Visualization and quantification of nascent RAD51 filament formation at single-monomer resolution

During recombinational repair of double-stranded DNA breaks, RAD51 recombinase assembles as a nucleoprotein filament around single-stranded DNA to form a catalytically proficient structure able to promote homology recognition and strand exchange. Mediators and accessory factors guide the action and...

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Veröffentlicht in:	Proceedings of the National Academy of Sciences - PNAS Jg. 111; H. 42; S. 15090
Hauptverfasser:	Candelli, Andrea, Holthausen, Jan Thomas, Depken, Martin, Brouwer, Ineke, Franker, Mariëlla A M, Marchetti, Margherita, Heller, Iddo, Bernard, Stéphanie, Garcin, Edwige B, Modesti, Mauro, Wyman, Claire, Wuite, Gijs J L, Peterman, Erwin J G
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 21.10.2014
Schlagworte:	Cell Nucleus - metabolism DNA, Single-Stranded - chemistry Fluorescent Dyes - chemistry Humans Likelihood Functions Microfluidics Microscopy, Fluorescence Optical Tweezers Rad51 Recombinase - chemistry Recombination, Genetic Reproducibility of Results RNA, Small Interfering - metabolism Stochastic Processes Substrate Specificity optical tweezers RAD51 homologous recombination single-molecule fluorescence BRCA2
ISSN:	1091-6490, 1091-6490
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Abstract	During recombinational repair of double-stranded DNA breaks, RAD51 recombinase assembles as a nucleoprotein filament around single-stranded DNA to form a catalytically proficient structure able to promote homology recognition and strand exchange. Mediators and accessory factors guide the action and control the dynamics of RAD51 filaments. Elucidation of these control mechanisms necessitates development of approaches to quantitatively probe transient aspects of RAD51 filament dynamics. Here, we combine fluorescence microscopy, optical tweezers, and microfluidics to visualize the assembly of RAD51 filaments on bare single-stranded DNA and quantify the process with single-monomer sensitivity. We show that filaments are seeded from RAD51 nuclei that are heterogeneous in size. This heterogeneity appears to arise from the energetic balance between RAD51 self-assembly in solution and the size-dependent interaction time of the nuclei with DNA. We show that nucleation intrinsically is substrate selective, strongly favoring filament formation on bare single-stranded DNA. Furthermore, we devised a single-molecule fluorescence recovery after photobleaching assay to independently observe filament nucleation and growth, permitting direct measurement of their contributions to filament formation. Our findings yield a comprehensive, quantitative understanding of RAD51 filament formation on bare single-stranded DNA that will serve as a basis to elucidate how mediators help RAD51 filament assembly and accessory factors control filament dynamics.
AbstractList	During recombinational repair of double-stranded DNA breaks, RAD51 recombinase assembles as a nucleoprotein filament around single-stranded DNA to form a catalytically proficient structure able to promote homology recognition and strand exchange. Mediators and accessory factors guide the action and control the dynamics of RAD51 filaments. Elucidation of these control mechanisms necessitates development of approaches to quantitatively probe transient aspects of RAD51 filament dynamics. Here, we combine fluorescence microscopy, optical tweezers, and microfluidics to visualize the assembly of RAD51 filaments on bare single-stranded DNA and quantify the process with single-monomer sensitivity. We show that filaments are seeded from RAD51 nuclei that are heterogeneous in size. This heterogeneity appears to arise from the energetic balance between RAD51 self-assembly in solution and the size-dependent interaction time of the nuclei with DNA. We show that nucleation intrinsically is substrate selective, strongly favoring filament formation on bare single-stranded DNA. Furthermore, we devised a single-molecule fluorescence recovery after photobleaching assay to independently observe filament nucleation and growth, permitting direct measurement of their contributions to filament formation. Our findings yield a comprehensive, quantitative understanding of RAD51 filament formation on bare single-stranded DNA that will serve as a basis to elucidate how mediators help RAD51 filament assembly and accessory factors control filament dynamics. During recombinational repair of double-stranded DNA breaks, RAD51 recombinase assembles as a nucleoprotein filament around single-stranded DNA to form a catalytically proficient structure able to promote homology recognition and strand exchange. Mediators and accessory factors guide the action and control the dynamics of RAD51 filaments. Elucidation of these control mechanisms necessitates development of approaches to quantitatively probe transient aspects of RAD51 filament dynamics. Here, we combine fluorescence microscopy, optical tweezers, and microfluidics to visualize the assembly of RAD51 filaments on bare single-stranded DNA and quantify the process with single-monomer sensitivity. We show that filaments are seeded from RAD51 nuclei that are heterogeneous in size. This heterogeneity appears to arise from the energetic balance between RAD51 self-assembly in solution and the size-dependent interaction time of the nuclei with DNA. We show that nucleation intrinsically is substrate selective, strongly favoring filament formation on bare single-stranded DNA. Furthermore, we devised a single-molecule fluorescence recovery after photobleaching assay to independently observe filament nucleation and growth, permitting direct measurement of their contributions to filament formation. Our findings yield a comprehensive, quantitative understanding of RAD51 filament formation on bare single-stranded DNA that will serve as a basis to elucidate how mediators help RAD51 filament assembly and accessory factors control filament dynamics.During recombinational repair of double-stranded DNA breaks, RAD51 recombinase assembles as a nucleoprotein filament around single-stranded DNA to form a catalytically proficient structure able to promote homology recognition and strand exchange. Mediators and accessory factors guide the action and control the dynamics of RAD51 filaments. Elucidation of these control mechanisms necessitates development of approaches to quantitatively probe transient aspects of RAD51 filament dynamics. Here, we combine fluorescence microscopy, optical tweezers, and microfluidics to visualize the assembly of RAD51 filaments on bare single-stranded DNA and quantify the process with single-monomer sensitivity. We show that filaments are seeded from RAD51 nuclei that are heterogeneous in size. This heterogeneity appears to arise from the energetic balance between RAD51 self-assembly in solution and the size-dependent interaction time of the nuclei with DNA. We show that nucleation intrinsically is substrate selective, strongly favoring filament formation on bare single-stranded DNA. Furthermore, we devised a single-molecule fluorescence recovery after photobleaching assay to independently observe filament nucleation and growth, permitting direct measurement of their contributions to filament formation. Our findings yield a comprehensive, quantitative understanding of RAD51 filament formation on bare single-stranded DNA that will serve as a basis to elucidate how mediators help RAD51 filament assembly and accessory factors control filament dynamics.
