Force spectroscopy 101: How to design, perform, and analyze an AFM-based single molecule force spectroscopy experiment

Current Opinion in Chemical Biology

Volumn 15, Issue 5, 2011, Pages 710-718

  Noy, Aleksandr ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; LIGAND; POLYMER; PROTEIN; RECEPTOR; RNA;

ATOMIC FORCE MICROSCOPY; CHEMICAL BOND; DISSOCIATION; DYNAMIC FORCE SPECTROSCOPY; ENERGY; EQUIPMENT DESIGN; EXPERIMENTAL DESIGN; FORCE; MECHANICS; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; MOLECULAR PROBE; MOLECULAR STABILITY; NOISE; PROTEIN DNA INTERACTION; PROTEIN INTERACTION; PROTEIN RNA BINDING; REVIEW; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY;

HUMANS; KINETICS; MICROSCOPY, ATOMIC FORCE; NANOTECHNOLOGY; NANOTUBES, CARBON; POLYETHYLENE GLYCOLS; RESEARCH DESIGN; SPECTRUM ANALYSIS; SULFHYDRYL COMPOUNDS; SURFACE PROPERTIES; THERMODYNAMICS;

EID: 80053564705     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.07.020     Document Type: Review

References (62)

1. Muller D.J., Dufrene Y.F. Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. Nat Nanotechnol 2008, 3:261-269.
2. Bustamante C., Bryant Z., Smith S.B. Ten years of tension: single-molecule DNA mechanics. Nature 2003, 421:423-427.
3. Bustamante C., Macosko J.C., Wuite G.J.L. Grabbing the cat by the tail: manipulating molecules one by one. Nat Rev Mol Cell Biol 2000, 1:130-136.
4. Handbook of Molecular Force Spectroscopy 2008, Springer, New York. A. Noy (Ed.).
5. Albrecht T.R., Akamine S., Carver T.E., Quate C.F. Microfabrication of cantilever styli for the atomic force microscope. J Vac Sci Technol A, Vac Surf Films 1990, 8:3386-3396.
6. Israelachvili J. Intermolecular and Surface Forces 1992, Academic Press, New York.
7. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Phys Rev Lett 1986, 56:930-933.
8. Mate C., McClelland G., Erlandsson R., Chiang S. Atomic scale friction of a tungsten tip on a graphite surface. Phys Rev Lett 1987, 59:1942-1945.
9. Meyer G., Amer N.M. Novel optical approach to atomic force microscopy. Appl Phys Lett 1988, 53:1045-1047.
10. Burnham N.A., Colton R.J., Pollock H.M. Interpretation issues in force microscopy. J Vac Sci Technol A 1991, 9:2548-2556.
11. Noy A., Frisbie C.D., Rozsnyai L.F., Wrighton M.S., Lieber C.M. Chemical force microscopy-exploiting chemically-modified tips to quantify adhesion, friction, and functional-group distributions in molecular assemblies. J Am Chem Soc 1995, 117:7943-7951.
12. Florin E.L., Moy V.T., Gaub H.E. Adhesion forces between individual ligand-receptor pairs. Science 1994, 264:415-417.
13. Ducker W.A., Senden T.J., Pashley R.M. Direct measurement of colloidal forces using an atomic force microscope. Nature 1991, 353:239-241.
14. Muller D.J., Helenius J., Alsteens D., Dufrene Y.F. Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 2009, 5:383-390.
15. Friddle R., Le Mieux M., Cicero G., Artyukhin A., Tsukruk V., Grossman J., Galli G., Noy A. Single functional group interactions with sidewalls of individual carbon nanotubes. Nat Nanotechnol 2007, 2:692-697.
16. Sinniah S.K., Steel A.B., Miller C.J., Reutt-Robey J.E. Solvent exclusion and chemical contrast in scanning force microscopy. J Am Chem Soc 1996, 118:8925-8931.
17. Hinterdorfer P., Dufrene Y.F. Detection and localization of single molecular recognition events using atomic force microscopy. Nat Meth 2006, 3:347-355.
18. Fuhrmann A., Ros R. Single-molecule force spectroscopy: a method for quantitative analysis of ligand-receptor interactions. Nanomedicine 2010, 5:657-666.
19. Clausen-Schaumann H., Seitz M., Krautbauer R., Gaub H.E. Force spectroscopy with single bio-molecules. Curr Opin Chem Biol 2000, 4:524-530.
