Differential regulation of S-region hypermutation and class-switch recombination by noncanonical functions of uracil DNA glycosylase

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

Volumn 111, Issue 11, 2014, Pages

  Yousif, Ashraf S ^a   Stanlie, Andre ^a   Mondal, Samiran ^a   Honjo, Tasuku ^a   Begum, Nasim A ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; CYCLINE; DNA DEPENDENT PROTEIN KINASE; DNA POLYMERASE; ENZYME; FLAP END PROCESSING ENZYME 1; P53 BINDING PROTEIN 1; PROTEIN; PROTEIN MSH2; UNCLASSIFIED DRUG; URACIL DNA GLYCOSIDASE;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA CLEAVAGE; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME SUBSTRATE COMPLEX; EXCISION REPAIR; GENE REARRANGEMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; SOMATIC HYPERMUTATION; SYNAPSE;

NHEJ; SYNAPSIS;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; CYTIDINE DEAMINASE; DNA END-JOINING REPAIR; DNA PRIMERS; FLOW CYTOMETRY; FLUORESCENCE; GREEN FLUORESCENT PROTEINS; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN SWITCH REGION; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; URACIL-DNA GLYCOSIDASE;

EID: 84896504436     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402391111     Document Type: Article

References (57)

1. Muramatsu M, et al. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102(5):553-563.
2. Muramatsu M, Nagaoka H, Shinkura R, Begum NA, Honjo T (2007) Discovery of activation-induced cytidine deaminase, the engraver of antibody memory. Adv Immunol 94:1-36. (Pubitemid 46863447)
3. Schrader CE, Guikema JE, Linehan EK, Selsing E, Stavnezer J (2007) Activation-induced cytidine deaminase-dependent DNA breaks in class switch recombination occur during G1 phase of the cell cycle and depend upon mismatch repair. J Immunol 179(9): 6064-6071.
4. 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.
5. Shinkura R, et al. (2004) Separate domains of AID are required for somatic hypermutation and class-switch recombination. Nat Immunol 5(7):707-712. (Pubitemid 39023302)
6. 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(2):501-508. (Pubitemid 37238934)
7. Ta VT, et al. (2003) AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat Immunol 4(9):843-848.
8. Faili A, et al. (2002) AID-dependent somatic hypermutation occurs as a DNA singlestrand event in the BL2 cell line. Nat Immunol 3(9):815-821.
9. Kinoshita K, Tashiro J, Tomita S, Lee CG, Honjo T (1998) Target specificity of immunoglobulin class switch recombination is not determined by nucleotide sequences of S regions. Immunity 9(6):849-858. (Pubitemid 29024464)
10. Conticello SG, Langlois MA, Yang Z, Neuberger MS (2007) DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv Immunol 94:37-73. (Pubitemid 46856607)
11. Saribasak H, et al. (2012) DNA polymerase ζ generates tandem mutations in immunoglobulin variable regions. J Exp Med 209(6):1075-1081.
12. Daly J, et al. (2012) Altered Ig hypermutation pattern and frequency in complementary mouse models of DNA polymerase ζ activity. J Immunol 188(11):5528-5537.
13. Honjo T, Kinoshita K, Muramatsu M (2002) Molecular mechanism of class switch recombination: Linkage with somatic hypermutation. Annu Rev Immunol 20:165-196. (Pubitemid 34293423)
14. Chaudhuri J, et al. (2007) Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 94:157-214. (Pubitemid 46856611)
15. Lindahl T, Ljungquist S, Siegert W, Nyberg B, Sperens B (1977) DNA N-glycosidases: Properties of uracil-DNA glycosidase from Escherichia coli. J Biol Chem 252(10): 3286-3294. (Pubitemid 8111183)
16. Caldecott KW (2007) Mammalian single-strand break repair: Mechanisms and links with chromatin. DNA Repair (Amst) 6(4):443-453. (Pubitemid 46357048)
17. Wilson SH, Kunkel TA (2000) Passing the baton in base excision repair. Nat Struct Biol 7(3):176-178. (Pubitemid 30140755)
18. Akbari M, et al. (2010) Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes. DNA Repair (Amst) 9(7):785-795.
19. Akbari M, et al. (2004) Repair of U/G and U/A in DNA by UNG2-associated repair complexes takes place predominantly by short-patch repair both in proliferating and growth-arrested cells. Nucleic Acids Res 32(18):5486-5498. (Pubitemid 39545666)
20. Parsons JL, Dianov GL (2013) Co-ordination of base excision repair and genome stability. DNA Repair (Amst) 12(5):326-333.
21. Dianov GL, Hübscher U (2013) Mammalian base excision repair: The forgotten archangel. Nucleic Acids Res 41(6):3483-3490.
22. Guenzel CA, et al. (2012) Recruitment of the nuclear form of uracil DNA glycosylase into virus particles participates in the full infectivity of HIV-1. J Virol 86(5):2533-2544.
23. De Silva FS, Moss B (2003) Vaccinia virus uracil DNA glycosylase has an essential role in DNA synthesis that is independent of its glycosylase activity: Catalytic site mutations reduce virulence but not virus replication in cultured cells. J Virol 77(1):159-166. (Pubitemid 36004956)
24. Stanitsa ES, Arps L, Traktman P (2006) Vaccinia virus uracil DNA glycosylase interacts with the A20 protein to form a heterodimeric processivity factor for the viral DNA polymerase. J Biol Chem 281(6):3439-3451. (Pubitemid 43845959)
