Grabbing the cat by the tail: manipulating molecules one by one

Nature Reviews Molecular Cell Biology

Volumn 1, Issue 2, 2000, Pages 130-136

  Bustamante, Carlos ^a   Macosko, Jed C ^a   Wuite, Gijs J L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FELIS CATUS;

DNA; DNA DIRECTED RNA POLYMERASE; MOLECULAR MOTOR; PROTEIN;

ATOMIC FORCE MICROSCOPY; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; METHODOLOGY; MOLECULAR BIOLOGY; PHYSIOLOGY; REVIEW; ULTRASTRUCTURE;

DNA; DNA-DIRECTED RNA POLYMERASES; MICROCHEMISTRY; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOLECULAR BIOLOGY; MOLECULAR MOTOR PROTEINS; PROTEINS;

EID: 0034328878     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/35040072     Document Type: Review

References (66)

1. Bustamante, C., Smith, S., Liphardt, J. & Smith, D. Single-molecule studies of DNA mechanics. Curr. Opin. Struct. Biol. 10, 279-285 (2000).
2. Svoboda, K. & Block, S. M. Biological applications of optical forces. Annu. Rev. Biophys. Biomol. Struct. 23, 247-285 (1994).
3. Ludwig, M. et al. AFM, a tool for single-molecule experiments. Appl. Phys. Mater. Sci. Process. 68, 173-176 (1999).
4. Mehta, A. D., Rief, M. & Spudich, J. A. Biomechanics, one molecule at a time. J. Biol. Chem. 274, 14517-14520 (1999).
5. Sarid, D. in Scanning Force Microscopy: With Applications to Electric, Magnetic, and Atomic Forces I-XI, 253 (Oxford Univ. Press, New York, 1991).
6. Carrion-Vazquez, M. et al. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl Acad. Sci. USA 96, 3694-3699 (1999).
7. Bustamante, C., Marko, J. F., Siggia, E. D. & Smith, S. Entropic elasticity of lambda-phage DNA. Science 265, 1599-1600 (1994).
8. Smith, S. B., Finzi, L. & Bustamante, C. Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122-1126 (1992). This first single-molecule study of DNA elasticity demonstrates the combined use of magnetic and flow fields.
9. Marko, J. F. & Siggia, E. D. Stretching DNA. Macromolecules 28, 8759-8770 (1995).
10. Erie, D. A., Yang, G., Schultz, H. C. & Bustamante, C. DNA bending by Cro protein in specific and nonspecific complexes: implications for protein site recognition and specificity. Science 266, 1562-1566 (1994).
11. Wuite, G. J., Smith, S. B., Young, M., Keller, D. & Bustamante, C. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404, 103-106(2000).
12. Kishino, A. & Yanagida, T. Force measurements by micromanipulation of a single actin filament by glass needles. Nature 334, 74-76 (1988). The basic premise of microneedle manipulation is illustrated here in one of the earliest measurements of the force from biological molecules using a mechanical transducer.
13. Svoboda, K., Schmidt, C. F., Schnapp, B. J. & Block, S. M. Direct observation of kinesin stepping by optical trapping interferometry. Nature 365, 721-727 (1993).
14. Howard, J., Hudspeth, A. J. & Vale, R. D. Movement of microtubules by single kinesin molecules. Nature 342, 154-158 (1989).
15. Ishijima, A., Doi, T., Sakurada, K. & Yanagida, T. Subpiconewton force fluctuations of actomyosin in vitro. Nature 352, 301-306 (1991).
16. Nakajima, H. et al. Scanning force microscopy of the interaction events between a single molecule of heavy meromyosin and actin. Biochem. Biophys. Res. Commun. 234, 178-182 (1997).
17. Rotsch, C., Jacobson, K. & Radmacher, M. Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Natl Acad. Sci. USA 96, 921-926 (1999).
18. Viani, M. B. et al. Small cantilevers for force spectroscopy of single molecules. J. Appl. Phys. 86, 2258-2262 (1999).
19. Müller, D. J., Baumeister, W. & Engel, A. Controlled unzipping of a bacterial surface layer with atomic force microscopy. Proc. Natl Acad Sci. USA 96, 13170-13174 (1999).
