Nanomechanics of Single Biomacromolecules

Chapter

Abstract

Single-molecule force spectroscopy has provided tremendous insights into the mechanical characteristics of biomacromolecules including proteins, nucleic acids, and sugars. This review provides the instrumentation framework for single-molecule force spectroscopy using atomic force microscopy and the experimental procedures for determining nanomechanics of biomacromolecules. The characteristic parameters determined by single-molecule force spectroscopy of proteins (unfolding forces, intrinsic unfolding/refolding rates, transition state distances, binding affinities), nucleic acids (elastic modulus, persistence length, overstretching percentages, plateau force levels), and sugars (force spectra) from the past 20 years are tabulated and their applications are discussed.

Keywords

Atomic force microscopy Force spectroscopy Nanomaterials Nanomechanics Protein folding Single molecules 

References

  1. 1.
    Seeman NC (2003) DNA in a material world. Nature 421(6921):427–431Google Scholar
  2. 2.
    Seeman NC (2005) From genes to machines: DNA nanomechanical devices. Trends Biochem Sci 30(3):119–125. doi:10.1016/j.tibs.2005.01.007Google Scholar
  3. 3.
    Seeman NC (2007) An overview of structural DNA nanotechnology. Mol Biotechnol 37(3):246–257. doi:10.1007/s12033-007-0059-4Google Scholar
  4. 4.
    Seeman NC (2010) Nanomaterials based on DNA. Annu Rev Biochem 79:65–87. doi:10.1146/annurev-biochem-060308-102244Google Scholar
  5. 5.
    Seeman NC, Belcher AM (2002) Emulating biology: building nanostructures from the bottom up. Proc Natl Acad Sci USA 99(Suppl 2):6451–6455. doi:10.1073/pnas.221458298Google Scholar
  6. 6.
    Ito Y, Fukusaki E (2004) DNA as a ‘nanomaterial’. J Mol Catal B: Enzym 28(4–6):155–166. doi:10.1016/j.molcatb.2004.01.016Google Scholar
  7. 7.
    Zhang SG (2003) Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 21(10):1171–1178. doi:10.1038/nbt874Google Scholar
  8. 8.
    Gothelf KV, LaBean TH (2005) DNA-programmed assembly of nanostructures. Org Biomol Chem 3(22):4023–4037. doi:10.1039/b510551jGoogle Scholar
  9. 9.
    Davis JT, Spada GP (2007) Supramolecular architectures generated by self-assembly of guanosine derivatives. Chem Soc Rev 36(2):296–313. doi:10.1039/b600282jGoogle Scholar
  10. 10.
    Bath J, Turberfield AJ (2007) DNA nanomachines. Nat Nanotechnol 2(5):275–284. doi:10.1038/nnano.2007.104Google Scholar
  11. 11.
    Aldaye FA, Palmer AL, Sleiman HF (2008) Assembling materials with DNA as the guide. Science 321(5897):1795–1799. doi:10.1126/science.1154533Google Scholar
  12. 12.
    Zhang DY, Seelig G (2011) Dynamic DNA nanotechnology using strand-displacement reactions. Nat Chem 3(2):103–113. doi:10.1038/nchem.957Google Scholar
  13. 13.
    Pinheiro AV, Han D, Shih WM, Yan H (2011) Challenges and opportunities for structural DNA nanotechnology. Nat Nanotechnol 6(12):763–772. doi:10.1038/nnano.2011.187Google Scholar
  14. 14.
    Adleman LM (1994) Molecular computation of solutions to combinatorial problems. Science 266(5187):1021–1024. doi:10.1126/science.7973651Google Scholar
  15. 15.
    Adleman LM (1998) Computing with DNA. Sci Am 279(2):54–61Google Scholar
  16. 16.
    Braich RS, Chelyapov N, Johnson C, Rothemund PWK, Adleman L (2002) Solution of a 20-variable 3-SAT problem on a DNA computer. Science 296(5567):499–502. doi:10.1126/science.1069528Google Scholar
  17. 17.
    Liu QH, Wang LM, Frutos AG, Condon AE, Corn RM, Smith LM (2000) DNA computing on surfaces. Nature 403(6766):175–179Google Scholar
  18. 18.
    Benenson Y, Adar R, Paz-Elizur T, Livneh Z, Shapiro E (2003) DNA molecule provides a computing machine with both data and fuel. Proc Natl Acad Sci USA 100(5):2191–2196. doi:10.1073/pnas.0535624100Google Scholar
  19. 19.
    Smith BL, Schaffer TE, Viani M, Thompson JB, Frederick NA, Kindt J, Belcher A, Stucky GD, Morse DE, Hansma PK (1999) Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399(6738):761–763Google Scholar
  20. 20.
    Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK (2001) Bone indentation recovery time correlates with bond reforming time. Nature 414(6865):773–776Google Scholar
  21. 21.
    Gutsmann T, Fantner GE, Kindt JH, Venturoni M, Danielsen S, Hansma PK (2004) Force spectroscopy of collagen fibers to investigate their mechanical properties and structural organization. Biophys J 86(5):3186–3193. doi:S0006-3495(04)74366-0 [pii], doi:10.1016/S0006-3495(04)74366-0Google Scholar
  22. 22.
    Oroudjev E, Soares J, Arcdiacono S, Thompson JB, Fossey SA, Hansma HG (2002) Segmented nanofibers of spider dragline silk: atomic force microscopy and single-molecule force spectroscopy. Proc Natl Acad Sci USA 99(14):9606. doi:10.1073/pnas.132282899 (Proc Natl Acad Sci USA 99:6460)Google Scholar
  23. 23.
    Oroudjev E, Soares J, Arcdiacono S, Thompson JB, Fossey SA, Hansma HG (2002) Segmented nanofibers of spider dragline silk: atomic force microscopy and single-molecule force spectroscopy. Proc Natl Acad Sci USA 99:6460–6465. doi:10.1073/pnas.082526499Google Scholar
  24. 24.
    Oroudjev EM, Hansma HG (2002) AFM and force spectroscopy of recombinant spider dragline silk protein nanofibers. Biophys J 82(1):41A–42AGoogle Scholar
  25. 25.
    Cao Y, Li H (2007) Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat Mater 6(2):109–114, http://www.nature.com/nmat/journal/v6/n2/suppinfo/nmat1825_S1.html Google Scholar
  26. 26.
    Cao Y, Li H (2008) Engineered elastomeric proteins with dual elasticity can be controlled by a molecular regulator. Nat Nanotechnol 3(8):512–516Google Scholar
  27. 27.
    Li HB, Cao Y (2010) Protein Mechanics: from single molecules to functional biomaterials. Acc Chem Res 43(10):1331–1341. doi:10.1021/ar100057aGoogle Scholar
  28. 28.
    Lv S, Dudek DM, Cao Y, Balamurali MM, Gosline J, Li H (2010) Designed biomaterials to mimic the mechanical properties of muscles. Nature 465(7294):69–73, http://www.nature.com/nmat/journal/v6/n2/suppinfo/nmat1825_S1.html Google Scholar
  29. 29.
    Kim M, Wang C-C, Benedetti F, Rabbi M, Bennett V, Marszalek PE (2011) Nanomechanics of Streptavidin hubs for molecular materials. Adv Mater 23(47):5684–5688. doi:10.1002/adma.201103316Google Scholar
  30. 30.
    Robyt JF (1998) Essentials of carbohydrate chemistry. Springer-Verlag, New York, p 163Google Scholar
  31. 31.
    Rao VSR, Qasba PK, Balaji PV, Chandrasekaran R (1998) Conformation of carbohydrates. Harwood Academic Publishers, The NetherlandsGoogle Scholar
  32. 32.
    Bustamante C, Bryant Z, Smith SB (2003) Ten years of tension: single-molecule DNA mechanics. Nature 421(6921):423–427Google Scholar
  33. 33.
    Bao G, Suresh S (2003) Cell and molecular mechanics of biological materials. Nat Mater 2(11):715–725. doi:10.1038/nmat1001Google Scholar
  34. 34.
    Bennett V, Baines AJ (2001) Spectrin and Ankyrin-based pathways: Metazoan inventions for integrating cells Into tissues. Physiol Rev 81(3):1353–1392Google Scholar
  35. 35.
    Benoit M, Gaub HE (2002) Measuring cell adhesion forces with the atomic force microscope at the molecular level. Cells Tissues Organs 172(3):174–189Google Scholar
  36. 36.
    Deguchi S, Ohashi T, Sato M (2006) Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells. J Biomech 39(14):2603–2610Google Scholar
  37. 37.
    del Rio A, Perez-Jimenez R, Liu RC, Roca-Cusachs P, Fernandez JM, Sheetz MP (2009) Stretching single talin rod molecules activates vinculin binding. Science 323(5914):638–641. doi:10.1126/science.1162912Google Scholar
  38. 38.
    Emerson RJ IV, Camesano TA (2004) Nanoscale investigation of pathogenic microbial adhesion to a biomaterial. Appl Environ Microbiol 70(10):6012–6022. doi:10.1128/aem.70.10.6012-6022.2004Google Scholar
  39. 39.
    Evans E (2001) Probing the relation between force – Lifetime – and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct 30:105–128. doi:10.1146/annurev.biophys.30.1.105Google Scholar
  40. 40.
    Evans E, Ritchie K (1997) Dynamic strength of molecular adhesion bonds. Biophys J 72(4):1541–1555Google Scholar
  41. 41.
    Evans E, Ritchie K, Merkel R (1995) Sensitive force technique to probe molecular adhesion and structural linkages at biological interfaces. Biophys J 68(6):2580–2587Google Scholar
  42. 42.
    Evans EA, Calderwood DA (2007) Forces and bond dynamics in cell adhesion. Science 316(5828):1148–1153. doi:10.1126/science.1137592Google Scholar
  43. 43.
