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Structure of the single-strand annealing domain of human RAD52 protein.

Singleton MR, Wentzell LM, Liu Y, West SC, Wigley DB
Proc Natl Acad Sci U S A 99 13492-7 (2002)
Cited: 161 times
EuropePMC logo PMID: 12370410

Abstract

In eukaryotic cells, RAD52 protein plays a central role in genetic recombination and DNA repair by (i) promoting the annealing of complementary single-stranded DNA and (ii) stimulation of the RAD51 recombinase. The single-strand annealing domain resides in the N-terminal region of the protein and is highly conserved, whereas the nonconserved RAD51-interaction domain is located in the C-terminal region. An N-terminal fragment of human RAD52 (residues 1-209) has been purified to homogeneity and, similar to the full-size protein (residues 1-418), shown to promote single-strand annealing in vitro. We have determined the crystal structure of this single-strand annealing domain at 2.7 A. The structure reveals an undecameric (11) subunit ring with extensive subunit contacts. A large, positively charged groove runs along the surface of the ring, readily suggesting a mechanism by which RAD52 presents the single strand for reannealing with complementary single-stranded DNA.

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  1. Mechanism of homologous recombination and implications for aging-related deletions in mitochondrial DNA. Chen XJ. Microbiol Mol Biol Rev 77 476-496 (2013)
  2. Novel Insights into RAD52's Structure, Function, and Druggability for Synthetic Lethality and Innovative Anticancer Therapies. Balboni B, Rinaldi F, Previtali V, Ciamarone A, Girotto S, Cavalli A. Cancers (Basel) 15 1817 (2023)

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  1. Detection of novel recombinases in bacteriophage genomes unveils Rad52, Rad51 and Gp2.5 remote homologs. Lopes A, Amarir-Bouhram J, Faure G, Petit MA, Guerois R. Nucleic Acids Res 38 3952-3962 (2010)
  2. Small-molecule inhibitors identify the RAD52-ssDNA interaction as critical for recovery from replication stress and for survival of BRCA2 deficient cells. Hengel SR, Malacaria E, Folly da Silva Constantino L, Bain FE, Diaz A, Koch BG, Yu L, Wu M, Pichierri P, Spies MA, Spies M. Elife 5 e14740 (2016)
  3. Biomolecular surface construction by PDE transform. Zheng Q, Yang S, Wei GW. Int J Numer Method Biomed Eng 28 291-316 (2012)
  4. Pirating conserved phage mechanisms promotes promiscuous staphylococcal pathogenicity island transfer. Bowring J, Neamah MM, Donderis J, Mir-Sanchis I, Alite C, Ciges-Tomas JR, Maiques E, Medmedov I, Marina A, Penadés JR. Elife 6 e26487 (2017)
  5. A properly configured ring structure is critical for the function of the mitochondrial DNA recombination protein, Mgm101. Nardozzi JD, Wang X, Mbantenkhu M, Wilkens S, Chen XJ. J Biol Chem 287 37259-37268 (2012)
  6. A short carboxyl-terminal tail is required for single-stranded DNA binding, higher-order structural organization, and stability of the mitochondrial single-stranded annealing protein Mgm101. Mbantenkhu M, Wierzbicki S, Wang X, Guo S, Wilkens S, Chen XJ. Mol Biol Cell 24 1507-1518 (2013)
  7. Molecular surface mesh generation by filtering electron density map. Giard J, Macq B. Int J Biomed Imaging 2010 923780 (2010)
  8. Structure of the human DNA-repair protein RAD52 containing surface mutations. Saotome M, Saito K, Onodera K, Kurumizaka H, Kagawa W. Acta Crystallogr F Struct Biol Commun 72 598-603 (2016)
  9. Rad52 Oligomeric N-Terminal Domain Stabilizes Rad51 Nucleoprotein Filaments and Contributes to Their Protection against Srs2. Ma E, Maloisel L, Le Falher L, Guérois R, Coïc E. Cells 10 1467 (2021)
  10. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


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  1. Mechanism of eukaryotic homologous recombination. San Filippo J, Sung P, Klein H. Annu Rev Biochem 77 229-257 (2008)
  2. Molecular views of recombination proteins and their control. West SC. Nat Rev Mol Cell Biol 4 435-445 (2003)
  3. Recombination proteins in yeast. Krogh BO, Symington LS. Annu Rev Genet 38 233-271 (2004)
  4. Homologous recombination in DNA repair and DNA damage tolerance. Li X, Heyer WD. Cell Res 18 99-113 (2008)
