Two replication fork maintenance pathways fuse inverted repeats to rearrange chromosomes

Nature

Volumn 501, Issue 7468, 2013, Pages 569-572

  Hu, Lingchuan ^a   Kim, Tae Moon ^a   Son, Mi Young ^a   Kim, Sung A ^a   Holland, Cory L ^a   Tateishi, Satoshi ^b   Kim, Dong Hyun ^a   Yew, P Renee ^a   Montagna, Cristina ^c   Dumitrache, Lavinia C ^a,d   Hasty, Paul ^a  

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

^b KUMAMOTO UNIVERSITY   (Japan)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; BRCA2 PROTEIN; CYCLINE; EXONUCLEASE; PROTEIN TREX2; RAD18 PROTEIN; RAD51 PROTEIN; RECQ HELICASE; UBIQUITIN CONJUGATING ENZYME 13; UNCLASSIFIED DRUG;

ANTIGEN; CANCER; CHROMOSOME; DNA; LIGHT EFFECT; MAINTENANCE; RECOMBINATION;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA REPLICATION; DNA STRAND BREAKAGE; EMBRYONIC STEM CELL; ENZYME ACTIVITY; EXON; GAMMA IRRADIATION; HOMOLOGOUS RECOMBINATION; INVERTED REPEAT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SISTER CHROMATID; SISTER CHROMATID EXCHANGE; UBIQUITINATION;

ANIMALS; BASE SEQUENCE; CHROMOSOMAL INSTABILITY; CHROMOSOME BREAKAGE; CHROMOSOMES, MAMMALIAN; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; EXODEOXYRIBONUCLEASES; HOMOLOGOUS RECOMBINATION; HYDROXYUREA; INVERTED REPEAT SEQUENCES; MICE; NUCLEOTIDES; PROLIFERATING CELL NUCLEAR ANTIGEN; RAD51 RECOMBINASE; RECQ HELICASES; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITINATION; ULTRAVIOLET RAYS;

EID: 84885626899     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12500     Document Type: Article

References (47)

