RAD51 paralogs promote homology-directed repair at diversifying immunoglobulin V regions

Ordinario, Ellen C.; Yabuki, Munehisa; Handa, Priya; Cummings, W. Jason; Maizels, Nancy

doi:10.1186/1471-2199-10-98

Title: RAD51 paralogs promote homology-directed repair at diversifying immunoglobulin V regions

Journal Article · 27 October 2009 · BMC Molecular Biology

DOI: https://doi.org/10.1186/1471-2199-10-98 · OSTI ID:1626498

Ordinario, Ellen C. ^[1]; Yabuki, Munehisa ^[2]; Handa, Priya ^[2]; Cummings, W. Jason ^[2]; Maizels, Nancy ^[3]

Univ. of Washington, Seattle, WA (United States). School of Medicine. Dept. of Biochemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; DOE/OSTI
Univ. of Washington, Seattle, WA (United States). Dept. of Immunology
Univ. of Washington, Seattle, WA (United States). School of Medicine. Dept. of Biochemistry; Univ. of Washington, Seattle, WA (United States). Dept. of Immunology

Background: Gene conversion depends upon the same factors that carry out more general process of homologous recombination, including homologous gene targeting and recombinational repair. Among these are the RAD51 paralogs, conserved factors related to the key recombination factor, RAD51. In chicken and other fowl, gene conversion (templated mutation) diversifies immunoglobulin variable region sequences. This allows gene conversion and recombinational repair to be studied using the chicken DT40 B cell line, which carries out constitutive gene conversion and provides a robust and physiological model for homology-directed repair in vertebrate cells. Results: We show that DT40 contains constitutive nuclear foci of the repair factors RAD51D and XRCC2, consistent with activated homologous recombination. Single-cell imaging of a DT40 derivative in which the rearranged and diversifying immunoglobulin λ_R light chain gene is tagged with polymerized lactose operator, DT40 PolyLacO-λ_R, showed that RAD51D and XRCC2 localize to the diversifying λ_R gene. Colocalizations correlate both functionally and physically with active immunoglobulin gene conversion. Ectopic expression of either RAD51D or XRCC2 accelerated the clonal rate of gene conversion, and conversion tracts were significantly longer in RAD51D than XRCC2 transfectants. Conclusion: These results demonstrate direct functions of RAD51D and XRCC2 in immunoglobulin gene conversion, and also suggest that modulation of levels of repair factors may be a useful strategy to promote gene correction in other cell types.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626498

Journal Information:: BMC Molecular Biology, Journal Name: BMC Molecular Biology Journal Issue: 1 Vol. 10; ISSN 1471-2199

