Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2011, Article ID 947212, 14 pages
http://dx.doi.org/10.4061/2011/947212
Research Article

Identification of Genes Regulating Gene Targeting by a High-Throughput Screening Approach

1Cellectis SA, 102 Avenue Gaston Roussel, 93340 Romainville Cedex, France
2Cellectis Bioresearch, 102 Avenue Gaston Roussel, 93340 Romainville Cedex, France

Received 25 November 2010; Accepted 23 January 2011

Academic Editor: Emery H. Bresnick

Copyright © 2011 Fabien Delacôte et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. S. Symington, “Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair,” Microbiology and Molecular Biology Reviews, vol. 66, no. 4, pp. 630–670, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. R. H. Schiestl, J. Zhu, and T. D. Petes, “Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae,” Molecular and Cellular Biology, vol. 14, no. 7, pp. 4493–4500, 1994. View at Google Scholar · View at Scopus
  3. O. Bezzubova, A. Silbergleit, Y. Yamaguchi-Iwai, S. Takeda, and J. M. Buerstedde, “Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line,” Cell, vol. 89, no. 2, pp. 185–193, 1997. View at Google Scholar · View at Scopus
  4. Y. Yamaguchi-Iwai, E. Sonoda, J. M. Buerstedde et al., “Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52,” Molecular and Cellular Biology, vol. 18, no. 11, pp. 6430–6435, 1998. View at Google Scholar · View at Scopus
  5. C. Morrison, A. Shinohara, E. Sonoda et al., “The essential functions of human Rad51 are independent of ATP hydrolysis,” Molecular and Cellular Biology, vol. 19, no. 10, pp. 6891–6897, 1999. View at Google Scholar · View at Scopus
  6. M. Takata, M. S. Sasaki, E. Sonoda et al., “The Rad51 paralog Rad51B promotes homologous recombinational repair,” Molecular and Cellular Biology, vol. 20, no. 17, pp. 6476–6482, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Takata, M. S. Sasaki, S. Tachiiri et al., “Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs,” Molecular and Cellular Biology, vol. 21, no. 8, pp. 2858–2866, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. M. E. Moynahan, A. J. Pierce, and M. Jasin, “BRCA2 is required for homology-directed repair of chromosomal breaks,” Molecular Cell, vol. 7, no. 2, pp. 263–272, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. M. E. Moynahan, J. W. Chiu, B. H. Koller, and M. Jasint, “Brca1 controls homology-directed DNA repair,” Molecular Cell, vol. 4, no. 4, pp. 511–518, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Essers, R. W. Hendriks, S. M. A. Swagemakers et al., “Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination,” Cell, vol. 89, no. 2, pp. 195–204, 1997. View at Google Scholar · View at Scopus
  11. L. J. Niedernhofer, J. Essers, G. Weeda et al., “The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells,” EMBO Journal, vol. 20, no. 22, pp. 6540–6549, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. J. E. Haber, “Alternative endings,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 2, pp. 405–406, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. J. Guirouilh-Barbat, S. Huck, P. Bertrand et al., “Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells,” Molecular Cell, vol. 14, no. 5, pp. 611–623, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. J. Guirouilh-Barbat, E. Rass, I. Plo, P. Bertrand, and B. S. Lopez, “Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 52, pp. 20902–20907, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. N. S. Verkaik, R. E. E. Esveldt-van Lange, D. Van Heemst et al., “Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells,” European Journal of Immunology, vol. 32, no. 3, pp. 701–709, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. E. B. Kabotyanski, L. Gomelsky, J. O. Han, T. D. Stamato, and D. B. Roth, “Double-strand break repair in Ku86- and XRCC4-deficient cells,” Nucleic Acids Research, vol. 26, no. 23, pp. 5333–5342, 1998. View at Google Scholar · View at Scopus
  17. A. A. Hamilton and J. Thacker, “Gene recombination in X-ray-sensitive hamster cells,” Molecular and Cellular Biology, vol. 7, no. 4, pp. 1409–1414, 1987. View at Google Scholar · View at Scopus
