A practical guide to single-molecule FRET

Nature Methods

Volumn 5, Issue 6, 2008, Pages 507-516

  Roy, Rahul ^a,b   Hohng, Sungchul ^c   Ha, Taekjip ^a,b,d  

^a United States of America   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c Seoul National University   (South Korea)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CYANINE DYE; DNA; FLUORESCENT DYE; GLUCOSE OXIDASE; HELICASE; MERCAPTOETHANOL; QUANTUM DOT; REACTIVE OXYGEN METABOLITE; RNA; TETRAMETHYLRHODAMINE; TROLOX C;

ALGORITHM; BLEACHING; CALIBRATION; COMPUTER PROGRAM; CONFOCAL MICROSCOPY; COST; DNA SEQUENCE; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH THROUGHPUT SCREENING; INFORMATION PROCESSING; NONHUMAN; OPTICAL RESOLUTION; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; RELIABILITY; REVIEW; SENSITIVITY ANALYSIS; SPECTROSCOPY;

ALGORITHMS; BIOPHYSICS; BIOTECHNOLOGY; BIOTIN; BIOTINYLATION; CALIBRATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; MICROCHEMISTRY; OXYGEN; QUANTUM THEORY; SOFTWARE; SPECTROPHOTOMETRY;

EID: 44449134820     PISSN: 15487091     EISSN: 15491676     Source Type: Journal    
DOI: 10.1038/nmeth.1208     Document Type: Review

References (95)