    Florin E, Moy V, Gaub H (1994) Adhesion forces between individual ligand-receptor pairs. Science 264(5157):415–417. doi:10.1126/science.8153628Google Scholar
  44. 44.
    Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, Schwartz MA (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466(7303):263–266. doi:http://www.nature.com/nature/journal/v466/n7303/abs/nature09198.html#supplementary-information Google Scholar
  45. 45.
    Hanley W, McCarty O, Jadhav S, Tseng Y, Wirtz D, Konstantopoulos K (2003) Single molecule characterization of P-selectin/ligand binding. J Biol Chem 278(12):10556–10561Google Scholar
  46. 46.
    Helenius J, Heisenberg CP, Gaub HE, Muller DJ (2008) Single-cell force spectroscopy. J Cell Sci 121(11):1785–1791. doi:10.1242/jcs.030999Google Scholar
  47. 47.
    Kienberger F, Ebner A, Gruber HJ, Hinterdorfer P (2006) Molecular recognition imaging and force spectroscopy of single biomolecules. Acc Chem Res 39(1):29–36. doi:10.1021/ar050084mGoogle Scholar
  48. 48.
    Krammer A, Craig D, Thomas WE, Schulten K, Vogel V (2002) A structural model for force regulated integrin binding to fibronectin’s RGD-synergy site. Matrix Biol 21(2):139–147Google Scholar
  49. 49.
    Krammer A, Lu H, Isralewitz B, Schulten K, Vogel V (1999) Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc Natl Acad Sci USA 96(4):1351–1356Google Scholar
  50. 50.
    Leckband D, Prakasam A (2006) Mechanism and dynamics of cadherin adhesion. Ann Rev Biomed Eng 8(1):259–287, 10.1146/annurev.bioeng.8.061505.095753Google Scholar
  51. 51.
    Leckband D, Sivasankar S (2012) Cadherin recognition and adhesion. Curr Opin Cell Biol 24(5):620–627. doi:10.1016/j.ceb.2012.05.014Google Scholar
  52. 52.
    Leckband D, Sivasankar S (2012) Biophysics of cadherin adhesion. In: Harris T (ed) Adherens junctions: from molecular mechanisms to tissue development and disease, vol 60, Subcellular biochemistry. Springer, Netherlands, pp 63–88. doi:10.1007/978-94-007-4186-7_4Google Scholar
  53. 53.
    Lee H, Scherer NF, Messersmith PB (2006) Single-molecule mechanics of mussel adhesion. PNAS 103(35):12999–13003. doi:10.1073/pnas.0605552103Google Scholar
  54. 54.
    Li F, Redick SD, Erickson HP, Moy VT (2003) Force measurements of the α5β1 integrin–fibronectin interaction. Biophys J 84(2):1252–1262. doi:10.1016/s0006-3495(03)74940-6Google Scholar
  55. 55.
    Litvinov RI, Shuman H, Bennett JS, Weisel JW (2002) Binding strength and activation state of single fibrinogen-integrin pairs on living cells. Proc Natl Acad Sci 99(11):7426–7431. doi:10.1073/pnas.112194999Google Scholar
  56. 56.
    Liu W, Montana V, Parpura V, Mohideen U (2009) Single molecule measurements of interaction free energies between the proteins within binary and ternary SNARE complexes. J Nanoneuroscience 1(2):120–129. doi:10.1166/jns.2009.1001Google Scholar
  57. 57.
    Liu Y, Pinzón-Arango PA, Gallardo-Moreno AM, Camesano TA (2010) Direct adhesion force measurements between E. coli and human uroepithelial cells in cranberry juice cocktail. Mol Nutr Food Res 54(12):1744–1752. doi:10.1002/mnfr.200900535Google Scholar
  58. 58.
    Liu Y, Strauss J, Camesano TA (2008) Adhesion forces between Staphylococcus epidermidis and surfaces bearing self-assembled monolayers in the presence of model proteins. Biomaterials 29(33):4374–4382. doi:10.1016/j.biomaterials.2008.07.044Google Scholar
  59. 59.
    Ludwig M, Moy VT, Rief M, Florin EL, Gaub HE (1994) Characterization of the adhesion force between avidin-functionalized Afm tips and biotinylated agarose beads. Microscop Microanal Microstruct 5(4–6):321–328Google Scholar
  60. 60.
    Marshall BT, Long M, Piper JW, Yago T, McEver RP, Zhu C (2003) Direct observation of catch bonds involving cell-adhesion molecules. Nature 423(6936):190–193Google Scholar
  61. 61.
    Ng SP, Billings KS, Ohashi T, Allen MD, Best RB, Randles LG, Erickson HP, Clarke J (2007) Designing an extracellular matrix protein with enhanced mechanical stability. Proc Natl Acad Sci USA 104(23):9633–9637. doi:10.1073/pnas.0609901104Google Scholar
  62. 62.
    Rakshit S, Zhang Y, Manibog K, Shafraz O, Sivasankar S (2012) Ideal, catch, and slip bonds in cadherin adhesion. Proc Natl Acad Sci 109(46):18815–18820. doi:10.1073/pnas.1208349109Google Scholar
  63. 63.
    Rico F, Chu C, Abdulreda MH, Qin Y, Moy VT (2010) Temperature modulation of integrin-mediated cell adhesion. Biophys J 99(5):1387–1396. doi:10.1016/j.bpj.2010.06.037Google Scholar
  64. 64.
    Rico F, Chu C, Moy VT (2011) Force-clamp measurements of receptor–ligand interactions atomic force microscopy in biomedical research. In: Braga PC, Ricci D (eds) Methods in molecular biology, vol 736. Humana Press, New York, pp 331–353. doi:10.1007/978-1-61779-105-5_20Google Scholar
  65. 65.
    Rief M, Pascual J, Saraste M, Gaub HE (1999) Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J Mol Biol 286(2):553–561Google Scholar
  66. 66.
    Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV (2002) Bacterial adhesion to target cells enhanced by shear force. Cell 109(7):913–923Google Scholar
  67. 67.
    Thomas WE, Vogel V, Sokurenko E (2008) Biophysics of catch bonds. Annu Rev Biophys 37(1):399–416. doi:10.1146/annurev.biophys.37.032807.125804Google Scholar
  68. 68.
    van Roy F, Berx G (2008) The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65(23):3756–3788. doi:10.1007/s00018-008-8281-1Google Scholar
  69. 69.
    Vogel V (2006) Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu Rev Biophys Biomol Struct 35:459–488. doi:10.1146/annurev.biophys.35.040405.102013Google Scholar
  70. 70.
    Wojcikiewicz EP, Abdulreda MH, Zhang X, Moy VT (2006) Force spectroscopy of LFA-1 and its ligands, ICAM-1 and ICAM-2. Biomacromolecules 7(11):3188–3195. doi:10.1021/bm060559cGoogle Scholar
  71. 71.
    Erickson HP (1994) Reversible unfolding of fibronectin type-III and immunoglobulin domains provides the structural basis for stretch and elasticity of titin and fibronectin. Proc Natl Acad Sci USA 91:10114–10118Google Scholar
  72. 72.
    Erickson HP (1997) Stretching single protein molecules: titin is a weird spring. Science 276(5315):1090–1092. doi:10.1126/science.276.5315.1090Google Scholar
  73. 73.
    Rief M, Oesterhelt F, Heymann B, Gaub HE (1997) Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 275(5304):1295–1297. doi:10.1126/science.275.5304.1295Google Scholar
  74. 74.
    Kellermayer MSZ, Smith SB, Granzier HL, Bustamante C (1997) Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276(5315):1112–1116Google Scholar
  75. 75.
    Li HB, Linke WA, Oberhauser AF, Carrion-Vazquez M, Kerkviliet JG, Lu H, Marszalek PE, Fernandez JM (2002) Reverse engineering of the giant muscle protein titin. Nature 418(6901):998–1002Google Scholar
  76. 76.
    Tskhovrebova L, Trinick J, Sleep JA, Simmons RM (1997) Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387(6630):308–312Google Scholar
  77. 77.
    Davies GJ, Mackenzie L, Varrot A, Dauter M, Brzozowski AM, Schülein M, Withers SG (1998) Snapshots along an enzymatic reaction coordinate: analysis of a retaining β-glycoside hydrolase. Biochemistry 37(34):11707–11713. doi:10.1021/bi981315iGoogle Scholar
  78. 78.
    Kim IL, Mauck RL, Burdick JA (2011) Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 32(34):8771–8782. doi:10.1016/j.biomaterials.2011.08.073Google Scholar
  79. 79.
    Hills BA (2000) Boundary lubrication in vivo. Proc Inst Mech Eng H 214(1):83–94. doi:10.1243/0954411001535264Google Scholar
  80. 80.
    Hui AY, McCarty WJ, Masuda K, Firestein GS, Sah RL (2012) A systems biology approach to synovial joint lubrication in health, injury, and disease. Wiley Interdiscip Rev Syst Biol Med 4(1):15–37. doi:10.1002/wsbm.157Google Scholar
  81. 81.
    Coles JM, Chang DP, Zauscher S (2010) Molecular mechanisms of aqueous boundary lubrication by mucinous glycoproteins. Curr Opin Colloid Interface Sci 15(6):406–416. doi:10.1016/j.cocis.2010.07.002Google Scholar
  82. 82.
    Fisher TE, Marszalek PE, Fernandez JM (2000) Stretching single molecules into novel conformations using the atomic force microscope. Nat Struct Mol Biol 7(9):719–724Google Scholar
  83. 83.
    Marszalek PE, Dufrene YF (2012) Stretching single polysaccharides and proteins using atomic force microscopy. Chem Soc Rev 41(9):3523–3534. doi:10.1039/c2cs15329gGoogle Scholar
  84. 84.