20. Neuman K.C., Nagy A. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat Meth 2008, 5:491-505.
21. Wong S.S., Joselevich E., Woolley A.T., Cheung C.L., Lieber C.M. Covalently functionalized nanotubes as nanometre-sized probes in chemistry and biology. Nature 1998, 394:52-55.
22. Wong S.S., Harper J.D., Lansbury P.T., Lieber C.M. Carbon nanotube tips: high-resolution probes for imaging biological systems. J Am Chem Soc 1998, 120:603-604.
23. Bell G.I. Models for the specific adhesion of cells to cells. Science 1978, 200:618-627.
24. Evans E., Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys J 1997, 72:1541-1555.
25. Merkel R., Nassoy P., Leung A., Ritchie K., Evans E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 1999, 397:50-53.
26. Evans E. Energy landscapes of biomolecular adhesion and receptor anchoring at interfaces explored with dynamic force spectroscopy. Farad Disc 1999, 111:1-16.
27. Dudko O.K., Hummer G., Szabo A. Intrinsic rates and activation free energies from single-molecule pulling experiments. Phys Rev Lett 2006, 96:108101-108104.
28. Hummer G., Szabo A. Kinetics from nonequilibrium single-molecule pulling experiments. Biophys J 2003, 85:5-15.
29. Hummer G., Szabo A. Free energy reconstruction from nonequilibrium single-molecule pulling experiments. Proc Natl Acad Sci U S A 2001, 98:3658-3661.
30. Dudko O.K., Filippov A.E., Klafter J., Urbakh M. Beyond the conventional description of dynamic force spectroscopy of adhesion bonds. Proc Natl Acad Sci U S A 2003, 100:11378-11381.
31. Getfert S., Evstigneev M., Reimann P. Single-molecule force spectroscopy: practical limitations beyond Bell's model. Phys A: Stat Mech Appl 2009, 388:1120-1132.
32. Dudko O.K., Hummer G., Szabo A. Theory, analysis, and interpretation of single-molecule force spectroscopy experiments. Proc Natl Acad Sci U S A 2008, 105:15755-15760.
33. Strunz T., Oroszlan K., Schafer R., Guntherodt H.J. Dynamic force spectroscopy of single DNA molecules. Proc Natl Acad Sci U S A 1999, 96:11277-11282.
34. Pope L.H., Davies M.C., Laughton C.A., Roberts C.J., Tendler S.J., Williams P.M. Force-induced melting of a short DNA double helix. Eur Biophys J 2001, 30:53-62.
35. Green N.H., Williams P.M., Wahab O., Davies M.C., Roberts C.J., Tendler S.J., Allen S. Single-molecule investigations of RNA dissociation. Biophys J 2004, 86:3811-3821.
36. Kuhner F., Costa L.T., Bisch P.M., Thalhammer S., Heckl W.M., Gaub H.E. LexA-DNA bond strength by single molecule force spectroscopy. Biophys J 2004, 87:2683-2690.
37. Williams P.M., Fowler S.B., Best R.B., Toca-Herrera J.L., Scott K.A., Steward A., Clarke J. Hidden complexity in the mechanical properties of titin. Nature 2003, 422:446-449.
38. Patel A.B., Allen S., Davies M.C., Roberts C.J., Tendler S.J.B., Williams P.M. Influence of architecture on the kinetic stability of molecular assemblies. J Am Chem Soc 2004, 126:1318-1319.
39. Rigby-Singleton S.M., Allen S., Davies M.C., Roberts C.J., Tendler S.J.B., Williams P.M. Direct measurement of drug-enzyme interactions by atomic force microscopy; dihydrofolate reductase and methotrexate. J Chem Soc-Perk Trans 2002, 2:1722-1727.
40. Carl P., Kwok C.H., Manderson G., Speicher D.W., Discher D.E. Forced unfolding modulated by disulfide bonds in the Ig domains of a cell adhesion molecule. Proc Natl Acad Sci U S A 2001, 98:1565.
41. Law R., Liao G., Harper S., Yang G., Speicher D.W., Discher D.E. Pathway shifts and thermal softening in temperature-coupled forced unfolding of spectrin domains. Biophys J 2003, 85:3286-3293.