1. Feynman, R.P. There's plenty of room at the bottom. J. Microelectromech. Syst. 1, 60-66 (1992).
2. Bustamante, C., Bryant, Z. & Smith, S.B. Ten years of tension: single-molecule DNA mechanics. Nature 421, 423-427 (2003).
3. Moerner, W.E. & Fromm, D.P. Methods of single-molecule fluorescence spectroscopy and microscopy. Rev. Sci. Instrum. 74, 3597-3619 (2003).
4. Förster, T. Experimental and theoretical investigation of the intermolecular transfer of electronic excitation energy. Z. Naturforsch. A 4, 321-327 (1949).
5. Ha, T. Single-molecule fluorescence resonance energy transfer. Methods 25, 78-86 (2001).
6. Weiss, S. Fluorescence spectroscopy of single biomolecules. Science 283, 1676-1683 (1999).
7. Joo, C. & Ha, T. Single-molecule FRET with total internal reflection microscopy. in Single Molecule Techniques: A Laboratory Manual. (eds. P. Selvin & T. Ha) 3-36 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2007).
8. Ha, T. et al. Probing the interaction between two single molecules: Fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA 93, 6264-6268 (1996).
9. Kapanidis, A.N. et al. Alternating-laser excitation of single molecules. Acc. Chem. Res. 38, 523-533 (2005).
10. Michalet, X., Weiss, S. & Jager, M. Single-molecule fluorescence studies of protein folding and conformational dynamics. Chem. Rev. 106 1785-1813 (2006).
11. Seidel, R. & Dekker, C. Single-molecule studies of nucleic acid motors. Curr. Opin. Struct. Biol. 17, 80-86 (2007).
12. Smiley, R.D. & Hammes, G.G. Single molecule studies of enzyme mechanisms. Chem. Rev. 106, 3080-3094 (2006).
13. Zhuang, X. Single-molecule RNA science. Annu. Rev. Biophys. Biomol. Struct. 34, 399-414 (2005).
14. Förster, T. Delocalized excitation and excitation transfer. in Modern Quantum Chemistry (ed., O. Shinanoglu) 93-137 (Academic Press, New York, 1967).
15. Stryer, L. & Haugland, R.P. Energy transfer: A spectroscopic ruler. Proc. Natl. Acad. Sci. USA 58, 719-726 (1967).
16. Deniz, A.A. et al. Single-pair fluorescence resonance energy transfer on freely diffusing molecules: Observation of Förster distance dependence and subpopulations. Proc. Natl. Acad. Sci. USA 96, 3670-3675 (1999).
17. Best, R.B. et al. Effect of flexibility and cis residues in single-molecule FRET studies of polyproline. Proc. Natl. Acad. Sci. USA 104, 18964-18969 (2007).
18. Merchant, K.A., Best, R.B., Louis, J.M., Gopich, I.V. & Eaton, W.A. Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations. Proc. Natl. Acad. Sci. USA 104, 1528-1533 (2007).
19. Schuler, B. & Eaton, W.A. Protein folding studied by singte-molecule FRET. Curr. Opin. Struct. Biol. 18, 16-26 (2008).
20. Ha, T., Chemla, D.S., Enderle, T. & Weiss, S. Single molecule spectroscopy with automated positioning. Appl. Phys. Lett. 70 782-784 (1997).
21. Sabanayagam, C.R., Eid, J.S. & Meller, A. High-throughput scanning confocal microscope for single molecule analysis. Appl. Phys. Lett. 84, 1216-1218 (2004).
22. Zhuang, X. et al. A single-molecule study of RNA catalysis and folding. Science 288, 2048-2051 (2000).
23. Brasselet, S., Peterman, E.J.G., Miyawaki, A. & Moerner, W.E. Single-molecule fluorescence resonant energy transfer in calcium concentration dependent cameleon. J. Phys. Chem. B 104, 3676-3682 (2000).
24. Hohng, S. & Ha, T. Single-molecule quantum-dot fluorescence resonance energy transfer. ChemPhysChem 6, 956-960 (2005).
25. Hohng, S. & Ha, T. Near-complete suppression of quantum dot blinking in ambient conditions. J. Am. Chem. Soc. 126, 1324-1325 (2004).
26. Kapanidis, A.N. & Weiss, S. Fluorescent probes and bioconjugation chemistries for single-molecule fluorescence analysis of biomolecules. J. Chem. Phys. 117, 10953-10964 (2002).
27. Hubner, C.G., Renn, A., Renge, I. & Wild, U.P. Direct observation of the triplet lifetime quenching of single dye molecules by molecular oxygen. J. Chem. Phys. 115, 9619-9622 (2001).
28. Rasnik, I., McKinney, S.A. & Ha, T. Nonblinking and long-lasting single-molecule fluorescence imaging. Nat. Methods 3, 891-893 (2006).
29. Rust, M.J., Bates, M. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793-795 (2006).
30. Widengren, J., Chmyrov, A., Eggeling, C., Lofdahl, P.A. & Seidel, C. Strategies to improve photostabilities in ultrasensitive fluorescence spectroscopy. J. Phys. Chem. A 111, 429-440 (2007).
31. Benesch, R.E. & Benesch, R. Enzymatic removal of oxygen for polarography and related methods. Science 118, 447-448 (1953).
32. Aitken, C.E., Marshall, R.A. & Puglisi, J. An oxygen scavenging system for improvement of dye stability in single-molecule fluorescence experiments. Biophys. J. 94, 1826-1835 (2008).
33. Wu, P.G. & Brand, L. Resonance energy transfer: Methods and applications. Anal. Biochem. 218, 1-13 (1994).
34. Clegg, R.M. Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211, 353-388 (1992).