    Puchner EM, Gaub HE (2009) Force and function: probing proteins with AFM-based force spectroscopy. Curr Opin Struct Biol 19(5):605–614. doi:S0959-440X(09)00135-3 [pii], doi:10.1016/j.sbi.2009.09.005Google Scholar
  85. 85.
    Dufrene YF, Evans E, Engel A, Helenius J, Gaub HE, Muller DJ (2011) Five challenges to bringing single-molecule force spectroscopy into living cells. Nat Meth 8(2):123–127Google Scholar
  86. 86.
    Muller DJ, Dufrene YF (2008) Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat Nanotechnol 3(5):261–269. doi:10.1038/nnano.2008.100Google Scholar
  87. 87.
    Muller DJ, Helenius J, Alsteens D, Dufrene YF (2009) Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5(6):383–390. doi:10.1038/nchembio.181Google Scholar
  88. 88.
    Hansma PK (2006) Molecular mechanics of single molecules. Structure 14(3):390–391Google Scholar
  89. 89.
    Viani MB, Schaffer TE, Paloczi GT, Pietrasanta LI, Smith BL, Thompson JB, Richter M, Rief M, Gaub HE, Plaxco KW, Cleland AN, Hansma HG, Hansma PK (1999) Fast imaging and fast force spectroscopy of single biopolymers with a new atomic force microscope designed for small cantilevers. Rev Sci Instrum 70(11):4300–4303Google Scholar
  90. 90.
    Rabbi M, Marszalek P (2008) Probing polysaccharide and protein mechanics by atomic force microscopy. In: Selvin PR, Ha T (eds) Single-molecule techniques: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 371–394Google Scholar
  91. 91.
    Flory PJ (1953) Principles of polymer chemistry. Cornell University Press, IthacaGoogle Scholar
  92. 92.
    Flory PJ (1989) Statistical Mechanics of Chain Molecules. Hanser Publishers, New YorkGoogle Scholar
  93. 93.
    Bustamante C, Marko JF, Siggia ED, Smith S (1994) Entropic elasticity of lambda-phage dna. Science 265(5178):1599–1600Google Scholar
  94. 94.
    Smith SB, Finzi L, Bustamante C (1992) Direct mechanical measurements of the elasticity of single DNA-molecules by using magnetic beads. Science 258(5085):1122–1126Google Scholar
  95. 95.
    Bustamante C (1994) Entropic elasticity of [lambda]-phage DNA. Science 265:1599–1600Google Scholar
  96. 96.
    Smith SB, Cui YJ, Bustamante C (1996) Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271(5250):795–799Google Scholar
  97. 97.
    Marszalek PE, Lu H, Li HB, Carrion-Vazquez M, Oberhauser AF, Schulten K, Fernandez JM (1999) Mechanical unfolding intermediates in titin modules. Nature 402(6757):100–103Google Scholar
  98. 98.
    Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM (1998) Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature 396(6712):661–664Google Scholar
  99. 99.
    Strick TR, Dessinges MN, Charvin G, Dekker NH, Allemand JF, Bensimon D, Croquette V (2003) Stretching of macromolecules and proteins. Rep Prog Phys 66(1):1–45Google Scholar
  100. 100.
    Frentrup H, Allen MS (2011) Error in dynamic spring constant calibration of atomic force microscope probes due to nonuniform cantilevers. Nanotechnology 22(29):295703Google Scholar
  101. 101.
    Burnham N, Chen X, Hodges C, Matei G, Thoreson E, Roberts C, Davies M, Tendler S (2003) Comparison of calibration methods for atomic-force microscopy cantilevers. Nanotechnology 14(1):1Google Scholar
  102. 102.
    Binnig G, Quate CF, Gerber C (1986) Atomic force microscope. Phys Rev Lett 56(9):930–933Google Scholar
  103. 103.
    Rugar D, Hansma P (1990) Atomic force microscopy. Physics Today 43(10):23–30Google Scholar
  104. 104.
    Binnig G, Rohrer H, Gerber C, Weibel E (1982) Tunneling through a controllable vacuum gap. Appl Phys Lett 40(2):178–180Google Scholar
  105. 105.
    Binnig G, Rohrer H, Gerber C, Weibel E (1983) 7x7 reconstruction on Si(111) resolved in real space. Phys Rev Lett 50(2):120–123Google Scholar
  106. 106.
    Hansma P, Elings V, Marti O, Bracker C (1988) Scanning tunneling microscopy and atomic force microscopy: application to biology and technology. Science 242:209–216Google Scholar
  107. 107.
    Oberhauser AF, Hansma PK, Carrion-Vazquez M, Fernandez JM (2001) Stepwise unfolding of titin under force-clamp atomic force microscopy. Proc Natl Acad Sci USA 98(2):468–472Google Scholar
  108. 108.
    Moffitt JR, Chemla YR, Smith SB, Bustamante C (2008) Recent advances in optical tweezers. Annu Rev Biochem 77:205–228. doi:10.1146/annurev.biochem.77.043007.090225Google Scholar
  109. 109.
    Visscher K, Block SM (1998) Versatile optical traps with feedback control. Molecular Motors and the Cytoskeleton, Pt B 298:460–489Google Scholar
  110. 110.
    Mehta AD, Rief M, Spudich JA, Smith DA, Simmons RM (1999) Single-molecule biomechanics with optical methods. Science 283(5408):1689–1695Google Scholar
  111. 111.
    Moffitt JR, Chemla YR, Izhaky D, Bustamante C (2006) Differential detection of dual traps improves the spatial resolution of optical tweezers. PNAS 103(24):9006–9011. doi:10.1073/pnas.0603342103Google Scholar
  112. 112.
    Ashkin A (1970) Acceleration and trapping of particles by radiation pressure. Phys Rev Lett 24(4):156–159. doi:10.1103/PhysRevLett.24.156Google Scholar
  113. 113.
    De Vlaminck I, Dekker C (2012) Recent advances in magnetic tweezers. Annu Rev Biophys 41:453–472Google Scholar
  114. 114.
    Lipfert J, Kerssemakers JWJ, Jager T, Dekker NH (2010) Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments. Nat Methods 7(12):977–980. doi:10.1038/nmeth.1520Google Scholar
  115. 115.
    Lipfert J, Hao XM, Dekker NH (2009) Quantitative modeling and optimization of magnetic tweezers. Biophys J 96(12):5040–5049. doi:10.1016/j.bpj.2009.03.055Google Scholar
  116. 116.
    Strick T, Allemand JF, Croquette V, Bensimon D (2000) Twisting and stretching single DNA molecules. Prog Biophys Mol Biol 74(1–2):115–140. doi:10.1016/s0079-6107(00)00018-3Google Scholar
  117. 117.
    Strick TR, Allemand JF, Bensimon D, Bensimon A, Croquette V (1996) The elasticity of a single supercoiled DNA molecule. Science 271(5257):1835–1837Google Scholar
  118. 118.
    Strick TR, Allemand JF, Bensimon D, Croquette V (1998) Behavior of supercoiled DNA. Biophys J 74(4):2016–2028Google Scholar
  119. 119.
    Simson DA, Ziemann F, Strigl M, Merkel R (1998) Micropipet-based pico force transducer: in depth analysis and experimental verification. Biophys J 74(4):2080–2088Google Scholar
  120. 120.
    Deamer DW, Akeson M (2000) Nanopores and nucleic acids: prospects for ultrarapid sequencing. Trends Biotechnol 18(4):147–151. doi:10.1016/S0167-7799(00)01426-8Google Scholar
  121. 121.
    Kasianowicz JJ, Brandin E, Branton D, Deamer DW (1996) Characterization of individual polynucleotide molecules using a membrane channel. Proc Natl Acad Sci 93(24):13770–13773Google Scholar
  122. 122.
    Dekker C (2007) Solid-state nanopores. Nat Nanotechnol 2(4):209–215. doi:10.1038/nnano.2007.27Google Scholar
  123. 123.
    Rodriguez-Larrea D, Bayley H (2013) Multistep protein unfolding during nanopore translocation. Nat Nanotechnol 8(4):288–295. doi:10.1038/nnano.2013.22Google Scholar
  124. 124.
    Dudko OK, Mathé J, Meller A (2010) Chapter twenty-one – nanopore force spectroscopy tools for analyzing single biomolecular complexes. In: Nils GW (ed) Methods in enzymology, vol 475. Academic Press, New York, pp 565–589. doi:10.1016/S0076-6879(10)75021-7Google Scholar
  125. 125.
    Perkins TT, Smith DE, Chu S (1997) Single polymer dynamics in an elongational flow. Science 276(5321):2016–2021Google Scholar
  126. 126.
    Perkins TT, Smith DE, Larson RG, Chu S (1995) Stretching of a single tethered polymer in a uniform-flow. Science 268(5207):83–87. doi:10.1126/science.7701345Google Scholar
  127. 127.
    Davenport RJ, Wuite GJL, Landick R, Bustamante C (2000) Single-molecule study of transcriptional pausing and arrest by E-coli RNA polymerase. Science 287(5462):2497–2500. doi:10.1126/science.287.5462.2497Google Scholar
  128. 128.
    Kim SJ, Blainey PC, Schroeder CM, Xie XS (2007) Multiplexed single-molecule assay for enzymatic activity on flow-stretched DNA. Nat Methods 4(5):397–399. doi:10.1038/nmeth1037Google Scholar
  129. 129.
    Schafer DA, Gelles J, Sheetz MP, Landick R (1991) Transcription by single molecules of RNA polymerase observed by light microscopy. Nature 352(6334):444–448. doi:10.1038/352444a0Google Scholar
  130. 130.
