Absence of DNA Polymerase η Reveals Targeting of C Mutations on the Nontranscribed Strand in Immunoglobulin Switch Regions

Journal of Experimental Medicine

Volumn 199, Issue 7, 2004, Pages 917-924

  Zeng, Xianmin ^a   Negrete, George A ^a   Kasmer, Cynthia ^a   Yang, William W ^a   Gearhart, Patricia J ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Activation induced cytosine deaminase; Gap filling repair; Somatic hypermutation; Translesion replication; Xeroderma pigmentosum variant

Indexed keywords

CYTOSINE DEAMINASE; DNA POLYMERASE; SINGLE STRANDED DNA;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE INSERTION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN GENE; LYMPHOCYTE; MUTATION RATE; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SOMATIC HYPERMUTATION; XERODERMA PIGMENTOSUM;

BASE SEQUENCE; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; DNA; DNA-DIRECTED DNA POLYMERASE; HUMANS; IMMUNOGLOBULIN GAMMA-CHAINS; IMMUNOGLOBULIN MU-CHAINS; IMMUNOGLOBULIN SWITCH REGION; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTATION; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; TRANSCRIPTION, GENETIC; XERODERMA PIGMENTOSUM;

EID: 1842732235     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20032022     Document Type: Article

References (56)

1. Muramatsu, M., K. Kinoshita, S. Faragasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell. 102:553-563.
2. Revy, P., T. Muto, Y. Levy, F. Geissmann, A. Piebani, O. Sanal, N. Catalan, M. Forveille, R. Dufourcq-Lagelouse, A. Gennery, et al. 2000. Activation-induced cytidine deaminase (AID) causes the autosomal recessive form of the hyper IgM syndrome (HIGM2). Cell. 102:565-575.
3. Petersen-Mahrt, S.K., R.S. Harris, and M.S. Neuberger. 2002. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature. 418:99-103.
4. Di Noia, J., and M.S. Neuberger. 2002. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature. 419:43-48.
5. Rada, C., G.T. Williams, H. Nilsen, D.E. Barnes, T. Lindahl, and M.S. Neuberger. 2002. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12:1748-1755.
6. Bransteitter, R., P. Pham, M.D. Scharff, and M.F. Goodman. 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.
7. Chaudhuri, J., M. Tian, C. Khuong, K. Chua, E. Pinaud, and F.W. Alt. 2003. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature. 422:726-730.
8. Ramiro, A.R., P. Stavropoulos, M. Jankovic, and M.C. Nussenzweig. 2003. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nat. Immunol. 4:452-456.
9. Dickerson, S.K., E. Market, E. Besmer, and F.N. Papavasiliou. 2003. AID mediates hypermutation by deaminating single stranded DNA. J. Exp. Med. 197:1291-1296.
10. Sohail, A., J. Klapacz, M. Samaranayake, A. Ullah, and A.S. Bhagwat. 2003. Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations. Nucleic Acids Res. 31:2990-2994.
11. Imai, K., G. Slupphaug, W.I. Lee, P. Revy, S. Nonoyama, N. Catalan, L. Yel, M. Forveille, B. Kavli, H.E. Krokan, et al. 2003. Human uracil-DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination. Nat. Immunol. 4:1023-1028.
12. Winter, D.B., Q.H. Phung, A. Umar, S.M. Baker, R.E. Tarone, K. Tanaka, R.M. Liskay, T.A. Kunkel, V.A. Bohr, and P.J. Gearhart. 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.
13. Phung, Q.H., D.B. Winter, A. Cranston, R.E. Tarone, V.A. Bohr, R. Fishel, and P.J. Gearhart. 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.
14. Frey, S., B. Bertocci, F. Delbos, L. Quint, J.C. Weill, and C.A. Reynaud. 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.
15. Rada, C., M.R. Ehrenstein, M.S. Neuberger, and C. Milstein. 1998. Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stage of mutational targeting. Immunity. 9:135-141.
16. Kim, N., G. Bozek, J.C. Lo, and U. Storb. 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.
