Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-23T02:12:03.643Z Has data issue: false hasContentIssue false
  • English
  • Français

Single-molecule views on homologous recombination

Published online by Cambridge University Press:  09 September 2013

Andrea Candelli ,
Mauro Modesti ,
Erwin J. G. Peterman  and
Gijs J. L. Wuite
Andrea Candelli
Affiliation:
LaserLaB and Department of Physics and Astronomy, VU University Amsterdam, Amsterdam, The Netherlands
Mauro Modesti
Affiliation:
Centre de Recherche en Cancérologie de Marseille, CNRS, UMR7258, Marseille F-13009, France Inserm U1068, Marseille F-13009, France Institut Paoli-Calmettes, Marseille F-13009, France Aix-Marseille Université, Marseille F-13284, France
Erwin J. G. Peterman
Affiliation:
LaserLaB and Department of Physics and Astronomy, VU University Amsterdam, Amsterdam, The Netherlands
Gijs J. L. Wuite*
Affiliation:
LaserLaB and Department of Physics and Astronomy, VU University Amsterdam, Amsterdam, The Netherlands
*
*Author for Correspondence: G. J. L. Wuite, LaserLaB and Department of Physics and Astronomy, VU University Amsterdam, Amsterdam, The Netherlands. [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

All organisms need homologous recombination (HR) to repair DNA double-strand breaks. Defects in recombination are linked to genetic instability and to elevated risks in developing cancers. The central catalyst of HR is a nucleoprotein filament, consisting of recombinase proteins (human RAD51 or bacterial RecA) bound around single-stranded DNA. Over the last two decades, single-molecule techniques have provided substantial new insights into the dynamics of homologous recombination. Here, we survey important recent developments in this field of research and provide an outlook on future developments.

Type
Review Article
Information
Quarterly Reviews of Biophysics , Volume 46 , Issue 4 , November 2013 , pp. 323 - 348
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

6. References

Abbondanzieri, E. A., Greenleaf, W. J., Shaevitz, J. W., Landick, R. & Block, S. M. (2005). Direct observation of base-pair stepping by RNA polymerase. Nature 438, 460–465.CrossRefGoogle ScholarPubMed
Adzuma, K. (1998). No sliding during homology search by RecA protein. Journal of Biological Chemistry 273, 31565–31573.CrossRefGoogle ScholarPubMed
Arata, H., Dupont, A., Miné-Hattab, J., Disseau, L., Renodon-Cornière, A., Takahashi, M., Viovy, J.-L. & Cappello, G. (2009). Direct observation of twisting steps during Rad51 polymerization on DNA. Proceedings of the National Academy of Sciences of the United States of America 106, 19239–19244.CrossRefGoogle ScholarPubMed
Ashkin, A., Dziedzic, J. M., Bjorkholm, J. E. & Chu, S. (1986). Observation of a single-beam gradient force optical trap for dielectric particles. Optics Letters 11, 288.CrossRefGoogle ScholarPubMed
Aylon, Y., Liefshitz, B., Bitan-Banin, G. & Kupiec, M. (2003). Molecular dissection of mitotic recombination in the yeast Saccharomyces cerevisiae. Molecular and Cellular Biology 23, 1403–1417.CrossRefGoogle ScholarPubMed
Barzel, A. & Kupiec, M. (2008). Finding a match: how do homologous sequences get together for recombination? Nature Reviews Genetics 9, 27–37.CrossRefGoogle ScholarPubMed
Baumann, P., Benson, F. E. & West, S. C. (1996). Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87, 757–766.CrossRefGoogle ScholarPubMed
Bazemore, L. R., Folta-Stogniew, E., Takahashi, M. & Radding, C. M. (1997). RecA tests homology at both pairing and strand exchange. Proceedings of the National Academy of Sciences of the United States of America 94, 11863–11868.CrossRefGoogle ScholarPubMed
Bell, J. C., Plank, J. L., Dombrowski, C. C. & Kowalczykowski, S. C. (2012). Direct imaging of RecA nucleation and growth on single molecules of SSB-coated ssDNA. Nature 491, 274–278.CrossRefGoogle ScholarPubMed