    Yin H, Landick R, Gelles J (1994) Tethered particle motion method for studying transcript elongation by a single RNA polymerase molecule. Biophys J 67(6):2468–2478. doi:10.1016/S0006-3495(94)80735-0Google Scholar
  131. 131.
    Finzi L, Gelles J (1995) Measurement of lactose repressor-mediated loop formation and breakdown in single DNA molecules. Science 267(5196):378–380Google Scholar
  132. 132.
    van den Broek B, Vanzi F, Normanno D, Pavone FS, Wuite GJ (2006) Real-time observation of DNA looping dynamics of Type IIE restriction enzymes NaeI and NarI. Nucleic Acids Res 34(1):167–174. doi:10.1093/nar/gkj432Google Scholar
  133. 133.
    Vanzi F, Broggio C, Sacconi L, Pavone FS (2006) Lac repressor hinge flexibility and DNA looping: single molecule kinetics by tethered particle motion. Nucleic Acids Res 34(12):3409–3420. doi:10.1093/nar/gkl393Google Scholar
  134. 134.
    Wong OK, Guthold M, Erie DA, Gelles J (2008) Interconvertible lac repressor-DNA loops revealed by single-molecule experiments. PLoS Biol 6(9):e232. doi:10.1371/journal.pbio.0060232Google Scholar
  135. 135.
    Han L, Garcia HG, Blumberg S, Towles KB, Beausang JF, Nelson PC, Phillips R (2009) Concentration and length dependence of DNA looping in transcriptional regulation. PLoS One 4(5):e5621. doi:10.1371/journal.pone.0005621Google Scholar
  136. 136.
    Rutkauskas D, Zhan H, Matthews KS, Pavone FS, Vanzi F (2009) Tetramer opening in LacI-mediated DNA looping. Proc Natl Acad Sci USA 106(39):16627–16632. doi:10.1073/pnas.0904617106Google Scholar
  137. 137.
    Zurla C, Manzo C, Dunlap D, Lewis DE, Adhya S, Finzi L (2009) Direct demonstration and quantification of long-range DNA looping by the lambda bacteriophage repressor. Nucleic Acids Res 37(9):2789–2795. doi:10.1093/nar/gkp134Google Scholar
  138. 138.
    Chen YF, Milstein JN, Meiners JC (2010) Protein-mediated DNA loop formation and breakdown in a fluctuating environment. Phys Rev Lett 104(25):258103Google Scholar
  139. 139.
    Chen Y-F, Milstein J, Meiners J-C (2010) Femtonewton entropic forces can control the formation of protein-mediated DNA loops. Phys Rev Lett 104(4):048301Google Scholar
  140. 140.
    Johnson S, Linden M, Phillips R (2012) Sequence dependence of transcription factor-mediated DNA looping. Nucleic Acids Res 40(16):7728–7738. doi:10.1093/nar/gks473Google Scholar
  141. 141.
    Laurens N, Rusling DA, Pernstich C, Brouwer I, Halford SE, Wuite GJ (2012) DNA looping by FokI: the impact of twisting and bending rigidity on protein-induced looping dynamics. Nucleic Acids Res 40(11):4988–4997. doi:10.1093/nar/gks184Google Scholar
  142. 142.
    Manzo C, Zurla C, Dunlap DD, Finzi L (2012) The effect of nonspecific binding of lambda repressor on DNA looping dynamics. Biophys J 103(8):1753–1761. doi:10.1016/j.bpj.2012.09.006Google Scholar
  143. 143.
    Pouget N, Turlan C, Destainville N, Salomé L, Chandler M (2006) IS911 transpososome assembly as analysed by tethered particle motion. Nucleic Acids Res 34(16):4313–4323Google Scholar
  144. 144.
    Tolic-Norrelykke SF, Rasmussen MB, Pavone FS, Berg-Sorensen K, Oddershede LB (2006) Stepwise bending of DNA by a single TATA-box binding protein. Biophys J 90(10):3694–3703. doi:10.1529/biophysj.105.074856Google Scholar
  145. 145.
    Mumm JP, Landy A, Gelles J (2006) Viewing single lambda site-specific recombination events from start to finish. EMBO J 25(19):4586–4595. doi:10.1038/sj.emboj.7601325Google Scholar
  146. 146.
    Fan HF (2012) Real-time single-molecule tethered particle motion experiments reveal the kinetics and mechanisms of Cre-mediated site-specific recombination. Nucleic Acids Res 40(13):6208–6222. doi:10.1093/nar/gks274Google Scholar
  147. 147.
    Monico C, Capitanio M, Belcastro G, Vanzi F, Pavone FS (2013) Optical methods to study protein-DNA interactions in vitro and in living cells at the single-molecule level. Int J Mol Sci 14(2):3961–3992Google Scholar
  148. 148.
    Vanzi F, Sacconi L, Pavone FS (2007) Analysis of kinetics in noisy systems: application to single molecule tethered particle motion. Biophys J 93(1):21–36. doi:10.1529/biophysj.106.094151Google Scholar
  149. 149.
    Segall DE, Nelson PC, Phillips R (2006) Volume-exclusion effects in tethered-particle experiments: bead size matters. Phys Rev Lett 96(8):088306Google Scholar
  150. 150.
    Milstein JN, Chen YF, Meiners JC (2011) Bead size effects on protein-mediated DNA looping in tethered-particle motion experiments. Biopolymers 95(2):144–150. doi:10.1002/bip.21547Google Scholar
  151. 151.
    Fan H-F, Li H-W (2009) Studying RecBCD Helicase translocation along Ç-DNA using tethered particle motion with a stretching force. Biophys J 96(5):1875–1883Google Scholar
  152. 152.
    Plenat T, Tardin C, Rousseau P, Salome L (2012) High-throughput single-molecule analysis of DNA-protein interactions by tethered particle motion. Nucleic Acids Res 40(12):e89. doi:10.1093/nar/gks250Google Scholar
  153. 153.
    Beausang JF, Zurla C, Manzo C, Dunlap D, Finzi L, Nelson PC (2007) DNA looping kinetics analyzed using diffusive hidden Markov model. Biophys J 92(8):L64–L66Google Scholar
  154. 154.
    Manzo C, Finzi L (2010) Quantitative analysis of DNA-looping kinetics from tethered particle motion experiments. Methods Enzymol 475:199–220. doi:10.1016/S0076-6879(10)75009-6Google Scholar
  155. 155.
    Bustamante C, Macosko JC, Wuite GJL (2000) Grabbing the cat by the tail: manipulating molecules one by one. Nat Rev Mol Cell Biol 1(2):130–136Google Scholar
  156. 156.
    Neuman KC, Nagy A (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Methods 5(6):491–505. doi:10.1038/nmeth.1218Google Scholar
  157. 157.
    Giannotti MI, Vancso GJ (2007) Interrogation of single synthetic polymer chains and polysaccharides by AFM-based force spectroscopy. Chemphyschem 8(16):2290–2307. doi:10.1002/cphc.200700175Google Scholar
  158. 158.
    Greenleaf WJ, Woodside MT, Block SM (2007) High-resolution, single-molecule measurements of biomolecular motion. Annu Rev Biophys Biomol Struct 36(1):171–190. doi:10.1146/annurev.biophys.36.101106.101451Google Scholar
  159. 159.
    Tinoco I, Li PTX, Bustamante C (2006) Determination of thermodynamics and kinetics of RNA reactions by force. Quart Rev Biophys 39(4):325–360. doi:10.1017/S0033583506004446Google Scholar
  160. 160.
    Dufrêne Y, Hinterdorfer P (2008) Recent progress in AFM molecular recognition studies. Pflügers Arch 456(1):237–245. doi:10.1007/s00424-007-0413-1Google Scholar
  161. 161.
    Moy VT, Florin EL, Gaub HE (1994) Adhesive forces between ligand and receptor measured by Afm. Colloid Surf A-Physicochem Eng 93:343–348Google Scholar
  162. 162.
    Wuite GJL, Smith SB, Young M, Keller D, Bustamante C (2000) Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404(6773):103–106Google Scholar
  163. 163.
    Onoa B, Dumont S, Liphardt J, Smith SB, Tinoco I, Bustamante C (2003) Identifying kinetic barriers to mechanical unfolding of the T-thermophila ribozyme. Science 299(5614):1892–1895Google Scholar
  164. 164.
    Stigler J, Ziegler F, Gieseke A, Gebhardt JCM, Rief M (2011) The complex folding network of single calmodulin molecules. Science 334(6055):512–516. doi:10.1126/science.1207598Google Scholar
  165. 165.
    Koster DA, Croquette V, Dekker C, Shuman S, Dekker NH (2005) Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 434(7033):671–674. doi:10.1038/nature03395Google Scholar
  166. 166.
    Gore J, Bryant Z, Stone MD, Nollmann MN, Cozzarelli NR, Bustamante C (2006) Mechanochemical analysis of DNA gyrase using rotor bead tracking. Nature 439(7072):100–104Google Scholar
  167. 167.
    Merkel R, Nassoy P, Leung A, Ritchie K, Evans E (1999) Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397(6714):50–53. doi:10.1038/16219Google Scholar
  168. 168.
    Dudko OK, Mathe J, Szabo A, Meller A, Hummer G (2007) Extracting kinetics from single-molecule force spectroscopy: nanopore unzipping of DNA hairpins. Biophys J 92(12):4188–4195. doi:10.1529/biophysj.106.102855Google Scholar
  169. 169.
    Hutter JL, Bechhoefer J (1993) Calibration of atomic-force microscope tips. Rev Sci Instrum 64:1868Google Scholar
  170. 170.
    Hinterdorfer P, Dufrêne YF (2006) Detection and localization of single molecular recognition events using atomic force microscopy. Nat Methods 3(5):347–355Google Scholar
  171. 171.