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Brca1 in immunoglobulin gene conversion and somatic hypermutation Longerich, Simonne; Orelli, Brian J.; Martin, Richard W. DNA Repair, Vol. 7, Issue 2 https://doi.org/10.1016/j.dnarep.2007.10.002	journal	February 2008
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AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification Petersen-Mahrt, Svend K.; Harris, Reuben S.; Neuberger, Michael S. Nature, Vol. 418, Issue 6893 https://doi.org/10.1038/nature00862	journal	July 2002
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Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells Tauchi, Hiroshi; Kobayashi, Junya; Morishima, Ken-ichi Nature, Vol. 420, Issue 6911 https://doi.org/10.1038/nature01125	journal	November 2002
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Computational redesign of endonuclease DNA binding and cleavage specificity Ashworth, Justin; Havranek, James J.; Duarte, Carlos M. Nature, Vol. 441, Issue 7093 https://doi.org/10.1038/nature04818	journal	June 2006
Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases Szczepek, Michal; Brondani, Vincent; Büchel, Janine Nature Biotechnology, Vol. 25, Issue 7 https://doi.org/10.1038/nbt1317	journal	July 2007
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Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand Ramiro, Almudena R.; Stavropoulos, Pete; Jankovic, Mila Nature Immunology, Vol. 4, Issue 5 https://doi.org/10.1038/ni920	journal	April 2003
Human uracil–DNA glycosylase deficiency associated with profoundly impaired immunoglobulin class-switch recombination Imai, Kohsuke; Slupphaug, Geir; Lee, Wen-I Nature Immunology, Vol. 4, Issue 10 https://doi.org/10.1038/ni974	journal	September 2003
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Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells Yamaguchi-Iwai, Y. The EMBO Journal, Vol. 18, Issue 23 https://doi.org/10.1093/emboj/18.23.6619	journal	December 1999
Differential effects of Rad52p overexpression on gene targeting and extrachromosomal homologous recombination in a human cell line Yanez, R. J. Nucleic Acids Research, Vol. 30, Issue 3 https://doi.org/10.1093/nar/30.3.740	journal	February 2002
Potentiation of gene targeting in human cells by expression of Saccharomyces cerevisiae Rad52 Di Primio, C. Nucleic Acids Research, Vol. 33, Issue 14 https://doi.org/10.1093/nar/gki778	journal	August 2005
Homologous recombination is required for AAV-mediated gene targeting Vasileva, A. Nucleic Acids Research, Vol. 34, Issue 11 https://doi.org/10.1093/nar/gkl455	journal	June 2006
Impact of non-homologous end-joining deficiency on random and targeted DNA integration: implications for gene targeting Iiizumi, Susumu; Kurosawa, Aya; So, Sairei Nucleic Acids Research, Vol. 36, Issue 19 https://doi.org/10.1093/nar/gkn649	journal	October 2008
Chicken IgL variable region gene conversions display pseudogene donor preference and 5' to 3' polarity. McCormack, W. T.; Thompson, C. B. Genes & Development, Vol. 4, Issue 4 https://doi.org/10.1101/gad.4.4.548	journal	April 1990
Enhanced gene targeting efficiency by siRNA that silences the expression of the Bloom syndrome gene in human cells So, Sairei; Nomura, Yuji; Adachi, Noritaka Genes to Cells, Vol. 11, Issue 4 https://doi.org/10.1111/j.1365-2443.2006.00944.x	journal	April 2006
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Requirement of the Activation-Induced Deaminase ( AID ) Gene for Immunoglobulin Gene Conversion Arakawa, Hiroshi; Hauschild, Jessica; Buerstedde, Jean-Marie Science, Vol. 295, Issue 5558 https://doi.org/10.1126/science.1067308	journal	February 2002
The Rad51 Paralog Rad51B Promotes Homologous Recombinational Repair Takata, M.; Sasaki, M. S.; Sonoda, E. Molecular and Cellular Biology, Vol. 20, Issue 17 https://doi.org/10.1128/MCB.20.17.6476-6482.2000	journal	September 2000
Chromosome Instability and Defective Recombinational Repair in Knockout Mutants of the Five Rad51 Paralogs Takata, M.; Sasaki, M. S.; Tachiiri, S. Molecular and Cellular Biology, Vol. 21, Issue 8 https://doi.org/10.1128/MCB.21.8.2858-2866.2001	journal	April 2001
Similar Effects of Brca2 Truncation and Rad51 Paralog Deficiency on Immunoglobulin V Gene Diversification in DT40 Cells Support an Early Role for Rad51 Paralogs in Homologous Recombination Hatanaka, Atsushi; Yamazoe, Mitsuyoshi; Sale, Julian E. Molecular and Cellular Biology, Vol. 25, Issue 3 https://doi.org/10.1128/MCB.25.3.1124-1134.2005	journal	February 2005
Immunoglobulin Gene Diversification Maizels, Nancy Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.110544	journal	December 2005
Activation-Induced Cytidine Deaminase Initiates Immunoglobulin Gene Conversion and Hypermutation by a Common Intermediate Arakawa, Hiroshi; Saribasak, Huseyin; Buerstedde, Jean-Marie PLoS Biology, Vol. 2, Issue 7 https://doi.org/10.1371/journal.pbio.0020179	journal	July 2004
Chromatin Structure Regulates Gene Conversion Cummings, W. Jason; Yabuki, Munehisa; Ordinario, Ellen C. PLoS Biology, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pbio.0050246	journal	September 2007
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Genetic Evidence for Single-Strand Lesions Initiating Nbs1-Dependent Homologous Recombination in Diversification of Ig V in Chicken B Lymphocytes Nakahara, Makoto; Sonoda, Eiichiro; Nojima, Kuniharu PLoS Genetics, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pgen.1000356	journal	January 2009
Temporal Regulation of Ig Gene Diversification Revealed by Single-Cell Imaging Ordinario, Ellen C.; Yabuki, Munehisa; Larson, Ryan P. The Journal of Immunology, Vol. 183, Issue 7 https://doi.org/10.4049/jimmunol.0900673	journal	September 2009
Uracil DNA Glycosylase Disruption Blocks Ig Gene Conversion and Induces Transition Mutations Saribasak, Huseyin; Saribasak, Nesibe Nur; Ipek, Fatih M. The Journal of Immunology, Vol. 176, Issue 1 https://doi.org/10.4049/jimmunol.176.1.365	journal	December 2005
E2A Acts in cis in G₁ Phase of Cell Cycle to Promote Ig Gene Diversification Yabuki, Munehisa; Ordinario, Ellen C.; Cummings, W. Jason The Journal of Immunology, Vol. 182, Issue 1 https://doi.org/10.4049/jimmunol.182.1.408	journal	December 2008

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