The BRC repeats of human BRCA2 differentially regulate RAD51 binding on single- versus double-stranded DNA to stimulate strand exchange

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 32, 2009, Pages 13254-13259

  Shivji, Mahmud K K ^a   Mukund, Shreyas R ^a,b   Rajendra, Eeson ^a   Chen, Shaoxia ^c   Short, Judith M ^c   Savill, Jane ^a   Klenerman, David ^b   Venkitaraman, Ashok R ^a  

^a HUTCHISON MRC RESEARCH CENTRE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

DNA recombination; Electron microscopy; Single molecule fluorescence spectroscopy; Tumor suppressor

Indexed keywords

BRCA2 PROTEIN; DOUBLE STRANDED DNA; RAD51 PROTEIN; REPETITIVE DNA; SINGLE STRANDED DNA;

ARTICLE; CONTROLLED STUDY; DNA RECOMBINATION; DNA STRAND; ELECTRON MICROSCOPY; ELECTROPHORETIC MOBILITY; FLUORESCENCE SPECTROSCOPY; HOMOLOGOUS RECOMBINATION; HUMAN; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; REGULATORY MECHANISM;

BRCA2 PROTEIN; COLOR; DNA, SINGLE-STRANDED; ELECTROPHORESIS; HUMANS; MODELS, BIOLOGICAL; PROTEIN BINDING; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; REPETITIVE SEQUENCES, AMINO ACID; SPECTROMETRY, FLUORESCENCE;

EID: 69449089443     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906208106     Document Type: Article

References (32)

1. Li X, Heyer WD (2008) Homologous recombination in DNA repair and DNA damage tolerance. Cell Res 18:99-113.
2. San Filippo J, Sung P, Klein H (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77:229-257.
3. Moynahan ME, Pierce AJ, Jasin M (2001) BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 7:263-272.
4. Thorslund T, West SC (2007) BRCA2: A universal recombinase regulator. Oncogene 26:7720-7730.
5. WongAK, Pero R, Ormonde PA, Tavtigian SV, Bartel PL (1997) RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J Biol Chem 272:31941-31944.
6. Sharan SK, et al. (1997) Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386:804-810.
7. Lo T, Pellegrini L, Venkitaraman AR, Blundell TL (2003) Sequence fingerprints in BRCA2 and RAD51: Implications for DNA repair and cancer. DNA Repair (Amst) 2:1015-1028. (Pubitemid 37088163)
8. Yang H, et al. (2002) BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297:1837-1848. (Pubitemid 35024337)
9. Yang H, Li Q, Fan J, Holloman WK, Pavletich NP (2005) The BRCA2 homologue Brh2 nucleates RAD51 filament formation at a dsDNA-ssDNA junction. Nature 433:653-657. (Pubitemid 40283000)
10. Saeki H, et al. (2006) Suppression of the DNA repair defects of BRCA2-deficient cells with heterologous protein fusions. Proc Natl Acad Sci USA 103:8768-8773. (Pubitemid 43878094)
11. San Filippo J, et al. (2006) Recombination mediator and Rad51 targeting activities of a human BRCA2 polypeptide. J Biol Chem 281:11649-11657.
12. Pellegrini L, et al. (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420:287-293. (Pubitemid 35398178)
13. Davies AA, et al. (2001) Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol Cell 7:273-282. (Pubitemid 32206495)
14. Chen CF, Chen PL, Zhong Q, Sharp ZD, Lee WH (1999) Expression of BRC repeats in breast cancer cells disrupts the BRCA2-Rad51 complex and leads to radiation hypersensitivity and loss of G(2)/M checkpoint control. J Biol Chem 274:32931-32935. (Pubitemid 129535331)
15. Galkin VE, et al. (2005) BRCA2 BRC motifs bind RAD51-DNA filaments. Proc Natl Acad Sci USA 102:8537-8542.
16. Shivji MK, et al. (2006) A region of human BRCA2 containing multiple BRC repeats promotes RAD51-mediated strand exchange. Nucleic Acids Res 34:4000-4011.
17. Carreira A, et al. (2009) The BRC repeats of BRCA2 modulate the DNA binding selectivity of RAD51. Cell 136:1032-1043.
18. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265:1241-1243.
19. Baumann P, Benson FE, West SC (1996) Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell 87:757-766. (Pubitemid 26386948)
20. Petalcorin MI, Galkin VE, Yu X, Egelman EH, Boulton SJ (2007) Stabilization of RAD-51-DNA filaments via an interaction domain in Caenorhabditis elegans BRCA2. Proc Natl Acad Sci USA 104:8299-8304. (Pubitemid 47175482)
21. Li H, Ying L, Green JJ, Balasubramanian S, Klenerman D (2003) Ultrasensitive coincidence fluorescence detection of single DNA molecules. Anal Chem 75:1664-1670. (Pubitemid 36512606)
22. van der Heijden T, et al. (2007) Real-time assembly and disassembly of human RAD51 filaments on individual DNA molecules. Nucleic Acids Res 35:5646-5657.
23. Chi P, Van Komen S, Sehorn MG, Sigurdsson S, Sung P (2006) Roles of ATP binding and ATP hydrolysis in human Rad51 recombinase function. DNA Repair (Amst) 5:381-391. (Pubitemid 43247603)
24. Ristic D, et al. (2005) Human Rad51 filaments on double- and single-stranded DNA: Correlating regular and irregular formswith recombination function. Nucleic Acids Res 33:3292-3302. (Pubitemid 41194473)
25. Mine J, et al. (2007) Real-time measurements of the nucleation, growth and dissociation of single Rad51-DNA nucleoprotein filaments. Nucleic Acids Res 35:7171-7187.
26. Galletto R, Amitani I, Baskin RJ, Kowalczykowski SC (2006) Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443:875-878. (Pubitemid 44622700)
27. Sung P, Robberson DL (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82:453-461.
28. Mazin AV, Zaitseva E, Sung P, Kowalczykowski SC (2000) Tailed duplex DNA is the preferred substrate for Rad51 protein-mediated homologous pairing. EMBO J 19:1148-1156. (Pubitemid 30119839)
29. Benson FE, Stasiak A, West SC (1994) Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J 13:5764-5771. (Pubitemid 24363044)
30. Sigurdsson S, Trujillo K, Song B, Stratton S, Sung P (2001) Basis for avid homologous DNA strand exchange by human Rad51 and RPA. J Biol Chem 276:8798-8806. (Pubitemid 37385450)
31. Liu Y, et al. (2004) Conformational changes modulate the activity of human RAD51 protein. J Mol Biol 337:817-827. (Pubitemid 38368927)
32. Orte A, et al. (2008) Direct characterization of amyloidogenic oligomers by single-molecule fluorescence. Proc Natl Acad Sci USA 105:14424-14429.