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Molecular and Cellular Biology Volume 19, 1999 - Issue 10
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DNA Dynamics and Chromosome Structure

The Essential Functions of Human Rad51 Are Independent of ATP Hydrolysis

Ciaran Morrison1 Bayer-Chair Department of Molecular Immunology and Allergology
,
Akira Shinohara2 Department of Radiation and Cellular Oncology, University of Chicago, Chicago, Illinois60637
,
Eiichiro Sonoda1 Bayer-Chair Department of Molecular Immunology and Allergology
,
Yuko Yamaguchi-Iwai1 Bayer-Chair Department of Molecular Immunology and Allergology
,
Minoru Takata1 Bayer-Chair Department of Molecular Immunology and Allergology
,
Ralph R. Weichselbaum2 Department of Radiation and Cellular Oncology, University of Chicago, Chicago, Illinois60637
&
Shunichi Takeda1 Bayer-Chair Department of Molecular Immunology and Allergology;3 Department of Experimental Radiology, Faculty of Medicine, Kyoto University, Sakyo-ku, Kyoto606-8501, JapanCorrespondence[email protected]
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Pages 6891-6897 | Received 24 Mar 1999, Accepted 23 Jul 1999, Published online: 28 Mar 2023

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Tae Moon Kim, Jun Ho Ko, Lingchuan Hu, Sung-A Kim, Alexander J. R. Bishop, Jan Vijg, Cristina Montagna & Paul Hasty. (2012) RAD51 Mutants Cause Replication Defects and Chromosomal Instability. Molecular and Cellular Biology 32:18, pages 3663-3680.
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Jie Liu, Kirk T. Ehmsen, Wolf-Dietrich Heyer & Scott W. Morrical. (2011) Presynaptic filament dynamics in homologous recombination and DNA repair. Critical Reviews in Biochemistry and Molecular Biology 46:3, pages 240-270.
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Cindy W. Fung, Gary S. Fortin, Shaun E. Peterson & Lorraine S. Symington. (2006) The rad51-K191R ATPase-Defective Mutant Is Impaired forPresynaptic Filament Formation. Molecular and Cellular Biology 26:24, pages 9544-9554.
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Kazuhiko Yamamoto, Seiki Hirano, Masamichi Ishiai, Kenichi Morishima, Hiroyuki Kitao, Keiko Namikoshi, Masayo Kimura, Nobuko Matsushita, Hiroshi Arakawa, Jean-Marie Buerstedde, Kenshi Komatsu, Larry H. Thompson & Minoru Takata. (2005) Fanconi Anemia Protein FANCD2 Promotes Immunoglobulin Gene Conversion and DNA Repair through a Mechanism Related to Homologous Recombination. Molecular and Cellular Biology 25:1, pages 34-43.
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Jeremy M. Stark, Andrew J. Pierce, Jin Oh, Albert Pastink & Maria Jasin. (2004) Genetic Steps of Mammalian Homologous Repair with Distinct Mutagenic Consequences. Molecular and Cellular Biology 24:21, pages 9305-9316.
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Kazuhiko Yamamoto, Masamichi Ishiai, Nobuko Matsushita, Hiroshi Arakawa, Jane E. Lamerdin, Jean-Marie Buerstedde, Mitsune Tanimoto, Mine Harada, Larry H. Thompson & Minoru Takata. (2003) Fanconi Anemia FANCG Protein in Mitigating Radiation- and Enzyme-Induced DNA Double-Strand Breaks by Homologous Recombination in Vertebrate Cells. Molecular and Cellular Biology 23:15, pages 5421-5430.
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Elizabeth A. Morgan, Naseem Shah & Lorraine S. Symington. (2002) The Requirement for ATP Hydrolysis by Saccharomyces cerevisiae Rad51 Is Bypassed by Mating-Type Heterozygosity or RAD54 in High Copy. Molecular and Cellular Biology 22:18, pages 6336-6343.
