Hijacked DNA repair proteins and unchained DNA polymerases

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1517, 2009, Pages 605-611

  Saribasak, Huseyin ^a   Rajagopal, Deepa ^a   Maul, Robert W ^a   Gearhart, Patricia J ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Class switch recombination; Cockayne syndrome B; DNA polymerase ; Immunoglobulin genes; MSH2 MSH6; Somatic hypermutation

Indexed keywords

ANTIBODY; DNA; ENZYME ACTIVITY; MUTATION; PROTEIN;

MUS;

EID: 60049088647     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0188     Document Type: Conference Paper

References (41)

1. Alrefai, R. H., Winter, D. B., Bohr, V. A. & Gearhart, P. J. 2007 Nucleotide excision repair in an immunoglobulin variable gene is less efficient than in a housekeeping gene. Mol. Immunol. 44, 2800-2805. (doi:10.1016/j.molimm.2007.01.018)
2. Bardwell, P. D., Woo, C. J., Wei, K., Li, Z., Martin, A., Sack, S. Z., Parris, T., Edelmann, W. & Scharff, M. D. 2004 Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice. Nat. Immunol. 5, 224-229. (doi:10.1038/ni1031)
3. Bertocci, B., De Smet, A., Flatter, E., Dahan, A., Bories, J.-C., Landreau, C., Weill, J.-C. & Reynaud, C.-A. 2002 Cutting edge: DNA polymerases μ and λ are dispensable for Ig gene hypermutation. J. Immunol. 168, 3702-3706.
4. Delbos, F., De Smet, A., Faili, A., Aoufouchi, S., Weill, J.-C. & Reynaud, C.-A. 2005 Contribution of DNA polymerase η to immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 201, 1191-1196. (doi:10.1084/jem.20050292)
5. Delbos, F., Aoufouchi, S., Faili, A., Weill, J.-C. & Reynaud, C.-A. 2007 DNA polymerase η is the sole contributor of A/T modifications during immunoglobulin gene hypermutation in the mouse. J. Exp. Med. 204, 17-23. (doi:10.1084/jem.20062131)
6. Diaz, M., Verkoczy, L. K., Flajnik, M. F. & Klinman, N. R. 2001 Decreased frequency of somatic hypermutation and impaired affinity maturation but intact germinal center formation in mice expressing antisense RNA to DNA polymerase z. J. Immunol. 167, 327-335.
7. 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)
8. Ehrenstein, M. R. & Neuberger, M. S. 1999 Deficiency in Msh2 affects the efficiency and local sequence specificity of immunoglobulin class-switch recombination: parallels with somatic hypermutation. EMBO J. 18, 3484-3490. (doi:10.1093/emboj/18.12.3484)
9. Ehrenstein, M. R., Rada, C., Jones, A.-M., Milstein, C. & Neuberger, M. S. 2001 Switch junction sequences in PMS2-deficient mice reveal a microhomology-mediated mechanism of Ig class switch recombination. Proc. Natl Acad. Sci. USA 98, 14 553-14 558. (doi:10.1073/pnas.241525998)
10. Faili, A., Aoufouchi, S., Weller, S., Vuillier, F., Stary, A., Sarasin, A., Reynaud, C.-A. & Weill, J.-C. 2004 DNA polymerase η is involved in hypermutation occurring during immunoglobulin class switch recombination. J. Exp. Med. 199, 265-270. (doi:10.1084/jem.20031831)
11. Frey, S., Bertocci, B., Delbos, F., Quint, L., Weill, J.-C. & Reynaud, C.-A. 1998 Mismatch repair deficiency interferes with the accumulation of mutations in chronically stimulated B cells and not with the hypermutation process. Immunity 9, 127-134. (doi:10.1016/S1074-7613(00)80594-4)
12. Guikema, J. E. J., 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)
13. Jacobs, H. et al. 1998 Hypermutation of immunoglobulin genes in memory B cells of DNA repair-deficient mice. J. Exp. Med. 187, 1735-1743. (doi:10.1084/jem.187.11.1735)
14. Jansen, J. G., Langerak, P., Tsaalbi-Shtylik, A., van den Berk, P., Jacobs, H. & de Wind, N. 2006 Strand-biased defect in C/G transversions in hypermutating immunoglobulin genes in Rev1-deficient mice. J. Exp. Med. 203, 319-323. (doi:10.1084/jem.20052227)
15. Kadyrov, F. A., Dzantiev, L., Constantin, N. & Modrich, P. 2006 Endonucleolytic function of MutLα in human mismatch repair. Cell 126, 297-308. (doi:10.1016/j.cell.2006.05.039)
16. Kim, N., Bozek, G., Lo, J. C. & Storb, U. 1999 Different mismatch repair deficiencies all have the same effects on somatic hypermutation: intact primary mechanism accompanied by secondary modifications. J. Exp. Med. 190, 21-30. (doi:10.1084/jem.190.1.21)
17. Li, Z. et al. 2004 Examination of Msh6- and Msh3-deficient mice in class switching reveals overlapping and distinct roles of MutS homologues in antibody diversification. J. Exp. Med. 200, 47-59. (doi:10.1084/jem.20040355)
18. Martomo, S. A., Yang, W. W. & Gearhart, P. J. 2004 A role of Msh6 but not Msh3 in somatic hypermutation and class switch recombination. J. Exp. Med. 200, 61-68. (doi:10.1084/jem.20040691)
