Multiple functions of MRN in end-joining pathways during isotype class switching

Nature Structural and Molecular Biology

Volumn 16, Issue 8, 2009, Pages 808-813

  Dinkelmann, Maria ^a   Spehalski, Elizabeth ^a   Stoneham, Trina ^a   Buis, Jeffrey ^a   Wu, Yipin ^a   Sekiguchi, Joann M ^b   Ferguson, David O ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CLASS SWITCH RECOMBINATION; CONTROLLED STUDY; DNA RECOMBINATION; ENZYME ACTIVITY; GENE REARRANGEMENT; MOUSE; NONHOMOLOGOUS END JOINING PATHWAY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; B-LYMPHOCYTES; BASE SEQUENCE; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; FEMALE; FLOW CYTOMETRY; HISTONES; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 68249135624     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1639     Document Type: Article

References (53)

1. McKinnon, P.J. & Caldecott, K.W. DNA strand break repair and human genetic disease. Annu. Rev. Genomics Hum. Genet. 8, 37-55 (2007).
2. Wyman, C. & Kanaar, R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40, 363-383 (2006).
3. Audebert, M., Salles, B. & Calsou, P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 279, 55117-55126 (2004).
4. Corneo, B. et al. Rag mutations reveal robust alternative end joining. Nature 449, 483-486 (2007).
5. Soulas-Sprauel, P. et al. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 204, 1717-1727 (2007).
6. Wang, H. et al. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 65, 4020-4030 (2005).
7. Yan, C.T. et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449, 478-482 (2007).
8. Han, L. & Yu, K. Altered kinetics of nonhomologous end joining and class switch recombination in ligase IV-deficient B cells. J. Exp. Med. 205, 2745-2753 (2008).
9. Buis, J. et al. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 135, 85-96 (2008).
10. Luo, G. et al. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 96, 7376-7381 (1999).
11. Zhu, J., Petersen, S., Tessarollo, L. & Nussenzweig, A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11, 105-109 (2001).
12. Berkovich, E., Monnat, R.J. Jr. & Kastan, M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9, 683-690 (2007).
13. Lisby, M., Barlow, J.H., Burgess, R.C. & Rothstein, R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713 (2004).
14. Shroff, R. et al. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14, 1703-1711 (2004).
15. Williams, R.S., Williams, J.S. & Tainer, J.A. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell Biol. 85, 509-520 (2007).
16. Lavin, M.F. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene 26, 7749-7758 (2007).
17. Lee, J.H. & Paull, T.T. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26, 7741-7748 (2007).
18. Shiloh, Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3, 155-168 (2003).
19. Honjo, T., Muramatsu, M. & Fagarasan, S. AID: how does it aid antibody diversity? Immunity 20, 659-668 (2004).
20. Stavnezer, J., Guikema, J.E. & Schrader, C.E. Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26, 261-292 (2008).
21. Rickert, R.C., Roes, J. & Rajewsky, K. B lymphocyte-specific, Cre-mediated mutagenesis in mice. Nucleic Acids Res. 25, 1317-1318 (1997).
22. Lumsden, J.M. et al. Immunoglobulin class switch recombination is impaired in Atm-deficient mice. J. Exp. Med. 200, 1111-1121 (2004).
23. Reina-San-Martin, B., Chen, H.T., Nussenzweig, A. & Nussenzweig, M.C. ATM is required for efficient recombination between immunoglobulin switch regions. J. Exp. Med. 200, 1103-1110 (2004).
24. Kracker, S. et al. Nibrin functions in Ig class-switch recombination. Proc. Natl. Acad. Sci. USA 102, 1584-1589 (2005).
25. Reina-San-Martin, B., Nussenzweig, M.C., Nussenzweig, A. & Difilippantonio, S. Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1. Proc. Natl. Acad. Sci. USA 102, 1590-1595 (2005).
26. Kraus, M., Alimzhanov, M.B., Rajewsky, N. & Rajewsky, K. Survival of resting mature B lymphocytes depends on BCR signaling via the Iga/b heterodimer. Cell 117, 787-800 (2004).
27. Franco, S. et al. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol. Cell 21, 201-214 (2006).
28. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. & Bonner, W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
29. Stucki, M. et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226 (2005).
30. Lou, Z. et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21, 187-200 (2006).
31. Manis, J.P. et al. 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat. Immunol. 5, 481-487 (2004).
32. Reina-San-Martin, B. et al. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J. Exp. Med. 197, 1767-1778 (2003).
33. Ward, I.M. et al. 53BP1 is required for class switch recombination. J. Cell Biol. 165, 459-464 (2004).
34. Williams, R.S. et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135, 97-109 (2008).
35. Cahill, D. & Carney, J.P. Dimerization of the Rad50 protein is independent of the conserved hook domain. Mutagenesis 22, 269-274 (2007).
36. Hopfner, K.P. et al. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418, 562-566 (2002).
37. Wiltzius, J.J., Hohl, M., Fleming, J.C. & Petrini, J.H. The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat. Struct. Mol. Biol. 12, 403-407 (2005).
38. Moreno-Herrero, F. et al. Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 437, 440-443 (2005).
39. Bressan, D.A., Baxter, B.K. & Petrini, J.H. The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 7681-7687 (1999).
40. Tauchi, H. et al. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 420, 93-98 (2002).
41. 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).
42. Sartori, A.A. et al. Human CtIP promotes DNA end resection. Nature 450, 509-514 (2007).
43. Paull, T.T. & Gellert, M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1, 969-979 (1998).
44. Paull, T.T. & Gellert, M. A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proc. Natl. Acad. Sci. USA 97, 6409-6414 (2000).
45. 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).
46. Helmink, B.A. et al. MRN complex function in the repair of chromosomal Rag-mediated DNA double-strand breaks. J. Exp. Med. 206, 669-679 (2009).
47. Deng, Y., Guo, X., Ferguson, D.O. & Chang, S. Multiple roles for Mre11 at uncapped telomeres. Nature advance online publication, doi:10.1038/nature08196. (26 July 2009).
48. Xie, A., Kwok, A. & Scully, R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. advance online publication, doi:10.1038/nsmb.1640 (26 July 2009).
49. Rass, E. et al. Role of MRE11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol. advance online publication, doi: 10.1038/nsmb.1641 (26 July 2009).
50. Difilippantonio, S. et al. 53BP1 facilitates long-range DNA end joining during V(D)J recombination. Nature 456, 529-533 (2008).
51. Dimitrova, N., Chen, Y.C., Spector, D.L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528 (2008).
52. Chaudhuri, J. et al. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422, 726-730 (2003).
53. Begum, N.A. et al. Requirement of non-canonical activity of uracil DNA glycosylase for class switch recombination. J. Biol. Chem. 282, 731-742 (2007).