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Articles from other publishers (77)

Robert Appleby, Daniel Bollschweiler, Dimitri Y. Chirgadze, Luay Joudeh & Luca Pellegrini. (2023) A metal ion-dependent mechanism of RAD51 nucleoprotein filament disassembly. iScience 26:5, pages 106689.
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Wenpeng Liu, Yuichiro Saito, Jessica JacksonRahul BhowmickMasato T. Kanemaki, Alessandro Vindigni & David Cortez. (2023) RAD51 bypasses the CMG helicase to promote replication fork reversal. Science 380:6643, pages 382-387.
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Swagata Halder, Aurore Sanchez, Lepakshi Ranjha, Giordano Reginato, Ilaria Ceppi, Ananya Acharya, Roopesh Anand & Petr Cejka. (2022) Double-stranded DNA binding function of RAD51 in DNA protection and its regulation by BRCA2. Molecular Cell 82:19, pages 3553-3565.e5.
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Diedre Reitz, Yuen-Ling Chan & Douglas K Bishop. (2021) How strand exchange protein function benefits from ATP hydrolysis. Current Opinion in Genetics & Development 71, pages 120-128.
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A. Demeyer, H. Benhelli-Mokrani, B. Chénais, P. Weigel & F. Fleury. (2021) Inhibiting homologous recombination by targeting RAD51 protein. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer 1876:2, pages 188597.
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Isabel E. Wassing, Emily Graham, Xanita Saayman, Lucia Rampazzo, Christine Ralf, Andrew Bassett & Fumiko Esashi. (2021) The RAD51 recombinase protects mitotic chromatin in human cells. Nature Communications 12:1.
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Aviv Meir & Eric C. Greene. (2021) Srs2 and Pif1 as Model Systems for Understanding Sf1a and Sf1b Helicase Structure and Function. Genes 12:9, pages 1319.
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Hang Phuong Le, Wolf-Dietrich Heyer & Jie Liu. (2021) Guardians of the Genome: BRCA2 and Its Partners. Genes 12:8, pages 1229.
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Isabel E. Wassing & Fumiko Esashi. (2021) RAD51: Beyond the break. Seminars in Cell & Developmental Biology 113, pages 38-46.
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Arik Townsend, Gabriella Lora, Justin Engel, Neysha Tirado-Class & Huzefa Dungrawala. (2021) DCAF14 promotes stalled fork stability to maintain genome integrity. Cell Reports 34:4, pages 108669.
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Wei-Hsuan LanSheng-Yao LinChih-Yuan KaoWen-Hsuan ChangHsin-Yi YehHao-Yen ChangPeter Chi & Hung-Wen Li. (2020) Rad51 facilitates filament assembly of meiosis-specific Dmc1 recombinase. Proceedings of the National Academy of Sciences 117:21, pages 11257-11264.
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Jennifer M. Mason, Yuen-Ling Chan, Ralph W. Weichselbaum & Douglas K. Bishop. (2019) Non-enzymatic roles of human RAD51 at stalled replication forks. Nature Communications 10:1.
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J. Brooks CrickardEric C. Greene. (2019) Helicase Mechanisms During Homologous Recombination in Saccharomyces cerevisiae . Annual Review of Biophysics 48:1, pages 255-273.
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Shan Jiang, Ting Lin, Qingji Xie & Lijing Wang. (2018) Network Analysis of RAD51 Proteins in Metazoa and the Evolutionary Relationships With Their Archaeal Homologs. Frontiers in Genetics 9.
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Kyle Kaniecki, Luisina De Tullio, Bryan Gibb, Youngho Kwon, Patrick Sung & Eric C. Greene. (2017) Dissociation of Rad51 Presynaptic Complexes and Heteroduplex DNA Joints by Tandem Assemblies of Srs2. Cell Reports 21:11, pages 3166-3177.
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Brendan Alligand, Magali Le Breton, Damien Marquis, François Vallette & Fabrice Fleury. (2017) Functional effects of diphosphomimetic mutations at cAbl-mediated phosphorylation sites on Rad51 recombinase activity. Biochimie 139, pages 115-124.