  5. Homologous recombination and its regulation. Krejci L, Altmannova V, Spirek M, Zhao X. Nucleic Acids Res 40 5795-5818 (2012)
  6. Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Symington LS, Rothstein R, Lisby M. Genetics 198 795-835 (2014)
  7. Molecular pathways: understanding the role of Rad52 in homologous recombination for therapeutic advancement. Lok BH, Powell SN. Clin Cancer Res 18 6400-6406 (2012)
  8. DNA Damage Signalling and Repair Inhibitors: The Long-Sought-After Achilles' Heel of Cancer. Velic D, Couturier AM, Ferreira MT, Rodrigue A, Poirier GG, Fleury F, Masson JY. Biomolecules 5 3204-3259 (2015)
  9. Reappearance from Obscurity: Mammalian Rad52 in Homologous Recombination. Hanamshet K, Mazina OM, Mazin AV. Genes (Basel) 7 E63 (2016)
  10. Structure and function of the double-strand break repair machinery. Shin DS, Chahwan C, Huffman JL, Tainer JA. DNA Repair (Amst) 3 863-873 (2004)
  11. Diversity and evolution of chromatin proteins encoded by DNA viruses. de Souza RF, Iyer LM, Aravind L. Biochim Biophys Acta 1799 302-318 (2010)
  12. The homologous recombination system of Ustilago maydis. Holloman WK, Schirawski J, Holliday R. Fungal Genet Biol 45 Suppl 1 S31-9 (2008)
  13. Mediators of homologous DNA pairing. Zelensky A, Kanaar R, Wyman C. Cold Spring Harb Perspect Biol 6 a016451 (2014)
  14. Emerging Roles of RAD52 in Genome Maintenance. Jalan M, Olsen KS, Powell SN. Cancers (Basel) 11 E1038 (2019)
  15. 'Black sheep' that don't leave the double-stranded RNA-binding domain fold. Gleghorn ML, Maquat LE. Trends Biochem Sci 39 328-340 (2014)
  16. RAD52 Functions in Homologous Recombination and Its Importance on Genomic Integrity Maintenance and Cancer Therapy. Nogueira A, Fernandes M, Fernandes M, Catarino R, Medeiros R. Cancers (Basel) 11 E1622 (2019)
  17. Structure and mechanism of the Red recombination system of bacteriophage λ. Caldwell BJ, Bell CE. Prog Biophys Mol Biol 147 33-46 (2019)
  18. RAD52: Paradigm of Synthetic Lethality and New Developments. Rossi MJ, DiDomenico SF, Patel M, Mazin AV. Front Genet 12 780293 (2021)
  19. Recent progress in understanding the molecular mechanisms of radioresistance in Deinococcus bacteria. Munteanu A, Uivarosi V, Andries A. Extremophiles 19 707-719 (2015)
  20. Advances in structural studies of recombination mediator proteins. Korolev S. Biophys Chem 225 27-37 (2017)
  21. Guardians of the Genome: BRCA2 and Its Partners. Le HP, Heyer WD, Liu J. Genes (Basel) 12 1229 (2021)
  22. There and back again: new single-molecule insights in the motion of DNA repair proteins. Spies M. Curr Opin Struct Biol 23 154-160 (2013)
  23. Protein cages, rings and tubes: useful components of future nanodevices? Heddle JG. Nanotechnol Sci Appl 1 67-78 (2008)
  24. A moving target for drug discovery: Structure activity relationship and many genome (de)stabilizing functions of the RAD52 protein. Bhat DS, Spies MA, Spies M. DNA Repair (Amst) 120 103421 (2022)

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  1. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. Mol Cell Biol 24 9305-9316 (2004)
  2. Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Nakanishi K, Yang YG, Pierce AJ, Taniguchi T, Digweed M, D'Andrea AD, Wang ZQ, Jasin M. Proc Natl Acad Sci U S A 102 1110-1115 (2005)
  3. Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. Shin DS, Pellegrini L, Daniels DS, Yelent B, Craig L, Bates D, Yu DS, Shivji MK, Hitomi C, Arvai AS, Volkmann N, Tsuruta H, Blundell TL, Venkitaraman AR, Tainer JA. EMBO J 22 4566-4576 (2003)
  4. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Iyer LM, Koonin EV, Leipe DD, Aravind L. Nucleic Acids Res 33 3875-3896 (2005)
  5. Mammalian RAD52 Functions in Break-Induced Replication Repair of Collapsed DNA Replication Forks. Sotiriou SK, Kamileri I, Lugli N, Evangelou K, Da-Ré C, Huber F, Padayachy L, Tardy S, Nicati NL, Barriot S, Ochs F, Lukas C, Lukas J, Gorgoulis VG, Scapozza L, Halazonetis TD. Mol Cell 64 1127-1134 (2016)
  6. Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. Garcia PL, Liu Y, Jiricny J, West SC, Janscak P. EMBO J 23 2882-2891 (2004)