20. Oesterhelt, F. et al. Unfolding pathways of individual bacteriorhodopsins. Science 288, 143-146 (2000). In this study of a membrane protein, the authors present an elegant example of combining force and imaging SFM.
21. Finer, J. T., Simmons, R. M. & Spudich, J. A. Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113-119 (1994).
22. Thomson, N.H. et al. Protein tracking and detection of protein motion using atomic force microscopy. Biophys. J. 70, 2421-2431 (1996).
23. Almqvist, N. et al. Methods for fabricating and characterizing a new generation of biomimetic materials. Mater. Sci. Eng. C 7, 37-43 (1999).
24. Viani, M. B. et al. Fast imaging and fast force spectroscopy of single biopolymers with a new atomic force microscope designed for small cantilevers. Rev. Sci Instrum. 70, 4300-4303 (1999).
25. Kitamura, K., Tokunaga, M., Iwane, A. H. & Yanagida, T. A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature 397, 129-134 (1999).
26. Kellermayer, M. S. & Granzier, H. L. Elastic properties of single titin molecules made visible through fluorescent F-actin binding. Biochem. Biophys. Res. Commun. 221, 491-497 (1996).
27. Ishijima, A. et al. Multiple- and single-molecule analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: unitary steps and forces. Biophys. J. 70, 383-400 (1996).
28. Essevaz-Roulet, B., Bockelmann, U. & Heslot, F. Mechanical separation of the complementary strands of DNA. Proc. Natl Acad. Sci USA 94, 11935-11940 (1997).
29. Cluzel, P. et al. DNA: an extensible molecule. Science 271, 792-794 (1996).
30. Leger, J. F., Robert, J., Bourdieu, L., Chatenay, D. & Marko, J. F. RecA binding to a single double-stranded DNA molecule: A possible role of DNA conformational fluctuations. Proc. Natl Acad. Sci. USA 95, 12295-12299 (1998).
31. Leger, J. F. et al. Structural transitions of a twisted and stretched DNA molecule. Phys. Rev. Lett. 83, 1066-1069 (1999).
32. Oosawa, F. Actin-actin bond strength and the conformational change of F-actin. Biorheology 14, 11-19 (1977).
33. Lorentz, H. A. Abhändlungen über Theoretische Physik (Teubner, Leipzig, 1907).
34. Happel, J. B., H. Low Reynolds Number Hydrodynamics with Special Applications to Particulate Media (Prentice Hall, Englewood Cliffs, New Jersey, 1991).
35. Berg, H. C. Random Walks in Biology (Princeton Univ. Press, New Jersey, 1983).
36. Davenport, R. J., Wuite, G. J., Landick, R. & Bustamante, C. Single-molecule study of transcriptional pausing and arrest by E. coli RNA polymerase. Science 287, 2497-2500 (2000).
37. Smith, D. E., Babcock, H. P. & Chu, S. Single-polymer dynamics in steady shear flow. Science 283, 1724-1727 (1999).
38. Perkins, T. T., Smith, D. E., Larson, R. G. & Chu, S. Stretching of a single tethered polymer in a uniform flow. Science 268, 83-87 (1995). This paper describes how flow fields can be used to stretch DNA and reveal new facets of single-molecule polymer rheology.
39. Perkins, T. T., Quake, S. R., Smith, D. E. & Chu, S. Relaxation of a single DNA molecule observed by optical microscopy. Science 264, 822-826 (1994).
40. Strick, T. R., Allemand, J. F., Bensimon, D., Bensimon, A. & Croquette, V. The elasticity of a single supercoiled DNA molecule. Science 271, 1835-1837 (1996).
41. Strick, T. R., Croquette, V. & Bensimon, D. Single-molecule analysis of DNA uncoiling by a type II topoisomerase. Nature 404, 901-904 (2000). Here, to investigate the activity of individual topoisomerase molecules, magnetic force is used to twist a molecule of DNA and supercoil it.
42. Ashkin, A., Dziedzic, J., Bjorkholm, J. & Chu, S. Observation of a single-beam gradient force optical trap for dielectric particles. Optical Lett. 11, 288-290 (1986).