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Shengfeng Xu, Xiao Wu, Ling Wu, Andy Castillo, Jianxin Liu, Erin Atkinson, Atanu Paul, Dan Su, Katharina Schlacher, Yoshihiro Komatsu, M. James You & Bin Wang. (2017) Abro1 maintains genome stability and limits replication stress by protecting replication fork stability. Genes & Development 31:14, pages 1469-1482.
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Andrew A. Kelso, Steven D. Goodson, Suchitra Chavan, Amanda F. Say, Audrey Turchick, Deepti Sharma, LeAnna L. Ledford, Erin Ratterman, Kristin Leskoske, Ada V. King, Christopher C. Attaway, Yura Bandera, Stephen H. Foulger, Alexander V. Mazin, Lesly A. Temesvari & Michael G. Sehorn. (2016) Characterization of the recombination activities of the Entamoeba histolytica Rad51 recombinase. Molecular and Biochemical Parasitology 210:1-2, pages 71-84.
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May E. Marsh, Duncan E. Scott, Matthias T. Ehebauer, Chris Abell, Tom L. Blundell & Marko Hyvönen. (2016) ATP half-sites in RadA and RAD51 recombinases bind nucleotides. FEBS Open Bio 6:5, pages 372-385.
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Gusztáv Schay, Bálint Borka, Linda Kernya, Éva Bulyáki, József Kardos, Melinda Fekete & Judit Fidy. (2016) Without Binding ATP, Human Rad51 Does Not Form Helical Filaments on ssDNA. The Journal of Physical Chemistry B 120:9, pages 2165-2178.
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Michael Tsabar, Jennifer M. Mason, Yuen-Ling Chan, Douglas K. Bishop & James E. Haber. (2015) Caffeine inhibits gene conversion by displacing Rad51 from ssDNA. Nucleic Acids Research 43:14, pages 6902-6918.
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Marcel Ander, Sivaraman Subramaniam, Karim Fahmy, A. Francis Stewart & Erik Schäffer. (2015) A Single-Strand Annealing Protein Clamps DNA to Detect and Secure Homology. PLOS Biology 13:8, pages e1002213.
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Shalini Verma & Basuthkar J. Rao. (2013) p53 suppresses BRCA2-stimulated ATPase and strand exchange functions of human RAD51. The Journal of Biochemistry 154:3, pages 237-248.
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Justin A. North, Ravindra Amunugama, Marcelina Klajner, Aaron N. Bruns, Michael G. Poirier & Richard Fishel. (2013) ATP-dependent nucleosome unwrapping catalyzed by human RAD51. Nucleic Acids Research 41:15, pages 7302-7312.
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Robyn L. Maher & Scott W. Morrical. (2013) Coordinated Binding of Single-Stranded and Double-Stranded DNA by UvsX Recombinase. PLoS ONE 8:6, pages e66654.
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William J. GrahamVV, Michael L. Rolfsmeier & Cynthia A. Haseltine. (2013) An archaeal RadA paralog influences presynaptic filament formation. DNA Repair 12:6, pages 403-413.
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Alissa C. Magwood, Maureen M. Mundia & Mark D. Baker. (2012) High Levels of Wild-Type BRCA2 Suppress Homologous Recombination. Journal of Molecular Biology 421:1, pages 38-53.
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Katharina Schlacher, Hong Wu & Maria Jasin. (2012) A Distinct Replication Fork Protection Pathway Connects Fanconi Anemia Tumor Suppressors to RAD51-BRCA1/2. Cancer Cell 22:1, pages 106-116.
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Fei Huang, Olga M. Mazina, Isaac J. Zentner, Simon Cocklin & Alexander V. Mazin. (2012) Inhibition of Homologous Recombination in Human Cells by Targeting RAD51 Recombinase. Journal of Medicinal Chemistry 55:7, pages 3011-3020.
Crossref
Ravindra Amunugama & Richard Fishel. 2012. Mechanisms of DNA Repair. Mechanisms of DNA Repair 155 206 .
Corentin Laulier, Anita Cheng & Jeremy M. Stark. (2011) The relative efficiency of homology-directed repair has distinct effects on proper anaphase chromosome separation. Nucleic Acids Research 39:14, pages 5935-5944.
