Activation induced deaminase C-terminal domain links DNA breaks to end protection and repair during class switch recombination

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

Volumn 111, Issue 11, 2014, Pages

  Zahn, Astrid ^a   Eranki, Anil K ^a   Patenaude, Anne Marie ^a   Methot, Stephen P ^a   Fifield, Heather ^b   Cortizas, Elena M ^c   Foster, Paul ^a   Imai, Kohsuke ^d   Durandy, Anne ^e,f   Larijani, Mani ^b   Verdun, Ramiro E ^c,g   Di Noia, Javier M ^a,h  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f PARIS DESCARTES SORBONNE PARIS CITÉ UNIVERSITY   (France)

^g GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^h UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Antibody gene diversification; Isotype switching; Somatic hypermutation

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; ATM PROTEIN; HISTONE H2AX; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; TRANSFORMING GROWTH FACTOR BETA1;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; B LYMPHOCYTE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; EXON; HELA CELL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HYPER IGM SYNDROME; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; SOMATIC HYPERMUTATION; WESTERN BLOTTING;

ANTIBODY GENE DIVERSIFICATION; ISOTYPE SWITCHING; SOMATIC HYPERMUTATION;

ANALYSIS OF VARIANCE; ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CYTIDINE DEAMINASE; DNA BREAKS; DNA END-JOINING REPAIR; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RNA, SMALL INTERFERING; TRANSLOCATION, GENETIC; URACIL-DNA GLYCOSIDASE;

EID: 84896522784     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1320486111     Document Type: Article

References (52)