Benson, F. E., Stasiak, A. & West, S. C. (1994). Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO Journal 13, 5764–5771.CrossRefGoogle ScholarPubMed
Blainey, P. C., van Oijen, A. M., Banerjee, A., Verdine, G. L. & Xie, X. S. (2006). A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proceedings of the National Academy of Sciences of the United States of America 103, 5752–5757.CrossRefGoogle ScholarPubMed
Brewer, L. & Bianco, P. (2008). Laminar flow cells for single-molecule studies of DNA-protein interactions. Nature Methods 5, 517–525.CrossRefGoogle ScholarPubMed
Bugreev, D. V. & Mazin, A. V. (2004). Ca2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proceedings of the National Academy of Sciences of the United States of America 101, 9988–9993.CrossRefGoogle ScholarPubMed
Candelli, A., Wuite, G. J. L. & Peterman, E. J. G. (2011). Combining optical trapping, fluorescence microscopy and micro-fluidics for single molecule studies of DNA-protein interactions. Physical Chemistry Chemical Physics: PCCP 13, 7263–7272.CrossRefGoogle ScholarPubMed
Cerbinskaite, a., Mukhopadhyay, a., Plummer, E. R., Curtin, N. J. & Edmondson, R. J. (2012). Defective homologous recombination in human cancers. Cancer Treatment Reviews 38, 89–100.CrossRefGoogle ScholarPubMed
Chabbert, M., Cazenave, C. & Hélène, C. (1987). Kinetic studies of recA protein binding to a fluorescent single-stranded polynucleotide. Biochemistry 26, 2218–2225.CrossRefGoogle ScholarPubMed
Chen, Z., Yang, H. & Pavletich, N. P. (2008). Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489–484.CrossRefGoogle ScholarPubMed
Comstock, M. J., Ha, T. & Chemla, Y. R. (2011). Ultrahigh-resolution optical trap with single-fluorophore sensitivity. Nature Methods 8, 335–340.CrossRefGoogle ScholarPubMed
Conover, A. J., Danilowicz, C., Gunaratne, R., Coljee, V. W., Kleckner, N., & Prentiss, M. (2011). Changes in the tension in dsDNA alter the conformation of RecA bound to dsDNA-RecA filaments. Nucleic Acids Research 39, 8833–8843.CrossRefGoogle ScholarPubMed
Conway, A. B., Lynch, T. W., Zhang, Y., Fortin, G. S., Fung, C. W., Symington, L. S., & Rice, P. A. (2004). Crystal structure of a Rad51 filament. Nature Structural and Molecular Biology 11, 791–796.CrossRefGoogle ScholarPubMed
Dame, R. T., Noom, M. C. & Wuite, G. J. L. (2006). Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444, 387–390.CrossRefGoogle ScholarPubMed
De Vlaminck, I. & Dekker, C. (2012). Recent advances in magnetic tweezers. Annual Review of Biophysics 41, 453–472.CrossRefGoogle ScholarPubMed
De Vlaminck, I., Henighan, T., van Loenhout, M. T. J., Pfeiffer, I., Huijts, J., Kerssemakers, J. W. J., Katan, A. J., van Langen-Suurling, A., van der Drift, E., Wyman, C. & Dekker, C. (2011). Highly parallel magnetic tweezers by targeted DNA tethering. Nano Letters 11, 5489–5493.CrossRefGoogle ScholarPubMed
De Vlaminck, I., van Loenhout, M. T. J., Zweifel, L., den Blanken, J., Hooning, K., Hage, S., Kerssemakers, J. & Dekker, C. (2012). Mechanism of homology recognition in DNA recombination from dual-molecule experiments. Molecular Cell 46, 616–624.CrossRefGoogle ScholarPubMed
DiCapua, E., Schnarr, M., Ruigrok, R. W., Lindner, P. & Timmins, P. A. (1990). Complexes of RecA protein in solution. A study by small angle neutron scattering. Journal of Molecular Biology 214, 557–570.CrossRefGoogle ScholarPubMed
Forget, A. L. & Kowalczykowski, S. C. (2012). Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search. Nature 482, 423–427.CrossRefGoogle ScholarPubMed
Galletto, R., Amitani, I., Baskin, R. J. & Kowalczykowski, S. C. (2006). Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443, 875–878.CrossRefGoogle ScholarPubMed
Gibb, B., Silverstein, T. D., Finkelstein, I. J. & Greene, E. C. (2012). Single-stranded DNA curtains for real-time single-molecule visualization of protein-nucleic acid interactions. Analytical Chemistry 84, 7607–7612.CrossRefGoogle ScholarPubMed