    Taniguchi Y, Kawakami M (2010) Application of HaloTag protein to covalent immobilization of recombinant proteins for single molecule force spectroscopy. Langmuir 26(13):10433–10436Google Scholar
  172. 172.
    Wong J, Chilkoti A, Moy VT (1999) Direct force measurements of the streptavidin–biotin interaction. Biomol Eng 16(1):45–55Google Scholar
  173. 173.
    Kienberger F, Kada G, Gruber HJ, Pastushenko VP, Riener C, Trieb M, Knaus HG, Schindler H, Hinterdorfer P (2000) Recognition force spectroscopy studies of the NTA-His6 bond. Single Molecules 1(1):59–65Google Scholar
  174. 174.
    Bustamante C, Marko J, Siggia E, Smith S (1994) Entropic elasticity of lambda-phage DNA. Science 265:1599–1601Google Scholar
  175. 175.
    Merkel R, Nassoy P, Leung A, Ritchie K, Evans E (1999) Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy. Nature 397(6714):50–53Google Scholar
  176. 176.
    Brockwell DJ, Paci E, Zinober RC, Beddard GS, Olmsted PD, Smith DA, Perham RN, Radford SE (2003) Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nat Struct Biol 10(9):731–737. doi:10.1038/nsb968Google Scholar
  177. 177.
    Dietz H, Rief M (2006) Protein structure by mechanical triangulation. Proc Natl Acad Sci USA 103(5):1244–1247Google Scholar
  178. 178.
    Lee W, Zeng X, Zhou H-X, Bennett V, Yang W, Marszalek PE (2010) Full reconstruction of a vectorial protein folding pathway by atomic force microscopy and molecular dynamics simulations. J Biol Chem 285(49):38167–38172. doi:10.1074/jbc.M110.179697Google Scholar
  179. 179.
    Li L, Wetzel S, Pluckthun A, Fernandez JM (2006) Stepwise unfolding of ankyrin repeats in a single protein revealed by atomic force microscopy. Biophys J 90(4):L30–L32. doi:10.1529/biophysj.105.078436Google Scholar
  180. 180.
    Lee G, Abdi K, Jiang Y, Michaely P, Bennett V, Marszalek PE (2006) Nanospring behaviour of ankyrin repeats. Nature 440(7081):246–249. doi:nature04437 [pii]. doi:10.1038/nature04437Google Scholar
  181. 181.
    Merz T, Wetzel SK, Firbank S, Pluckthun A, Grutter MG, Mittl PR (2008) Stabilizing ionic interactions in a full-consensus ankyrin repeat protein. J Mol Biol 376(1):232–240. doi:10.1016/j.jmb.2007.11.047Google Scholar
  182. 182.
    Kim M, Abdi K, Lee G, Rabbi M, Lee W, Yang M, Schofield CJ, Bennett V, Marszalek PE (2010) Fast and forceful refolding of stretched alpha-helical solenoid proteins. Biophys J 98(12):3086–3092. doi:10.1016/j.bpj.2010.02.054Google Scholar
  183. 183.
    Valbuena A, Vera Andrés M, Oroz J, Menéndez M, Carrión-Vázquez M (2012) Mechanical properties of β-catenin revealed by single-molecule experiments. Biophys J 103(8):1744–1752. doi:10.1016/j.bpj.2012.07.051Google Scholar
  184. 184.
    Xing Y, Takemaru K, Liu J, Berndt JD, Zheng JJ, Moon RT, Xu W (2008) Crystal structure of a full-length beta-catenin. Structure 16(3):478–487. doi:10.1016/j.str.2007.12.021Google Scholar
  185. 185.
    Best RB, Li B, Steward A, Daggett V, Clarke J (2001) Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophys J 81(4):2344–2356. doi:10.1016/S0006-3495(01)75881-XGoogle Scholar
  186. 186.
    Martin C, Richard V, Salem M, Hartley R, Mauguen Y (1999) Refinement and structural analysis of barnase at 1.5 A resolution. Acta Crystallogr D Biol Crystallogr 55(Pt 2):386–398Google Scholar
  187. 187.
    Junker JP, Ziegler F, Rief M (2009) Ligand-dependent equilibrium fluctuations of single calmodulin molecules. Science 323(5914):633–637. doi:10.1126/science.1166191Google Scholar
  188. 188.
    Chattopadhyaya R, Meador WE, Means AR, Quiocho FA (1992) Calmodulin structure refined at 1.7 Å resolution. J Mol Biol 228(4):1177–1192Google Scholar
  189. 189.
    Hoffmann T, Tych KM, Brockwell DJ, Dougan L (2013) Single-molecule force spectroscopy identifies a small cold shock protein as being mechanically robust. J Phys Chem B 117(6):1819–1826. doi:10.1021/jp310442sGoogle Scholar
  190. 190.
    Kremer W, Schuler B, Harrieder S, Geyer M, Gronwald W, Welker C, Jaenicke R, Kalbitzer HR (2001) Solution NMR structure of the cold-shock protein from the hyperthermophilic bacterium Thermotoga maritima. Eur J Biochem 268(9):2527–2539Google Scholar
  191. 191.
    Ainavarapu SRK, Li L, Badilla CL, Fernandez JM (2005) Ligand binding modulates the mechanical stability of dihydrofolate reductase. Biophys J 89(5):3337–3344Google Scholar
  192. 192.
    Lewis WS, Cody V, Galitsky N, Luft JR, Pangborn W, Chunduru SK, Spencer HT, Appleman JR, Blakley RL (1995) Methotrexate-resistant variants of human dihydrofolate reductase with substitutions of leucine 22 Kinetics, crystallography, and potential as selectable markers. J Biol Chem 270(10):5057–5064Google Scholar
  193. 193.
    Tang L, Whittingham JL, Verma CS, Caves LS, Dodson GG (1999) Structural consequences of the B5 histidine –> tyrosine mutation in human insulin characterized by X-ray crystallography and conformational analysis. Biochemistry 38(37):12041–12051Google Scholar
  194. 194.
    Perez-Jimenez R, Garcia-Manyes S, Ainavarapu SRK, Fernandez JM (2006) Mechanical unfolding pathways of the enhanced yellow fluorescent protein revealed by single molecule force spectroscopy. J Biol Chem 281(52):40010–40014Google Scholar
  195. 195.
    Wachter RM, Elsliger MA, Kallio K, Hanson GT, Remington SJ (1998) Structural basis of spectral shifts in the yellow-emission variants of green fluorescent protein. Structure 6(10):1267–1277Google Scholar
  196. 196.
    Brown André E, Litvinov RI, Discher DE, Weisel JW (2007) Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys J 92(5):L39–L41Google Scholar
  197. 197.
    Cao Y, Lam C, Wang M, Li H (2006) Nonmechanical protein can have significant mechanical stability. Angew Chem 118(4):658–661Google Scholar
  198. 198.
    Cao Y, Li H (2007) Polyprotein of GB1 is an ideal artificial elastomeric protein. Nat Mater 6(2):109–114Google Scholar
  199. 199.
    Nieuwkoop AJ, Wylie BJ, Franks WT, Shah GJ, Rienstra CM (2009) Atomic resolution protein structure determination by three-dimensional transferred echo double resonance solid-state nuclear magnetic resonance spectroscopy. J Chem Phys 131(9):095101. doi:10.1063/1.3211103Google Scholar
  200. 200.
    Cao Y, Yoo T, Li H (2008) Single molecule force spectroscopy reveals engineered metal chelation is a general approach to enhance mechanical stability of proteins. Proc Natl Acad Sci 105(32):11152–11157Google Scholar
  201. 201.
    Abu-Lail NI, Ohashi T, Clark RL, Erickson HP, Zauscher S (2006) Understanding the elasticity of fibronectin fibrils: unfolding strengths of FN-III and GFP domains measured by single molecule force spectroscopy. Matrix Biol 25(3):175–184Google Scholar
  202. 202.
    Dietz H, Rief M (2004) Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc Natl Acad Sci USA 101(46):16192–16197Google Scholar
  203. 203.
    Battistutta R, Negro A, Zanotti G (2000) Crystal structure and refolding properties of the mutant F99S/M153T/V163A of the green fluorescent protein. Proteins 41(4):429–437Google Scholar
  204. 204.
    Newman J, Peat TS, Richard R, Kan L, Swanson PE, Affholter JA, Holmes IH, Schindler JF, Unkefer CJ, Terwilliger TC (1999) Haloalkane dehalogenases: structure of a Rhodococcus enzyme. Biochemistry 38(49):16105–16114Google Scholar
  205. 205.
    Ybe JA, Brodsky FM, Hofmann K, Lin K, Liu SH, Chen L, Earnest TN, Fletterick RJ, Hwang PK (1999) Clathrin self-assembly is mediated by a tandemly repeated superhelix. Nature 399(6734):371–375. doi:10.1038/20708Google Scholar
  206. 206.
    Schwaiger I, Kardinal A, Schleicher M, Noegel AA, Rief M (2003) A mechanical unfolding intermediate in an actin-crosslinking protein. Nat Struct Mol Biol 11(1):81–85Google Scholar
  207. 207.
    Schwaiger I, Schleicher M, Noegel AA, Rief M (2004) The folding pathway of a fast-folding immunoglobulin domain revealed by single-molecule mechanical experiments. EMBO Rep 6(1):46–51Google Scholar
  208. 208.
    Bullard B, Garcia T, Benes V, Leake MC, Linke WA, Oberhauser AF (2006) The molecular elasticity of the insect flight muscle proteins projectin and kettin. Proc Natl Acad Sci USA 103(12):4451–4456Google Scholar
  209. 209.
    Johnson RJ, McCoy JG, Bingman CA, Phillips GN Jr, Raines RT (2007) Inhibition of human pancreatic ribonuclease by the human ribonuclease inhibitor protein. J Mol Biol 368(2):434–449. doi:10.1016/j.jmb.2007.02.005Google Scholar
  210. 210.