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Katharina Schlacher, Nicole Christ, Nicolas Siaud, Akinori Egashira, Hong Wu & Maria Jasin. (2011) Double-Strand Break Repair-Independent Role for BRCA2 in Blocking Stalled Replication Fork Degradation by MRE11. Cell 145:4, pages 529-542.
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Fabien Delacôte, Christophe Perez, Valérie Guyot, Catherine Mikonio, Pierrick Potrel, Jean-Pierre Cabaniols, Christophe Delenda, Frédéric Pâques & Philippe Duchateau. (2011) Identification of Genes Regulating Gene Targeting by a High-Throughput Screening Approach. Journal of Nucleic Acids 2011, pages 1-14.
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D.G. Schaefer, F. Delacote, F. Charlot, N. Vrielynck, A. Guyon-Debast, S. Le Guin, J.M. Neuhaus, M.P. Doutriaux & F. Nogué. (2010) RAD51 loss of function abolishes gene targeting and de-represses illegitimate integration in the moss Physcomitrella patens. DNA Repair 9:5, pages 526-533.
Crossref
Kamakshi Balakrishnan, Neeraja M Krishnan, Anagha Kulkarni & Basuthkar J Rao. (2009) Human Rad51 mediated DNA unwinding is facilitated by conditions that favour Rad51-dsDNA aggregation. BMC Biochemistry 10:1.
Crossref
Arabela A. Grigorescu, Joseph H. A. Vissers, Dejan Ristic, Ying Z. Pigli, Thomas W. Lynch, Claire Wyman & Phoebe A. Rice. (2009) Inter-subunit interactions that coordinate Rad51's activities. Nucleic Acids Research 37:2, pages 557-567.
Crossref
Shauna A. Lee, Céline Roques, Alissa C. Magwood, Jean-Yves Masson & Mark D. Baker. (2009) Recovery of deficient homologous recombination in Brca2-depleted mouse cells by wild-type Rad51 expression. DNA Repair 8:2, pages 170-181.
Crossref
Alexander A. Volodin, Tatiana N. Bocharova, Elena A. Smirnova & R. Daniel Camerini-Otero. (2009) Reversibility, Equilibration, and Fidelity of Strand Exchange Reaction between Short Oligonucleotides Promoted by RecA Protein from Escherichia coli and Human Rad51 and Dmc1 Proteins. Journal of Biological Chemistry 284:3, pages 1495-1504.
Crossref
Krishanthi JayathilakaSean D. Sheridan, Tyler D. BoldKatarzyna BochenskaHillary L. LoganRalph R. WeichselbaumDouglas K. Bishop & Philip P. Connell. (2008) A chemical compound that stimulates the human homologous recombination protein RAD51. Proceedings of the National Academy of Sciences 105:41, pages 15848-15853.
Crossref
Nicholas Renzette & Steven J. Sandler. (2008) Requirements for ATP binding and hydrolysis in RecA function in Escherichia coli. Molecular Microbiology 67:6, pages 1347-1359.
Crossref
Ting-Fang Wang, Li-Tzu Chen & Andrew H.-J. Wang. (2008) Right or left turn? RecA family protein filaments promote homologous recombination through clockwise axial rotation. BioEssays 30:1, pages 48-56.
Crossref
Ania Rukść, Erin C. Birmingham & Mark D. Baker. (2007) Altered DNA repair and recombination responses in mouse cells expressing wildtype or mutant forms of RAD51. DNA Repair 6:12, pages 1876-1889.
Crossref
Peter Chi, Joseph San Filippo, Michael G. Sehorn, Galina V. Petukhova & Patrick Sung. (2007) Bipartite stimulatory action of the Hop2–Mnd1 complex on the Rad51 recombinase. Genes & Development 21:14, pages 1747-1757.
Crossref
Michael M. Cox. 2007. Molecular Genetics of Recombination. Molecular Genetics of Recombination 53 94 .
