The roles of APE1, APE2, DNA polymerase β and mismatch repair in creating S region DNA breaks during antibody class switch

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1517, 2009, Pages 645-652

  Schrader, Carol E ^a   Guikema, Jeroen E J ^a   Wu, Xiaoming ^a,b   Stavnezer, Janet ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Activation induced cytidine deaminase; Antibody class switch; DNA recombination

Indexed keywords

ANTIBODY; DNA; ENZYME ACTIVITY; MUTATION; RECOMBINATION;

EID: 60049083259     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0200     Document Type: Conference Paper

References (39)

1. Bransteitter, R., Pham, P., Scharff, M. D. & Goodman, M. F. 2003 Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl Acad. Sci. USA 100, 4102-4107. (doi:10.1073/pnas.0730835100)
2. Bransteitter, R., Pham, P., Calabrese, P. & Goodman, M. F. 2004 Biochemical analysis of hypermutational targeting by wild type and mutant activation-induced cytidine deaminase. J. Biol. Chem. 279, 51 612-51 621. (doi:10.1074/jbc.M408135200)
3. Casellas, R. et al. 1998 Ku80 is required for immunoglobulin isotype switching. EMBO J. 17, 2404-2411. (doi:10.1093/emboj/17.8. 2404)
4. Catalan, N., Selz, F., Imai, K., Revy, P., Fischer, A. & Durandy, A. 2003 The block in immunoglobulin class switch recombination caused by activation-induced cytidine deaminase deficiency occurs prior to the generation of DNA double strand breaks in switch mu region. J. Immunol. 171, 2504-2509.
5. Chaudhuri, J., Tian, M., Khuong, C., Chua, K., Pinaud, E. & Alt, F. W. 2003 Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422, 726-730. (doi:10.1038/ nature01574)
6. Di Noia, J. & Neuberger, M. S. 2002 Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419, 43-48. (doi:10.1038/nature00981)
7. Esposito, G., Texido, G., Betz, U. A., Gu, H., Muller, W., Klein, U. & Rajewsky, K. 2000 Mice reconstituted with DNA polymerase beta-deficient fetal liver cells are able to mount a T cell-dependent immune response and mutate their Ig genes normally. Proc. Natl Acad. Sci. USA 97, 1166-1171. (doi:10.1073/pnas.97.3.1166)
8. Fedyk, E. R. & Phipps, R. P. 1994 Reactive oxygen species and not lipoxygenase products are required for mouse B-lymphocyte activation and differentiation. Int. J. Immunopharmacol. 16, 533-546. (doi:10.1016/0192-0561(94)90105-8)
9. Guikema, J. E., Linehan, E. K., Tsuchimoto, D., Nakabeppu, Y., Strauss, P. R., Stavnezer, J. & Schrader, C. E. 2007 APE1- and APE2-dependent DNA breaks in immunoglobulin class switch recombination. J. Exp. Med. 204, 3017-3026. (doi:10.1084/jem.20071289)
10. Hadi, M. Z., Ginalski, K., Nguyen, L. H. & Wilson III, D. M. 2002 Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III. J. Mol. Biol. 316, 853-866. (doi:10.1006/jmbi.2001.5382)
11. Ide, Y., Tsuchimoto, D., Tominaga, Y., Nakashima, M., Watanabe, T., Sakumi, K., Ohno, M. & Nakabeppu, Y. 2004 Growth retardation and dyslymphopoiesis accompanied by G2/M arrest in APEX2-null mice. Blood 104, 4097-4103. (doi:10.1182/blood-2004-04-1476)
12. Imai, K. et al. 2003 Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination. Nat. Immunol. 4, 1023-1028. (doi:10.1038/ni974)
13. Ito, K. et al. 2004 Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431, 997-1002. (doi:10.1038/nature02989)
14. Ito, K. et al. 2007 Regulation of reactive oxygen species by Atm is essential for proper response to DNA double-strand breaks in lymphocytes. J. Immunol. 178, 103-110.
15. Li, Z., Woo, C. J., Iglesias-Ussel, M. D., Ronai, D. & Scharff, M. D. 2004 The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev. 18, 1-11. (doi:10.1101/gad.1161904)
16. Longerich, S., Basu, U., Alt, F. & Storb, U. 2006 AID in somatic hypermutation and class switch recombination. Curr. Opin. Immunol. 18, 164-174. (doi:10.1016/j.coi.2006.01.008)
17. Manis, J. P., Gu, Y., Lansford, R., Sonoda, E., Ferrini, R., Davidson, L., Rajewsky, K. & Alt, F. W. 1998 Ku70 is required for late B cell development and immunoglobulin heavy chain switching. J. Exp. Med. 187, 2081-2089. (doi:10.1084/jem.187.12.2081)
18. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y. & Honjo, T. 2000 Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563. (doi:10.1016/S0092-8674(00)00078-7)
19. Nagaoka, H., Muramatsu, M., Yamamura, N., Kinoshita, K. & Honjo, T. 2002 Activation-induced deaminase (AID)-directed hypermutation in the immunoglobulin Sm region: implication of AID involvement in a common step of class switch recombination and somatic hypermutation. J. Exp. Med. 195, 529-534. (doi:10.1084/jem.20012144)
20. Petersen, S. et al. 2001 AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 414, 660-665. (doi:10.1038/414660a)
21. Petersen-Mahrt, S. K., Harris, R. S. & Neuberger, M. S. 2002 AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418, 99-104. (doi:10.1038/nature00862)
22. Pham, P., Bransteitter, R., Petruska, J. & Goodman, M. F. 2003 Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 424, 103-107. (doi:10.1038/ nature01760)
23. Poltoratsky, V., Prasad, R., Horton, J. K. & Wilson, S. H. 2007 Down-regulation of DNA polymerase beta accompanies somatic hypermutation in human BL2 cell lines. DNA Repair (Amst.) 6, 244-253. (doi:10.1016/j.dnarep.2006.10.003)
24. Rada, C., Williams, G. T., Nilsen, H., Barnes, D. E., Lindahl, T. & Neuberger, M. S. 2002 Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12, 1748-1755. (doi:10.1016/S0960-9822(02)01215-0)
25. 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. (doi:10.1016/S0092-8674(00)00079-9)
26. Rush, J. S., Fugmann, S. D. & Schatz, D. G. 2004 Staggered AID-dependent DNA double strand breaks are the predominant DNA lesions targeted to S mu in Ig class switch recombination. Int. Immunol. 16, 549-557. (doi:10.1093/intimm/dxh057)
27. Schrader, C. E., Edelmann, W., Kucherlapati, R. & Stavnezer, J. 1999 Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes. J. Exp. Med. 190, 323-330. (doi:10.1084/jem.190.3. 323)
28. Schrader, C. E., Bradley, S. P., Vardo, J., Mochegova, S. N., Flanagan, E. & Stavnezer, J. 2003 Mutations occur in the Ig Sm region but rarely in Sg regions prior to class switch recombination. EMBO J. 22, 5893-5903. (doi:10.1093/emboj/cdg550)
29. Schrader, C. E., Linehan, E. K., Mochegova, S. N., Woodland, R. T. & Stavnezer, J. 2005 Inducible DNA breaks in Ig S regions are dependent upon AID and UNG. J. Exp. Med. 202, 561-568. (doi:10.1084/jem.20050872)
30. Schrader, C. E., Guikema, J. E., Linehan, E. K., 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, 6064-6071.
31. Srivastava, D. K., Berg, B. J., Prasad, R., Molina, J. T., Beard, W. A., Tomkinson, A. E. & Wilson, S. H. 1998 Mammalian abasic site base excision repair. Identification of the reaction sequence and rate-determining steps. J. Biol. Chem. 273, 21 203-21 209. (doi:10.1074/jbc.273.33.21203)
32. Stavnezer, J. & Schrader, C. E. 2006 Mismatch repair converts AID-instigated nicks to double-strand breaks for antibody class-switch recombination. Trends Genet. 22, 23-28. (doi:10.1016/j.tig.2005. 11.002)
33. Stavnezer, J., Guikema, J. E. J. & Schrader, C. E. 2008 Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26, 261-292. (doi:10.1146/annurev.immunol.26.021607.090248)
34. Tsuchimoto, D., Sakai, Y., Sakumi, K., Nishioka, K., Sasaki, M., Fujiwara, T. & Nakabeppu, Y. 2001 Human APE2 protein is mostly localized in the nuclei and to some extent in the mitochondria, while nuclear APE2 is partly associated with proliferating cell nuclear antigen. Nucleic Acids Res. 29, 2349-2360. (doi:10.1093/nar/29.11.2349)
35. 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, 1677-1689. (doi:10.1084/jem.20070285)
36. -/- mice. J. Exp. Med. 203, 2085-2094. (doi:10.1084/jem.20061067)
37. Yan, C. T. et al. 2007 IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449, 478-482. (doi:10.1038/nature06020)
38. Yu, K., Huang, F. T. & Lieber, M. R. 2004 DNA substrate length and surrounding sequence affect the activation-induced deaminase activity at cytidine. J. Biol. Chem. 279, 6496-6500. (doi:10.1074/jbc. M311616200)
39. Zarrin, A. A., Del Vecchio, C., Tseng, E., Gleason, M., Zarin, P., Tian, M. & Alt, F. W. 2007 Antibody class switching mediated by yeast endonuclease-generated DNA breaks. Science 315, 377-381. (doi:10.1126/science.1136386)