35. Murphy, M.C., Rasnik, I., Cheng, W., Lohman, T.M. & Ha, T. Probing single stranded DNA conformationat flexibility using fluorescence spectroscopy. Biophys. J. 86, 2530-2537 (2004).
36. Ryu, Y.H. & Schultz, P.G. Efficient incorporation of unnatural amino acids into proteins in Escherichia coli. Nat. Methods 3, 263-265 (2006).
37. Higuchi, R., Krummel, B. & Saiki, R.K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: Study of protein and DNA interactions. Nucleic Acids Res. 16, 7351-7367 (1988).
38. Braman, J. In vitro mutagenesis protocols, vol. 182, 2nd edn. (Humana Press, Totowa, New Jersey, 2001).
39. Pennington, M.W. Site-specific chemical modification procedures. Methods Mol. Biol. 35, 171-185 (1994).
40. Axelrod, D. Total internal reflection fluorescence at biological surfaces. in Noninvasive Techniques in Cell Biology. (eds. J.K. Foskett & S. Grinstein) 93-127 (Wiley-Liss, New York, 1990).
41. Axelrod, D. Total internal reflection fluorescence microscopy in cell biology. Methods Enzymol. 361, 1-33 (2003).
42. Michalet, X. et al. Detectors for single-molecule fluorescence imaging and spectroscopy. J. Mod. Opt. 54, 239-281 (2007).
43. Hohng, S., Joo, C. & Ha, T. Single-molecule three-color FRET. Biophys. J. 87, 1328-1337 (2004).
44. Ha, T. et al. Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419, 638-641 (2002).
45. Sofia, S.J., Premnath, V.V. & Merrill, E.W. Poly(ethylene oxide) grafted to silicon surfaces: Grafting density and protein adsorption. Macromolecules 31, 5059-5070 (1998).
46. Schroeder, C.M., Blainey, P.C., Kim, S. & Xie, X.S. Hydrodynamic flow-stretching assay for single-molecule studies of nucleic acid-protein interactions. in Single Molecule Techniques: A Laboratory Manual. (eds, P. Selvin & T. Ha) 461-492 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York; 2007).
47. Heyes, C.D., Kobitski, A.Y., Amirgoulova, E.V. & Nienhaus, G.U. Biocompatible surfaces for specific tethering of individual protein molecules. J. Phys. Chem. B 108, 13387-13394 (2004).
48. Heyes, C.D., Groll, J., Moller, M. & Nienhaus, G.U. Synthesis, patterning and applications of star-shaped poly(ethylene glycol) biofunctionalized surfaces. Mol. Biosyst. 3, 419-430 (2007).
49. Cha, T., Guo, A. & Zhu, X.Y. Enzymatic activity on a chip: The critical role of protein orientation. Proteomics 5, 416-419 (2005).
50. Rhoades, E., Gussakovsky, E. & Haran, G. Watching proteins fold one molecule at a time. Proc. Natl. Acad. Sci. USA 100, 3197-3202 (2003).
51. Okumus, B., Wilson, T.J., Lilley, D.M. & Ha, T. Vesicle encapsulation studies reveal that single molecule ribozyme heterogeneities are intrinsic. Biophys. J. 87, 2798-2806 (2004).
52. Benitez, J.J. et al. Probing transient copper chaperone-Wilson disease protein interactions at the single-molecule level with nanovesicle trapping. J. Am. Chem. Soc. 130, 2446-2447 (2008).
53. Cisse, I., Okumus, B., Joo, C. & Ha, T. Fueling protein-DNA interactions inside porous nanocontainers. Proc. Natl. Acad. Sci. USA 104 12646-12650 (2007).
54. Myong, S., Rasnik, I., Joo, C., Lohman, T.M. & Ha, T. Repetitive shuttling of a motor protein on DNA. Nature 437, 1321-1325 (2005).
55. Van der Meer, B.W. Resonance energy transfer. (Wiley, Chichester, UK, 1999).
56. Ha, T. et al. Single-molecule fluorescence spectroscopy of enzyme conformational dynamics and cleavage mechanism. Proc. Natl. Acad. Sci. USA 96, 893-898 (1999).
57. Joo, C. et al. Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126, 515-527 (2006).
58. Luo, G., Wang, M., Konigsberg, W.H. & Xie, X.S. Single-molecule and ensemble fluorescence assays for a functionally important conformational change in T7 DNA polymerase. Proc. Natl. Acad. Sci. USA 104, 12610-12615 (2007).
59. Clegg, R.M., Murchie, A.I., Zechel, A. & Lilley, D.M. Observing the helical geometry of double-stranded DNA in solution by fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 90, 2994-2998 (1993).
60. Cooper, J.P. & Hagerman, P.J. Analysis of fluorescence energy transfer in duplex and branched DNA molecules. Biochemistry 29, 9261-9268 (1990).
61. Lee, S.P., Porter, D., Chirikjian, J.G., Knutson, J.R. & Han, M.K. A fluorometric assay for DNA cleavage reactions characterized with BamHI restriction endonuclease. Anal. Biochem. 220, 377-383 (1994).
62. Ha, T.J. et al. Temporal fluctuations of fluorescence resonance energy transfer between two dyes conjugated to a single protein. Chem. Phys. 247, 107-118 (1999).
63. Colquhoun, D. & Hawkes, A.G. The principles of the stochastic interpretation of ion-channel mechanism. in Single Channel Recording (eds. B. Sakmann & E. Neher) 397-482 (Plenum Press, New York, 1995).
64. Kim, H.D. et al. Mg2+-dependent conformational change of RNA-studied by fluorescence correlation and FRET on immobilized single molecules. Proc. Natl. Acad. Sci. USA 99, 4284-4289 (2002).
65. McKinney, S.A., Joo, C. & Ha, T. Analysis of single-molecule FRET trajectories using hidden Markov modeling. Biophys. J. 91, 1941-1951 (2006).