Author	Franker, Mariëlla A M Heller, Iddo Bernard, Stéphanie Garcin, Edwige B Wuite, Gijs J L Peterman, Erwin J G Depken, Martin Candelli, Andrea Holthausen, Jan Thomas Wyman, Claire Brouwer, Ineke Marchetti, Margherita Modesti, Mauro
Author_xml	– sequence: 1 givenname: Andrea surname: Candelli fullname: Candelli, Andrea organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands – sequence: 2 givenname: Jan Thomas surname: Holthausen fullname: Holthausen, Jan Thomas organization: Department of Genetics, Cancer Genomics Center, Erasmus University Medical Center, NL-3015CN, Rotterdam, The Netherlands – sequence: 3 givenname: Martin surname: Depken fullname: Depken, Martin organization: Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, NL-2600GA, Delft, The Netherlands – sequence: 4 givenname: Ineke surname: Brouwer fullname: Brouwer, Ineke organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands – sequence: 5 givenname: Mariëlla A M surname: Franker fullname: Franker, Mariëlla A M organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands – sequence: 6 givenname: Margherita surname: Marchetti fullname: Marchetti, Margherita organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands – sequence: 7 givenname: Iddo surname: Heller fullname: Heller, Iddo organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands – sequence: 8 givenname: Stéphanie surname: Bernard fullname: Bernard, Stéphanie organization: Centre de Recherche en Cancérologie de Marseille, CNRS UMR 7258, F-13009 Marseille, France; Institut National de la Santé et de la Recherche Médicale U1068, F-13009 Marseille, France; Institut Paoli-Calmettes, F-13009 Marseille, France; Aix-Marseille Université, F-13284 Marseille, France; and – sequence: 9 givenname: Edwige B surname: Garcin fullname: Garcin, Edwige B organization: Centre de Recherche en Cancérologie de Marseille, CNRS UMR 7258, F-13009 Marseille, France; Institut National de la Santé et de la Recherche Médicale U1068, F-13009 Marseille, France; Institut Paoli-Calmettes, F-13009 Marseille, France; Aix-Marseille Université, F-13284 Marseille, France; and – sequence: 10 givenname: Mauro surname: Modesti fullname: Modesti, Mauro organization: Centre de Recherche en Cancérologie de Marseille, CNRS UMR 7258, F-13009 Marseille, France; Institut National de la Santé et de la Recherche Médicale U1068, F-13009 Marseille, France; Institut Paoli-Calmettes, F-13009 Marseille, France; Aix-Marseille Université, F-13284 Marseille, France; and – sequence: 11 givenname: Claire surname: Wyman fullname: Wyman, Claire organization: Department of Genetics, Cancer Genomics Center, Erasmus University Medical Center, NL-3015CN, Rotterdam, The Netherlands; Department of Radiation Oncology, Erasmus University Medical Center, NL-3015CE, Rotterdam, The Netherlands – sequence: 12 givenname: Gijs J L surname: Wuite fullname: Wuite, Gijs J L organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands – sequence: 13 givenname: Erwin J G surname: Peterman fullname: Peterman, Erwin J G email: e.j.g.peterman@vu.nl organization: LaserLaB Amsterdam and Department of Physics and Astronomy, VU University, NL-1081HV, Amsterdam, The Netherlands; e.j.g.peterman@vu.nl
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SubjectTerms	Cell Nucleus - metabolism DNA, Single-Stranded - chemistry Fluorescent Dyes - chemistry Humans Likelihood Functions Microfluidics Microscopy, Fluorescence Optical Tweezers Rad51 Recombinase - chemistry Recombination, Genetic Reproducibility of Results RNA, Small Interfering - metabolism Stochastic Processes Substrate Specificity
Title	Visualization and quantification of nascent RAD51 filament formation at single-monomer resolution
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