17. Ehrenstein, M.R., and M.S. Neuberger. 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.
18. Schrader, C.E., W. Edelmann, R. Kucherlapati, and J. Stavnezer. 1999. Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes. J. Exp. Med. 190:323-330.
19. Zeng, X., D.B. Winter, C. Kasmer, K.H. Kraemer, A.R. Lehmann, and P.J. Gearhart. 2001. DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat. Immunol. 2:537-541.
20. Dunnick, W., M. Wilson, and J. Stavnezer. 1989. Mutations, duplication, and deletion of recombined switch regions suggest a role for DNA replication in the immunoglobulin heavy-chain switch. Mol. Cell. Biol. 9:1850-1856.
21. Petersen, S., R. Casellas, B. Reina-San-Martin, H.T. Chen, M.J. Difilippantonio, P.C. Wilson, L. Hanitsch, A. Celeste, M. Muramatsu, D.R. Pilch, et al. 2001. AID is required to initiate Nbs1/γ-H2AX focus formation and mutations at sites of class switching. Nature. 414:660-665.
22. Nagaoka, H., M. Muramatsu, N. Yamamura, K. Kinoshita, and T. Honjo. 2002. Activation-induced deaminase (AID)-directed hypermutation in the immunoglobulin Sμ region: implication of AID involvement in a common step of class switch recombination and somatic hypermutation. Exp. Med. 195:529-534.
23. Ta, V.T., H. Nagaoka, N. Catalan, A. Durandy, A. Fischer, K. Imai, S. Nonoyama, J. Tashiro, M. Ikegawa, S. Ito, et al. 2003. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat. Immunol. 4:843-848.
24. Barreto, V., B. Reina-San-Martin, A.R. Ramiro, K.M. McBride, and M.C. Nussenzweig. 2003. C-terminal eletion of AID uncouples class switch recombination from somatic hypermutation and gene conversion. Mol. Cell. 12:501-508.
25. Pham, P., R. Bransteitter, J. Petruska, and M.F. Goodman. 2003. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature. 424:103-107.
26. Smith D.S., G. Creadon, P.K. Jena, J.P. Portanova, B.L. Kotzin, and L.J. Wysocki. 1996. Di- and trinucleotide target preferences of somatic mutagenesis in normal and auto-reactive B cells. J. Immunol. 156:2642-2652.
27. Rosner, K., D.B. Winter, C. Kasmer, G.L. Skovgaard, R.E. Tarone, V.A. Bohr, and P.J. Gearhart. 2001. Impact of age on hypermutation of immunoglobulin variable genes in humans. J. Clin. Immunol. 21:102-115.
28. Mills, F.C., M.P. Mitchell, N. Harindranath, and E.E. Max. 1995. Human Ig Sγ regions and their participation in sequential switching to IgE. J. Immunol. 155:3021-3036.
29. Schrader C.E., S.P. Bradley, J. Vardo, S.N. Mochegova, E. Flanagan, and J. Stavnezer. 2003. Mutations occur in the Ig Sμ region but rarely in Sγ regions prior to class switch recombination. EMBO J. 22:5893-5903.
30. Cariello, N.F., W.W. Piegorsch, W.T. Adams, and T.R. Skopek. 1994. Computer program for the analysis of mutational spectra: application to p53 mutations. Carcinogenesis. 15:2281-2285.
31. Rogozin, I.B., and N.A. Kolchanov. 1992. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim. Biophys. Acta. 1171:11-18.
32. H, but is involved in the introduction of mutations in the switch μ region. J. Immunol. 170:3707-3716.
33. Storb, U., and J. Stavnezer. 2002. Immunoglobulin genes: generating diversity with AID and UNG. Curr. Biol. 12:R725-R727.
34. Stavnezer-Nordgren, J., and S. Sirlin. 1986. Specificity of immunoglobulin heavy chain switch correlates with activity of germline heavy chain genes prior to switching. EMBO J. 5:95-102.
35. Dunnick, W., G.Z. Hertz, L. Scappino, and C. Gritzmacher. 1993. DNA sequences at immunoglobulin switch region recombination sites. Nucleic Acids Res. 21:365-372.
36. Zhang, K., H.K. Cheah, and A. Saxon. 1995. Secondary deletional recombination of rearranged switch region in Ig isotype-switched B cells. J. Immunol. 154:2237-2247.