  18. P. A. Jeggo and J. Smith-Ravin, “Decreased stable transfection frequencies of six X-ray-sensitive CHO strains, all members of the xrs complementation group,” Mutation Research, vol. 218, no. 2, pp. 75–86, 1989. View at Google Scholar · View at Scopus
  19. K. Sado, D. Ayusawa, A. Enomoto et al., “Identification of a Mutated DNA Ligase IV Gene in the X-ray-hypersensitive Mutant SX10 of Mouse FM3A Cells,” Journal of Biological Chemistry, vol. 276, no. 13, pp. 9742–9748, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. J. Friesner and A. B. Britt, “Ku80- and DNA ligase IV-deficient plants are sensitive to ionizing radiation and defective in T-DNA integration,” Plant Journal, vol. 34, no. 4, pp. 427–440, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. F. Pâques and P. Duchateau, “Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy,” Current Gene Therapy, vol. 7, no. 1, pp. 49–66, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. J. A. Aten, J. Stap, P. M. Krawczyk et al., “Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains,” Science, vol. 303, no. 5654, pp. 92–95, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  23. S. L. Gasior, H. Olivares, UY. Ear, D. M. Hari, R. Weichselbaum, and D. K. Bishop, “Assembly of RecA-like recombinases: distinct roles for mediator proteins in mitosis and meiosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 15, pp. 8411–8418, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. J. M. Hinz, N. A. Yamada, E. P. Salazar, R. S. Tebbs, and L. H. Thompson, “Influence of double-strand-break repair pathways on radiosensitivity throughout the cell cycle in CHO cells,” DNA Repair, vol. 4, no. 7, pp. 782–792, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. J. S. Kim, T. B. Krasieva, H. Kurumizaka, D. J. Chen, A. M. R. Taylor, and K. Yokomori, “Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells,” Journal of Cell Biology, vol. 170, no. 3, pp. 341–347, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. K. Rothkamm, I. Krüger, L. H. Thompson, and M. Löbrich, “Pathways of DNA double-strand break repair during the mammalian cell cycle,” Molecular and Cellular Biology, vol. 23, no. 16, pp. 5706–5715, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. Y. Saintigny, F. Delacôte, D. Boucher, D. Averbeck, and B. S. Lopez, “XRCC4 in G1 suppresses homologous recombination in S/G2, in G1 checkpoint-defective cells,” Oncogene, vol. 26, no. 19, pp. 2769–2780, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. M. Takata, M. S. Sasaki, E. Sonoda et al., “Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells,” EMBO Journal, vol. 17, no. 18, pp. 5497–5508, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. F. Delacôte and B. S. Lopez, “Importance of the cell cycle phase for the choice of the appropriate DSB repair pathway, for genome stability maintenance: the trans-S double-strand break repair model,” Cell Cycle, vol. 7, no. 1, pp. 33–38, 2008. View at Google Scholar · View at Scopus
  30. K. D. Hanson and J. M. Sedivy, “Analysis of biological selections for high-efficiency gene targeting,” Molecular and Cellular Biology, vol. 15, no. 1, pp. 45–51, 1995. View at Google Scholar · View at Scopus
  31. S. L. Mansour, K. R. Thomas, and M. R. Capecchi, “Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes,” Nature, vol. 336, no. 6197, pp. 348–352, 1988. View at Google Scholar · View at Scopus
  32. B. S. Chevalier and B. L. Stoddard, “Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility,” Nucleic Acids Research, vol. 29, no. 18, pp. 3757–3774, 2001. View at Google Scholar · View at Scopus
  33. B. L. Stoddard, “Homing endonuclease structure and function,” Quarterly Reviews of Biophysics, vol. 38, no. 1, pp. 49–95, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. J. Smith, M. Bibikova, F. G. Whitby, A. R. Reddy, S. Chandrasegaran, and D. Carroll, “Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains,” Nucleic Acids Research, vol. 28, no. 17, pp. 3361–3369, 2000. View at Google Scholar · View at Scopus