Gorman, J. & Greene, E. C. (2008). Visualizing one-dimensional diffusion of proteins along DNA. Nature Structural and Molecular Biology 15, 768–774.CrossRefGoogle ScholarPubMed
Gorman, J., Fazio, T., Wang, F., Wind, S. & Greene, E. C. (2010). Nanofabricated racks of aligned and anchored DNA substrates for single-molecule imaging. Langmuir: the ACS Journal of Surfaces and Colloids 26, 1372–1379.CrossRefGoogle ScholarPubMed
Gross, P., Laurens, N., Oddershede, L. B., Bockelmann, U., Peterman, E. J. G. & Wuite, G. J. L. (2011). Quantifying how DNA stretches, melts and changes twist under tension. Nature Physics 7, 731–736.CrossRefGoogle Scholar
Gupta, R. C., Folta-Stogniew, E., O'Malley, S., Takahashi, M. & Radding, C. M. (1999). Rapid exchange of A:T base pairs is essential for recognition of DNA homology by human Rad51 recombination protein. Molecular Cell 4, 705–714.CrossRefGoogle ScholarPubMed
Ha, T., Enderle, T., Ogletree, D. F., Chemla, D. S., Selvin, P. R. & Weiss, S. (1996). Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proceedings of the National Academy of Sciences of the United States of America 93, 6264–6268.CrossRefGoogle Scholar
Ha, T., Kozlov, A. G. & Lohman, T. M. (2012). Single-molecule views of protein movement on single-stranded DNA. Annual Review of Biophysics 41, 295–319.CrossRefGoogle ScholarPubMed
Hegner, M., Smith, S. B. & Bustamante, C. (1999). Polymerization and mechanical properties of single RecA-DNA filaments. Proceedings of the National Academy of Sciences 96, 10109–10114.CrossRefGoogle ScholarPubMed
Heyer, W. -D., Ehmsen, K. T. & Liu, J. (2010). Regulation of homologous recombination in eukaryotes. Annual Review of Genetics 44, 113–139.CrossRefGoogle ScholarPubMed
Hilario, J., Amitani, I., Baskin, R. J. & Kowalczykowski, S. C. (2009). Direct imaging of human Rad51 nucleoprotein dynamics on individual DNA molecules. Proceedings of the National Academy of Sciences of the United States of America 106, 361–368.CrossRefGoogle ScholarPubMed
Hoeijmakers, J. H. (2001). Genome maintenance mechanisms for preventing cancer. Nature 411, 366–374.CrossRefGoogle ScholarPubMed
Holden, S. J., Uphoff, S., Hohlbein, J., Yadin, D., Le Reste, L., Britton, O. J. & Kapanidis, A. N. (2010). Defining the limits of single-molecule FRET resolution in TIRF microscopy. Biophysical Journal 99, 3102–3111.CrossRefGoogle ScholarPubMed
Holloman, W. K. (2011). Unraveling the mechanism of BRCA2 in homologous recombination. Nature Structural and Molecular Biology 18, 748–754.CrossRefGoogle ScholarPubMed
Howard-Flanders, P., West, S. C. & Stasiak, A. (1984). Role of RecA protein spiral filaments in genetic recombination. Nature 309, 215–220.CrossRefGoogle ScholarPubMed
Inoue, K. & Lupski, J. R. (2002). Molecular mechanisms for genomic disorders. Annual Review of Genomics and Human Genetics 3, 199–242.CrossRefGoogle ScholarPubMed
Jensen, R. B., Carreira, A. & Kowalczykowski, S. C. (2010). Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467, 678–683.CrossRefGoogle ScholarPubMed
Joo, C., McKinney, S. A., Nakamura, M., Rasnik, I., Myong, S., Ha, T. (2006). Real-time observation of RecA filament dynamics with single monomer resolution. Cell 126, 515–527.CrossRefGoogle ScholarPubMed
Kim, K. & Saleh, O. A. (2009). A high-resolution magnetic tweezer for single-molecule measurements. Nucleic Acids Research 37, e136.CrossRefGoogle ScholarPubMed
Kowalczykowski, S. C., Dixon, D. A., Eggleston, a. K., Lauder, S. D. & Rehrauer, W. M. (1994). Biochemistry of homologous recombination in Escherichia coli. Microbiological Reviews 58, 401–465.CrossRefGoogle ScholarPubMed
Lipfert, J., Kerssemakers, J. W. J., Jager, T. & Dekker, N. H. (2010). Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA–DNA filaments. Nature Methods 7, 977–980.CrossRefGoogle ScholarPubMed