66. Munro, J.B., Altman, R.B., O'Connor, N. & Blanchard, S.C. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell 25, 505-517 (2007).
67. Myong, S., Bruno, M.M., Pyle, A.M. & Ha, T. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 317 513-516 (2007).
68. Yang, H. & Xie, X.S. Probing single-molecule dynamics photon by photon. J. Chem. Phys. 117, 10965-10979 (2002).
69. Andrec, M., Levy, R.M. & Talaga, D.S. Direct determination of kinetic rates from single-molecule photon arrival trajectories using hidden Markov models. J. Phys. Chem. A 107, 7454-7464 (2003).
70. Schroder, G.F. & Grubmuller, H. Maximum likelihood trajectories from single molecule fluorescence resonance energy transfer experiments. J. Chem. Phys. 119, 9920-9924 (2003).
71. Blanchard, S.C., Gonzalez, R.L., Kim, H.D., Chu, S. & Puglisi, J.D. tRNA selection and kinetic proofreading in translation. Nat. Struct. Mol.-Biol. 11, 1008-1014 (2004).
72. Smith, G.J., Sosnick, T.R., Scherer, N.F. & Pan, T. Efficient fluorescence labeling of a large RNA through oligonucleotide hybridization. RNA 11, 234-239 (2005).
73. Dorywalska, M. et al. Site-specific labeling of the ribosome for single-molecule spectroscopy. Nucleic Acids Res. 33, 182-189 (2005).
74. Deniz, A.A. et al. Single-molecule protein folding: Diffusion fluorescence resonance energy transfer studies of the denaturation of chymotrypsin inhibitor 2. Proc. Natl. Acad. Sci. USA 97, 5179-5184 (2000).
75. Jager, M., Nir, E. & Weiss, S. Site-specific labeling of proteins for single-molecule FRET by combining chemical and enzymatic modification. Protein Sci. 15, 640-646 (2006).
76. Dale, R.E., Eisinger, J. & Blumberg, W.E. Orientational freedom of molecular probes: Orientation factor in intra-molecular energy transfer. Biophys. J. 26, 161-193 (1979).
77. Schuler, B., Lipman, E.A., Steinbach, P.J., Kumke, M. & Eaton, W.A. Polyprotine and the "spectroscopic ruler" revisited with single-molecule fluorescence. Proc. Natl. Acad. Sci. USA 102 2754-2759 (2005).
78. Rothwell, P.J. et al. Multiparameter single-molecule fluorescence spectroscopy reveals heterogeneity of HIV-1 reverse transcriptase:pRimer/ template complexes. Proc. Natl. Acad. Sci. USA 100, 1655-1660 (2003).
79. Rasnik, I., Myong, S., Cheng, W., Lohman, T.M. & Ha, T. DNA-binding orientation and domain conformation of the E. coli rep helicase monomer bound to a partial duplex junction: Single-molecule studies of fluorescently labeled enzymes. J. Mol. Biol. 336, 395-408 (2004).
80. Andrecka, J. et al. Single-molecule tracking of mRNA exiting from RNA polymerase II. Proc. Natl. Acad. Sci. USA 105, 135-140 (2008).
81. Clamme, J.P. & Deniz, A.A. Three-color single-molecule fluorescence resonance energy transfer. ChemPhysChem 6, 74-77 (2005).
82. Heinze, K.G., Jahnz, M. & Schwille, P. Triple-color coincidence analysis: One step further in following higher order molecular complex formation. Biophys. J. 86, 506-516 (2004).
83. Kapanidis, A.N. et al. Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc. Natl. Acad. Sci. USA 101, 8936-8941 (2004).
84. Muller, B.K., Zaychikov, E., Brauchle, C. & Lamb, D.C. Pulsed interleaved excitation. Biophys. J. 89, 3508-3522 (2005).
85. Lee, N.K. et al. Three-color alternating-laser excitation of single molecules: Monitoring multiple interactions and distances. Biophys. J. 92, 303-312 (2007).
86. Heilemann, M. et al. Multistep energy transfer in single molecular photonic wires. J. Am. Chem. Soc. 126, 6514-6515 (2004).
87. Lang, M., Fordyce, P. & Block, S. Combined optical trapping and single-molecule fluorescence. J. Biol. 2, 6 (2003).
88. Tarsa, P.B. et al. Detecting force-induced molecular transitions with fluorescence resonant energy transfer. Angew. Chem. Int. Ed. 46, 1999-2001 (2007).
89. Shroff, H. et al. Biocompatible force sensor with optical readout and dimensions of 6 nm(3). Nano Lett. 5, 1509-1514 (2005).
90. Hohng, S. et al. Fluorescence-force spectroscopy maps two-dimensional reaction landscape of the holliday junction. Science 318, 279-283 (2007).
91. Borisenko, V. et al. Simultaneous optical and electrical recording of single gramicidin channels. Biophys. J. 84, 612-622 (2003).
92. Harms, G.S. et al. Probing conformational changes of gramicidin ion channels by single-molecule patch-clamp fluorescence microscopy. Biophys. J. 85, 1826-1838 (2003).
93. Tan, E. et al. A four-way junction accelerates hairpin ribozyme folding via a discrete intermediate. Proc. Natl. Acad. Sci. USA 100, 9308-9313 (2003).
94. Jager, M., Michalet, X. & Weiss, S. Protein-protein interactions as a tool for site-specific labeling of proteins. Protein Sci. 14 2059-2068 (2005).
95. Ratner, V., Kahani, E., Eichler, M. & Haas, E. A general strategy for site-specific double labeling of globular proteins for kinetic FRET studies. Bioconjug. Chem. 13, 1163-1170 (2002).