High-throughput single-molecule studies of protein-DNA interactions

FEBS Letters

Volumn 588, Issue 19, 2014, Pages 3539-3546

  Robison, Aaron D ^a   Finkelstein, Ilya J ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

DNA curtains; Force spectroscopy; Particle tracking

Indexed keywords

FLUORESCENT DYE; DNA; PROTEIN;

CELL LABELING; CONCENTRATION (PARAMETERS); DATA ANALYSIS; DNA DETERMINATION; EQUIPMENT DESIGN; FLUORESCENCE IMAGING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIGH THROUGHPUT SCREENING; MAGNETIC TWEEZER; MICROFLUIDIC ANALYSIS; MOLECULAR IMAGING; NONHUMAN; OPTICAL INSTRUMENTATION; OPTICAL RESOLUTION; OPTICAL TWEEZERS; PROCESS CONTROL; PROCESS DESIGN; PROCESS DEVELOPMENT; PROCESS OPTIMIZATION; PROCESS TECHNOLOGY; PROTEIN DNA INTERACTION; PROTEIN NUCLEIC ACID INTERACTION; REVIEW; SINGLE MOLECULAR IMAGING; DNA CURTAINS; FORCE SPECTROSCOPY; METABOLISM; PARTICLE TRACKING; PROTEIN BINDING; SPECTROSCOPY;

DNA CURTAINS; FORCE SPECTROSCOPY; PARTICLE TRACKING;

DNA; PROTEIN BINDING; PROTEINS; SPECTRUM ANALYSIS;

EID: 84907811769     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.05.021     Document Type: Review

References (93)