37. Dudley, D.D., J.P. Manis, A.A. Zarrin, L. Kaylor, M. Tian, and F.W. Alt. 2002. Internal IgH class switch region deletions are position-independent and enhanced by AID expression. Proc. Natl. Acad. Sci. USA. 99:9984-9989.
38. Dunnick, W., and J. Stavnezer. 1990. Copy choice mechanism of immunoglobulin heavy chain switch recombination. Mol. Cell. Biol. 10:397-400.
39. Gearhart, P.J., J.L. Hurwitz, and J.J. Cebra. 1980. Successive switching of antibody isotypes expressed within the lines of a B-cell clone. Proc. Natl. Acad. Sci. USA. 77:5424-5428.
40. Chen, X., K. Kinoshita, and T. Honjo. 2001. Variable deletion and duplication at recombination junction ends: implication for staggered double-strand cleavage in class-switch recombination. Proc. Natl. Acad. Sci. USA. 98:13860-13865.
41. Rogozin, I.B., Y.I. Pavlov, K. Bebenek, T. Matsuda, and T.A. Kunkel. 2001. Somatic mutation hotspots correlate with DNA polymerase η error spectrum. Nat. Immunol. 2:530-536.
42. Pavlov, Y.I., I.B. Rogozin, A.P. Galkin, A.Y. Aksenova, F. Hanaoka, C. Rada, and T.A. Kunkel. 2002. Correlation of somatic hypermutation specificity and A-T base pair substitution errors by DNA polymerase η during copying of a mouse immunoglobulin κ light chain transgene. Proc. Natl. Acad. Sci. USA. 99:9954-9959.
43. McDonald, J.P., E.G. Frank, B.S. Plosky, I.B. Rogozin, C. Masutani, F. Hanaoka, R. Woodgate, and P.J. Gearhart. 2003. 129-derived strains of mice are deficient in DNA polymerase ι and have normal immunoglobulin hypermutation. J. Exp. Med. 198:635-643.
44. Mizuta, R., K. Iwai, M. Shigeno, M. Mizuta, T. Uemura, T. Ushiki, and D. Kitamura. 2003. Molecular visualization of immunoglobulin switch region RNA/DNA complex by atomic force microscope. J. Biol. Chem. 278:4431-4434.
45. Yu, K., F. Chedin, C.L. Hsieh, T.E. Wilson, and M.R. Lieber. 2003. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4:442-451.
46. Hun, H., A. Yabuki, and N. Maizels. 2001. A human nuclease specific for G4 DNA. Proc. Natl. Acad. Sci. USA. 98:12444-12449.
47. Tashiro, J., K. Kinoshita, and T. Honjo. 2000. Palindromic but not G-rich sequences are targets of class switch recombination. Int. Immunol. 13:495-505.
48. Shinkura, R., M. Tian, M. Smith, K. Chua, Y. Fujiwara, and F.W. Alt. 2003. The influence of transcriptional orientation on endogenous switch region function. Nat. Immunol. 4:435-441.
49. Bardwell, P.D., C.J. Woo, K. Wei, Z. Li, A. Martin, S.Z. Sack, T. Parris, W. Edelmann, and M.D. Scharff. 2004. Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice. Nat. Immunol. 5:224-229.
50. Nelson, J.R., C.W. Lawrence, and D.C. Hinkle. 1996. Deoxycytidyl transferase activity of yeast REV1 protein. Nature. 382:729-731.
51. Lin, W., H. Xin, Y. Zhang, X. Wu, F. Yuan, and Z. Wang. 1999. The human REV1 gene codes for a DNA template-dependent dCMP transferase. Nucleic Acids Res. 27:4468-4475.
52. Sale, J.E., D.M. Calandrini, M. Takata, S. Takeda, and M.S. Neuberger. 2001. Ablation of XRCC2/3 transforms immunoglobulin V gene conversion into somatic hypermutation. Nature. 412:921-926.
53. Simpson, L.J., and J.E. Sale. 2003. Rev1 is essential for DNA damage tolerance and non-templated immunoglobulin gene mutation in a vertebrate cell line. EMBO J. 22:1654-1664.
54. Guo, C., P.L. Fischhaber, M.J. Luk-Paszyc, Y. Masuda, J. Zhou, K. Kamiya, C. Kisker, and E.C. Friedberg. 2003. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 122:6621-6630.
55. Cook, A.J.L., L. Oganesian, P. Harumal, A. Basten, R. Brink, and C.J. Jolly. 2003. Reduced switching in SCID B cells is associated with altered somatic mutation of recombined S regions. J. Immunol. 171:6556-6564.
56. Faili, A., S. Aoufouchi, S. Weller, F. Vuillier, A. Stary, A. Sarasin, C.-A. Reynaud, and J.-C. Weill. 2004. DNA polymerase η is involved in hypermutation occurring during immunoglobulin class switch recombination. J. Exp. Med. 199:265-270.