Tekkatte Krishnamurthy Prasad, Caitlyn C. Yeykal & Eric C. Greene. (2006) Visualizing the Assembly of Human Rad51 Filaments on Double-stranded DNA. Journal of Molecular Biology 363:3, pages 713-728.
Crossref
Kang-Sup Shim, Christoph Schmutte, Kristine Yoder & Richard Fishel. (2006) Defining the salt effect on human RAD51 activities. DNA Repair 5:6, pages 718-730.
Crossref
Kang-Sup Shim, Gregory Tombline, Christopher D. Heinen, Nicole Charbonneau, Christoph Schmutte & Richard Fishel. (2006) Magnesium influences the discrimination and release of ADP by human RAD51. DNA Repair 5:6, pages 704-717.
Crossref
C. Wiese, J. M. Hinz, R. S. Tebbs, P. B. Nham, S. S. Urbin, D. W. Collins, L. H. Thompson & D. Schild. (2006) Disparate requirements for the Walker A and B ATPase motifs of human RAD51D in homologous recombination. Nucleic Acids Research 34:9, pages 2833-2843.
Crossref
Joseph San Filippo, Peter Chi, Michael G. Sehorn, Julia Etchin, Lumir Krejci & Patrick Sung. (2006) Recombination Mediator and Rad51 Targeting Activities of a Human BRCA2 Polypeptide. Journal of Biological Chemistry 281:17, pages 11649-11657.
Crossref
Peter Chi, Stephen Van Komen, Michael G. Sehorn, Stefan Sigurdsson & Patrick Sung. (2006) Roles of ATP binding and ATP hydrolysis in human Rad51 recombinase function. DNA Repair 5:3, pages 381-391.
Crossref
Errol C. Friedberg, Graham C. Walker, Wolfram Siede, Richard D. Wood, Roger A. Schultz & Tom Ellenberger. 2005. DNA Repair and Mutagenesis. DNA Repair and Mutagenesis 663 710 .
Julia M Cox, Oleg V Tsodikov & Michael M Cox. (2005) Organized Unidirectional Waves of ATP Hydrolysis within a RecA Filament. PLoS Biology 3:2, pages e52.
Crossref
Yan Wu, Xinguo Qian, Yujiong He, Ignace A. Moya & Yu Luo. (2005) Crystal Structure of an ATPase-active Form of Rad51 Homolog from Methanococcus voltae. Journal of Biological Chemistry 280:1, pages 722-728.
Crossref
Mrinal Kanti Bhattacharyya, Sunanda Bhattacharyya nee Deb, Bamini Jayabalasingham & Nirbhay Kumar. (2005) Characterization of kinetics of DNA strand-exchange and ATP hydrolysis activities of recombinant PfRad51, a Plasmodium falciparum recombinase. Molecular and Biochemical Parasitology 139:1, pages 33-39.
Crossref
Kang Sup Shim, Christoph Schmutte, Gregory Tombline, Christopher D. Heinen & Richard Fishel. (2004) hXRCC2 Enhances ADP/ATP Processing and Strand Exchange by hRAD51. Journal of Biological Chemistry 279:29, pages 30385-30394.
Crossref
Nazumi Alice Yamada, John M. Hinz, Vicki L. Kopf, Kathryn D. Segalle & Larry H. Thompson. (2004) XRCC3 ATPase Activity Is Required for Normal XRCC3-Rad51C Complex Dynamics and Homologous Recombination. Journal of Biological Chemistry 279:22, pages 23250-23254.
Crossref
Christine Richardson, Jeremy M Stark, Melissa Ommundsen & Maria Jasin. (2004) Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene 23:2, pages 546-553.
Crossref
Catherine A. French, Cathryn E. Tambini & John Thacker. (2003) Identification of Functional Domains in the RAD51L2 (RAD51C) Protein and Its Requirement for Gene Conversion. Journal of Biological Chemistry 278:46, pages 45445-45450.
Crossref
Michael M. Cox. (2003) The Bacterial RecA Protein as a Motor Protein. Annual Review of Microbiology 57:1, pages 551-577.
