Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand

Nature Immunology

Volumn 4, Issue 5, 2003, Pages 452-456

  Ramiro, Almudena R ^a   Stavropoulos, Pete ^a   Jankovic, Mila ^a   Nussenzweig, Michel C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTIDINE DEAMINASE; RNA POLYMERASE; SINGLE STRANDED DNA;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DEAMINATION; DNA MODIFICATION; DNA TEMPLATE; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENE TARGETING; GENETIC CODE; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN GENE; MOUSE; MUTATION RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SOMATIC HYPERMUTATION; TRANSCRIPTION INITIATION;

ANIMALS; BASE SEQUENCE; CYTIDINE; CYTIDINE DEAMINASE; DNA, BACTERIAL; DNA, SINGLE-STRANDED; ESCHERICHIA COLI; GENES, BACTERIAL; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; MODELS, IMMUNOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PLASMIDS; RECOMBINATION, GENETIC; RNA; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 0038293484     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni920     Document Type: Article

References (58)

1. Stavnezer, J. Antibody class switching. Adv. Immunol. 61, 79-146 (1996).
2. Matsuoka, M., Yoshida, K., Maeda, T., Usuda, S. & Sakano, H. Switch circular DNA formed in cytokine-treated mouse splenocytes: evidence for intramolecular DNA deletion in immunoglobulin class switching. Cell 62, 135-142 (1990).
3. Iwasato, T., Shimizu, A., Honjo, T. & Yamagishi, H. Circular DNA is excised by immunoglobulin class switch recombination. Cell 62, 143-149 (1990).
4. von Schwedler, U., Jack, H.M. & Wabl, M. Circular DNA is a product of the immunoglobulin class switch rearrangement. Nature 345, 452-456 (1990).
5. μ-S epsilon heavy chain class switching. Immunity 5, 319-330 (1996).
6. Manis, J.P. et al. Ku70 is required for late B cell development and immunoglobulin heavy chain class switching. J. Exp. Med. 187, 2081-2089 (1998).
7. Casellas, R. et al. Ku80 is required for immunoglobulin isotype switching. EMBO J. 17, 2404-2411 (1998).
8. Petersen, S. et al. AID is required to initiate NbsI/γ-H2AX focus formation and mutations at sites of class switching. Nature 414, 660-665 (2001).
9. Muramatsu, M. et al. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563 (2000).
10. Petersen-Mahrt, S.K., Harris, R.S. & Neuberger, M.S. AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418, 99-103 (2002).
11. Revy, P. et al. Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the hyper-IgM syndrome (HIGM2). Cell 102, 565-575 (2000).
12. Arakawa, H., Hauschild, J. & Buerstedde, J.M. Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science 29S, 1301-1306 (2002).
13. Harris, R.S., Sale, J.E., Petersen-Mahrt, S.K. & Neuberger, M.S. AID is essential for immunoglobulin V gene conversion in a cultured B cell line. Curr. Biol. 12, 435-438 (2002).
14. Okazaki, I.M., Kinoshita, K., Muramatsu, M., Yoshikawa, K. & Honjo, T. The AID enzyme induces class switch recombination in fibroblasts. Nature 416, 340-345 (2002).
15. Yoshikawa, K. et al. AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science 296, 2033-2036 (2002).
16. Martin, A. et al. Activation-induced cytidine deaminase turns on somatic hypermutation in hybridomas. Nature 415, 802-806 (2002).
17. Teng, B., Burant, C.F. & Davidson, N.O. Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260, 1816-1819 (1993).
18. Di Noia, J. & Neuberger, M.S. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419, 43-48 (2002).
19. Rada, C. et al. Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr. Biol. 12, 1748-1755 (2002).
20. Faili, A. et al. Induction of somatic hypermutation in immunoglobulin genes is dependent on DNA polymerase I. Nature 419, 944-947 (2002).
21. Zeng, X. et al. DNA polymerase E is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nat. Immunol. 2, 537-541 (2001).
22. Rogozin, I.B., Pavlov, Y.I., Bebenek, K., Matsuda, T. & Kunkel, T.A. Somatic mutation hotspots correlate with DNA polymerase E error spectrum. Nat. Immunol. 2, 530-536 (2001).
23. Zan, H. et al. The translesion DNA polymerase ζ plays a major role in Ig and Bcl-6 somatic hypermutation. Immunity 14, 643-653 (2001).
24. Wiesendanger, M., Kneitz, B., Edelmann, W. & Scharff, M.D. 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 (2000).
25. Schrader, C.E., Edelmann, W., Kucherlapati, R. & Stavnezer, J. Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes. J. Exp. Med. 190, 323-330 (1999).
26. Rada, C., Ehrenstein, M.R., Neuberger, M.S. & Milstein, C. Hot spot focusing of somatic hypermutation in MSH2-deficient mice suggests two stages of mutational targeting. Immunity 9, 135-141 (1998).