Lipfert, J., Wiggin, M., Kerssemakers, J. W. J., Pedaci, F. & Dekker, N. H. (2011). Freely orbiting magnetic tweezers to directly monitor changes in the twist of nucleic acids. Nature Communications 2, 439.CrossRefGoogle ScholarPubMed
Liu, J., Doty, T., Gibson, B. & Heyer, W. -D. (2010). Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nature Structural and Molecular Biology 17, 1260–1262.CrossRefGoogle ScholarPubMed
Mani, A., Braslavsky, I., Arbel-Goren, R. & Stavans, J. (2010). Caught in the act: the lifetime of synaptic intermediates during the search for homology on DNA. Nucleic Acids Research 38, 2036–2043.CrossRefGoogle ScholarPubMed
Mazin, A. V. & Kowalczykowski, S. C. (1996). The specificity of the secondary DNA binding site of RecA protein defines its role in DNA strand exchange. Proceedings of the National Academy of Sciences of the United States of America 93, 10673–10678.CrossRefGoogle ScholarPubMed
Mazin, A. V. & Kowalczykowski, S. C. (1998). The function of the secondary DNA-binding site of RecA protein during DNA strand exchange. EMBO Journal 17, 1161–1168.CrossRefGoogle ScholarPubMed
McKinnon, P. J. & Caldecott, K. W. (2007). DNA strand break repair and human genetic disease. Annual Review of Genomics and Human Genetics 8, 37–55.CrossRefGoogle ScholarPubMed
McKinney, S. a., Joo, C. & Ha, T. (2006). Analysis of single-molecule FRET trajectories using hidden Markov modeling. Biophysical Journal 91, 1941–1951.CrossRefGoogle ScholarPubMed
Moffitt, J. R., Chemla, Y. R., Smith, S. B. & Bustamante, C. (2008). Recent advances in optical tweezers. Annual Review of Biochemistry 77, 205–228.CrossRefGoogle ScholarPubMed
Negrini, S., Gorgoulis, V. G. & Halazonetis, T. D. (2010). Genomic instability–an evolving hallmark of cancer. Nature Reviews Molecular Cell Biology 11, 220–228.CrossRefGoogle ScholarPubMed
Neuman, K. C. & Block, S. M. (2004). Optical trapping. Review of Scientific Instruments 75, 2787–2809.CrossRefGoogle ScholarPubMed
Nomme, J., Takizawa, Y., Martinez, S. F., Renodon-Cornière, A., Fleury, F., Weigel, P., Yamamoto, K., Kurumizaka, H., Takahashi, M. (2008). Inhibition of filament formation of human Rad51 protein by a small peptide derived from the BRC-motif of the BRCA2 protein. Genes to Cells: Devoted to Molecular and Cellular Mechanisms 13, 471–481.CrossRefGoogle ScholarPubMed
Noom, M. C., Van den Broek, B., Van Mameren, J. & Wuite, G. J. L. (2007). Visualizing single DNA-bound proteins using DNA as a scanning probe. Nature Methods 4, 1031–1036.CrossRefGoogle ScholarPubMed
Pierobon, P., Miné-Hattab, J., Cappello, G., Viovy, J. -L. & Lagomarsino, M. (2010). Separation of time scales in one-dimensional directed nucleation-growth processes. Physical Review E 82, 061904.CrossRefGoogle ScholarPubMed
Prvost, C. & Takahashi, M. (2003). Geometry of the DNA strands within the RecA nucleofilament: role in homologous recombination. Quarterly Reviews of Biophysics 36, 429–453.CrossRefGoogle Scholar
Quake, S. R., Babcock, H. & Chu, S. (1997). The dynamics of partially extended single molecules of DNA. Nature 388, 151–154.CrossRefGoogle ScholarPubMed
Ragunathan, K., Joo, C. & Ha, T. (2011). Real-time observation of strand exchange reaction with high spatiotemporal resolution. Structure (London, England: 1993) 19, 1064–1073.CrossRefGoogle ScholarPubMed
Reymer, A., Frykholm, K., Morimatsu, K., Takahashi, M. & Nordén, B. (2009). Structure of human Rad51 protein filament from molecular modeling and site-specific linear dichroism spectroscopy. Proceedings of the National Academy of Sciences of the United States of America 106, 13248–13253.CrossRefGoogle ScholarPubMed
Robertson, R. B., Moses, D. N., Kwon, Y., Chan, P., Chi, P., Klein, H., Sung, P., Greene, E. C. (2009). Structural transitions within human Rad51 nucleoprotein filaments. Proceedings of the National Academy of Sciences of the United States of America 106, 12688–12693.CrossRefGoogle ScholarPubMed
