RAD51 mutants cause replication defects and chromosomal instability

Molecular and Cellular Biology

Volumn 32, Issue 18, 2012, Pages 3663-3680

  Kim, Tae Moon ^a   Ko, Jun Ho ^a   Hu, Lingchuan ^a   Kim, Sung A ^a   Bishop, Alexander J R ^a,b,c   Vijg, Jan ^d   Montagna, Cristina ^d   Hasty, Paul ^a,c  

^a University of Texas Health Science Center at San Antonio   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c San Antonio Cancer Institute   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; CAMPTOTHECIN; DOUBLE STRANDED DNA; ENHANCED GREEN FLUORESCENT PROTEIN; LYSINE; MUTANT PROTEIN; RAD51 PROTEIN;

ANIMAL CELL; ARTICLE; CHROMOSOMAL INSTABILITY; CHROMOSOME; CHROMOSOME STRUCTURE; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA REPAIR; DNA REPLICATION; EMBRYONIC STEM CELL; ENZYME BINDING; GENE REARRANGEMENT; HUMAN; HYDROLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CAMPTOTHECIN; CELL LINE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATIONS; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; EMBRYONIC STEM CELLS; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; PROMOTER REGIONS, GENETIC; RAD51 RECOMBINASE; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84866424521     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00406-12     Document Type: Article

References (75)