  7. RAD52 inactivation is synthetically lethal with deficiencies in BRCA1 and PALB2 in addition to BRCA2 through RAD51-mediated homologous recombination. Lok BH, Carley AC, Tchang B, Powell SN. Oncogene 32 3552-3558 (2013)
  8. Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. Makarova KS, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Lapidus A, Copeland A, Kim E, Land M, Mavrommatis K, Pitluck S, Richardson PM, Detter C, Brettin T, Saunders E, Lai B, Ravel B, Kemner KM, Wolf YI, Sorokin A, Gerasimova AV, Gelfand MS, Fredrickson JK, Koonin EV, Daly MJ. PLoS One 2 e955 (2007)
  9. The Bloom's syndrome helicase promotes the annealing of complementary single-stranded DNA. Cheok CF, Wu L, Garcia PL, Janscak P, Hickson ID. Nucleic Acids Res 33 3932-3941 (2005)
  10. Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52-ssDNA complexes. Grimme JM, Honda M, Wright R, Okuno Y, Rothenberg E, Mazin AV, Ha T, Spies M. Nucleic Acids Res 38 2917-2930 (2010)
  11. Clustered telomeres in phase-separated nuclear condensates engage mitotic DNA synthesis through BLM and RAD52. Min J, Wright WE, Shay JW. Genes Dev 33 814-827 (2019)
  12. In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. Miyazaki T, Bressan DA, Shinohara M, Haber JE, Shinohara A. EMBO J 23 939-949 (2004)
  13. DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. McIlwraith MJ, West SC. Mol Cell 29 510-516 (2008)
  14. Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1. Kinebuchi T, Kagawa W, Enomoto R, Tanaka K, Miyagawa K, Shibata T, Kurumizaka H, Yokoyama S. Mol Cell 14 363-374 (2004)
  15. Rad52 Inverse Strand Exchange Drives RNA-Templated DNA Double-Strand Break Repair. Mazina OM, Keskin H, Hanamshet K, Storici F, Mazin AV. Mol Cell 67 19-29.e3 (2017)
  16. Suppression of the DNA repair defects of BRCA2-deficient cells with heterologous protein fusions. Saeki H, Siaud N, Christ N, Wiegant WW, van Buul PP, Han M, Zdzienicka MZ, Stark JM, Jasin M. Proc Natl Acad Sci U S A 103 8768-8773 (2006)
  17. Preserving genome integrity: the DdrA protein of Deinococcus radiodurans R1. Harris DR, Tanaka M, Saveliev SV, Jolivet E, Earl AM, Cox MM, Battista JR. PLoS Biol 2 e304 (2004)
  18. Mechanism of RecO recruitment to DNA by single-stranded DNA binding protein. Ryzhikov M, Koroleva O, Postnov D, Tran A, Korolev S. Nucleic Acids Res 39 6305-6314 (2011)
  19. Conservative repair of a chromosomal double-strand break by single-strand DNA through two steps of annealing. Storici F, Snipe JR, Chan GK, Gordenin DA, Resnick MA. Mol Cell Biol 26 7645-7657 (2006)
  20. Protein dynamics during presynaptic-complex assembly on individual single-stranded DNA molecules. Gibb B, Ye LF, Kwon Y, Niu H, Sung P, Greene EC. Nat Struct Mol Biol 21 893-900 (2014)
  21. Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Rothenberg E, Grimme JM, Spies M, Ha T. Proc Natl Acad Sci U S A 105 20274-20279 (2008)
  22. Poly-small ubiquitin-like modifier (PolySUMO)-binding proteins identified through a string search. Sun H, Hunter T. J Biol Chem 287 42071-42083 (2012)
  23. Small-Molecule Disruption of RAD52 Rings as a Mechanism for Precision Medicine in BRCA-Deficient Cancers. Chandramouly G, McDevitt S, Sullivan K, Kent T, Luz A, Glickman JF, Andrake M, Skorski T, Pomerantz RT. Chem Biol 22 1491-1504 (2015)
  24. The HSV-1 exonuclease, UL12, stimulates recombination by a single strand annealing mechanism. Schumacher AJ, Mohni KN, Kan Y, Hendrickson EA, Stark JM, Weller SK. PLoS Pathog 8 e1002862 (2012)
  25. Efficient targeted integration directed by short homology in zebrafish and mammalian cells. Wierson WA, Welker JM, Almeida MP, Mann CM, Webster DA, Torrie ME, Weiss TJ, Kambakam S, Vollbrecht MK, Lan M, McKeighan KC, Levey J, Ming Z, Wehmeier A, Mikelson CS, Haltom JA, Kwan KM, Chien CB, Balciunas D, Ekker SC, Clark KJ, Webber BR, Moriarity BS, Solin SL, Carlson DF, Dobbs DL, McGrail M, Essner J. Elife 9 e53968 (2020)
  26. Identification of a second DNA binding site in the human Rad52 protein. Kagawa W, Kagawa A, Saito K, Ikawa S, Shibata T, Kurumizaka H, Yokoyama S. J Biol Chem 283 24264-24273 (2008)
  27. The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. Lettier G, Feng Q, de Mayolo AA, Erdeniz N, Reid RJ, Lisby M, Mortensen UH, Rothstein R. PLoS Genet 2 e194 (2006)
