Impaired induction of DNA lesions during immunoglobulin class-switch recombination in humans influences end-joining repair

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 51, 2010, Pages 22225-22230

  Kracker, Sven ^a,b   Imai, Kohsuke ^c   Gardès, Pauline ^a,b   Ochs, Hans D ^d   Fischer, Alain ^a,b   Durandy, Anne H ^a,b  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; B LYMPHOCYTE; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; GENE MUTATION; GENE REARRANGEMENT; HETEROZYGOTE; HUMAN; HUMAN CELL; MICROHOMOLOGY MEDIATED END-JOINING; PRIORITY JOURNAL;

ANTIGENS, NUCLEAR; CYTIDINE DEAMINASE; DNA; DNA BREAKS; DNA GLYCOSYLASES; DNA REPAIR; DNA-BINDING PROTEINS; FEMALE; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; MALE; RECOMBINATION, GENETIC;

EID: 78650674433     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012591108     Document Type: Article

References (43)

1. Revy P, et al. (2000) Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell 102:565-575.
2. Petersen-Mahrt SK, Harris RS, Neuberger MS (2002) AID mutates E. coli, suggesting a DNA deamination mechanism for antibody diversification. Nature 418:99-103.
3. Muramatsu M, et al. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA-editing enzyme. Cell 102:553-563.
4. Imai K, et al. (2003) Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination. Nat Immunol 4:1023-1028.
5. Rada C, Di Noia JM, Neuberger MS (2004) Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol Cell 16:163-171.
6. Petersen S, et al. (2001) AID is required to initiate Nbs1/γ-H2AX focus formation and mutations at sites of class switching. Nature 414:660-665.
7. Guikema JE, et al. (2007) APE1- and APE2-dependent DNA breaks in immunoglobulin class switch recombination. J Exp Med 204:3017-3026.
8. Manis JP, et al. (2004) 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat Immunol 5:481-487.
9. Reina-San-Martin B, Chen HT, Nussenzweig A, Nussenzweig MC (2004) ATM is required for efficient recombination between immunoglobulin switch regions. J Exp Med 200:1103-1110.
10. Celeste A, et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296:922-927.
11. Kracker S, et al. (2005) Nibrin functions in Ig class-switch recombination. Proc Natl Acad Sci USA 102:1584-1589.
12. Reina-San-Martin B, Nussenzweig MC, Nussenzweig A, Difilippantonio S (2005) Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1. Proc Natl Acad Sci USA 102:1590-1595.
13. Franco S, et al. (2006) H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol Cell 21:201-214.
14. Dinkelmann M, et al. (2009) Multiple functions of MRN in end-joining pathways during isotype class switching. Nat Struct Mol Biol 16:808-813.
15. Yan CT, et al. (2007) IgH class switching and translocations use a robust nonclassical end-joining pathway. Nature 449:478-482.
16. Boboila C, et al. (2010) Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. J Exp Med 207:417-427.
17. Pan-Hammarström Q, et al. (2005) Impact of DNA ligase IV on nonhomologous end joining pathways during class switch recombination in human cells. J Exp Med 201:189-194.
18. Soulas-Sprauel P, et al. (2007) Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J Exp Med 204:1717-1727.
19. Corneo B, et al. (2007) Rag mutations reveal robust alternative end joining. Nature 449:483-486.
20. Imai K, et al. (2005) Analysis of class switch recombination and somatic hypermutation in patients affected with autosomal dominant hyper-IgM syndrome type 2. Clin Immunol 115:277-285.
21. Takizawa M, et al. (2008) AID expression levels determine the extent of cMyc oncogenic translocations and the incidence of B cell tumor development. J Exp Med 205:1949-1957.
22. Sernández IV, de Yébenes VG, Dorsett Y, Ramiro AR (2008) Haploinsufficiency of activation-induced deaminase for antibody diversification and chromosome translocations both in vitro and in vivo. PLoS ONE 3:e3927.
23. Robbiani DF, et al. (2009) AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations. Mol Cell 36:631-641.
24. Pan Q, et al. (2002) Alternative end joining during switch recombination in patients with ataxia-telangiectasia. Eur J Immunol 32:1300-1308.
25. He B, et al. (2007) Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial cell secretion of the cytokine APRIL. Immunity 26:812-826.
26. Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T (2001) In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413:639-643.
27. Du L, et al. (2008) Involvement of Artemis in nonhomologous end-joining during immunoglobulin class switch recombination. J Exp Med 205:3031-3040.
28. Schrader CE, et al. (2003) Mutations occur in the Ig Smu region but rarely in Sgamma regions prior to class switch recombination. EMBO J 22:5893-5903.
29. Nagaoka H, Muramatsu M, Yamamura N, Kinoshita K, Honjo T (2002) Activationinduced deaminase (AID)-directed hypermutation in the immunoglobulin Smu region: Implication of AID involvement in a common step of class switch recombination and somatic hypermutation. J Exp Med 195:529-534.
30. Faili A, et al. (2004) DNA polymerase eta is involved in hypermutation occurring during immunoglobulin class switch recombination. J Exp Med 199:265-270.
31. Péron S, et al. (2008) Human PMS2 deficiency is associated with impaired immunoglobulin class switch recombination. J Exp Med 205:2465-2472.
32. Barreto V, Reina-San-Martin B, Ramiro AR, McBride KM, Nussenzweig MC (2003) C-terminal deletion of AID uncouples class switch recombination from somatic hypermutation and gene conversion. Mol Cell 12:501-508.
33. Geisberger R, Rada C, Neuberger MS (2009) The stability of AID and its function in class-switching are critically sensitive to the identity of its nuclear-export sequence. Proc Natl Acad Sci USA 106:6736-6741.
34. Gu J, et al. (2007) XRCC4:DNA ligase IV can ligate incompatible DNA ends and can ligate across gaps. EMBO J 26:1010-1023.
35. Schenten D, et al. (2009) Pol zeta ablation in B cells impairs the germinal center reaction, class switch recombination, DNA break repair, and genome stability. J Exp Med 206:477-490.
36. Lieber MR, Wilson TE (2010) SnapShot: Nonhomologous DNA end-joining (NHEJ). Cell 142:496.
37. Bothmer A, et al. (2010) 53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination. J Exp Med 207:855-865.
38. Roberts SA, et al. (2010) Ku is a 5′-dRP/AP lyase that excises nucleotide damage near broken ends. Nature 464:1214-1217.
39. Ta VT, et al. (2003) AID mutant analyses indicate requirement for class-switch specific cofactors. Nat Immunol 4:843-848.
40. Begum NA, et al. (2009) Further evidence for involvement of a noncanonical function of uracil DNA glycosylase in class switch recombination. Proc Natl Acad Sci USA 106:2752-2757.
41. Schrader CE, Vardo J, Stavnezer J (2002) Role for mismatch repair proteins Msh2, Mlh1, and Pms2 in immunoglobulin class switching shown by sequence analysis of recombination junctions. J Exp Med 195:367-373.
42. van Oers JM, et al. (2010) PMS2 endonuclease activity has distinct biological functions and is essential for genome maintenance. Proc Natl Acad Sci USA 107:13384-13389.
43. Lieber MR (2010) NHEJ and its backup pathways in chromosomal translocations. Nat Struct Mol Biol 17:393-395.