (1995) Sharpened electron beam deposited tips for high resolution atomic force microscope lithography and imaging. Appl Phys Lett 67:3732 (3 pp)Google Scholar
  130. Wickham SFJ, Endo M, Katsuda Y, Hidaka K, Bath J, Sugiyama H, Turberfield AJ (2011) Direct observation of stepwise movement of a synthetic molecular transporter. Nat Nanotechnol 6:166–169PubMedGoogle Scholar
  131. Wood TM, McCrae SI (1978) The cellulase of Trichoderma koningii purification and properties of some endoglucanase components with special reference to their action on cellulose when acting alone and in synergism with the cellobiohydrolase. Biochem J 171:61–72PubMedGoogle Scholar
  132. Yamamoto D, Nagura N, Omote S, Taniguchi M, Ando T (2009) Streptavidin 2D crystal substrates for visualizing biomolecular processes by atomic force microscopy. Biophys J 97:2358–2367PubMedGoogle Scholar
  133. Yamamoto D, Uchihashi T, Kodera N, Ando T (2008) Anisotropic diffusion of point defects in a two-dimensional crystal of streptavidin observed by high-speed atomic force microscopy. Nanotechnology 19:384009 (9 pp)PubMedGoogle Scholar
  134. Yamamoto D, Uchihashi T, Kodera N, Yamashita H, Nishikori S, Ogura T, Shibata M, Ando T (2010) High-speed atomic force microscopy techniques for observing dynamic biomolecular processes. Methods Enzymol 475:541–564PubMedGoogle Scholar
  135. Yamashita H, Voïtchovsky K, Uchihashi T, Contera SA, Ryan JF, Ando T (2009) Dynamics of bacteriorhodopsin 2D crystal observed by high-speed atomic force microscopy. J Struct Biol 167:153–158PubMedGoogle Scholar
  136. Yanagida T, Ishii Y (eds) (2008) Single molecule dynamics in life science. Wiley, WeinheimGoogle Scholar
  137. Yasuda R, Noji H, Kinosita K, Yoshida M (1998) F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell 93:1117–1124PubMedGoogle Scholar
  138. Yildiz A, Forkey JN, McKinney SA, Ha T, Goldman YE, Selvin PR (2003) Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 300:2061–2065PubMedGoogle Scholar
  139. Yokokawa M, Carnally SM, Henderson RM, Takeyasu K, Edwardson JM (2010) Acid-sensing ion channel (ASIC) 1a undergoes a height transition in response to acidification. FEBS Lett 584:3107–3110PubMedGoogle Scholar
  140. Yokokawa M, Wada C, Ando T, Sakai N, Yagi A, Yoshimura SH, Takeyasu K (2006a) Fast-scanning atomic force microscopy reveals the ATP/ADP-dependent conformational changes of GroEL. EMBO J 25:4567–4576PubMedGoogle Scholar
  141. Yokokawa M, Yoshimura SH, Naito Y, Ando T, Yagi A, Sakai N, Takeyasu K (2006b) Fast-scanning atomic force microscopy reveals the molecular mechanism of DNA cleavage by ApaI endonuclease. IEE Proc Nanobiotechnol 153:60–66PubMedGoogle Scholar
  142. Yoshida M, Allison WS (1990) The ATPase activity of the alpha 3 beta 3 complex of the F1-ATPase of the thermophilic bacterium PS3 is inactivated on modification of tyrosine 307 in a single beta subunit by 7-chloro-4-nitrobenzofurazan. J Biol Chem 265:2483–2487PubMedGoogle Scholar
  143. Zhong Q, Inniss D, Kjoller K, Elings VB (1993) Fractured polymer/silica fiber surface studied by tapping mode atomic force. Surf Sci Lett 290:L688–L692Google Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Takayuki Uchihashi
    • 1
  • Noriyuki Kodera
    • 2
  • Toshio Ando
    • 1
  1. 1.Department of Physics and Bio-AFM Frontier Research CenterKanazawa UniversityKanawazaJapan
  2. 2.Bio-AFM Frontier Research CenterKanazawa UniversityKanawazaJapan

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