1. S.M. Hamdan, J.J. Loparo, M. Takahashi, C.C. Richardson, and A.M. van Oijen Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis Nature 457 2008 336 339
2. H. Yardimci, X. Wang, A.B. Loveland, I. Tappin, D.Z. Rudner, J. Hurwitz, A.M. van Oijen, and J.C. Walter Bypass of a protein barrier by a replicative DNA helicase Nature 492 2012 205 209
3. N.Y. Yao, R.E. Georgescu, J. Finkelstein, and M.E. O'Donnell Single-molecule analysis reveals that the lagging strand increases replisome processivity but slows replication fork progression Proc. Natl. Acad. Sci. 106 2009 13236 13241
4. E.A. Galburt, S.W. Grill, and C. Bustamante Single molecule transcription elongation Methods 48 2009 323 332
5. F. Wang, and E.C. Greene Single-molecule studies of transcription: from one RNA polymerase at a time to the gene expression profile of a cell J. Mol. Biol. 412 2011 814 831
6. M.H. Larson, R. Landick, and S.M. Block Single-molecule studies of RNA polymerase: one singular sensation, every little step it takes Mol. Cell 41 2011 249 262
7. H. Neumann, S.M. Hancock, R. Buning, A. Routh, L. Chapman, J. Somers, T. Owen-Hughes, J. van Noort, D. Rhodes, and J.W. Chin A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation Mol. Cell 36 2009 153 163
8. I.J. Finkelstein, and E.C. Greene Single molecule studies of homologous recombination Mol. Biosyst. 4 2008 1094
9. N.M. Kad, H. Wang, G.G. Kennedy, D.M. Warshaw, and B. Van Houten Collaborative dynamic DNA scanning by nucleotide excision repair proteins investigated by single- molecule imaging of quantum-dot-labeled proteins Mol. Cell 37 2010 702 713
10. A.A. Hoskins, L.J. Friedman, S.S. Gallagher, D.J. Crawford, E.G. Anderson, R. Wombacher, N. Ramirez, V.W. Cornish, J. Gelles, and M.J. Moore Ordered and dynamic assembly of single spliceosomes Science 331 2011 1289 1295
11. H. Yardimci, A.B. Loveland, A.M. van Oijen, and J.C. Walter Single-molecule analysis of DNA replication in Xenopus egg extracts Methods 57 2012 179 186
12. R. Krishnan, M.R. Blanco, M.L. Kahlscheuer, J. Abelson, C. Guthrie, and N.G. Walter Biased Brownian ratcheting leads to pre-mRNA remodeling and capture prior to first-step splicing Nat. Struct. Mol. Biol. 20 2013 1450 1457
13. Z.W. Zhao, R. Roy, J.C.M. Gebhardt, D.M. Suter, A.R. Chapman, and X.S. Xie Spatial organization of RNA polymerase II inside a mammalian cell nucleus revealed by reflected light-sheet superresolution microscopy Proc. Natl. Acad. Sci. 111 2014 681 686
14. Y. Doksani, J.Y. Wu, T. de Lange, and X. Zhuang Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent T-loop formation Cell 155 2013 345 356
15. R. Roy, S. Hohng, and T. Ha A practical guide to single-molecule FRET Nat. Methods 5 2008 507 516
16. S. Preus, and L.M. Wilhelmsson Advances in quantitative FRET-based methods for studying nucleic acids Chembiochem Eur. J. Chem. Biol. 13 2012 1990 2001
17. H. Kim, and T. Ha Single-molecule nanometry for biological physics Rep. Prog. Phys. 76 2013 016601
18. S. Hohng, S. Lee, J. Lee, and M.H. Jo Maximizing information content of single-molecule FRET experiments: multi-color FRET and FRET combined with force or torque Chem. Soc. Rev. 43 2014 1007
19. J. Hohlbein, T.D. Craggs, and T. Cordes Alternating-laser excitation: single-molecule FRET and beyond Chem. Soc. Rev. 43 2014 1156
20. T. Plenat, C. Tardin, P. Rousseau, and L. Salome High-throughput single-molecule analysis of DNA-protein interactions by tethered particle motion Nucleic Acids Res. 40 2012 e89-e89
21. O.K. Wong, M. Guthold, D.A. Erie, and J. Gelles interconvertible lac repressor-DNA loops revealed by single-molecule experiments PLoS Biol. 6 2008 e232
22. D. Dunlap, C. Zurla, C. Manzo, and L. Finzi Probing DNA topology using tethered particle motion Methods Mol. Biol. Clifton NJ 783 2011
23. I. Schomburg, A. Chang, S. Placzek, C. Sohngen, M. Rother, M. Lang, C. Munaretto, S. Ulas, M. Stelzer, A. Grote, M. Scheer, and D. Schomburg BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA Nucleic Acids Res. 41 2013 D764 D772
24. A.M. Van Oijen Single-molecule kinetics of exonuclease reveal base dependence and dynamic disorder Science 301 2003 1235 1238