  28. Different quaternary structures of human RECQ1 are associated with its dual enzymatic activity. Muzzolini L, Beuron F, Patwardhan A, Popuri V, Cui S, Niccolini B, Rappas M, Freemont PS, Vindigni A. PLoS Biol 5 e20 (2007)
  29. CeBRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing. Petalcorin MI, Sandall J, Wigley DB, Boulton SJ. J Mol Biol 361 231-242 (2006)
  30. FANCA Promotes DNA Double-Strand Break Repair by Catalyzing Single-Strand Annealing and Strand Exchange. Benitez A, Liu W, Palovcak A, Wang G, Moon J, An K, Kim A, Zheng K, Zhang Y, Bai F, Mazin AV, Pei XH, Yuan F, Zhang Y. Mol Cell 71 621-628.e4 (2018)
  31. Crystal structure and DNA-binding analysis of RecO from Deinococcus radiodurans. Leiros I, Timmins J, Hall DR, McSweeney S. EMBO J 24 906-918 (2005)
  32. Identification of plant RAD52 homologs and characterization of the Arabidopsis thaliana RAD52-like genes. Samach A, Melamed-Bessudo C, Avivi-Ragolski N, Pietrokovski S, Levy AA. Plant Cell 23 4266-4279 (2011)
  33. Rad52 prevents excessive replication fork reversal and protects from nascent strand degradation. Malacaria E, Pugliese GM, Honda M, Marabitti V, Aiello FA, Spies M, Franchitto A, Pichierri P. Nat Commun 10 1412 (2019)
  34. Molecular anatomy of the recombination mediator function of Saccharomyces cerevisiae Rad52. Seong C, Sehorn MG, Plate I, Shi I, Song B, Chi P, Mortensen U, Sung P, Krejci L. J Biol Chem 283 12166-12174 (2008)
  35. Identification of a Small Molecule Inhibitor of RAD52 by Structure-Based Selection. Sullivan K, Cramer-Morales K, McElroy DL, Ostrov DA, Haas K, Childers W, Hromas R, Skorski T. PLoS One 11 e0147230 (2016)
  36. Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding. Honda M, Okuno Y, Yoo J, Ha T, Spies M. EMBO J 30 3368-3382 (2011)
  37. Conformational adaptability of Redbeta during DNA annealing and implications for its structural relationship with Rad52. Erler A, Wegmann S, Elie-Caille C, Bradshaw CR, Maresca M, Seidel R, Habermann B, Muller DJ, Stewart AF. J Mol Biol 391 586-598 (2009)
  38. Structure-function analysis of pneumococcal DprA protein reveals that dimerization is crucial for loading RecA recombinase onto DNA during transformation. Quevillon-Cheruel S, Campo N, Mirouze N, Mortier-Barrière I, Brooks MA, Boudes M, Durand D, Soulet AL, Lisboa J, Noirot P, Martin B, van Tilbeurgh H, Noirot-Gros MF, Claverys JP, Polard P. Proc Natl Acad Sci U S A 109 E2466-75 (2012)
  39. Functional and structural basis for a bacteriophage homolog of human RAD52. Ploquin M, Bransi A, Paquet ER, Stasiak AZ, Stasiak A, Yu X, Cieslinska AM, Egelman EH, Moineau S, Masson JY. Curr Biol 18 1142-1146 (2008)
  40. Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. Bouchard JD, Moineau S. J Bacteriol 186 3649-3652 (2004)
  41. Human and yeast Rad52 proteins promote DNA strand exchange. Bi B, Rybalchenko N, Golub EI, Radding CM. Proc Natl Acad Sci U S A 101 9568-9572 (2004)
  42. Identification of residues important for DNA binding in the full-length human Rad52 protein. Lloyd JA, McGrew DA, Knight KL. J Mol Biol 345 239-249 (2005)
  43. A novel structure of DNA repair protein RecO from Deinococcus radiodurans. Makharashvili N, Koroleva O, Bera S, Grandgenett DP, Korolev S. Structure 12 1881-1889 (2004)
  44. Role for RAD18 in homologous recombination in DT40 cells. Szüts D, Simpson LJ, Kabani S, Yamazoe M, Sale JE. Mol Cell Biol 26 8032-8041 (2006)
  45. HSV-I and the cellular DNA damage response. Smith S, Weller SK. Future Virol 10 383-397 (2015)
  46. Human RAD52 interactions with replication protein A and the RAD51 presynaptic complex. Ma CJ, Kwon Y, Sung P, Greene EC. J Biol Chem 292 11702-11713 (2017)
  47. Mutational signatures reveal the role of RAD52 in p53-independent p21-driven genomic instability. Galanos P, Pappas G, Polyzos A, Kotsinas A, Svolaki I, Giakoumakis NN, Glytsou C, Pateras IS, Swain U, Souliotis VL, Georgakilas AG, Geacintov N, Scorrano L, Lukas C, Lukas J, Livneh Z, Lygerou Z, Chowdhury D, Sørensen CS, Bartek J, Gorgoulis VG. Genome Biol 19 37 (2018)
