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Science 14 June 2002:
Vol. 296. no. 5575, pp. 2033 - 2036
DOI: 10.1126/science.1071556
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Reports

AID Enzyme-Induced Hypermutation in an Actively Transcribed Gene in Fibroblasts

Kiyotsugu Yoshikawa,12 Il-mi Okazaki,1 Tomonori Eto,1 Kazuo Kinoshita,1 Masamichi Muramatsu,1 Hitoshi Nagaoka,1 Tasuku Honjo1*

Activation-induced cytidine deaminase (AID), a putative RNA-editing enzyme, is indispensable for somatic hypermutation (SHM), class switch recombination, and gene conversion of immunoglobulin genes, which indicates a common molecular mechanism for these phenomena. Here we show that ectopic expression of AID alone can induce hypermutation in an artificial GFP substrate in NIH 3T3 murine fibroblast cells. The frequency of mutations was closely correlated with the level of transcription of the target gene, and the distribution of mutations in NIH 3T3 cells was similar to those of SHM in B lymphocytes. These results indicate that AID is sufficient for the generation of SHM in an actively transcribed gene in fibroblasts, as well as B cells, and that any of the required cofactors must be present in these fibroblasts.

1 Department of Medical Chemistry and Molecular Biology, Graduate School of Medicine; and
2 Radioisotope Research Center, Kyoto University, Yoshida Konoe-cho, Sakyo-ku, Kyoto, 606-8501, Japan.
*   To whom correspondence should be addressed. E-mail: honjo{at}mfour.med.kyoto-u.ac.jp