42. Smith D.A., Brockwell D.J., Zinober R.C., Blake A.W., Beddard G.S., Olmsted P.D., Radford S.E. Unfolding dynamics of proteins under applied force. Phil Trans Roy Soc Lond Ser A 2003, 361:713-728.
43. Tskhovrebova L., Trinick J., Sleep J., Simmons R. Elasticity and unforlding of single molecules of the giant muscle protein titin. Nature 1997, 387:308-312.
44. Evans E., Williams P. Dynamic force spectroscopy. II. Multiple bonds. Physics of Bio-Molecules and Cells 2002, 187-203. Springer and EDP Sciences, [Les Houches-Ecole d'Ete de Physique Theorique, vol 75]. H. Flyvbjerg, F. Jülicher, P. Ormos, F. David (Eds.).
45. Luan B., Robbins M.O. The breakdown of continuum models for mechanical contacts. Nature 2005, 435:929-932.
46. Sulchek T., Friddle R.W., Noy A. Strength of multiple parallel biological bonds. Biophys J 2006, 90:4686-4691.
47. Evans E. Probing the relation between force-lifetime and chemistry in single molecular bonds. Ann Rev Biophys Biomol Struct 2001, 30:105-128.
48. Friddle R., Podsiadlo P., Artyukhin A.B., Noy A. Near-equilibrium chemical force microscopy. J Phys Chem C 2008, 112:4986-4990.
49. Ashby P.D., Lieber C.M. Brownian force profile reconstruction of interfacial 1-nonanol solvent structure. J Am Chem Soc 2004, 126:16973-16980.
50. Morfill J., Neumann J., Blank K., Steinbach U., Puchner E.M., Gottschalk K.E., Gaub H.E. Force-based analysis of multidimensional energy landscapes: application of dynamic force spectroscopy and steered molecular dynamics simulations to an antibody fragment-peptide complex. J Mol Biol 2008, 381:1253-1266.
51. Sulchek T.A., Friddle R.W., Langry K., Lau E.Y., Albrecht H., Ratto T.V., DeNardo S.J., Colvin M.E., Noy A. Dynamic force spectroscopy of parallel individual Mucin1-antibody bonds. Proc Natl Acad Sci U S A 2005, 102:16638-16643.
52. Brockwell D.J., Paci E., Zinober R.C., Beddard G.S., Olmsted P.D., Smith D.A., Perham R.N., Radford S.E. Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nat Struct Biol 2003, 10:731-737.
53. Dietz H., Rief M. Exploring the energy landscape of GFP by single-molecule mechanical experiments. Proc Natl Acad Sci U S A 2004, 101:16192-16197.
54. Fritz J., Katopodis A.G., Kolbinger F., Anselmetti D. Force-mediated kinetics of single P-selectin/ligand complexes observed by atomic force microscopy. Proc Natl Acad Sci U S A 1998, 95:12283.
55. Friedsam C., Wehle A.K., Kuhner F., Gaub H.E. Dynamic single-molecule force spectroscopy: bond rupture analysis with variable spacer length. J Phys Condens Matter 2003, 15:S1709-S1723.
56. Ray C., Brown J.R., Akhremitchev B.B. Correction of systematic errors in single-molecule force spectroscopy with polymeric tethers by atomic force microscopy. J Phys Chem B 2007, 111:1963-1974.
57. Li N., Guo S., Akhremitchev B.B. Apparent dependence of rupture force on loading rate in single molecule force spectroscopy. ChemPhysChem 2010, 11:2096-2098.
58. Oesterhelt F., Rief M., Gaub H.E. Single molecule force spectroscopy by AFM indicates helical structure of poly(ethylene-glycol) in water. New J Phys 1999, 1:1-11.
59. Heymann B., Grubmuller H. Dynamic force spectroscopy of molecular adhesion bonds. Phys Rev Lett 2000, 84:6126-6129.
60. Zepeda S., Yeh Y., Noy A. Determination of energy barriers for intermolecular interactions by variable temperature dynamic force spectroscopy. Langmuir 2003, 19:1457-1461.
61. Guo B., Guilford W.H. Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction. Proc Natl Acad Sci U S A 2006, 103:9844-9849.
62. Lulevich V., Kim S., Grigoropoulos C.P., Noy A. Frictionless sliding of single-stranded dna in a carbon nanotube pore observed by single molecule force spectroscopy. Nano Lett 2011, 11:1171-1176.