  48. Human replication protein A-Rad52-single-stranded DNA complex: stoichiometry and evidence for strand transfer regulation by phosphorylation. Deng X, Prakash A, Dhar K, Baia GS, Kolar C, Oakley GG, Borgstahl GE. Biochemistry 48 6633-6643 (2009)
  49. Structural Basis of Homology-Directed DNA Repair Mediated by RAD52. Saotome M, Saito K, Yasuda T, Ohtomo H, Sugiyama S, Nishimura Y, Kurumizaka H, Kagawa W. iScience 3 50-62 (2018)
  50. Presynaptic filament dynamics in homologous recombination and DNA repair. Liu J, Ehmsen KT, Heyer WD, Morrical SW. Crit Rev Biochem Mol Biol 46 240-270 (2011)
  51. DNA binding, annealing, and strand exchange activities of Brh2 protein from Ustilago maydis. Mazloum N, Zhou Q, Holloman WK. Biochemistry 46 7163-7173 (2007)
  52. Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. Ohuchi T, Seki M, Branzei D, Maeda D, Ui A, Ogiwara H, Tada S, Enomoto T. DNA Repair (Amst) 7 879-889 (2008)
  53. Mgm101 is a Rad52-related protein required for mitochondrial DNA recombination. Mbantenkhu M, Wang X, Nardozzi JD, Wilkens S, Hoffman E, Patel A, Cosgrove MS, Chen XJ. J Biol Chem 286 42360-42370 (2011)
  54. Rad52 and Ku bind to different DNA structures produced early in double-strand break repair. Ristic D, Modesti M, Kanaar R, Wyman C. Nucleic Acids Res 31 5229-5237 (2003)
  55. Rad52 and Rad59 exhibit both overlapping and distinct functions. Feng Q, Düring L, de Mayolo AA, Lettier G, Lisby M, Erdeniz N, Mortensen UH, Rothstein R. DNA Repair (Amst) 6 27-37 (2007)
  56. Loss of Rad52 partially rescues tumorigenesis and T-cell maturation in Atm-deficient mice. Treuner K, Helton R, Barlow C. Oncogene 23 4655-4661 (2004)
  57. Compensatory role for Rad52 during recombinational repair in Ustilago maydis. Kojic M, Mao N, Zhou Q, Lisby M, Holloman WK. Mol Microbiol 67 1156-1168 (2008)
  58. Human RAD52 Captures and Holds DNA Strands, Increases DNA Flexibility, and Prevents Melting of Duplex DNA: Implications for DNA Recombination. Brouwer I, Zhang H, Candelli A, Normanno D, Peterman EJG, Wuite GJL, Modesti M. Cell Rep 18 2845-2853 (2017)
  59. Association of a functional RAD52 genetic variant locating in a miRNA binding site with risk of HBV-related hepatocellular carcinoma. Li Z, Guo Y, Zhou L, Ge Y, Wei L, Li L, Zhou C, Wei J, Yuan Q, Li J, Yang M. Mol Carcinog 54 853-858 (2015)
  60. The Rad52 homologs Rad22 and Rti1 of Schizosaccharomyces pombe are not essential for meiotic interhomolog recombination, but are required for meiotic intrachromosomal recombination and mating-type-related DNA repair. Octobre G, Lorenz A, Loidl J, Kohli J. Genetics 178 2399-2412 (2008)
  61. A quantitative model of the major pathways for radiation-induced DNA double-strand break repair. Belov OV, Krasavin EA, Lyashko MS, Batmunkh M, Sweilam NH. J Theor Biol 366 115-130 (2015)
  62. Lactococcal phage p2 ORF35-Sak3 is an ATPase involved in DNA recombination and AbiK mechanism. Scaltriti E, Launay H, Genois MM, Bron P, Rivetti C, Grolli S, Ploquin M, Campanacci V, Tegoni M, Cambillau C, Moineau S, Masson JY. Mol Microbiol 80 102-116 (2011)
  63. Rad52/Rad59-dependent recombination as a means to rectify faulty Okazaki fragment processing. Lee M, Lee CH, Demin AA, Munashingha PR, Amangyeld T, Kwon B, Formosa T, Seo YS. J Biol Chem 289 15064-15079 (2014)
  64. RecO-mediated DNA homology search and annealing is facilitated by SsbA. Manfredi C, Suzuki Y, Yadav T, Takeyasu K, Alonso JC. Nucleic Acids Res 38 6920-6929 (2010)
  65. Biochemistry of eukaryotic homologous recombination. Heyer WD. Top Curr Genet 17 95-133 (2007)
  66. Deciphering the function of lactococcal phage ul36 Sak domains. Scaltriti E, Moineau S, Launay H, Masson JY, Rivetti C, Ramoni R, Campanacci V, Tegoni M, Cambillau C. J Struct Biol 170 462-469 (2010)
  67. Mechanism for accurate, protein-assisted DNA annealing by Deinococcus radiodurans DdrB. Sugiman-Marangos SN, Weiss YM, Junop MS. Proc Natl Acad Sci U S A 113 4308-4313 (2016)
  68. Novel function of HATs and HDACs in homologous recombination through acetylation of human RAD52 at double-strand break sites. Yasuda T, Kagawa W, Ogi T, Kato TA, Suzuki T, Dohmae N, Takizawa K, Nakazawa Y, Genet MD, Saotome M, Hama M, Konishi T, Nakajima NI, Hazawa M, Tomita M, Koike M, Noshiro K, Tomiyama K, Obara C, Gotoh T, Ui A, Fujimori A, Nakayama F, Hanaoka F, Sugasawa K, Okayasu R, Jeggo PA, Tajima K. PLoS Genet 14 e1007277 (2018)