25. E.C. Greene, and K. Mizuuchi Direct observation of single MuB polymers evidence for a DNA-dependent conformational change for generating an active target complex Mol. Cell 9 2002 1079 1089
26. A. Granéli, C.C. Yeykal, T.K. Prasad, and E.C. Greene Organized arrays of individual DNA molecules tethered to supported lipid bilayers Langmuir 22 2006 292 299
27. I.J. Finkelstein, and E.C. Greene Supported lipid bilayers and DNA curtains for high-throughput single-molecule studies Methods Mol. Biol. Clifton NJ 745 2011 447 461
28. M.-L. Visnapuu, T. Fazio, S. Wind, and E.C. Greene Parallel arrays of geometric nanowells for assembling curtains of DNA with controlled lateral dispersion Langmuir 24 2008 11293 11299
29. J. Gorman, T. Fazio, F. Wang, S. Wind, and E.C. Greene Nanofabricated racks of aligned and anchored DNA substrates for single-molecule imaging Langmuir 26 2010 1372 1379
30. J. Gorman, F. Wang, S. Redding, A.J. Plys, T. Fazio, S. Wind, E.E. Alani, and E.C. Greene Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair Proc. Natl. Acad. Sci. 109 2012 E3074 E3083
31. S.H. Sternberg, S. Redding, M. Jinek, E.C. Greene, and J.A. Doudna DNA interrogation by the CRISPR RNA-guided endonuclease Cas9 Nature 507 2014 62 67
32. I.J. Finkelstein, and E.C. Greene Molecular traffic jams on DNA Annu. Rev. Biophys. 42 2013 241 263
33. B. Gibb, T.D. Silverstein, I.J. Finkelstein, and E.C. Greene Single-stranded DNA curtains for real-time single-molecule visualization of protein-nucleic acid interactions Anal. Chem. 84 2012 7607 7612
34. B. Gibb, L.F. Ye, S.C. Gergoudis, Y. Kwon, H. Niu, P. Sung, and E.C. Greene Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging PLoS One 9 2014 e87922
35. S.K. Deng, B. Gibb, M.J. de Almeida, E.C. Greene, and L.S. Symington RPA antagonizes microhomology-mediated repair of DNA double-strand breaks Nat. Struct. Mol. Biol. 21 2014 405 412
36. D.C. Duffy, J.C. McDonald, O.J.A. Schueller, and G.M. Whitesides Rapid prototyping of microfluidic systems in poly(dimethylsiloxane) Anal. Chem. 70 1998 4974 4984
37. A.D. Robison, and I.J. Finkelstein Rapid prototyping of multichannel microfluidic devices for single-molecule DNA curtain imaging Anal. Chem. 2014 (140423153406003)
38. I.J. Finkelstein, M.-L. Visnapuu, and E.C. Greene Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase Nature 468 2010 983 987
39. P.R. Bianco, L.R. Brewer, M. Corzett, R. Balhorn, Y. Yeh, S.C. Kowalczykowski, and R.J. Baskin Processive translocation and DNA unwinding by individual RecBCD enzyme molecules Nature 409 2001 374 378
40. D. Axelrod Total internal reflection fluorescence microscopy Methods in Cell Biology 1989 Elsevier 245 270 (Chapter 9)
41. J.J. Benítez, A.M. Keller, P. Ochieng, L.A. Yatsunyk, D.L. Huffman, A.C. Rosenzweig, and P. Chen Probing transient copper chaperone-wilson disease protein interactions at the single-molecule level with nanovesicle trapping J. Am. Chem. Soc. 130 2008 2446 2447
42. Y. Ishitsuka, B. Okumus, S. Arslan, K.H. Chen, and T. Ha Temperature-independent porous nanocontainers for single-molecule fluorescence studies Anal. Chem. 82 2010 9694 9701
43. I.I. Cisse, H. Kim, and T. Ha A rule of seven in Watson-Crick base-pairing of mismatched sequences Nat. Struct. Mol. Biol. 19 2012 623 627
44. B. Okumus, S. Arslan, S.M. Fengler, S. Myong, and T. Ha Single molecule nanocontainers made porous using a bacterial toxin J. Am. Chem. Soc. 131 2009 14844 14849
45. M. Pirchi, G. Ziv, I. Riven, S.S. Cohen, N. Zohar, Y. Barak, and G. Haran Single-molecule fluorescence spectroscopy maps the folding landscape of a large protein Nat. Commun. 2 2011 493
46. S. Tyagi, V. VanDelinder, N. Banterle, G. Fuertes, S. Milles, M. Agez, and E.A. Lemke Continuous throughput and long-term observation of single-molecule FRET without immobilization Nat. Methods 11 2014 297 300
47. S.R. Leslie, A.P. Fields, and A.E. Cohen Convex lens-induced confinement for imaging single molecules Anal. Chem. 82 2010 6224 6229