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J. Exp. Med. 202, 733-738
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J. Immunol. 174, 7787-7791
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Hypermutation Rate Normalized by Chronological Time.
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J. Immunol. 174, 5650-5654
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J. Exp. Med. 201, 1191-1196
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A target selection of somatic hypermutations is regulated similarly between T and B cells upon activation-induced cytidine deaminase expression.
A. Kotani, I.-m. Okazaki, M. Muramatsu, K. Kinoshita, N. A. Begum, T. Nakajima, H. Saito, and T. Honjo (2005)
PNAS 102, 4506-4511
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MSH2-MSH6 stimulates DNA polymerase {eta}, suggesting a role for A:T mutations in antibody genes.
T. M. Wilson, A. Vaisman, S. A. Martomo, P. Sullivan, L. Lan, F. Hanaoka, A. Yasui, R. Woodgate, and P. J. Gearhart (2005)
J. Exp. Med. 201, 637-645
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DNA cleavage in immunoglobulin somatic hypermutation depends on de novo protein synthesis but not on uracil DNA glycosylase.
H. Nagaoka, S. Ito, M. Muramatsu, M. Nakata, and T. Honjo (2005)
PNAS 102, 2022-2027
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Biochemical Analysis of Hypermutational Targeting by Wild Type and Mutant Activation-induced Cytidine Deaminase.
R. Bransteitter, P. Pham, P. Calabrese, and M. F. Goodman (2004)
J. Biol. Chem. 279, 51612-51621
   Abstract »    Full Text »    PDF »
Expression of the AID protein in normal and neoplastic B cells.
L. Pasqualucci, R. Guglielmino, J. Houldsworth, J. Mohr, S. Aoufouchi, R. Polakiewicz, R. S. K. Chaganti, and R. Dalla-Favera (2004)
Blood 104, 3318-3325
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Non-B DNA Conformations, Genomic Rearrangements, and Human Disease.
A. Bacolla and R. D. Wells (2004)
J. Biol. Chem. 279, 47411-47414
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Transcriptional Regulation of APOBEC3G, a Cytidine Deaminase That Hypermutates Human Immunodeficiency Virus.
K. M. Rose, M. Marin, S. L. Kozak, and D. Kabat (2004)
J. Biol. Chem. 279, 41744-41749
   Abstract »    Full Text »    PDF »
Directed molecular evolution by somatic hypermutation.
C. L. Wang, D. C. Yang, and M. Wabl (2004)
Protein Eng. Des. Sel. 17, 659-664
   Abstract »    Full Text »    PDF »
Endogenous Expression of Activation-Induced Cytidine Deaminase in Cell Line WEHI-231.
F. J. X. Spillmann and M. Wabl (2004)
J. Immunol. 173, 1858-1867
   Abstract »    Full Text »    PDF »
A Role for Msh6 But Not Msh3 in Somatic Hypermutation and Class Switch Recombination.
S. A. Martomo, W. W. Yang, and P. J. Gearhart (2004)
J. Exp. Med. 200, 61-68
   Abstract »    Full Text »    PDF »
Activation-induced Cytosine Deaminase (AID) Is Actively Exported out of the Nucleus but Retained by the Induction of DNA Breaks.
S. S. Brar, M. Watson, and M. Diaz (2004)
J. Biol. Chem. 279, 26395-26401
   Abstract »    Full Text »    PDF »
The structure of a yeast RNA-editing deaminase provides insight into the fold and function of activation-induced deaminase and APOBEC-1.
K. Xie, M. P. Sowden, G. S. C. Dance, A. T. Torelli, H. C. Smith, and J. E. Wedekind (2004)
PNAS 101, 8114-8119
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DNA Acrobats of the Ig Class Switch.
C. L. Wang and M. Wabl (2004)
J. Immunol. 172, 5815-5821
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Immunoglobulin class-switch recombination in mice devoid of any S{micro} tandem repeat.
A. A. Khamlichi, F. Glaudet, Z. Oruc, V. Denis, M. Le Bert, and M. Cogne (2004)
Blood 103, 3828-3836
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Genome-wide somatic hypermutation.
C. L. Wang, R. A. Harper, and M. Wabl (2004)
PNAS 101, 7352-7356
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Somatic Hypermutation Is Limited by CRM1-dependent Nuclear Export of Activation-induced Deaminase.
K. M. McBride, V. Barreto, A. R. Ramiro, P. Stavropoulos, and M. C. Nussenzweig (2004)
J. Exp. Med. 199, 1235-1244
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Rectification of age-related impairment in Ig gene hypermutation during a memory response.
S. Han, E. Marinova, and B. Zheng (2004)
Int. Immunol. 16, 525-532
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Recombinogenic Phenotype of Human Activation-Induced Cytosine Deaminase.
V. P. Poltoratsky, S. H. Wilson, T. A. Kunkel, and Y. I. Pavlov (2004)
J. Immunol. 172, 4308-4313
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Hepatitis C virus induces a mutator phenotype: Enhanced mutations of immunoglobulin and protooncogenes.
K. Machida, K. T.-N. Cheng, V. M.-H. Sung, S. Shimodaira, K. L. Lindsay, A. M. Levine, M.-Y. Lai, and M. M. C. Lai (2004)
PNAS 101, 4262-4267
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Cutting Edge: DGYW/WRCH Is a Better Predictor of Mutability at G:C Bases in Ig Hypermutation Than the Widely Accepted RGYW/WRCY Motif and Probably Reflects a Two-Step Activation-Induced Cytidine Deaminase-Triggered Process.
I. B. Rogozin and M. Diaz (2004)
J. Immunol. 172, 3382-3384
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Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NF{kappa}B.
F. Dedeoglu, B. Horwitz, J. Chaudhuri, F. W. Alt, and R. S. Geha (2004)
Int. Immunol. 16, 395-404
   Abstract »    Full Text »    PDF »
Mapping of a Functional Recombination Motif that Defines Isotype Specificity for {micro}->{gamma}3 Switch Recombination Implicates NF-{kappa}B p50 as the Isotype-specific Switching Factor.
A. L. Kenter, R. Wuerffel, C. Dominguez, A. Shanmugam, and H. Zhang (2004)
J. Exp. Med. 199, 617-627
   Abstract »    Full Text »    PDF »
