CtIP promotes microhomology-mediated alternative end joining during class-switch recombination

Nature Structural and Molecular Biology

Volumn 18, Issue 1, 2011, Pages 75-80

  Lee Theilen, Mieun ^a   Matthews, Allysia J ^b   Kelly, Dierdre ^c   Zheng, Simin ^b   Chaudhuri, Jayanta ^a,b,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Gerstner Sloan Kettering Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; CYTIDINE DEAMINASE; DNA; KU ANTIGEN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE REARRANGEMENT; HOMOLOGOUS RECOMBINATION; IMMUNOGLOBULIN GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE; DNA; DNA BREAKS, DOUBLE-STRANDED; GENE KNOCKDOWN TECHNIQUES; IMMUNOGLOBULIN CLASS SWITCHING; MICE; MODELS, GENETIC; RECOMBINATION, GENETIC; RNA, SMALL INTERFERING; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 78650988959     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1942     Document Type: Article

References (39)

1. Stavnezer, J., Guikema, J.E. & Schrader, C.E. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26, 261-292 (2008).
2. Muramatsu, M. et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563 (2000).
3. Revy, P. et al. Activation-induced cytidine deaminase (AID) defciency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102, 565-575 (2000).
4. Delker, R.K., Fugmann, S.D. & Papavasiliou, F.N. A coming-of-age story: activation-induced cytidine deaminase turns 10. Nat. Immunol. 10, 1147-1153 (2009).
5. Zarrin, A.A. et al. Antibody class switching mediated by yeast endonuclease-generated DNA breaks. Science 315, 377-381 (2007).
6. Lieber, M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181-211 (2010).
7. Chaudhuri, J. & Alt, F.W. Class-switch recombination: interplay of transcription, DNA deamination and DNA repair. Nat. Rev. Immunol. 4, 541-552 (2004).
8. Soulas-Sprauel, P. et al. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 204, 1717-1727 (2007).
9. Yan, C.T. et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449, 478-482 (2007).
10. Han, L. & Yu, K. Altered kinetics of nonhomologous end joining and class switch recombination in ligase IV-defcient B cells. J. Exp. Med. 205, 2745-2753 (2008).
11. Boboila, C. et al. Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. J. Exp. Med. 207, 417-427 (2010).
12. 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).
13. 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).
14. 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).
15. Rass, E. et al. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. 16, 819-824 (2009).
16. Lee, G.S., Neiditch, M.B., Salus, S.S. & Roth, D.B. RAG proteins shepherd double-strand breaks to a specifc pathway, suppressing error-prone repair, but RAG nicking initiates homologous recombination. Cell 117, 171-184 (2004).
17. Corneo, B. et al. Rag mutations reveal robust alternative end joining. Nature 449, 483-486 (2007).
18. 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).
19. 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).
20. Zha, S., Boboila, C. & Alt, F.W. Mre11: roles in DNA repair beyond homologous recombination. Nat. Struct. Mol. Biol. 16, 798-800 (2009).
21. Dinkelmann, M. et al. Multiple functions of MRN in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol. 16, 808-813 (2009).
22. Deriano, L., Stracker, T.H., Baker, A., Petrini, J.H. & Roth, D.B. Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Mol. Cell 34, 13-25 (2009).
23. Chinnadurai, G. CtIP, a candidate tumor susceptibility gene is a team player with luminaries. Biochim. Biophys. Acta 1765, 67-73 (2006).
24. Yu, X., Wu, L.C., Bowcock, A.M., Aronheim, A. & Baer, R. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem. 273, 25388-25392 (1998).
25. Chen, L., Nievera, C.J., Lee, A.Y. & Wu, X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem. 283, 7713-7720 (2008).
26. Huertas, P., Cortes-Ledesma, F., Sartori, A.A., Aguilera, A. & Jackson, S.P. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455, 689-692 (2008).
27. 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).
28. Sartori, A.A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
29. Lengsfeld, B.M., Rattray, A.J., Bhaskara, V., Ghirlando, R. & Paull, T.T. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28, 638-651 (2007).
30. 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).
31. Mimitou, E.P. & Symington, L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774 (2008).
32. You, Z. et al. CtIP links DNA double-strand break sensing to resection. Mol. Cell 36, 954-969 (2009).
33. Tran, T.H. et al. B cell-specifc and stimulation-responsive enhancers derepress Aicda by overcoming the effects of silencers. Nat. Immunol. 11, 148-154 (2010).
34. Chen, P.L. et al. Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insuffciency. Mol. Cell. Biol. 25, 3535-3542 (2005).
35. Rush, J.S., Fugmann, S.D. & Schatz, D.G. Staggered AID-dependent DNA double strand breaks are the predominant DNA lesions targeted to Sm in immunoglobulin class switch recombination. Int. Immunol. 16, 549-557 (2004).
36. Lähdesmäki, A., Taylor, A.M., Chrzanowska, K.H. & Pan-Hammarstrom, Q. Delineation of the role of the Mre11 complex in class switch recombination. J. Biol. Chem. 279, 16479-16487 (2004).
37. Kracker, S. et al. Nibrin functions in Ig class-switch recombination. Proc. Natl. Acad. Sci. USA 102, 1584-1589 (2005).
38. Reina-San-Martin, B., Nussenzweig, M.C., Nussenzweig, A. & Diflippantonio, S. Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1. Proc. Natl. Acad. Sci. USA 102, 1590-1595 (2005).
39. Chaudhuri, J. et al. Transcription-targeted DNA deamination by the AID antibody diversifcation enzyme. Nature 422, 726-730 (2003).