Roy, R., Hohng, S. & Ha, T. (2008). A practical guide to single-molecule FRET. Nature Methods 5, 507–516.CrossRefGoogle ScholarPubMed
San Filippo, J., Sung, P. & Klein, H. (2008). Mechanism of eukaryotic homologous recombination. Annual Review of Biochemistry 77, 229–257.CrossRefGoogle ScholarPubMed
Santoso, Y., Joyce, C. M., Potapova, O., Le Reste, L., Hohlbein, J., Torella, J. P., Grindley, N. D. F., Kapanidis, A. N. (2010). Conformational transitions in DNA polymerase I revealed by single-molecule FRET. Proceedings of the National Academy of Sciences of the United States of America 107, 715–720.CrossRefGoogle ScholarPubMed
Shaevitz, J. W., Abbondanzieri, E. A., Landick, R. & Block, S. M. (2003). Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 426, 684–687.CrossRefGoogle ScholarPubMed
Smith, S., Finzi, L. & Bustamante, C. (1992). Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122–1126.CrossRefGoogle ScholarPubMed
Strick, T. R., Allemand, J. -F. F., Bensimon, D., Bensimon, A. & Croquette, V. (1996). The Elasticity of a Single Supercoiled DNA Molecule. Science 271, 1835–1837.CrossRefGoogle ScholarPubMed
Takahashi, M. (1989). Analysis of DNA-RecA protein interactions involving the protein self-association reaction. Journal of Biological Chemistry 264, 288–295.CrossRefGoogle ScholarPubMed
Tombline, G. & Fishel, R. (2002). Biochemical characterization of the human RAD51 protein. I. ATP hydrolysis. Journal of Biological Chemistry 277, 14417–14425.CrossRefGoogle ScholarPubMed
Van der Heijden, T. & Dekker, C. (2008). Monte Carlo simulations of protein assembly, disassembly, and linear motion on DNA. Biophysical Journal 95, 4560–4569.CrossRefGoogle ScholarPubMed
van der Heijden, T., Seidel, R., Modesti, M., Kanaar, R., Wyman, C., Dekker, C. (2007). Real-time assembly and disassembly of human RAD51 filaments on individual DNA molecules. Nucleic Acids Research 35, 5646–5657.CrossRefGoogle ScholarPubMed
van der Heijden, T., Modesti, M., Hage, S., Kanaar, R., Wyman, C., Dekker, C. (2008). Homologous recombination in real time: DNA strand exchange by RecA. Molecular Cell 30, 530–538.CrossRefGoogle ScholarPubMed
Van Loenhout, M. T. J., Van der Heijden, T., Kanaar, R., Wyman, C. & Dekker, C. (2009). Dynamics of RecA filaments on single-stranded DNA. Nucleic Acids Research 37, 4089–4099.CrossRefGoogle ScholarPubMed
van Mameren, J., Modesti, M., Kanaar, R., Wyman, C., Peterman, E. J. G., Wuite, G. J. L. (2009a). Counting RAD51 proteins disassembling from nucleoprotein filaments under tension. Nature 457, 745–748.CrossRefGoogle ScholarPubMed
van Mameren, J., Gross, P., Farge, G., Hooijman, P., Modesti, M., Falkenberg, M., Wuite, G. J. L., Peterman, E. J. G. (2009b). Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proceedings of the National Academy of Sciences of the United States of America 106, 18231–18236.CrossRefGoogle ScholarPubMed
Wold, M. S. (1997). Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annual Review of Biochemistry 66, 61–92.CrossRefGoogle ScholarPubMed
Wyman, C. & Kanaar, R. (2006). DNA double-strand break repair: all's well that ends well. Annual Review of Genetics 40, 363–383.CrossRefGoogle ScholarPubMed
Xiao, J., Lee, A. M. & Singleton, S. F. (2006). Direct evaluation of a kinetic model for RecA-mediated DNA-strand exchange: the importance of nucleic acid dynamics and entropy during homologous genetic recombination. Chembiochem: a European Journal of Chemical Biology 7, 1265–1278.CrossRefGoogle ScholarPubMed
Yodh, J. G., Schlierf, M. & Ha, T. (2010). Insight into helicase mechanism and function revealed through single-molecule approaches.CrossRefGoogle Scholar
Yu, X., Jacobs, S. a., West, S. C., Ogawa, T. & Egelman, E. H. (2001). Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proceedings of the National Academy of Sciences of the United States of America 98, 8419–8424.CrossRefGoogle ScholarPubMed