1. Adra CN, Boer PH, McBurney MW. 1987. Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene 60:65-74.
2. Araki K, Araki M, Yamamura K. 1997. Targeted integration of DNA using mutant lox sites in embryonic stem cells. Nucleic Acids Res. 25:868-872.
3. Araki K, Okada Y, Araki M, Yamamura K. 2010. Comparative analysis of right element mutant lox sites on recombination efficiency in embryonic stem cells. BMC Biotechnol. 10:29. doi:10.1186/1472-6750-10-29.
4. Badie S, et al. 2010. BRCA2 acts as a RAD51 loader to facilitate telomere replication and capping. Nat. Struct. Mol. Biol. 17:1461-1469.
5. Bailey JA, Eichler EE. 2006. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat. Rev. Genet. 7:552-564.
6. Bessho T. 2003. Induction of DNA replication-mediated double strand breaks by psoralen DNA interstrand cross-links. J. Biol. Chem. 278:5250-5254.
7. Bowater R, Doherty AJ. 2006. Making ends meet: repairing breaks in bacterial DNA by non-homologous end-joining. PLoS Genet. 2:e8. doi: 10.1371/journal.pgen.0020008.
8. Carr AM, Paek AL, Weinert T. 2011. DNA replication: failures and inverted fusions. Semin. Cell Dev. Biol. 22:866-874.
9. Chen MJ, et al. 2007. Cisplatin depletes TREX2 and causes Robertsonian translocations as seen in TREX2 knockout cells. Cancer Res. 67:9077-9083.
10. Chen YT, Bradley A. 2000. A new positive/negative selectable marker, puDeltatk, for use in embryonic stem cells. Genesis 28:31-35.
11. Cheung J, et al. 2003. Recent segmental and gene duplications in the mouse genome. Genome Biol. 4:R47. doi:10.1186/gb-2003-4-8-r47.
12. 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.
13. Colnaghi R, Carpenter G, Volker M, O'Driscoll M. 2011. The consequences of structural genomic alterations in humans: genomic disorders, genomic instability and cancer. Semin. Cell Dev. Biol. 22:875-885.
14. Dong Z, Fasullo M. 2003. Multiple recombination pathways for sister chromatid exchange in Saccharomyces cerevisiae: role of RAD1 and the RAD52 epistasis group genes. Nucleic Acids Res. 31:2576-2585.
15. Dronkert ML, et al. 2000. Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol. Cell. Biol. 20:3147-3156.
16. Dumitrache LC, et al. 2011. Trex2 enables spontaneous sister chromatid exchanges without facilitating DNA double-strand break repair. Genetics 188:787-797.
17. Essers J, et al. 2002. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J. 21:2030-2037.
18. Festing MF, Simpson EM, Davisson MT, Mobraaten LE. 1999. Revised nomenclature for strain 129 mice. Mamm. Genome 10:836.
19. Forget AL, Loftus MS, McGrew DA, Bennett BT, Knight KL. 2007. The human Rad51 K133A mutant is functional for DNA double-strand break repair in human cells. Biochemistry 46:3566-3575.
20. Friedrich G, Soriano P. 1991. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5:1513-1523.
21. Guenatri M, Bailly D, Maison C, Almouzni G. 2004. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 166:493-505.
22. Hastings PJ, Ira G, Lupski JR. 2009. A microhomology-mediated breakinduced replication model for the origin of human copy number variation. PLoS Genet. 5:e1000327. doi:10.1371/journal.pgen.1000327.
23. Hastings PJ, Lupski JR, Rosenberg SM, Ira G. 2009. Mechanisms of change in gene copy number. Nat. Rev. Genet. 10:551-564.
24. Holcomb VB, et al. 2007. HPRT minigene generates chimeric transcripts as a by-product of gene targeting. Genesis 45:275-281.
25. Horvath JE, et al. 2003. Using a pericentromeric interspersed repeat to recapitulate the phylogeny and expansion of human centromeric segmental duplications. Mol. Biol. Evol. 20:1463-1479.
26. Hu Y, et al. 2007. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 21:3073-3084.
27. Kim TM, Choi YJ, Ko JH, Hasty P. 2008. High-throughput knock-in coupling gene targeting with the HPRT minigene and Cre-mediated recombination. Genesis 46:732-737.
28. Kim TM, Ko JH, Choi YJ, Hu L, Hasty P. 2011. The phenotype of FancB-mutant mouse embryonic stem cells. Mutat. Res. 712:20-27.
29. Klein HL. 2008. The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair (Amst.) 7:686-693.
30. Kozak M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229-241.
31. Laulier C, Cheng A, Stark JM. 2011. The relative efficiency of homologydirected repair has distinct effects on proper anaphase chromosome separation. Nucleic Acids Res. 39:5935-5944.
32. Lee JA, Carvalho CM, Lupski JR. 2007. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131:1235-1247.
33. Lee SA, Roques C, Magwood AC, Masson JY, Baker MD. 2009. Recovery of deficient homologous recombination in Brca2-depleted mouse cells by wild-type Rad51 expression. DNA Repair (Amst.) 8:170-181.
34. Lim DS, Hasty P. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:7133-7143.
35. Liu P, Carvalho CM, Hastings P, Lupski JR. 2012. Mechanisms for recurrent and complex human genomic rearrangements. Curr. Opin. Genet. Dev. 22:211-229.
36. Liu P, et al. 2011. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 146:889-903.
37. Luo G, et al. 2000. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 26:424-429.