  69. Replication protein A binds RNA and promotes R-loop formation. Mazina OM, Somarowthu S, Kadyrova LY, Baranovskiy AG, Tahirov TH, Kadyrov FA, Mazin AV. J Biol Chem 295 14203-14213 (2020)
  70. The N-terminal DNA-binding domain of Rad52 promotes RAD51-independent recombination in Saccharomyces cerevisiae. Tsukamoto M, Yamashita K, Miyazaki T, Shinohara M, Shinohara A. Genetics 165 1703-1715 (2003)
  71. Biochemistry of Meiotic Recombination: Formation, Processing, and Resolution of Recombination Intermediates. Ehmsen KT, Heyer WD. Genome Dyn Stab 3 91 (2008)
  72. DNA-binding properties of T4 UvsY recombination mediator protein: polynucleotide wrapping promotes high-affinity binding to single-stranded DNA. Xu H, Beernink HT, Morrical SW. Nucleic Acids Res 38 4821-4833 (2010)
  73. Novel RNA and DNA strand exchange activity of the PALB2 DNA binding domain and its critical role for DNA repair in cells. Deveryshetty J, Peterlini T, Ryzhikov M, Brahiti N, Dellaire G, Masson JY, Korolev S. Elife 8 e44063 (2019)
  74. Rev7 and 53BP1/Crb2 prevent RecQ helicase-dependent hyper-resection of DNA double-strand breaks. Leland BA, Chen AC, Zhao AY, Wharton RC, King MC. Elife 7 e33402 (2018)
  75. Structural and functional characterization of the Redβ recombinase from bacteriophage λ. Matsubara K, Malay AD, Curtis FA, Sharples GJ, Heddle JG. PLoS One 8 e78869 (2013)
  76. The in vitro activity of a Rad55 homologue from Sulfolobus tokodaii, a candidate mediator in RadA-catalyzed homologous recombination. Sheng D, Zhu S, Wei T, Ni J, Shen Y. Extremophiles 12 147-157 (2008)
  77. Crystal structure of the Redβ C-terminal domain in complex with λ Exonuclease reveals an unexpected homology with λ Orf and an interaction with Escherichia coli single stranded DNA binding protein. Caldwell BJ, Zakharova E, Filsinger GT, Wannier TM, Hempfling JP, Chun-Der L, Pei D, Church GM, Bell CE. Nucleic Acids Res 47 1950-1963 (2019)
  78. Heteroduplex joint formation free of net topological change by Mhr1, a mitochondrial recombinase. Ling F, Yoshida M, Shibata T. J Biol Chem 284 9341-9353 (2009)
  79. Functional analyses of the C-terminal half of the Saccharomyces cerevisiae Rad52 protein. Kagawa W, Arai N, Ichikawa Y, Saito K, Sugiyama S, Saotome M, Shibata T, Kurumizaka H. Nucleic Acids Res 42 941-951 (2014)
  80. Mutational analysis of Brh2 reveals requirements for compensating mediator functions. Kojic M, Zhou Q, Fan J, Holloman WK. Mol Microbiol 79 180-191 (2011)
  81. The putative nuclear localization signal of the human RAD52 protein is a potential sumoylation site. Saito K, Kagawa W, Suzuki T, Suzuki H, Yokoyama S, Saitoh H, Tashiro S, Dohmae N, Kurumizaka H. J Biochem 147 833-842 (2010)
  82. Nucleic acid-binding properties of the RRM-containing protein RDM1. Hamimes S, Bourgeon D, Stasiak AZ, Stasiak A, Van Dyck E. Biochem Biophys Res Commun 344 87-94 (2006)
  83. The function of RAD52 N-terminal domain is essential for viability of BRCA-deficient cells. Hanamshet K, Mazin AV. Nucleic Acids Res 48 12778-12791 (2020)
  84. Crystal structure of the DdrB/ssDNA complex from Deinococcus radiodurans reveals a DNA binding surface involving higher-order oligomeric states. Sugiman-Marangos SN, Peel JK, Weiss YM, Ghirlando R, Junop MS. Nucleic Acids Res 41 9934-9944 (2013)
  85. DNA annealing by Redβ is insufficient for homologous recombination and the additional requirements involve intra- and inter-molecular interactions. Subramaniam S, Erler A, Fu J, Kranz A, Tang J, Gopalswamy M, Ramakrishnan S, Keller A, Grundmeier G, Müller D, Sattler M, Stewart AF. Sci Rep 6 34525 (2016)
  86. Domain Structure of the Redβ Single-Strand Annealing Protein: the C-terminal Domain is Required for Fine-Tuning DNA-binding Properties, Interaction with the Exonuclease Partner, and Recombination in vivo. Smith CE, Bell CE. J Mol Biol 428 561-578 (2016)
  87. Rad52 multimerization is important for its nuclear localization in Saccharomyces cerevisiae. Plate I, Albertsen L, Lisby M, Hallwyl SC, Feng Q, Seong C, Rothstein R, Sung P, Mortensen UH. DNA Repair (Amst) 7 57-66 (2008)