1. Rajewsky K (1996) Clonal selection and learning in the antibody system. Nature 381(6585): 751-758. (Pubitemid 26243107)
2. Peled JU, et al. (2008) The biochemistry of somatic hypermutation. Annu Rev Immunol 26:481-511. (Pubitemid 351600383)
3. Stavnezer J, Guikema JEJ, Schrader CE (2008) Mechanism and regulation of class switch recombination. Annu Rev Immunol 26:261-292. (Pubitemid 351600377)
4. Daniel JA, Nussenzweig A (2013) The AID-induced DNA damage response in chromatin. Mol Cell 50(3):309-321.
5. Petersen S, et al. (2001) AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 414(6864):660-665. (Pubitemid 33151264)
6. Boboila C, Alt FW, Schwer B (2012) Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA double-strand breaks. Adv Immunol 116:1-49.
7. Ramiro AR, et al. (2004) AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118(4):431-438. (Pubitemid 39485663)
8. Lee GS, Neiditch MB, Salus SS, Roth DB (2004) RAG proteins shepherd double-strand breaks to a specific pathway, suppressing error-prone repair, but RAG nicking initiates homologous recombination. Cell 117(2):171-184. (Pubitemid 38496238)
9. Corneo B, et al. (2007) Rag mutations reveal robust alternative end joining. Nature 449(7161):483-486. (Pubitemid 47509551)
10. Wuerffel R, et al. (2007) S-S synapsis during class switch recombination is promoted by distantly located transcriptional elements and activation-induced deaminase. Immunity 27(5):711-722. (Pubitemid 350110545)
11. Barreto V, Reina-San-Martin BR, 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(2):501-508. (Pubitemid 37238934)
12. Ta V-T, et al. (2003) AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat Immunol 4(9):843-848. (Pubitemid 37098654)
13. Ranjit S, et al. (2011) AID binds cooperatively with UNG and Msh2-Msh6 to Ig switch regions dependent upon the AID C terminus. J Immunol 187(5):2464-2475.
14. Doi T, et al. (2009) The C-terminal region of activation-induced cytidine deaminase is responsible for a recombination function other than DNA cleavage in class switch recombination. Proc Natl Acad Sci USA 106(8):2758-2763.
15. 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(3):277-285. (Pubitemid 40712323)
16. Zarrin AA, et al. (2007) Antibody class switching mediated by yeast endonucleasegenerated DNA breaks. Science 315(5810):377-381. (Pubitemid 46175518)
17. Revy P, et al. (2000) Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102(5):565-575.
18. Quartier P, et al. (2004) Clinical, immunologic and genetic analysis of 29 patients with autosomal recessive hyper-IgM syndrome due to Activation-Induced Cytidine Deaminase deficiency. Clin Immunol 110(1):22-29. (Pubitemid 38177417)
19. Durandy AH, Taubenheim N, Péron S, Fischer A (2007) Pathophysiology of B-cell intrinsic immunoglobulin class switch recombination deficiencies. Adv Immunol 94: 275-306. (Pubitemid 46856614)
20. Mu Y, Prochnow C, Pham P, Chen XS, Goodman MF (2012) A structural basis for the biochemical behavior of activation-induced deoxycytidine deaminase class-switch recombination-defective hyper-IgM-2 mutants. J Biol Chem 287(33):28007-28016.
21. Patenaude A-M, et al. (2009) Active nuclear import and cytoplasmic retention of activation-induced deaminase. Nat Struct Mol Biol 16(5):517-527.
22. Uchimura Y, Barton LF, Rada C, Neuberger MS (2011) REG-γ associates with and modulates the abundance of nuclear activation-induced deaminase. J Exp Med 208(12): 2385-2391.
23. Kohli RM, et al. (2009) A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activation-induced cytidine deaminase. J Biol Chem 284(34):22898-22904.
24. Petersen-Mahrt SK, Harris RS, Neuberger MS (2002) AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418(6893):99-103. (Pubitemid 34742579)
25. Arakawa H, Saribasak H, Buerstedde J-M (2004) Activation-induced cytidine deaminase initiates immunoglobulin gene conversion and hypermutation by a common intermediate. PLoS Biol 2(7):E179.
26. 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(2):163-171. (Pubitemid 39388832)
27. Klemm L, et al. (2009) The B cell mutator AID promotes B lymphoid blast crisis and drug resistance in chronic myeloid leukemia. Cancer Cell 16(3):232-245.
28. Orthwein A, et al. (2010) Regulation of activation-induced deaminase stability and antibody gene diversification by Hsp90. J Exp Med 207(12):2751-2765.
29. Zaheen A, et al. (2009) AID constrains germinal center size by rendering B cells susceptible to apoptosis. Blood 114(3):547-554.
30. Ouyang L, et al. (2012) Programmed cell death pathways in cancer: A review of apoptosis, autophagy and programmed necrosis. Cell Prolif 45(6):487-498.
31. Wang M, Yang Z, Rada C, Neuberger MS (2009) AID upmutants isolated using a highthroughput screen highlight the immunity/cancer balance limiting DNA deaminase activity. Nat Struct Mol Biol 16(7):769-776.
32. Manis JP, et al. (2004) 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat Immunol 5(5):481-487. (Pubitemid 38660459)
33. 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(2):417-427.
34. Kracker S, et al. (2010) Impaired induction of DNA lesions during immunoglobulin class-switch recombination in humans influences end-joining repair. Proc Natl Acad Sci USA 107(51):22225-22230.
35. Sartori AA, et al. (2007) Human CtIP promotes DNA end resection. Nature 450(7169): 509-514. (Pubitemid 350190253)
36. Lee-Theilen M, Matthews AJ, Kelly D, Zheng S, Chaudhuri J (2011) CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat Struct Mol Biol 18(1):75-79.
37. Bothmer A, et al. (2013) Mechanism of DNA resection during intrachromosomal recombination and immunoglobulin class switching. J Exp Med 210(1):115-123.
38. Cortizas EM, et al. (2013) Alternative end-joining and classical nonhomologous endjoining pathways repair different types of double-strand breaks during class-switch recombination. J Immunol 191(11):5751-5763.
39. Yamane A, et al. (2013) RPA accumulation during class switch recombination represents 5′-3′ DNA-end resection during the S-G2/M phase of the cell cycle. Cell Rep 3(1): 138-147.
40. Moynahan ME, Jasin M (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 11(3):196-207.
41. Barreto VM, et al. (2005) AID from bony fish catalyzes class switch recombination. J Exp Med 202(6):733-738. (Pubitemid 41345962)
42. Sabouri S, et al. (2014) C-terminal region of activation-induced cytidine deaminase (AID) is required for efficient class switch recombination and gene conversion. Proc Natl Acad Sci USA.
43. Zahn A, et al. (2013) Separation of function between isotype switching and affinity maturation in vivo during acute immune responses and circulating autoantibodies in UNG-deficient mice. J Immunol 190(12):5949-5960.
44. Staszewski O, et al. (2011) Activation-induced cytidine deaminase induces reproducible DNA breaks at many non-Ig Loci in activated B cells. Mol Cell 41(2): 232-242.
45. Wu X, Geraldes P, Platt JL, Cascalho M (2005) The double-edged sword of activationinduced cytidine deaminase. J Immunol 174(2):934-941. (Pubitemid 40094289)
46. 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(4):855-865.
47. Deriano L, et al. (2011) The RAG2 C terminus suppresses genomic instability and lymphomagenesis. Nature 471(7336):119-123.
48. Xu Z, et al. (2010) 14-3-3 adaptor proteins recruit AID to 5′-AGCT-3′-rich switch regions for class switch recombination. Nat Struct Mol Biol 17(9):1124-1135.
49. Reina-San-Martin BR, Chaudhuri J (2010) DNA Deamination and the Immune System: AID in Health and Disease, eds Fugmann SD, Diaz M, Papavasiliou FN (Imperial College Press, London), pp 62-82.
50. Vuong BQ, et al. (2013) A DNA break- and phosphorylation-dependent positive feedback loop promotes immunoglobulin class-switch recombination. Nat Immunol 14(11):1183-1189.
51. Dancyger AM, et al. (2012) Differences in the enzymatic efficiency of human and bony fish AID are mediated by a single residue in the C terminus modulating singlestranded DNA binding. FASEB J 26(4):1517-1525.
52. Larijani M, et al. (2007) AID associates with single-stranded DNA with high affinity and a long complex half-life in a sequence-independent manner. Mol Cell Biol 27(1): 20-30. (Pubitemid 46013229)