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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. 201, 637-645
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H. Nagaoka, S. Ito, M. Muramatsu, M. Nakata, and T. Honjo (2005)
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L. Pasqualucci, R. Guglielmino, J. Houldsworth, J. Mohr, S. Aoufouchi, R. Polakiewicz, R. S. K. Chaganti, and R. Dalla-Favera (2004)
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J. Biol. Chem. 279, 47411-47414
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J. Biol. Chem. 279, 41744-41749
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Directed molecular evolution by somatic hypermutation.
C. L. Wang, D. C. Yang, and M. Wabl (2004)
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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 »
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S. A. Martomo, W. W. Yang, and P. J. Gearhart (2004)
J. Exp. Med. 200, 61-68
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S. S. Brar, M. Watson, and M. Diaz (2004)
J. Biol. Chem. 279, 26395-26401
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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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Blood 103, 3828-3836
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Genome-wide somatic hypermutation.
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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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J. Immunol. 172, 3382-3384
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Int. Immunol. 16, 395-404
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J. Exp. Med. 199, 617-627
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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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   Abstract »    Full Text »    PDF »
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J. Exp. Med. 198, 1427-1437
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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)
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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.
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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)
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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)
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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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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
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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
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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.
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J. Immunol. 170, 1620-1624
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