Crossref
Mrinal Kanti Bhattacharyya & Nirbhay Kumar. (2003) Identification and molecular characterisation of DNA damaging agent induced expression of Plasmodium falciparum recombination protein PfRad51. International Journal for Parasitology 33:12, pages 1385-1392.
Crossref
Stephen C. West. (2003) Molecular views of recombination proteins and their control. Nature Reviews Molecular Cell Biology 4:6, pages 435-445.
Crossref
Juan Domínguez-Bendala, Helen Priddle, Alan Clarke & Jim McWhir. (2003) Elevated expression of exogenous Rad51 leads to identical increases in gene-targeting frequency in murine embryonic stem (ES) cells with both functional and dysfunctional p53 genes. Experimental Cell Research 286:2, pages 298-307.
Crossref
Lumir Krejci, Ling Chen, Stephen Van Komen, Patrick Sung & Alan Tomkinson. 2003. Progress in Nucleic Acid Research and Molecular Biology Volume 74. Progress in Nucleic Acid Research and Molecular Biology Volume 74 159 201 .
Manfred GossenHermann Bujard. (2002) Studying Gene Function in Eukaryotes by Conditional Gene Inactivation. Annual Review of Genetics 36:1, pages 153-173.
Crossref
Lorraine S. Symington. (2002) Role of RAD52 Epistasis Group Genes in Homologous Recombination and Double-Strand Break Repair . Microbiology and Molecular Biology Reviews 66:4, pages 630-670.
Crossref
Stefan Sigurdsson, Stephen Van Komen, Galina Petukhova & Patrick Sung. (2002) Homologous DNA Pairing by Human Recombination Factors Rad51 and Rad54. Journal of Biological Chemistry 277:45, pages 42790-42794.
Crossref
Jeremy M. Stark, Peng Hu, Andrew J. Pierce, Mary Ellen Moynahan, Nathan Ellis & Maria Jasin. (2002) ATP Hydrolysis by Mammalian RAD51 Has a Key Role during Homology-directed DNA Repair. Journal of Biological Chemistry 277:23, pages 20185-20194.
Crossref
Gregory Tombline, Kang-Sup Shim & Richard Fishel. (2002) Biochemical Characterization of the Human RAD51 Protein. Journal of Biological Chemistry 277:17, pages 14426-14433.
Crossref
Gregory Tombline & Richard Fishel. (2002) Biochemical Characterization of the Human RAD51 Protein. Journal of Biological Chemistry 277:17, pages 14417-14425.
Crossref
Kevin P. Rice, Aimee L. Eggler, Patrick Sung & Michael M. Cox. (2001) DNA Pairing and Strand Exchange by the Escherichia coli RecA and Yeast Rad51 Proteins without ATP Hydrolysis. Journal of Biological Chemistry 276:42, pages 38570-38581.
Crossref
Michael Fasullo, Peter Giallanza, Zheng Dong, Cinzia Cera & Thomas Bennett. (2001) Saccharomyces cerevisiae rad51 Mutants Are Defective in DNA Damage-Associated Sister Chromatid Exchanges but Exhibit Increased Rates of Homology-Directed Translocations . Genetics 158:3, pages 959-972.
Crossref
Paul O'Regan, Caroline Wilson, Stuart Townsend & John Thacker. (2001) XRCC2 Is a Nuclear RAD51-like Protein Required for Damage-dependent RAD51 Focus Formation without the Need for ATP Binding. Journal of Biological Chemistry 276:25, pages 22148-22153.
Crossref
Larry H Thompson & David Schild. (2001) Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 477:1-2, pages 131-153.
Crossref
Pernille Winding & Martin W Berchtold. (2001) The chicken B cell line DT40: a novel tool for gene disruption experiments. Journal of Immunological Methods 249:1-2, pages 1-16.
Crossref
James E Haber. (2000) Recombination: a frank view of exchanges and vice versa. Current Opinion in Cell Biology 12:3, pages 286-292.
Crossref
Douglas L. Pittman & John C. Schimenti. (2000) Midgestation lethality in mice deficient for the RecA-related gene,Rad51d/Rad51l3. genesis 26:3, pages 167-173.
Crossref

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