An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway

Nature Structural and Molecular Biology

Volumn 18, Issue 1, 2011, Pages 80-85

  Zhang, Yu ^a   Jasin, Maria ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; KU ANTIGEN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTIP; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMOSOME BREAKAGE; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; GENE DELETION; MOUSE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; ANTIGENS, NUCLEAR; CARRIER PROTEINS; CELL CYCLE PROTEINS; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; GENE KNOCKDOWN TECHNIQUES; MICE; MODELS, GENETIC; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSLOCATION, GENETIC;

EID: 78650995499     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1940     Document Type: Article

References (37)

1. Lieber, M.R., Yu, K. & Raghavan, S.C. Roles of nonhomologous DNA end joining, V(D)J recombination, and class switch recombination in chromosomal translocations. DNA Repair (Amst.) 5, 1234-1245 (2006).
2. Zhang, Y. & Rowley, J.D. Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair (Amst.) 5, 1282-1297 (2006).
3. Brandt, V.L. & Roth, D.B. Recent insights into the formation of RAG-induced chromosomal translocations. Adv. Exp. Med. Biol. 650, 32-45 (2009).
4. Wang, J.H. et al. Mechanisms promoting translocations in editing and switching peripheral B cells. Nature 460, 231-236 (2009).
5. Robbiani, D.F. et al. AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol. Cell 36, 631-641 (2009).
6. Yan, C.T. et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449, 478-482 (2007).
7. Boboila, C. et al. Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proc. Natl. Acad. Sci. USA 107, 3034-3039 (2010).
8. Nussenzweig, A. & Nussenzweig, M.C. Origin of chromosomal translocations in lymphoid cancer. Cell 141, 27-38 (2010).
9. Weinstock, D.M., Elliott, B. & Jasin, M. A model of oncogenic rearrangements: differences between chromosomal translocation mechanisms and simple double-strand break repair. Blood 107, 777-780 (2006).
10. Stephens, P.J. et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 462, 1005-1010 (2009).
11. Richardson, C., Moynahan, M.E. & Jasin, M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12, 3831-3842 (1998).
12. Elliott, B., Richardson, C. & Jasin, M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol. Cell 17, 885-894 (2005).
13. Lieber, M.R. The mechanism of human nonhomologous DNA end joining. J. Biol. Chem. 283, 1-5 (2008).
14. Weinstock, D.M., Brunet, E. & Jasin, M. Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol. 9, 978-981 (2007).
15. Simsek, D. & Jasin, M. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat. Struct. Mol. Biol. 17, 410-416 (2010).
16. Diflippantonio, M.J. et al. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 404, 510-514 (2000).
17. Boulton, S.J. & Jackson, S.P. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15, 5093-5103 (1996).
18. Liang, F. & Jasin, M. Ku80-defcient cells exhibit excess degradation of extrachromosomal DNA. J. Biol. Chem. 271, 14405-14411 (1996).
19. McVey, M. & Lee, S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 24, 529-538 (2008).
20. Sartori, A.A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
21. Clerici, M., Mantiero, D., Lucchini, G. & Longhese, M.P. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280, 38631-38638 (2005).
22. Lee, K. & Lee, S.E. Saccharomyces cerevisiae Sae2-and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 176, 2003-2014 (2007).
23. Bennardo, N., Cheng, A., Huang, N. & Stark, J.M. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 4, e1000110 (2008).
24. Lee-Theilen, M., Matthews, A.J., Kelly, D., Zheng, S. & Chaudhuri, J. CtIP promotes microhomology-mediated alternative end-joining during class-switch recombination. Nat. Struct. Mol. Biol. advance online publication, doi:10.1038/nsmb.1942 (5 December 2010).
25. Rass, E. et al. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 16, 819-824 (2009).
26. Xie, A., Kwok, A. & Scully, R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 16, 814-818 (2009).
27. Mimitou, E.P. & Symington, L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774 (2008).
28. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E. & Ira, G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994 (2008).
29. Yun, M.H. & Hiom, K. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 459, 460-463 (2009).
30. Lee, S.E. et al. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94, 399-409 (1998).
31. Zhang, Y. et al. Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat. Struct. Mol. Biol. 14, 639-646 (2007).
32. Pierce, A.J., Hu, P., Han, M., Ellis, N. & Jasin, M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242 (2001).
33. Weinstock, D.M. & Jasin, M. Alternative pathways for the repair of RAG-induced DNA breaks. Mol. Cell. Biol. 26, 131-139 (2006).
34. Roth, D.B. & Wilson, J.H. Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol. Cell. Biol. 6, 4295-4304 (1986).
35. Blackwell, T.K. et al. Isolation of scid pre-B cells that rearrange kappa light chain genes: formation of normal signal and abnormal coding joins. EMBO J. 8, 735-742 (1989).
36. Brummelkamp, T.R., Bernards, R. & Agami, R. A system for stable expression of short interfering RNAs in mammalian cells. Science 296, 550-553 (2002).
37. Yu, X. & Baer, R. Nuclear localization and cell cycle-specifc expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J. Biol. Chem. 275, 18541-18549 (2000).