  88. RecO protein initiates DNA recombination and strand annealing through two alternative DNA binding mechanisms. Ryzhikov M, Gupta R, Glickman M, Korolev S. J Biol Chem 289 28846-28855 (2014)
  89. Selective killing of homologous recombination-deficient cancer cell lines by inhibitors of the RPA:RAD52 protein-protein interaction. Al-Mugotir M, Lovelace JJ, George J, Bessho M, Pal D, Struble L, Kolar C, Rana S, Natarajan A, Bessho T, Borgstahl GEO. PLoS One 16 e0248941 (2021)
  90. A RAD52 genetic variant located in a miRNA binding site is associated with glioma risk in Han Chinese. Lu C, Chen YD, Han S, Wei J, Ge Y, Pan W, Jiang T, Qiu XG, Yang M. J Neurooncol 120 11-17 (2014)
  91. Cells expressing murine RAD52 splice variants favor sister chromatid repair. Thorpe PH, Marrero VA, Savitzky MH, Sunjevaric I, Freeman TC, Rothstein R. Mol Cell Biol 26 3752-3763 (2006)
  92. Structure and mechanism of the phage T4 recombination mediator protein UvsY. Gajewski S, Waddell MB, Vaithiyalingam S, Nourse A, Li Z, Woetzel N, Alexander N, Meiler J, White SW. Proc Natl Acad Sci U S A 113 3275-3280 (2016)
  93. Compound F779-0434 causes synthetic lethality in BRCA2-deficient cancer cells by disrupting RAD52-ssDNA association. Li J, Yang Q, Zhang Y, Huang K, Sun R, Zhao Q. RSC Adv 8 18859-18869 (2018)
  94. Brh2 domain function distinguished by differential cellular responses to DNA damage and replication stress. Kojic M, Holloman WK. Mol Microbiol 83 351-361 (2012)
  95. Characterization of zebrafish Rad52 and replication protein A for oligonucleotide-mediated mutagenesis. Takahashi N, Dawid IB. Nucleic Acids Res 33 e120 (2005)
  96. Identification of an SCLC susceptibility rs7963551 genetic polymorphism in a previously GWAS-identified 12p13.33 RAD52 lung cancer risk locus in the Chinese population. Han S, Gao F, Yang W, Ren Y, Liang X, Xiong X, Pan W, Zhou L, Zhou C, Ma F, Yang M. Int J Clin Exp Med 8 16528-16535 (2015)
  97. The rad52-Y66A allele alters the choice of donor template during spontaneous chromosomal recombination. de Mayolo AA, Sunjevaric I, Reid R, Mortensen UH, Rothstein R, Lisby M. DNA Repair (Amst) 9 23-32 (2010)
  98. Identification of a RAD52 Inhibitor Inducing Synthetic Lethality in BRCA2-Deficient Cancer Cells. Yang Q, Li Y, Sun R, Li J. Front Pharmacol 12 637825 (2021)
  99. Mgm101: A double-duty Rad52-like protein. Rendeková J, Ward TA, Šimoničová L, Thomas PH, Nosek J, Tomáška Ľ, McHugh PJ, Chovanec M. Cell Cycle 15 3169-3176 (2016)
  100. Oligomeric complexes formed by Redβ single strand annealing protein in its different DNA bound states. Caldwell BJ, Norris A, Zakharova E, Smith CE, Wheat CT, Choudhary D, Sotomayor M, Wysocki VH, Bell CE. Nucleic Acids Res 49 3441-3460 (2021)
  101. Roles of C-Terminal Region of Yeast and Human Rad52 in Rad51-Nucleoprotein Filament Formation and ssDNA Annealing. Khade NV, Sugiyama T. PLoS One 11 e0158436 (2016)
  102. XAB2 promotes Ku eviction from single-ended DNA double-strand breaks independently of the ATM kinase. Sharma AB, Erasimus H, Pinto L, Caron MC, Gopaul D, Peterlini T, Neumann K, Nazarov PV, Fritah S, Klink B, Herold-Mende CC, Niclou SP, Pasero P, Calsou P, Masson JY, Britton S, Van Dyck E. Nucleic Acids Res 49 9906-9925 (2021)
  103. DNA mediated disassembly of hRad51 and hRad52 proteins and recruitment of hRad51 to ssDNA by hRad52. Navadgi VM, Shukla A, Vempati RK, Rao BJ. FEBS J 273 199-207 (2006)
  104. Impeding the single-strand annealing pathway of DNA double-strand break repair by withaferin A-mediated FANCA degradation. Liu W, Wang G, Palovcak A, Li Y, Hao S, Liu ZJ, Landgraf R, Yuan F, Zhang Y. DNA Repair (Amst) 77 10-17 (2019)
  105. The cryo-EM structure of full-length RAD52 protein contains an undecameric ring. Kinoshita C, Takizawa Y, Saotome M, Ogino S, Kurumizaka H, Kagawa W. FEBS Open Bio 13 408-418 (2023)
  106. Deinococcus radiodurans DR1088 is a novel RecF-interacting protein that stimulates single-stranded DNA annealing. Cheng K, Xu G, Xu H, Zhao Y, Hua Y. Mol Microbiol 106 518-529 (2017)
  107. Hybrid inhibitors of DNA and HDACs remarkably enhance cytotoxicity in leukaemia cells. Song Y, Park SY, Wu Z, Liu KH, Seo YH. J Enzyme Inhib Med Chem 35 1069-1079 (2020)