    Bornschlögl T, Rief M (2006) Single molecule unzipping of coiled coils: sequence resolved stability profiles. Phys Rev Lett 96(11):118102Google Scholar
  211. 211.
    Bertz M, Rief M (2008) Mechanical unfoldons as building blocks of maltose-binding protein. J Mol Biol 378(2):447–458Google Scholar
  212. 212.
    Quiocho FA, Spurlino JC, Rodseth LE (1997) Extensive features of tight oligosaccharide binding revealed in high-resolution structures of the maltodextrin transport/chemosensory receptor. Structure 5(8):997–1015Google Scholar
  213. 213.
    Berkemeier F, Bertz M, Xiao S, Pinotsis N, Wilmanns M, Grater F, Rief M (2011) Fast-folding alpha-helices as reversible strain absorbers in the muscle protein myomesin. Proc Natl Acad Sci USA 108(34):14139–14144. doi:10.1073/pnas.1105734108Google Scholar
  214. 214.
    Pinotsis N, Lange S, Perriard JC, Svergun DI, Wilmanns M (2008) Molecular basis of the C-terminal tail-to-tail assembly of the sarcomeric filament protein myomesin. EMBO J 27(1):253–264. doi:10.1038/sj.emboj.7601944Google Scholar
  215. 215.
    Schwaiger I, Sattler C, Hostetter DR, Rief M (2002) The myosin coiled-coil is a truly elastic protein structure. Nat Mater 1(4):232–235. doi:10.1038/nmat776Google Scholar
  216. 216.
    Kaiser CM, Bujalowski PJ, Ma L, Anderson J, Epstein HF, Oberhauser AF (2012) Tracking UNC-45 chaperone-myosin interaction with a titin mechanical reporter. Biophys J 102(9):2212–2219Google Scholar
  217. 217.
    Yadavalli VK, Forbes JG, Wang K (2009) Nanomechanics of full-length nebulin: an elastic strain gauge in the skeletal muscle sarcomere. Langmuir 25(13):7496–7505. doi:10.1021/la9009898Google Scholar
  218. 218.
    Cao Y, Kuske R, Li H (2008) Direct observation of Markovian behavior of the mechanical unfolding of individual proteins. Biophys J 95(2):782–788Google Scholar
  219. 219.
    Nauli S, Kuhlman B, Le Trong I, Stenkamp RE, Teller D, Baker D (2002) Crystal structures and increased stabilization of the protein G variants with switched folding pathways NuG1 and NuG2. Protein Sci 11(12):2924–2931Google Scholar
  220. 220.
    Ma L, Xu M, Forman JR, Clarke J, Oberhauser AF (2009) Naturally occurring mutations alter the stability of polycystin-1 polycystic kidney disease (PKD) domains. J Biol Chem 284(47):32942–32949Google Scholar
  221. 221.
    Bycroft M, Bateman A, Clarke J, Hamill SJ, Sandford R, Thomas RL, Chothia C (1999) The structure of a PKD domain from polycystin-1: implications for polycystic kidney disease. EMBO J 18(2):297–305Google Scholar
  222. 222.
    Brockwell DJ, Beddard GS, Paci E, West DK, Olmsted PD, Smith DA, Radford SE (2005) Mechanically unfolding the small, topologically simple protein L. Biophys J 89(1):506Google Scholar
  223. 223.
    O’Neill JW, Kim DE, Baker D, Zhang KY (2001) Structures of the B1 domain of protein L from Peptostreptococcus magnus with a tyrosine to tryptophan substitution. Acta Crystallogr D Biol Crystallogr 57(Pt 4):480–487Google Scholar
  224. 224.
    Valbuena A, Oroz J, Hervás R, Vera AM, Rodríguez D, Menéndez M, Sulkowska JI, Cieplak M, Carrión-Vázquez M (2009) On the remarkable mechanostability of scaffoldins and the mechanical clamp motif. Proc Natl Acad Sci 106(33):13791–13796Google Scholar
  225. 225.
    Spinelli S, Fierobe HP, Belaich A, Belaich JP, Henrissat B, Cambillau C (2000) Crystal structure of a cohesin module from Clostridium cellulolyticum: implications for dockerin recognition. J Mol Biol 304(2):189–200. doi:10.1006/jmbi.2000.4191Google Scholar
  226. 226.
    Shimon LJ, Bayer EA, Morag E, Lamed R, Yaron S, Shoham Y, Frolow F (1997) A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly. Structure 5(3):381–390Google Scholar
  227. 227.
    Tavares GA, Béguin P, Alzari PM (1997) The crystal structure of a type I cohesin domain at 1.7 Å resolution. J Mol Biol 273(3):701–713Google Scholar
  228. 228.
    Alegre-Cebollada J, Badilla CL, Fernández JM (2010) Isopeptide bonds block the mechanical extension of pili in pathogenic Streptococcus pyogenes. J Biol Chem 285(15):11235–11242Google Scholar
  229. 229.
    Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN (2007) Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Science 318(5856):1625–1628Google Scholar
  230. 230.
    Wang C-C, Tsong T-Y, Hsu Y-H, Marszalek PE (2011) Inhibitor binding increases the mechanical stability of Staphylococcal Nuclease. Biophys J 100(4):1094–1099. doi:10.1016/j.bpj.2011.01.011Google Scholar
  231. 231.
    Cotton FA, Hazen EE, Legg MJ (1979) Staphylococcal nuclease: proposed mechanism of action based on structure of enzyme—thymidine 3′, 5′-bisphosphate—calcium ion complex at 1.5-Å resolution. Proc Natl Acad Sci 76(6):2551–2555Google Scholar
  232. 232.
    Kotamarthi HC, Sharma R, Koti Ainavarapu SR (2013) Single-molecule studies on PolySUMO proteins reveal their mechanical flexibility. Biophys J 104(10):2273–2281Google Scholar
  233. 233.
    Bayer P, Arndt A, Metzger S, Mahajan R, Melchior F, Jaenicke R, Becker J (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 280(2):275–286Google Scholar
  234. 234.
    Huang WC, Ko TP, Li SSL, Wang AHJ (2004) Crystal structures of the human SUMO‐2 protein at 1.6 Å and 1.2 Å resolution. Eur J Biochem 271(20):4114–4122Google Scholar
  235. 235.
    Randles LG, Rounsevell RWS, Clarke J (2007) Spectrin domains lose cooperativity in forced unfolding. Biophys J 92(2):571–577. doi:10.1529/biophysj.106.093690Google Scholar
  236. 236.
    Law R, Carl P, Harper S, Dalhaimer P, Speicher DW, Discher DE (2003) Cooperativity in forced unfolding of tandem spectrin repeats. Biophys J 84(1):533–544Google Scholar
  237. 237.
    Kusunoki H, MacDonald RI, Mondragón A (2004) Structural insights into the stability and flexibility of unusual erythroid spectrin repeats. Structure 12(4):645–656Google Scholar
  238. 238.
    Fuson KL, Ma L, Sutton RB, Oberhauser AF (2009) The c2 domains of human synaptotagmin 1 have distinct mechanical properties. Biophys J 96(3):1083–1090Google Scholar
  239. 239.
    Fuson KL, Montes M, Robert JJ, Sutton RB (2007) Structure of human synaptotagmin 1 C2AB in the absence of Ca2+ reveals a novel domain association. Biochemistry 46(45):13041–13048Google Scholar
  240. 240.
    Peng Q, Li H (2008) Atomic force microscopy reveals parallel mechanical unfolding pathways of T4 lysozyme: evidence for a kinetic partitioning mechanism. Proc Natl Acad Sci 105(6):1885–1890Google Scholar
  241. 241.
    Nicholson H, Anderson D, Dao Pin S, Matthews B (1991) Analysis of the interaction between charged side chains and the. alpha.-helix dipole using designed thermostable mutants of phage T4 lysozyme. Biochemistry 30(41):9816–9828Google Scholar
  242. 242.
    Oberhauser AF, Marszalek PE, Erickson HP, Fernandez JM (1998) The molecular elasticity of the extracellular matrix protein tenascin. Nature 393(6681):181–185Google Scholar
  243. 243.
    Ng SP, Rounsevell RW, Steward A, Geierhaas CD, Williams PM, Paci E, Clarke J (2005) Mechanical unfolding of TNfn3: the unfolding pathway of a fnIII domain probed by protein engineering, AFM and MD simulation. J Mol Biol 350(4):776–789Google Scholar
  244. 244.
    Leahy DJ, Hendrickson WA, Aukhil I, Erickson HP (1992) Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein. Science 258(5084):987–991Google Scholar
  245. 245.
    Carrion-Vazquez M, Oberhauser AF, Fowler SB, Marszalek PE, Broedel SE, Clarke J, Fernandez JM (1999) Mechanical and chemical unfolding of a single protein: a comparison. Proc Natl Acad Sci 96(7):3694–3699Google Scholar
  246. 246.
    Stacklies W, Vega MC, Wilmanns M, Grater F (2009) Mechanical network in titin immunoglobulin from force distribution analysis. PLoS Comput Biol 5(3):e1000306. doi:10.1371/journal.pcbi.1000306Google Scholar
  247. 247.
    Puchner EM, Alexandrovich A, Kho AL, Hensen U, Schäfer LV, Brandmeier B, Gräter F, Grubmüller H, Gaub HE, Gautel M (2008) Mechanoenzymatics of titin kinase. Proc Natl Acad Sci 105(36):13385–13390Google Scholar
  248. 248.
    Mayans O, van der Ven PF, Wilm M, Mues A, Young P, Fürst DO, Wilmanns M, Gautel M (1998) Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature 395(6705):863–869Google Scholar
  249. 249.