DNA Substrate Length and Surrounding Sequence Affect the Activation-induced Deaminase Activity at Cytidine.
K. Yu, F.-T. Huang, and M. R. Lieber (2004)
J. Biol. Chem. 279, 6496-6500
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Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1.
S. Ito, H. Nagaoka, R. Shinkura, N. Begum, M. Muramatsu, M. Nakata, and T. Honjo (2004)
PNAS 101, 1975-1980
   Abstract »    Full Text »    PDF »
The generation of antibody diversity through somatic hypermutation and class switch recombination.
Z. Li, C. J. Woo, M. D. Iglesias-Ussel, D. Ronai, and M. D. Scharff (2004)
Genes & Dev. 18, 1-11
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The Balance Between Pax5 and Id2 Activities Is the Key to AID Gene Expression.
H. Gonda, M. Sugai, Y. Nambu, T. Katakai, Y. Agata, K. J. Mori, Y. Yokota, and A. Shimizu (2003)
J. Exp. Med. 198, 1427-1437
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Activation-induced cytidine deaminase in chronic lymphocytic leukemia B cells: expression as multiple forms in a dynamic, variably sized fraction of the clone.
E. Albesiano, B. T. Messmer, R. N. Damle, S. L. Allen, K. R. Rai, and N. Chiorazzi (2003)
Blood 102, 3333-3339
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RNA-editing cytidine deaminase Apobec-1 is unable to induce somatic hypermutation in mammalian cells.
T. Eto, K. Kinoshita, K. Yoshikawa, M. Muramatsu, and T. Honjo (2003)
PNAS 100, 12895-12898
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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 {micro} Region.
N. Catalan, F. Selz, K. Imai, P. Revy, A. Fischer, and A. Durandy (2003)
J. Immunol. 171, 2504-2509
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Expression of Activation-induced Cytidine Deaminase Is Confined to B-Cell Non-Hodgkin's Lymphomas of Germinal-Center Phenotype.
L. A. Smit, R. J. Bende, J. Aten, J. E. J. Guikema, W. M. Aarts, and C. J. M. van Noesel (2003)
Cancer Res. 63, 3894-3898
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Unmutated Immunoglobulin M Can Protect Mice from Death by Influenza Virus Infection.
Y. Harada, M. Muramatsu, T. Shibata, T. Honjo, and K. Kuroda (2003)
J. Exp. Med. 197, 1779-1785
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H2AX Is Required for Recombination Between Immunoglobulin Switch Regions but Not for Intra-Switch Region Recombination or Somatic Hypermutation.
B. Reina-San-Martin, S. Difilippantonio, L. Hanitsch, R. F. Masilamani, A. Nussenzweig, and M. C. Nussenzweig (2003)
J. Exp. Med. 197, 1767-1778
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Human activation-induced cytidine deaminase causes transcription-dependent, strand-biased C to U deaminations.
A. Sohail, J. Klapacz, M. Samaranayake, A. Ullah, and A. S. Bhagwat (2003)
Nucleic Acids Res. 31, 2990-2994
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High expression of activation-induced cytidine deaminase (AID) and splice variants is a distinctive feature of poor-prognosis chronic lymphocytic leukemia.
H. McCarthy, W. G. Wierda, L. L. Barron, C. C. Cromwell, J. Wang, K. R. Coombes, R. Rangel, K. S. J. Elenitoba-Johnson, M. J. Keating, and L. V. Abruzzo (2003)
Blood 101, 4903-4908
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Selective Inhibition of Class Switching to IgG and IgE by Recruitment of the HoxC4 and Oct-1 Homeodomain Proteins and Ku70/Ku86 to Newly Identified ATTT cis-Elements.
A. Schaffer, E. C. Kim, X. Wu, H. Zan, L. Testoni, S. Salamon, A. Cerutti, and P. Casali (2003)
J. Biol. Chem. 278, 23141-23150
   Abstract »    Full Text »    PDF »
AID Mediates Hypermutation by Deaminating Single Stranded DNA.
S. K. Dickerson, E. Market, E. Besmer, and F. N. Papavasiliou (2003)
J. Exp. Med. 197, 1291-1296
   Abstract »    Full Text »    PDF »
Chronic lymphocytic leukemia B cells expressing AID display dissociation between class switch recombination and somatic hypermutation.
P. Oppezzo, F. Vuillier, Y. Vasconcelos, G. Dumas, C. Magnac, B. Payelle-Brogard, O. Pritsch, and G. Dighiero (2003)
Blood 101, 4029-4032
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Constitutive Expression of AID Leads to Tumorigenesis.
I.-m. Okazaki, H. Hiai, N. Kakazu, S. Yamada, M. Muramatsu, K. Kinoshita, and T. Honjo (2003)
J. Exp. Med. 197, 1173-1181
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Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas.
J. Greeve, A. Philipsen, K. Krause, W. Klapper, K. Heidorn, B. E. Castle, J. Janda, K. B. Marcu, and R. Parwaresch (2003)
Blood 101, 3574-3580
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Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase.
R. Bransteitter, P. Pham, M. D. Scharff, and M. F. Goodman (2003)
PNAS 100, 4102-4107
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Somatic hypermutation of the B cell receptor genes B29 (Igbeta , CD79b) and mb1 (Igalpha , CD79a).
M. S. Gordon, C. M. Kanegai, J. R. Doerr, and R. Wall (2003)
PNAS 100, 4126-4131
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Inaugural Article: De novo protein synthesis is required for the activation-induced cytidine deaminase function in class-switch recombination.
T. Doi, K. Kinoshita, M. Ikegawa, M. Muramatsu, and T. Honjo (2003)
PNAS 100, 2634-2638
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Cutting Edge: The G-U Mismatch Glycosylase Methyl-CpG Binding Domain 4 Is Dispensable for Somatic Hypermutation and Class Switch Recombination.
P. D. Bardwell, A. Martin, E. Wong, Z. Li, W. Edelmann, and M. D. Scharff (2003)
J. Immunol. 170, 1620-1624
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Human Activation-Induced Cytidine Deaminase Is Induced by IL-4 and Negatively Regulated by CD45: Implication of CD45 as a Janus Kinase Phosphatase in Antibody Diversification.
C. Zhou, A. Saxon, and K. Zhang (2003)
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