1. Hastings, P. J., Lupski, J. R., Rosenberg, S. M. & Ira, G. Mechanisms of change in gene copy number. Nature Rev. Genet. 10, 551-564 (2009).
2. Carr, A. M., Paek, A. L. & Weinert, T. DNA replication: failures and inverted fusions. Semin. Cell Dev. Biol. 22, 866-874 (2011).
3. Lee, J. A., Carvalho, C. M. & Lupski, J. R. A. DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131, 1235-1247 (2007).
4. San Filippo, J., Sung, P. & Klein, H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257 (2008).
5. Wu, L. & Hickson, I. D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874 (2003).
6. Schlacher, K. et al. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145, 529-542 (2011).
7. Schlacher, K., Wu, H. & Jasin, M. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22, 106-116 (2012).
8. Mizuno, K., Lambert, S., Baldacci, G., Murray, J. M. & Carr, A. M. Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism. Genes Dev. 23, 2876-2886 (2009).
9. Mizuno, K., Miyabe, I., Schalbetter, S. A., Carr, A. M. & Murray, J. M. Recombinationrestarted replication makes inverted chromosome fusions at inverted repeats. Nature 493, 246-249 (2013).
10. Petermann, E., Orta, M. L., Issaeva, N., Schultz, N. & Helleday, T. Hydroxyureastalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 37, 492-502 (2010).
11. Carr, A. M. & Lambert, S. Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J. Mol. Biol. http://dx.doi.org/10.1016/j.jmb.2013.04.023 (30 April 2013).
12. Ulrich, H. D. Regulating post-translational modifications of the eukaryotic replication clamp PCNA. DNA Repair (Amst.) 8, 461-469 (2009).
13. Falbo, K. B. et al. Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nature Struct. Mol. Biol. 16, 1167-1172 (2009).
14. Huang, J. et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nature Cell Biol. 11, 592-603 (2009).
15. Kim, T. M. et al. RAD51 mutants cause replication defects and chromosomal instability. Mol. Cell. Biol. 32, 3663-3680 (2012).
16. Shimizu, N., Shingaki, K., Kaneko-Sasaguri, Y., Hashizume, T. & Kanda, T. When, where andhowthe bridge breaks: anaphase bridge breakage plays a crucial role in gene amplification and HSR generation. Exp. Cell Res. 302, 233-243 (2005).
17. Cavalli, G. & Misteli, T. Functional implications of genome topology. Nature Struct. Mol. Biol. 20, 290-299 (2013).
18. Harada, S., Sekiguchi, N. & Shimizu, N. Amplification of a plasmid bearing a mammalian replication initiation region in chromosomal and extrachromosomal contexts. Nucleic Acids Res. 39, 958-969 (2011).
19. Horvath, J. E. et al. Using a pericentromeric interspersed repeat to recapitulate the phylogeny and expansion of human centromeric segmental duplications. Mol. Biol. Evol. 20, 1463-1479 (2003).
20. Luo, G. et al. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nature Genet. 26, 424-429 (2000).
21. Motegi, A. et al. Polyubiquitination of proliferating cell nuclear antigen byHLTF and SHPRHprevents genomic instability fromstalled replication forks. Proc. Natl Acad. Sci. USA 105, 12411-12416 (2008).
22. Tateishi, S. et al. Enhanced genomic instability and defective postreplication repair in RAD18 knockout mouse embryonic stem cells. Mol. Cell. Biol. 23, 474-481 (2003).
23. Chen, M. J., Ma, S. M., Dumitrache, L. C. & Hasty, P. Biochemical and cellular characteristics of the 39R59 exonuclease TREX2. Nucleic Acids Res. 35, 2682-2694 (2007).
24. Dumitrache, L. C., Hu, L. & Hasty, P. TREX2 exonuclease defective cells exhibit double-strand breaks and chromosomal fragments but not Robertsonian translocations. Mutat. Res. 662, 84-87 (2009).
25. Chen, M. J. et al. Cisplatin depletes TREX2 and causes Robertsonian translocations as seen in TREX2 knockout cells. Cancer Res. 67, 9077-9083 (2007).
26. Dumitrache, L. C. et al. Trex2 enables spontaneous sister chromatid exchanges without facilitating DNA double-strand break repair. Genetics 188, 787-797 (2011).
27. Goldfless, S. J., Morag, A. S., Belisle, K. A., Sutera, V. A. Jr & Lovett, S. T. DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. Mol. Cell 21, 595-604 (2006).
28. Dutra, B. E. & Lovett, S. T. Cis and trans-acting effects on a mutational hotspot involving a replication template switch. J. Mol. Biol. 356, 300-311 (2006).
29. Sirbu, B. M. et al. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 25, 1320-1327 (2011).
30. Blastyák, A., Hajdú , I., Unk, I. & Haracska, L. Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Mol. Cell. Biol. 30, 684-693 (2010).
31. Reid, L. H., Gregg, R. G., Smithies, O. & Koller, B. H. Regulatory elements in the introns of the human HPRT gene are necessary for its expression in embryonic stem cells. Proc. Natl Acad. Sci. USA 87, 4299-4303 (1990).
32. Adra, C. N., Boer, P. H. & McBurney, M. W. Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene 60, 65-74 (1987).
33. Guenatri, M., Bailly, D., Maison, C. & Almouzni, G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 166, 493-505 (2004).
34. Montagna, C., Andrechek, E. R., Padilla-Nash, H., Muller, W. J.&Ried, T.Centrosome abnormalities, recurring deletions of chromosome 4, and genomic amplification of HER2/neu define mouse mammary gland adenocarcinomas induced by mutant HER2/neu. Oncogene 21, 890-898 (2002).
35. Davisson, M. T. Rules and guidelines for nomenclature ofmouse genes. Gene 147, 157-160 (1994).
36. Holcomb, V. B. et al. HPRT minigene generates chimeric transcripts as a byproduct of gene targeting. Genesis 45, 275-281 (2007).
37. Ram?́rez-Solis, R. et al. Genomic DNA microextraction: a method to screen numerous samples. Anal. Biochem. 201, 331-335 (1992).
38. Soriano, P.,Montgomery, C., Geske, R.&Bradley,A. Targeted disruptionof the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64, 693-702 (1991).
39. Kim, D. H. et al. The CRL4Cdt2 ubiquitin ligase mediates the proteolysis of cyclindependent kinase inhibitor Xic1 through a direct association with PCNA. Mol. Cell. Biol. 30, 4120-4133 (2010).
40. Krijger, P. H. et al. HLTF and SHPRH are not essential for PCNA polyubiquitination, survival and somatic hypermutation: existence of an alternative E3 ligase. DNA Repair (Amst.) 10, 438-444 (2011).
41. Friedrich, G.&Soriano, P. Promoter traps inembryonic stemcells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5, 1513-1523 (1991).
42. Araki, K., Araki, M. & Yamamura, K. Targeted integration of DNA using mutant lox sites in embryonic stem cells. Nucleic Acids Res. 25, 868-872 (1997).
43. Kim, T. M., Choi, Y. J., Ko, J. H. & Hasty, P. High-throughput knock-in coupling gene targeting with the HPRT minigene and Cre-mediated recombination. Genesis 46, 732-737 (2008).
44. Donoho, G. et al. Deletion of Brca2 exon 27 causes hypersensitivity to DNA crosslinks, chromosomal instability, and reduced life span in mice. Genes Chromosom. Cancer 36, 317-331 (2003).
45. Morimatsu, M., Donoho, G. & Hasty, P. Cells deleted for Brca2 COOH terminus exhibit hypersensitivity to gamma-radiation and premature senescence. Cancer Res. 58, 3441-3447 (1998).
46. Moynahan, M. E., Pierce, A. J. & Jasin, M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 7, 263-272 (2001).
47. Terai, K., Abbas, T., Jazaeri, A. A. & Dutta, A. CRL4Cdt2 E3 ubiquitin ligase monoubiquitinates PCNA to promote translesion DNA synthesis. Mol. Cell 37, 143-149 (2010).