19. Martomo, S. A., Yang, W. W., Wersto, R. P., Ohkumo, T., Kondo, Y., Yokoi, M., Masutani, C., Hanaoka, F. & Gearhart, P. J. 2005 Different mutation signatures in DNA polymerase η- and MSH6-deficient mice suggest separate roles in antibody diversification. Proc. Natl Acad. Sci. USA 102, 8656-8661. (doi:10.1073/pnas.0501852102)
20. Martomo, S. A., Yang, W. W., Vaisman, A., Maas, A., Yokoi, M., Hoeijmakers, J. H., Hanaoka, F., Woodgate, R. & Gearhart, P. J. 2006 Normal hypermutation in antibody genes from congenic mice defective for DNA polymerase ι. DNA Repair 5, 392-398. (doi:10.1016/j.dnarep.2005.12.006)
21. Martomo, S. A., Saribasak, H., Yokoi, M., Hanaoka, F. & Gearhart, P. J. 2008 Reevaluation of the role of DNA polymerase θ in somatic hypermutation of immunoglobulin genes. DNA Repair 7, 1603-1608. (doi:10.1016/j.dnarep.2008.04.002)
22. Masuda, K. et al. 2007 DNA polymerases η and θ function in the same genetic pathway to generate mutations at A/T during somatic hypermutation of Ig genes. J. Biol. Chem. 282, 17 387-17 394. (doi:10.1074/jbc.M611849200)
23. Matsuda, T., Bebenek, K., Masutani, C., Rogozin, I. G., Hanaoka, F. & Kunkel, T. A. 2001 Error rate and specificity of human and murine DNA polymerase η. J. Mol. Biol. 312, 335-346. (doi:10.1006/jmbi. 2001.4937)
24. Mayorov, V. I., Rogozin, I. B., Adkison, L. R. & Gearhart, P. J. 2005 DNA polymerase η contributes to strand bias of mutations of A versus T in immunoglobulin genes. J. Immunol. 174, 7781-7786.
25. McDonald, J. P., Frank, E. G., Plosky, B. S., Rogozin, I. B., Masutani, C., Hanaoka, F., Woodgate, R. & Gearhart, P. J. 2003 129-derived strains of mice are deficient in DNA polymerase ι and have normal immunoglobulin hypermutation. J. Exp. Med. 198, 635-643. (doi:10.1084/jem. 20030767)
26. 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)
27. 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, 99-103. (doi:10.1038/nature00862)
28. Phung, Q. H., Winter, D. B., Cranston, A., Tarone, R. E., Bohr, V. A., Fishel, R. & Gearhart, P. J. 1998 Increased hypermutation at G and C nucleotides in immunoglobulin variable genes from mice deficient in the MSH2 mismatch repair protein. J. Exp. Med. 187, 1745-1751. (doi:10.1084/jem.187.11.1745)
29. Phung, Q. H., Winter, D. B., Alrefai, R. & Gearhart, P. J. 1999 Cutting edge: hypermutation in Ig V genes from mice deficient in the MLH1 mismatch repair protein. J. Immunol. 162, 3121-3124.
30. Rada, C., Ehrenstein, M. R., Neuberger, M. S. & Milstein, C. 1998 Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting. Immunity 9, 135-141. (doi:10.1016/S1074-7613(00)80595-6)
31. 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)
32. Ross, A.-L. & Sale, J. E. 2006 The catalytic activity of REV1 is employed during immunoglobulin gene diversification in DT40. Mol. Immunol. 43, 1587-1594. (doi:10.1016/j.molimm.2005.09.017)
33. Schenten, D., Gerlach, V. L., Guo, C., Velasco-Miguel, S., Hladik, C. L., White, C. L., Friedberg, E. C., Rajewsky, K. & Esposito, G. 2002 DNA polymerase κ deficiency does not affect somatic hypermutation in mice. Eur. J. Immunol. 32, 3152-3160. (doi:10.1002/1521-4141(200211)32: 11〈3152::AID-IMMU3152〉3.0.CO;2-2)
34. 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)
35. Wiesendanger, M., Kneitz, B., Edelmann, W. & Scharff, M. D. 2000 Somatic hypermutation in MutS homologue (MSH)3-, MSH6-, and MSH3/MSH6-deficient mice reveals a role for the MSH2-MSH6 heterodimer in modulating the base substitution pattern. J. Exp. Med. 191, 579-584. (doi:10.1084/jem.191.3.579)
36. Wilson, T. M., Vaisman, A., Martomo, S. A., Sullivan, P., Lan, L., Hanaoka, F., Yasui, A., Woodgate, R. & Gearhart, P. J. 2005 MSH2-MSH6 stimulates DNA polymerase η, suggesting a role for A:T mutations in antibody genes. J. Exp. Med. 201, 637-645. (doi:10.1084/jem.20042066)
37. Winter, D. B. et al. 1998 Altered spectra of hypermutation in antibodies from mice deficient for the DNA mismatch repair protein PMS2. Proc. Natl Acad. Sci. USA 95, 6953-6958. (doi:10.1073/pnas.95.12. 6953)
38. Wong, H.-K., Muftuoglu, M., Beck, G., Iman, S. Z., Bohr, V. A. & Wilson III, D. M. 2007 Cockayne syndrome B protein stimulates apurinic endonuclease 1 activity and protects against agents that introduce base excision repair intermediates. Nucleic Acids Res. 35, 4103-4113. (doi:10.1093/nar/gkm404)
39. Wu, X. & Stavnezer, J. 2007 DNA polymerase β 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)
40. Zeng, X., Winter, D. B., Kasmer, C., Kraemer, K. H., Lehmann, A. R. & Gearhart, P. J. 2001 DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat. Immunol. 2, 537-541. (doi:10.1038/88740)
41. Zeng, X., Negrete, G. A., Kasmer, C., Yang, W. W. & Gearhart, P. J. 2004 Absence of DNA polymerase η reveals targeting of C mutations on the nontranscribed strand in immunoglobulin switch regions. J. Exp. Med. 199, 917-924. (doi:10.1084/jem.20032022)