48. J. Chen, R.V. Dalal, A.N. Petrov, A. Tsai, S.E. O'Leary, K. Chapin, J. Cheng, M. Ewan, P.-L. Hsiung, P. Lundquist, S.W. Turner, D.R. Hsu, and J.D. Puglisi High-throughput platform for real-time monitoring of biological processes by multicolor single-molecule fluorescence Proc. Natl. Acad. Sci. 2013 (201315735)
49. C.D. Kinz-Thompson, M. Palma, D.K. Pulukkunat, D. Chenet, J. Hone, S.J. Wind, and R.L. Gonzalez Robustly passivated, gold nanoaperture arrays for single-molecule fluorescence microscopy ACS Nano 7 2013 8158 8166
50. M.W. Elting, S.R. Leslie, L.S. Churchman, J. Korlach, C.M.J. McFaul, J.S. Leith, M.J. Levene, A.E. Cohen, and J.A. Spudich Single-molecule fluorescence imaging of processive myosin with enhanced background suppression using linear zero-mode waveguides (ZMWs) and convex lens induced confinement (CLIC) Opt. Express 21 2013 1189 1202
51. G.P. Acuna, F.M. Möller, P. Holzmeister, S. Beater, B. Lalkens, and P. Tinnefeld Fluorescence enhancement at docking sites of DNA-directed self-assembled nanoantennas Science 338 2012 506 510
52. D. Punj, M. Mivelle, S.B. Moparthi, T.S. van Zanten, H. Rigneault, N.F. van Hulst, M.F. García-Parajó, and J. Wenger A plasmonic /'antenna-in-box/' platform for enhanced single-molecule analysis at micromolar concentrations Nat. Nanotechnol. 8 2013 512 516
53. P. Holzmeister, G.P. Acuna, D. Grohmann, and P. Tinnefeld Breaking the concentration limit of optical single-molecule detection Chem. Soc. Rev. 43 2014 1014 1028
54. A.B. Loveland, S. Habuchi, J.C. Walter, and A.M. van Oijen A general approach to break the concentration barrier in single-molecule imaging Nat. Methods 9 2012 987 992
55. S. Habuchi, H. Tsutsui, A.B. Kochaniak, A. Miyawaki, and A.M. van Oijen MKikGR, a monomeric photoswitchable fluorescent protein PLoS One 3 2008 e3944
56. H. Hoi, N.C. Shaner, M.W. Davidson, C.W. Cairo, J. Wang, and R.E. Campbell A monomeric photoconvertible fluorescent protein for imaging of dynamic protein localization J. Mol. Biol. 401 2010 776 791
57. J. Fuchs, S. Böhme, F. Oswald, P.N. Hedde, M. Krause, J. Wiedenmann, and G.U. Nienhaus A photoactivatable marker protein for pulse-chase imaging with superresolution Nat. Methods 7 2010 627 630
58. S. Smith, L. Finzi, and C. Bustamante Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads Science 258 1992 1122 1126
59. T.R. Strick, J.-F. Allemand, D. Bensimon, A. Bensimon, and V. Croquette The elasticity of a single supercoiled DNA molecule Science 271 1996 1835 1837
60. M.D. Wang, H. Yin, R. Landick, J. Gelles, and S.M. Block Stretching DNA with optical tweezers Biophys. J. 72 1997 1335 1346
61. J. Liphardt Reversible unfolding of single RNA molecules by mechanical force Science 292 2001 733 737
62. U. Bockelmann, P. Thomen, B. Essevaz-Roulet, V. Viasnoff, and F. Heslot Unzipping DNA with optical tweezers: high sequence sensitivity and force flips Biophys. J. 82 2002 1537 1553
63. M.A. Hall, A. Shundrovsky, L. Bai, R.M. Fulbright, J.T. Lis, and M.D. Wang High-resolution dynamic mapping of histone-DNA interactions in a nucleosome Nat. Struct. Mol. Biol. 16 2009 124 129
64. D.A. Koster, V. Croquette, C. Dekker, S. Shuman, and N.H. Dekker Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB Nature 434 2005 671 674
65. K. Halvorsen, and W.P. Wong Massively parallel single-molecule manipulation using centrifugal force Biophys. J. 98 2010 L53 L55
66. M.-N. Dessinges, T. Lionnet, X.G. Xi, D. Bensimon, and V. Croquette Single-molecule assay reveals strand switching and enhanced processivity of UvrD Proc. Natl. Acad. Sci. 101 2004 6439 6444
67. P. Kollmannsberger, and B. Fabry High-force magnetic tweezers with force feedback for biological applications Rev. Sci. Instrum. 78 2007 114301
68. M.T.J. Van Loenhout, T. van der Heijden, R. Kanaar, C. Wyman, and C. Dekker Dynamics of RecA filaments on single-stranded DNA Nucleic Acids Res. 37 2009 4089 4099
69. X.J.A. Janssen, A.J. Schellekens, K. van Ommering, L.J. van IJzendoorn, and M.W.J. Prins Controlled torque on superparamagnetic beads for functional biosensors Biosens. Bioelectron. 24 2009 1937 1941