  108. Integrating Experimental and In Silico HTS in the Discovery of Inhibitors of Protein-Nucleic Acid Interactions. Li Q, Folly da Silva Constantino L, Spies MA. Methods Enzymol 601 243-273 (2018)
  109. RNA Expression of DNA Damage Response Genes in Muscle-Invasive Bladder Cancer: Influence on Outcome and Response to Adjuvant Cisplatin-Based Chemotherapy. Herrmann J, Schmidt H, Nitschke K, Weis CA, Nuhn P, von Hardenberg J, Michel MS, Erben P, Worst TS. Int J Mol Sci 22 4188 (2021)
  110. Redβ177 annealase structure reveals details of oligomerization and λ Red-mediated homologous DNA recombination. Newing TP, Brewster JL, Fitschen LJ, Bouwer JC, Johnston NP, Yu H, Tolun G. Nat Commun 13 5649 (2022)
  111. A Spotlight on Rad52 in Cyanidiophytina (Rhodophyta): A Relic in Algal Heritage. Del Mondo A, Iovinella M, Petriccione M, Nunziata A, Davis SJ, Cioppa D, Ciniglia C. Plants (Basel) 8 E46 (2019)
  112. Biochemical characterization of plant Rad52 protein from rice (Oryza sativa). Nair A, Agarwal R, Chittela RK. Plant Physiol Biochem 106 108-117 (2016)
  113. Mutational Analysis of Redβ Single Strand Annealing Protein: Roles of the 14 Lysine Residues in DNA Binding and Recombination In Vivo. Zakharova K, Caldwell BJ, Ta S, Wheat CT, Bell CE. Int J Mol Sci 22 7758 (2021)
  114. Mutagenesis identifies the critical regions and amino acid residues of suid herpesvirus 1 DNA-binding protein required for DNA binding and strand invasion. Wu SL, Li CC, Ho TY, Hsiang CY. Virus Res 140 147-154 (2009)
  115. Nuclear localization of Rad52 is pre-requisite for its sumoylation. Ohuchi T, Seki M, Enomoto T. Biochem Biophys Res Commun 372 126-130 (2008)
  116. Replication Protein A Phosphorylation Facilitates RAD52-Dependent Homologous Recombination in BRCA-Deficient Cells. Carley AC, Jalan M, Subramanyam S, Roy R, Borgstahl GEO, Powell SN. Mol Cell Biol 42 e0052421 (2022)
  117. Variants of the human RAD52 gene confer defects in ionizing radiation resistance and homologous recombination repair in budding yeast. Clear AD, Manthey GM, Lewis O, Lopez IY, Rico R, Owens S, Negritto MC, Wolf EW, Xu J, Kenjić N, Perry JJP, Adamson AW, Neuhausen SL, Bailis AM. Microb Cell 7 270-285 (2020)
  118. Giardia duodenalis Rad52 protein: biochemical characterization and response upon DNA damage. Martínez-Miguel RM, Sandoval-Cabrera A, Bazán-Tejeda ML, Torres-Huerta AL, Martínez-Reyes DA, Bermúdez-Cruz RM, Bermúdez-Cruz RM. J Biochem 162 123-135 (2017)
  119. Structure of a RecT/Redβ family recombinase in complex with a duplex intermediate of DNA annealing. Caldwell BJ, Norris AS, Karbowski CF, Wiegand AM, Wysocki VH, Bell CE. Nat Commun 13 7855 (2022)
  120. Yeast Rad52 is a homodecamer and possesses BRCA2-like bipartite Rad51 binding modes. Deveryshetty J, Chadda R, Mattice JR, Karunakaran S, Rau MJ, Basore K, Pokhrel N, Englander N, Fitzpatrick JAJ, Bothner B, Antony E. Nat Commun 14 6215 (2023)
  121. Biochemical characterization of the RNA-binding and RNA-DNA strand exchange activities of the human RAD52 protein. Tsuchiya R, Saotome M, Kinoshita C, Kamoi K, Kagawa W. J Biochem 174 59-69 (2023)
  122. FIRRM cooperates with FIGNL1 to promote RAD51 disassembly during DNA repair. Pinedo-Carpio E, Dessapt J, Beneyton A, Sacre L, Bérubé MA, Villot R, Lavoie EG, Coulombe Y, Blondeau A, Boulais J, Malina A, Luo VM, Lazaratos AM, Côté JF, Mallette FA, Guarné A, Masson JY, Fradet-Turcotte A, Orthwein A. Sci Adv 9 eadf4082 (2023)
  123. Human RAD52 stimulates the RAD51-mediated homology search. Muhammad AA, Basto C, Peterlini T, Guirouilh-Barbat J, Thomas M, Veaute X, Busso D, Lopez B, Mazon G, Le Cam E, Masson JY, Dupaigne P. Life Sci Alliance 7 e202201751 (2024)
  124. The Rad52 SSAP superfamily and new insight into homologous recombination. Al-Fatlawi A, Schroeder M, Stewart AF. Commun Biol 6 87 (2023)
  125. Therapeutic disruption of RAD52-ssDNA complexation via novel drug-like inhibitors. Bhat DS, Malacaria E, Biagi LD, Razzaghi M, Honda M, Hobbs KF, Hengel SR, Pichierri P, Spies MA, Spies M. NAR Cancer 5 zcad018 (2023)


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