43. Gordon, J. P. Radiation forces and momenta in dielectric media. Phys. Rev. A 8, 14-21 (1973).
44. Ashkin, A. Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime. Biophys. J. 61, 569-582 (1992).
45. Wright, W. H., Sonek, G. J. & Berns, M. W. Parametric study of the forces on microspheres held by optical tweezers. Appl. Optics 33, 1735-1748 (1994).
46. Chu, S. Laser manipulation of atoms and particles. Science 253, 861-866 (1991).
47. Smith, S. B., Cui, Y. & Bustamante, C. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271, 795-799 (1996).
48. Yin, H. et al. Transcription against an applied force. Science 270, 1653-1657 (1995).
49. Kuo, S. C. & Sheetz, M. P. Force of single kinesin molecules measured with optical tweezers. Science 260, 232-234 (1993).
50. Ashkin, A. & Dziedzic, J. M. Optical trapping and manipulation of viruses and bacteria. Science 235, 1517-1520 (1987). This landmark paper demonstrates the power of optical traps to manipulate microscopic objects.
51. Wang, M. D. et al. Force and velocity measured for single molecules of RNA polymerase. Science 282, 902-907 (1998). By using an optical trap, the authors reveal aspects of transcription on a single molecule level.
52. Kellermayer, M. S., Smith, S. B., Granzier, H. L. & Bustamante, C. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276, 1112-1116 (1997); erratum 277, 1117 (1997).
53. Tskhovrebova, L., Trinick, J., Sleep, J. A. & Simmons, R. M. Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387, 308-312 (1997).
54. 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 394, 52-55 (1998).
55. Cheung, C. L., Hafner, J. H. & Lieber, C. M. Carbon nanotube atomic force microscopy tips: direct growth by chemical vapor deposition and application to high-resolution imaging. Proc. Natl Acad. Sci. USA 97, 3809-3813 (2000).
56. Kim, P. & Lieber, C. M. Nanotube nanotweezers. Science 286, 2148-2150 (1999).
57. Skibbens, R. V. & Salmon, E. D. Micromanipulation of chromosomes in mitotic vertebrate tissue cells: tension controls the state of kinetochore movement. Exp. Cell Res. 235, 314-324 (1997).
58. Roy, P., Petroll, W. M., Cavanagh, H. D., Chuong, C. J. & Jester, J. V. An in vitro force measurement assay to study the early mechanical interaction between corneal fibroblasts and collagen matrix. Exp. Cell Res. 232, 106-117 (1997).
59. Rotsch, C., Braet, F., Wisse, E. & Radmacher, M. AFM imaging and elasticity measurements on living rat liver macrophages. Cell Biol. Int. 21, 685-696 (1997).
60. Muramoto, K. et al. High-speed rotation and speed stability of the sodium-driven flagellar motor in Vibrio alginolyticus. J. Mol. Biol. 251, 50-58 (1995).
61. Muramoto, K. et al. Rotational fluctuation of the sodium-driven flagellar motor of Vibrio alginolyticus induced by binding of inhibitors. J. Mol. Biol. 259, 687-695 (1996).
62. Chand, A., Viani, M. B., Schaffer, T. E. & Hansma, P. K. Microfabricated small metal cantilevers with silicon tip for atomic force microscopy. J. Microelectromech. Sys. 9, 112-116 (2000).
63. Osheroff, N., Shelton, E. R. & Brutlag, D. L. DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem. 258, 9536-9543 (1983).
64. Fisher, T. E., Oberhauser, A. F., Carrion-Vazquez, M., Marszalek, P. E. & Fernandez, J. M. The study of protein mechanics with the atomic force microscope. Trends Biochem. Sci. 24, 379-384 (1999); erratum 25, 6 (2000).
65. Florin, E. L., Moy, V. T. & Gaub, H. E. Adhesion forces between individual ligand-receptor pairs. Science 264, 415-417 (1994).
66. Lee, G. U., Chrisey, L. A. & Colton, R. J. Direct measurement of the forces between complementary strands of DNA. Science 266, 771-773 (1994).