70. I. De Vlaminck, T. Henighan, M.T.J. van Loenhout, I. Pfeiffer, J. Huijts, J.W.J. Kerssemakers, A.J. Katan, A. van Langen-Suurling, E. van der Drift, C. Wyman, and C. Dekker Highly parallel magnetic tweezers by targeted DNA tethering Nano Lett. 11 2011 5489 5493
71. I. De Vlaminck, T. Henighan, M.T.J. van Loenhout, D.R. Burnham, and C. Dekker Magnetic forces and DNA mechanics in multiplexed magnetic tweezers PLoS One 7 2012 e41432
72. K. Visscher, S.P. Gross, and S.M. Block Construction of multiple-beam optical traps with nanometer-resolution position sensing IEEE J. Sel. Top. Quantum Electron. 2 1996 1066 1076
73. D.G. Grier A revolution in optical manipulation Nature 424 2003 810 816
74. D.G. Grier, and Y. Roichman Holographic optical trapping Appl. Opt. 45 2006 880
75. M. Werner, F. Merenda, J. Piguet, R.-P. Salathé, and H. Vogel Microfluidic array cytometer based on refractive optical tweezers for parallel trapping, imaging and sorting of individual cells Lab. Chip 11 2011 2432
76. A. Lafong, W.J. Hossack, J. Arlt, T.J. Nowakowski, and N.D. Read Time-multiplexed Laguerre-Gaussian holographic optical tweezers for biological applications Opt. Express 14 2006 3065
77. J.A. Dharmadhikari, A.K. Dharmadhikari, V.S. Makhija, and D. Mathur Multiple optical traps with a single laser beam using a simple and inexpensive mechanical element Curr. Sci. 00113891 93 2007 1265 1270
78. M.C. Noom, B. van den Broek, J. van Mameren, and G.J.L. Wuite Visualizing single DNA-bound proteins using DNA as a scanning probe Nat. Methods 4 2007 1031 1036
79. R.T. Dame, M.C. Noom, and G.J.L. Wuite Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation Nature 444 2006 387 390
80. M. Soltani, J.T. Inman, M. Lipson, and M.D. Wang Electro-optofluidics: achieving dynamic control on-chip Opt. Express 20 2012 22314 22326
81. S. Lin, and K.B. Crozier Planar silicon microrings as wavelength-multiplexed optical traps for storing and sensing particles Lab. Chip 11 2011 4047
82. M. Manesse, A.F. Phillips, C.N. LaFratta, M.A. Palacios, R.B. Hayman, and D.R. Walt Dynamic microbead arrays for biosensing applications Lab. Chip 13 2013 2153
83. A. Candelli, G.J.L. Wuite, and E.J.G. Peterman Combining optical trapping, fluorescence microscopy and micro-fluidics for single molecule studies of DNA-protein interactions Phys. Chem. Chem. Phys. 13 2011 7263
84. R.R. Brau, P.B. Tarsa, J.M. Ferrer, P. Lee, and M.J. Lang Interlaced optical force-fluorescence measurements for single molecule biophysics Biophys. J. 91 2006 1069 1077
85. J. Van Mameren, M. Modesti, R. Kanaar, C. Wyman, E.J.G. Peterman, and G.J.L. Wuite Counting RAD51 proteins disassembling from nucleoprotein filaments under tension Nature 457 2009 745 748
86. T. Hugel, J. Michaelis, C.L. Hetherington, P.J. Jardine, S. Grimes, J.M. Walter, W. Falk, D.L. Anderson, and C. Bustamante Experimental test of connector rotation during DNA packaging into bacteriophage φ29 capsids PLoS Biol. 5 2007 e59
87. L. Disseau, J. Miné, M. Dilhan, H. Camon, and J.-L. Viovy A novel way to combine magnetic tweezers and fluorescence microscopy for single molecule studies Biophys. J. 96 2009 556a
88. J.S. Graham, R.C. Johnson, and J.F. Marko Counting proteins bound to a single DNA molecule Biochem. Biophys. Res. Commun. 415 2011 131 134
89. Y. Chen, A.A. Nawaz, Y. Zhao, P.-H. Huang, J.P. McCoy, S.J. Levine, L. Wang, and T.J. Huang Standing surface acoustic wave (SSAW)-based microfluidic cytometer Lab. Chip 14 2014 916
90. M. Tanyeri, and C.M. Schroeder Manipulation and confinement of single particles using fluid flow Nano Lett. 13 2013 2357 2364
91. Q. Wang, R.H. Goldsmith, Y. Jiang, S.D. Bockenhauer, and W.E. Moerner Probing single biomolecules in solution using the anti-brownian electrokinetic (ABEL) trap Acc. Chem. Res. 45 2012 1955 1964
92. J. Lin, P. Countryman, N. Buncher, P. Kaur, E. Longjiang, Y. Zhang, G. Gibson, C. You, S.C. Watkins, J. Piehler, P.L. Opresko, N.M. Kad, and H. Wang TRF1 and TRF2 use different mechanisms to find telomeric DNA but share a novel mechanism to search for protein partners at telomeres Nucleic Acids Res 2013 (gkt1132)
93. N. Ribeck, and O.A. Saleh Multiplexed single-molecule measurements with magnetic tweezers Rev. Sci. Instrum. 79 2008 094301