25. Zeitlin SG, et al. (2011) Uracil DNA N-glycosylase promotes assembly of human centromere protein A. PLoS ONE 6(3):e17151.
26. Begum NA, et al. (2007) Requirement of non-canonical activity of uracil DNA glycosylase for class switch recombination. J Biol Chem 282(1):731-742. (Pubitemid 47076591)
27. Begum NA, et al. (2004) Uracil DNA glycosylase activity is dispensable for immunoglobulin class switch. Science 305(5687):1160-1163. (Pubitemid 39100330)
28. 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(8): 2752-2757.
29. Shroyer MJ, Bennett SE, Putnam CD, Tainer JA, Mosbaugh DW (1999) Mutation of an active site residue in Escherichia coli uracil-DNA glycosylase: Effect on DNA binding, uracil inhibition and catalysis. Biochemistry 38(15):4834-4845.
30. Rada C, et al. (2002) Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr Biol 12(20):1748-1755. (Pubitemid 35169790)
31. Chaudhuri J, Alt FW (2004) Class-switch recombination: Interplay of transcription, DNA deamination and DNA repair. Nat Rev Immunol 4(7):541-552.
32. Zan H, et al. (2012) Rev1 recruits ung to switch regions and enhances du glycosylation for immunoglobulin class switch DNA recombination. Cell Rep 2(5):1220-1232.
33. 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.
34. Liu M, et al. (2008) Two levels of protection for the B cell genome during somatic hypermutation. Nature 451(7180):841-845. (Pubitemid 351253166)
35. Mol CD, et al. (1995) Crystal structure and mutational analysis of human uracil-DNA glycosylase: Structural basis for specificity and catalysis. Cell 80(6):869-878.
36. 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.
37. Saribasak H, et al. (2011) XRCC1 suppresses somatic hypermutation and promotes alternative nonhomologous end joining in Igh genes. J Exp Med 208(11):2209-2216.
38. Poltoratsky V, Prasad R, Horton JK, Wilson SH (2007) Down-regulation of DNA polymerase beta accompanies somatic hypermutation in human BL2 cell lines. DNA Repair (Amst) 6(2):244-253. (Pubitemid 46074496)
39. Wu X, Stavnezer J (2007) DNA polymerase beta is able to repair breaks in switch regions and plays an inhibitory role during immunoglobulin class switch recombination. J Exp Med 204(7):1677-1689. (Pubitemid 47048033)
40. Larsen E, et al. (2008) Early-onset lymphoma and extensive embryonic apoptosis in two domain-specific Fen1 mice mutants. Cancer Res 68(12):4571-4579.
41. Guo C, et al. (2003) Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J 22(24):6621-6630. (Pubitemid 38009608)
42. Masuda K, et al. (2009) A critical role for REV1 in regulating the induction of C:G transitions and A:T mutations during Ig gene hypermutation. J Immunol 183(3): 1846-1850.
43. Auerbach P, Bennett RA, Bailey EA, Krokan HE, Demple B (2005) Mutagenic specificity of endogenously generated abasic sites in Saccharomyces cerevisiae chromosomal DNA. Proc Natl Acad Sci USA 102(49):17711-17716. (Pubitemid 41803562)
44. Roche H, Gietz RD, Kunz BA (1995) Specificities of the Saccharomyces cerevisiae rad6, rad18, and rad52 mutators exhibit different degrees of dependence on the REV3 gene product, a putative nonessential DNA polymerase. Genetics 140(2):443-456.
45. Rada C, Ehrenstein MR, Neuberger MS, Milstein C (1998) Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting. Immunity 9(1):135-141. (Pubitemid 28361302)
46. Bardwell PD, et al. (2004) Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice. Nat Immunol 5(2):224-229. (Pubitemid 38208365)
47. Adams MM, Carpenter PB (2006) Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div 1:19.
48. 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(9):1103-1110. (Pubitemid 39507050)
49. Reina-San-Martin B, et al. (2003) H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J Exp Med 197(12):1767-1778. (Pubitemid 36745351)
50. Reina-San-Martin B, Chen J, Nussenzweig A, Nussenzweig MC (2007) Enhanced intraswitch region recombination during immunoglobulin class switch recombination in 53BP1-/- B cells. Eur J Immunol 37(1):235-239. (Pubitemid 46128803)
51. Callén E, et al. (2009) Essential role for DNA-PKcs in DNA double-strand break repair and apoptosis in ATM-deficient lymphocytes. Mol Cell 34(3):285-297.
52. 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)
53. Wang M, et al. (2006) PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 34(21):6170-6182. (Pubitemid 44942738)
54. 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.
55. 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(3):367-373. (Pubitemid 34461495)
56. Grippon S, et al. (2011) Differential modes of DNA binding by mismatch uracil DNA glycosylase from Escherichia coli: Implications for abasic lesion processing and enzyme communication in the base excision repair pathway. Nucleic Acids Res 39(7): 2593-2603.
57. Ueyama TKT, et al. (2008) Sequential binding of cytosolic Phox complex to phagosomes through regulated adaptor proteins: Evaluation using the novel monomeric Kusabira- Green System and live imaging of phagocytosis. J Immunol 181(1):629-640.