    Greene DN, Garcia T, Sutton RB, Gernert KM, Benian GM, Oberhauser AF (2008) Single-molecule force spectroscopy reveals a stepwise unfolding of Caenorhabditis elegans giant protein kinase domains. Biophys J 95(3):1360–1370Google Scholar
  250. 250.
    Kobe B, Heierhorst J, Feil SC, Parker MW, Benian GM, Weiss KR, Kemp BE (1996) Giant protein kinases: domain interactions and structural basis of autoregulation. EMBO J 15(24):6810–6821Google Scholar
  251. 251.
    Sharma D, Perisic O, Peng Q, Cao Y, Lam C, Lu H, Li H (2007) Single-molecule force spectroscopy reveals a mechanically stable protein fold and the rational tuning of its mechanical stability. Proc Natl Acad Sci 104(22):9278–9283Google Scholar
  252. 252.
    Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, Baker D (2003) Design of a novel globular protein fold with atomic-level accuracy. Science 302(5649):1364–1368Google Scholar
  253. 253.
    Carrion-Vazquez M, Li H, Lu H, Marszalek PE, Oberhauser AF, Fernandez JM (2003) The mechanical stability of ubiquitin is linkage dependent. Nat Struct Mol Biol 10(9):738–743Google Scholar
  254. 254.
    Vijay-Kumar S, Bugg CE, Cook WJ (1987) Structure of ubiquitin refined at 1.8 Å resolution. J Mol Biol 194(3):531–544Google Scholar
  255. 255.
    Isralewitz B, Gao M, Schulten K (2001) Steered molecular dynamics and mechanical functions of proteins. Curr Opin Struct Biol 11(2):224–230Google Scholar
  256. 256.
    Neumann J, Gottschalk K-E (2009) The effect of different force applications on the protein-protein complex barnase-barstar. Biophys J 97(6):1687–1699Google Scholar
  257. 257.
    Gao M, Craig D, Lequin O, Campbell ID, Vogel V, Schulten K (2003) Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc Natl Acad Sci 100(25):14784–14789Google Scholar
  258. 258.
    Krammer A, Lu H, Isralewitz B, Schulten K, Vogel V (1999) Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc Natl Acad Sci 96(4):1351–1356Google Scholar
  259. 259.
    Lee W, Strümpfer J, Bennett V, Schulten K, Marszalek PE (2012) Mutation of conserved histidines alters tertiary structure and nanomechanics of consensus ankyrin repeats. J Biol Chem 287(23):19115–19121. doi:10.1074/jbc.M112.365569Google Scholar
  260. 260.
    Paramore S, Voth GA (2006) Examining the influence of linkers and tertiary structure in the forced unfolding of multiple-repeat spectrin molecules. Biophys J 91(9):3436–3445Google Scholar
  261. 261.
    Paci E, Karplus M (2000) Unfolding proteins by external forces and temperature: the importance of topology and energetics. Proc Natl Acad Sci USA 97(12):6521–6526Google Scholar
  262. 262.
    Cao Y, Er KS, Parhar R, Li H (2009) A force spectroscopy based single molecule metal binding assay. Chemphyschem 10(9–10):1450–1454Google Scholar
  263. 263.
    Cao Y, Balamurali M, Sharma D, Li H (2007) A functional single-molecule binding assay via force spectroscopy. Proc Natl Acad Sci 104(40):15677–15681Google Scholar
  264. 264.
    Bertz M, Rief M (2009) Ligand binding mechanics of maltose binding protein. J Mol Biol 393(5):1097–1105Google Scholar
  265. 265.
    Krasnoslobodtsev AV, Peng J, Asiago JM, Hindupur J, Rochet J-C, Lyubchenko YL (2012) Effect of spermidine on misfolding and interactions of alpha-synuclein. PLoS One 7(5):e38099Google Scholar
  266. 266.
    Kim B-H, Palermo NY, Lovas S, Zaikova T, Keana JF, Lyubchenko YL (2011) Single-molecule atomic force microscopy force spectroscopy study of Aβ-40 interactions. Biochemistry 50(23):5154–5162Google Scholar
  267. 267.
    Lv Z, Condron MM, Teplow DB, Lyubchenko YL (2013) Nanoprobing of the effect of Cu2+ cations on misfolding, interaction and aggregation of amyloid β peptide. J Neuroimmune Pharmacol 8(1):262–273Google Scholar
  268. 268.
    Schwesinger F, Ros R, Strunz T, Anselmetti D, Güntherodt H-J, Honegger A, Jermutus L, Tiefenauer L, Plückthun A (2000) Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates. Proc Natl Acad Sci 97(18):9972–9977Google Scholar
  269. 269.
    Berquand A, Xia N, Castner DG, Clare BH, Abbott NL, Dupres V, Adriaensen Y, Dufrêne YF (2005) Antigen binding forces of single antilysozyme Fv fragments explored by atomic force microscopy. Langmuir 21(12):5517–5523Google Scholar
  270. 270.
    Kienberger F, Kada G, Mueller H, Hinterdorfer P (2005) Single molecule studies of antibody–antigen interaction strength versus intra-molecular antigen stability. J Mol Biol 347(3):597–606Google Scholar
  271. 271.
    Bonanni B, Kamruzzahan A, Bizzarri A, Rankl C, Gruber H, Hinterdorfer P, Cannistraro S (2005) Single molecule recognition between cytochrome C 551 and gold-immobilized azurin by force spectroscopy. Biophys J 89(4):2783–2791Google Scholar
  272. 272.
    De Paris R, Strunz T, Oroszlan K, Güntherodt H-J, Hegner M (2000) Force spectroscopy and dynamics of the biotin-avidin bond studied by scanning force microscopy. Single Molecules 1(4):285–290Google Scholar
  273. 273.
    Baumgartner W, Hinterdorfer P, Ness W, Raab A, Vestweber D, Schindler H, Drenckhahn D (2000) Cadherin interaction probed by atomic force microscopy. Proc Natl Acad Sci 97(8):4005–4010Google Scholar
  274. 274.
    Leckband D, Sivasankar S (2012) Cadherin recognition and adhesion. Curr Opin Cell Biol 24(5):620–627Google Scholar
  275. 275.
    Bartels FW, Baumgarth B, Anselmetti D, Ros R, Becker A (2003) Specific binding of the regulatory protein ExpG to promoter regions of the galactoglucan biosynthesis gene cluster of Sinorhizobium meliloti − a combined molecular biology and force spectroscopy investigation. J Struct Biol 143(2):145–152Google Scholar
  276. 276.
    Hinterdorfer P, Kienberger F, Raab A, Gruber HJ, Baumgartner W, Kada G, Riener C, Wielert‐Badt S, Borken C, Schindler H (2000) Poly (ethylene glycol): an ideal spacer for molecular recognition force microscopy/spectroscopy. Single Molecules 1(2):99–103Google Scholar
  277. 277.
    Schmitt L, Ludwig M, Gaub HE, Tampe R (2000) A metal-chelating microscopy tip as a new toolbox for single-molecule experiments by atomic force microscopy. Biophys J 78(6):3275–3285Google Scholar
  278. 278.
    Taranta M, Bizzarri AR, Cannistraro S (2008) Probing the interaction between p53 and the bacterial protein azurin by single molecule force spectroscopy. J Mol Recognit 21(1):63–70Google Scholar
  279. 279.
    Fritz J, Katopodis AG, Kolbinger F, Anselmetti D (1998) Force-mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy. Proc Natl Acad Sci 95(21):12283–12288Google Scholar
  280. 280.
    Kim M, Wang CC, Benedetti F, Marszalek PE (2012) A nanoscale force probe for gauging intermolecular interactions. Angew Chem 124(8):1939–1942Google Scholar
  281. 281.
    Tang J, Ebner A, Badelt-Lichtblau H, Völlenkle C, Rankl C, Kraxberger B, Leitner M, Wildling L, Gruber HJ, Sleytr UB (2008) Recognition imaging and highly ordered molecular templating of bacterial S-layer nanoarrays containing affinity-tags. Nano Letters 8(12):4312–4319Google Scholar
  282. 282.
    Garcia-Manyes S, Badilla CL, Alegre-Cebollada J, Javadi Y, Fernández JM (2012) Spontaneous dimerization of titin protein Z1Z2 domains induces strong nanomechanical anchoring. J Biol Chem 287(24):20240–20247. doi:10.1074/jbc.M112.355883Google Scholar
  283. 283.
    Lv S, Dudek DM, Cao Y, Balamurali M, Gosline J, Li H (2010) Designed biomaterials to mimic the mechanical properties of muscles. Nature 465(7294):69–73Google Scholar
  284. 284.
    Cluzel P, Lebrun A, Heller C, Lavery R, Viovy J-L, Chatenay D, Caron F (1996) DNA: an extensible molecule. Science 271:792–794Google Scholar
  285. 285.
    Cocco S, Yan J, Leger J-F, Chatenay D, Marko JF (2004) Overstretching and force-driven strand separation of double-helix DNA. Phys Rev E 70(1):011910Google Scholar
  286. 286.
    Leger J, Romano G, Sarkar A, Robert J, Bourdieu L, Chatenay D, Marko J (1999) Structural transitions of a twisted and stretched DNA molecule. Phys Rev Lett 83(5):1066Google Scholar
  287. 287.
    Strick T, Dessinges M, Charvin G, Dekker N, Allemand J, Bensimon D, Croquette V (2003) Stretching of macromolecules and proteins. Rep Prog Phys 66(1):1Google Scholar
  288. 288.
    van Mameren J, Gross P, Farge G, Hooijman P, Modesti M, Falkenberg M, Wuite GJ, Peterman EJ (2009) Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proc Natl Acad Sci 106(43):18231–18236Google Scholar
  289. 289.