38. Marple T, Kim TM, Hasty P. 2006. Embryonic stem cells deficient for Brca2 or Blm exhibit divergent genotoxic profiles that support opposing activities during homologous recombination. Mutat. Res. 602:110-120.
39. Marple T, Li H, Hasty P. 2004. A genotoxic screen: rapid analysis of cellular dose-response to a wide range of agents that either damage DNA or alter genome maintenance pathways. Mutat. Res. 554:253-266.
40. Mazur DJ, Perrino FW. 2001. Excision of 3' termini by the Trex1 and TREX2 3'→5' exonucleases. Characterization of the recombinant proteins. J. Biol. Chem. 276:17022-17029.
41. Michor F, Iwasa Y, Vogelstein B, Lengauer C, Nowak MA. 2005. Can chromosomal instability initiate tumorigenesis? Semin. Cancer Biol. 15: 43-49.
42. Morita T, et al. 1993. A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae RAD51 genes. Proc. Natl. Acad. Sci. U. S. A. 90:6577-6580.
43. Morrison C, et al. 1999. The essential functions of human Rad51 are independent of ATP hydrolysis. Mol. Cell. Biol. 19:6891-6897.
44. Motegi A, et al. 2008. Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Natl. Acad. Sci. U. S. A. 105:12411-12416.
45. Park WH, et al. 2005. Direct DNA binding activity of the Fanconi anemia D2 protein. J. Biol. Chem. 280:23593-23598.
46. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D. 2006. Genetic evidence for complex speciation of humans and chimpanzees. Nature 441: 1103-1108.
47. Paulsen RD, Cimprich KA. 2007. The ATR pathway: fine-tuning the fork. DNA Repair (Amst.) 6:953-966.
48. Pellegrini L, et al. 2002. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420:287-293.
49. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. 2010. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 37:492-502.
50. Ramirez-Solis R, et al. 1992. Genomic DNA microextraction: a method to screen numerous samples. Anal. Biochem. 201:331-335.
51. Reid LH, Gregg RG, Smithies O, Koller BH. 1990. Regulatory elements in the introns of the human HPRT gene are necessary for its expression in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 87:4299-4303.
52. Rivory LP. 1996. Irinotecan (CPT-11): a brief overview. Clin. Exp. Pharmacol. Physiol. 23:1000-1004.
53. Robertson RB, et al. 2009. Structural transitions within human Rad51 nucleoprotein filaments. Proc. Natl. Acad. Sci. U. S. A. 106:12688-12693.
54. Ruksc A, Birmingham EC, Baker MD. 2007. Altered DNA repair and recombination responses in mouse cells expressing wildtype or mutant forms of RAD51. DNA Repair (Amst.) 6:1876-1889.
55. San Filippo J, Sung P, Klein H. 2008. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77:229-257.
56. Schröck E, et al. 1996. Multicolor spectral karyotyping of human chromosomes. Science 273:494-497.
57. Schwab RA, Niedzwiedz W. 2011. Visualization of DNA replication in the vertebrate model system DT40 using the DNA fiber technique. J. Vis. Exp. 56:e3255. doi:10.3791/3255.
58. She X, et al. 2004. The structure and evolution of centromeric transition regions within the human genome. Nature 430:857-864.
59. Shinohara A, et al. 1993. Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat. Genet. 4:239-243.
60. Sigurdsson S, Van Komen S, Petukhova G, Sung P. 2002. Homologous DNA pairing by human recombination factors Rad51 and Rad54. J. Biol. Chem. 277:42790-42794.
61. Sirbu BM, et al. 2011. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25:1320-1327.
62. Sonoda E, et al. 1998. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:598-608.
63. Sonoda E, et al. 1999. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19:5166-5169.
64. Stark JM, et al. 2002. ATP hydrolysis by mammalian RAD51 has a key role during homology-directed DNA repair. J. Biol. Chem. 277:20185-20194.
65. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. 2004. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol. Cell. Biol. 24:9305-9316.
66. Stephens PJ, et al. 2011. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144:27-40.
67. Takata M, et al. 2000. The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol. Cell. Biol. 20:6476-6482.
68. Takata M, et al. 2001. Chromosome instability and defective recombina-tional repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 21:2858-2866.
69. Taniguchi T, et al. 2002. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100:2414-2420.
70. Tsuzuki T, et al. 1996. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. U. S. A. 93:6236-6240.
71. Wang W. 2007. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8:735-748.
72. Wilson DM, III, Thompson LH. 2007. Molecular mechanisms of sisterchromatid exchange. Mutat. Res. 616:11-23.
73. Yu DS, et al. 2003. Dynamic control of Rad51 recombinase by selfassociation and interaction with BRCA2. Mol. Cell 12:1029-1041.
74. Zhang F, Carvalho CM, Lupski JR. 2009. Complex human chromosomal and genomic rearrangements. Trends Genet. 25:298-307.
75. Zhang F, et al. 2009. The DNA replication FoSTeS/MMBIR mechanism can generate genomic, genic and exonic complex rearrangements in humans. Nat. Genet. 41:849-853.