27. Kim, N., Bozek, G., Lo,J.C. & Storb, U. 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 (1999).
28. k transgenes show clonal recruitment of hypermutation: a role for both MAR and the enhancers. EMBO J. 16, 3987-3994 (1997).
29. Peters, A. & Storb, U. Somatic hypermutation of immunoglobulin genes is linked to transcription initiation. Immunity 4, 57-65 (1996).
30. Fukita, Y., Jacobs, H. & Rajewsky, K. Somatic hypermutation in the heavy chain locus correlates with transcription. Immunity 9, 105-114 (1998).
31. Stavnezer, J. Immunoglobulin class switching. Curr. Opin. Immunol. 8, 199-205 (1996).
32. Stavnezer-Nordgren, J. & Sirlin, S. Specificity of immunoglobulin heavy chain switch correlates with activity of germline heavy chain genes prior to switching. EMBO J. 5, 95-102 (1986).
33. H replacement by a LINE-I sequence and directed class switching. EMBO J. 5, 3259-3266 (1986 ).
34. Gu, H., Zou, Y.R. & Rajewsky, K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-IoxP-mediated gene targeting. Cell 73, 1155-1164 (1993).
35. Jung, S., Rajewsky, K. & Radbruch, A. Shutdown of class switch recombination by deletion of a switch region control element. Science 259, 984-987 (1993).
36. Pinaud, E. et al. Localization of the 3′ IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 15, 187-199 (2001).
37. Lee, C.G. et al. Quantitative regulation of class switch recombination by switch region transcription. J. Exp. Med. 194, 365-374 (2001).
38. Bachl, J., Carlson, C., Gray-Schopfer, V., Dessing, M. & Olsson, C. Increased transcription levels induce higher mutation rates in a hypermutating cell line. J. Immunol. 166, 5051-5057 (2001).
39. Betz, A.G. et al. Elements regulating somatic hypermutation of an immunoglobulin κ gene: critical role for the intron enhancer/matrix attachment region. Cell 77, 239-248 (1994).
40. γ2b promoter and exon. EMBO J. 12, 3529-3537 (1993).
41. Harris, R.S., Petersen-Mahrt, S.K. & Neuberger, M.S. RNA editing enzyme APOBEC I and some of its homologs can act as DNA mutators. Mol. Cell. 10, 1247-1253 (2002).
42. Kane, J.F. Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Curr. Opin. Biotechnol. 6, 494-500 (1995).
43. Beletskii, A. & Bhagwat, A.S. Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli. Proc. Natl. Acad. Sci. USA 93, 13919-13924 (1996).
44. Lebecque, S.G. & Gearhart, P.J. Boundaries of somatic mutation in rearranged immunoglobulin genes: 5′ boundary is near the promoter, and 3′ boundary is approximately I kb from V(D)J gene. J. Exp. Med. 172, 1717-1727 (1990).
45. Both, G.W., Taylor, L., Pollard, J.W. & Steele, E.J. Distribution of mutations around rearranged heavy-chain antibody variable-region genes. Mol. Cell. Biol. 10, 5187-5196 (1990).
46. Yelamos. J. et al. Targeting of non-Ig sequences in place of the V segment by somatic hypermutation. Nature 376, 225-229 (1995).
47. Azuma, T., Motoyama, N., Fields, L.E. & Loh, D.Y. Mutations of the chloramphenicol acetyl transferase transgene driven by the immunoglobulin promoter and intron enhancer. Int. Immunol. 5, 121-130 (1993).
48. Storb, U. & Stavnezer, J. Immunoglobulin genes: generating diversity with AID and UNG. Curr. Biol. 12, R725-R727 (2002).
49. Shen, H.M., Peters, A., Baron, B., Zhu, X. & Storb, U. Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes. Science 280, 1750-1752 (1998).
50. Pasqualucci, L. et al. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 412, 341-346 (2001).
51. Rogozin, I.B. & Kolchanov, N.A. Somatic hypermutagenesis in immunoglobulin genes. II. Influence of neighbouring base sequences on mutagenesis. Biochim. Biophys. Acta 1171, 11-18 (1992).
52. Kogoma, T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61, 212-238 (1997).
53. Tian, M. & Alt, F.W. Transcription-induced cleavage of immunoglobulin switch regions by nucleotide excision repair nucleases in vitro. J. Biol. Chem. 275, 24163-24172 (2000).
54. Korzheva, N. et al. A structural model of transcription elongation. Science 289, 619-625 (2000).
55. Darst, S.A. Bacterial RNA polymerase. Curr. Opin. Struct. Biol. 11, 155-162 (2001).
56. Wang, D. & Landick, R. Nuclease cleavage of the upstream half of the nontemplate strand DNA in an Escherichia coli transcription elongation complex causes upstream translocation and transcriptional arrest. J. Biol. Chem. 272, 5989-5994 (1997).
57. Artsimovitch, I. & Landick, R. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109, 193-203 (2002).
58. Espeli, O., Moulin, L. & Boccard, F. Transcription attenuation associated with bacterial repetitive extragenic BIME elements. J. Mol. Biol. 314, 375-386 (2001).