    Williams MC, Rouzina I, Bloomfield VA (2002) Thermodynamics of DNA interactions from single molecule stretching experiments. Acc Chem Res 35(3):159–166Google Scholar
  290. 290.
    Williams MC, Rouzina I, McCauley MJ (2009) Peeling back the mystery of DNA overstretching. Proc Natl Acad Sci 106(43):18047–18048Google Scholar
  291. 291.
    Williams MC, Wenner JR, Rouzina I, Bloomfield VA (2001) Entropy and heat capacity of DNA melting from temperature dependence of single molecule stretching. Biophys J 80(4):1932–1939Google Scholar
  292. 292.
    Bustamante C, Smith SB, Liphardt J, Smith D (2000) Single-molecule studies of DNA mechanics. Curr Opin Struct Biol 10(3):279–285Google Scholar
  293. 293.
    Baumann CG, Smith SB, Bloomfield VA, Bustamante C (1997) Ionic effects on the elasticity of single DNA molecules. Proc Natl Acad Sci 94(12):6185–6190Google Scholar
  294. 294.
    Wang MD, Yin H, Landick R, Gelles J, Block SM (1997) Stretching DNA with optical tweezers. Biophys J 72(3):1335–1346Google Scholar
  295. 295.
    Wenner JR, Williams MC, Rouzina I, Bloomfield VA (2002) Salt dependence of the elasticity and overstretching transition of single DNA molecules. Biophys J 82(6):3160Google Scholar
  296. 296.
    Chiou C-H, Huang Y-Y, Chiang M-H, Lee H-H, Lee G-B (2006) New magnetic tweezers for investigation of the mechanical properties of single DNA molecules. Nanotechnology 17(5):1217Google Scholar
  297. 297.
    Goodman RP, Schaap IA, Tardin CF, Erben CM, Berry RM, Schmidt CF, Turberfield AJ (2005) Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science 310(5754):1661–1665Google Scholar
  298. 298.
    Morii T, Mizuno R, Haruta H, Okada T (2004) An AFM study of the elasticity of DNA molecules. Thin Solid Films 464:456–458Google Scholar
  299. 299.
    Vafabakhsh R, Ha T (2012) Extreme bendability of DNA less than 100 base pairs long revealed by single-molecule cyclization. Science 337(6098):1097–1101Google Scholar
  300. 300.
    Ke C, Humeniuk M, S-Gracz H, Marszalek PE (2007) Direct measurements of base stacking interactions in DNA by single-molecule atomic-force spectroscopy. Phys Rev Lett 99(1):018302–018304Google Scholar
  301. 301.
    W-s C, Chen W-H, Chen Z, Gooding AA, Lin K-J, Kiang C-H (2010) Direct observation of multiple pathways of single-stranded DNA stretching. Phys Rev Lett 105(21):218104Google Scholar
  302. 302.
    Ke C, Loksztejn A, Jiang Y, Kim M, Humeniuk M, Rabbi M, Marszalek PE (2009) Detecting solvent-driven transitions of poly (A) to double-stranded conformations by atomic force microscopy. Biophys J 96(7):2918–2925Google Scholar
  303. 303.
    Seol Y, Skinner GM, Visscher K, Buhot A, Halperin A (2007) Stretching of homopolymeric RNA reveals single-stranded helices and base-stacking. Phys Rev Lett 98(15):158103Google Scholar
  304. 304.
    Rief M, Clausen-Schaumann H, Gaub HE (1999) Sequence-dependent mechanics of single DNA molecules. Nat Struct Mol Biol 6(4):346–349Google Scholar
  305. 305.
    Clausen-Schaumann H, Rief M, Tolksdorf C, Gaub HE (2000) Mechanical stability of single DNA molecules. Biophys J 78(4):1997–2007Google Scholar
  306. 306.
    Lee G, Rabbi M, Clark RL, Marszalek PE (2007) Nanomechanical fingerprints of UV damage to DNA. Small 3(5):809–813Google Scholar
  307. 307.
    Saenger W (1984) Principles of nucleic acid structure, vol 7. Springer-Verlag, New YorkGoogle Scholar
  308. 308.
    Marszalek PE, Pang YP, Li HB, El Yazal J, Oberhauser AF, Fernandez JM (1999) Atomic levers control pyranose ring conformations. Proc Natl Acad Sci USA 96(14):7894–7898Google Scholar
  309. 309.
    Zhang QM, Lee GR, Marszalek PE (2005) Atomic cranks and levers control sugar ring conformations. J Phys Condens Matter 17(18):S1427–S1442Google Scholar
  310. 310.
    Zhang QM, Marszalek PE (2006) Solvent effects on the elasticity of polysaccharide molecules in disordered and ordered states by single-molecule force spectroscopy. Polymer 47(7):2526–2532Google Scholar
  311. 311.
    Li HB, Rief M, Oesterhelt F, Gaub HE, Zhang X, Shen JC (1999) Single-molecule force spectroscopy on polysaccharides by AFM – nanomechanical fingerprint of alpha-(1,4)-linked polysaccharides. Chem Phys Lett 305(3–4):197–201Google Scholar
  312. 312.
    Lee W, Zeng X, Yang W, Marszalek PE (2012) Mechanics of polysaccharides. In: Anne-Sophie Duwez NW (ed) Molecular manipulation with atomic force microscopy. CRC Press, Boca Raton/London/New YorkGoogle Scholar
  313. 313.
    Lee G, Nowak W, Jaroniec J, Zhang Q, Marszalek PE (2004) Nanomechanical control of glucopyranose rotamers. J Am Chem Soc 126(20):6218–6219Google Scholar
  314. 314.
    Lee G, Nowak W, Jaroniec J, Zhang Q, Marszalek PE (2004), Molecular dynamics simulations of forced conformational transitions in 1,6-linked polysaccharides. Biophys J, 87(3):1456–1465.Google Scholar
  315. 315.
    Li H, Rief M, Oesterhelt F, Gaub HE (1999) Force spectroscopy on single xanthan molecules. Appl Phys A-Mater Sci Process 68(4):407–410Google Scholar
  316. 316.
    Li HB, Rief M, Oesterhelt F, Gaub HE (1998) Single-molecule force spectroscopy on Xanthan by AFM. Adv Mater 10(4):316–319Google Scholar
  317. 317.
    Marszalek PE, Li HB, Fernandez JM (2001) Fingerprinting polysaccharides with single-molecule atomic force microscopy. Nat Biotechnol 19(3):258–262Google Scholar
  318. 318.
    Marszalek PE, Li HB, Oberhauser AF, Fernandez JM (2002) Chair-boat transitions in single polysaccharide molecules observed with force-ramp AFM. Proc Natl Acad Sci USA 99(7):4278–4283Google Scholar
  319. 319.
    Zhang Q, Jaroniec J, Lee G, Marszalek PE (2005) Direct detection of inter-residue hydrogen bonds in polysaccharides by single-molecule force spectroscopy. Angew Chem Int Ed 44(18):2723–2727Google Scholar
  320. 320.
    Zhang Q, Lu Z, Hu H, Yang W, Marszalek PE (2006) Direct detection of the formation of V-Amylose helix by single molecule force spectroscopy. J Am Chem Soc 128(29):9387–9393Google Scholar
  321. 321.
    Zhang Q, Marszalek PE (2006) Solvent effects on the elasticity of polysaccharide molecules in disordered and ordered states by single-molecule force spectroscopy. Polymer 47(7):2526–2532Google Scholar
  322. 322.
    Lu ZY, Nowak W, Lee GR, Marszalek PE, Yang WT (2004) Elastic properties of single amylose chains in water: a quantum mechanical and AFM study. J Am Chem Soc 126(29):9033–9041Google Scholar
  323. 323.
    Lee G, Nowak W, Jaroniec J, Zhang Q, Marszalek PE (2004) Molecular dynamics simulations of forced conformational transitions in 1,6-linked polysaccharides. Biophys J 87(3):1456–1465Google Scholar
  324. 324.
    Zhang QM, Marszalek PE (2006) Identification of sugar isomers by single-molecule force spectroscopy. J Am Chem Soc 128(17):5596–5597Google Scholar
  325. 325.
    Xu Q, Zhang W, Zhang X (2002) Oxygen bridge inhibits conformational transition of 1,4-linked -galactose detected by single-molecule atomic force microscopy. Macromolecules 35(3):871–876Google Scholar
  326. 326.
    Marszalek PE, Oberhauser AF, Li HB, Fernandez JM (2003) The force-driven conformations of heparin studied with single molecule force microscopy. Biophys J 85(4):2696–2704Google Scholar
  327. 327.
    Zhang L, Wang C, Cui S, Wang Z, Zhang X (2003) Single-molecule force spectroscopy on curdlan: unwinding helical structures and random coils. Nano Lett 3(8):1119–1124. doi:10.1021/nl034298dGoogle Scholar
  328. 328.
    Struckmeier J, Wahl R, Leuschner M, Nunes J, Janovjak H, Geisler U, Hofmann G, Jähnke T, Müller DJ (2008) Fully automated single-molecule force spectroscopy for screening applications. Nanotechnology 19(38):384020Google Scholar
  329. 329.
    Churnside AB, Sullan RMA, Nguyen DM, Case SO, Bull MS, King GM, Perkins TT (2012) Routine and timely sub-picoNewton force stability and precision for biological applications of atomic force microscopy. Nano Lett 12(7):3557–3561Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Qing Li
    • 1
  • Zackary N. Scholl
    • 2
  • Piotr E. Marszalek
    • 1
  1. 1.Department of Mechanical Engineering and Materials ScienceCenter for Biologically Inspired Materials and Material Systems, and Duke UniversityDurhamUSA
  2. 2.Program in Computational Biology and BioinformaticsDuke UniversityDurhamUSA

Personalised recommendations