  35. M. H. Porteus and D. Carroll, “Gene targeting using zinc finger nucleases,” Nature Biotechnology, vol. 23, no. 8, pp. 967–973, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. Y. G. Kim, J. Cha, and S. Chandrasegaran, “Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 3, pp. 1156–1160, 1996. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Lombardo, P. Genovese, C. M. Beausejour et al., “Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery,” Nature Biotechnology, vol. 25, no. 11, pp. 1298–1306, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. M. L. Maeder, S. Thibodeau-Beganny, A. Osiak et al., “Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification,” Molecular Cell, vol. 31, no. 2, pp. 294–301, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. F. D. Urnov, J. C. Miller, YA. L. Lee et al., “Highly efficient endogenous human gene correction using designed zinc-finger nucleases,” Nature, vol. 435, no. 7042, pp. 646–651, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. J. Zou, M. L. Maeder, P. Mali et al., “Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells,” Cell Stem Cell, vol. 5, no. 1, pp. 97–110, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. R. C. DeKelver, V. M. Choi, E. A. Moehle et al., “Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome,” Genome Research, vol. 20, no. 8, pp. 1133–1142, 2010. View at Publisher · View at Google Scholar
  42. R. J. Yáñez and A. C. G. Porter, “Differential effects of Rad52p overexpression on gene targeting and extrachromosomal homologous recombination in a human cell line,” Nucleic Acids Research, vol. 30, no. 3, pp. 740–748, 2002. View at Google Scholar · View at Scopus
  43. R. J. Yáñez and A. C. G. Porter, “Gene targeting is enhanced in human cells overexpressing hRAD51,” Gene Therapy, vol. 6, no. 7, pp. 1282–1290, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. O. G. Shcherbakova, V. A. Lanzov, H. Ogawa, and M. V. Filatov, “Overexpression of bacterial RecA protein stimulates homologous recombination in somatic mammalian cells,” Mutation Research, vol. 459, no. 1, pp. 65–71, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Shaked, C. Melamed-Bessudo, and A. A. Levy, “High-frequency gene targeting in Arabidopsis plants expressing the yeast RAD54 gene,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 34, pp. 12265–12269, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. C. Di Primio, A. Galli, T. Cervelli, M. Zoppè, and G. Rainaldi, “Potentiation of gene targeting in human cells by expression of Saccharomyces cerevisiae Rad52,” Nucleic Acids Research, vol. 33, no. 14, pp. 4639–4648, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. A. J. Pierce, P. Hu, M. Han, N. Ellis, and M. Jasin, “Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells,” Genes and Development, vol. 15, no. 24, pp. 3237–3242, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. J. Domínguez-Bendala, M. Masutani, and J. McWhir, “Down-regulation of PARP-1, but not of Ku80 or DNA-PK, results in higher gene targeting efficiency,” Cell Biology International, vol. 30, no. 4, pp. 389–393, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. L. R. Bertolini, M. Bertolini, E. A. Maga, K. R. Madden, and J. D. Murray, “Increased gene targeting in Ku70 and Xrcc4 transiently deficient human somatic cells,” Molecular Biotechnology, vol. 41, no. 2, pp. 106–114, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  50. S. Lambert and B. S. Lopez, “Characterization of mammalian RAD51 double strand break repair using non-lethal dominant-negative forms,” EMBO Journal, vol. 19, no. 12, pp. 3090–3099, 2000. View at Google Scholar · View at Scopus
  51. F. Delacôte, M. Han, T. D. Stamato, M. Jasin, and B. S. Lopez, “An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells,” Nucleic Acids Research, vol. 30, no. 15, pp. 3454–3463, 2002. View at Google Scholar · View at Scopus
  52. S. R. Bartz, Z. Zhang, J. Burchard et al., “Small interfering RNA screens reveal enhanced cisplatin cytotoxicity in tumor cells having both BRCA network and TP53 disruptions,” Molecular and Cellular Biology, vol. 26, no. 24, pp. 9377–9386, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. C. J. Lord, S. McDonald, S. Swift, N. C. Turner, and A. Ashworth, “A high-throughput RNA interference screen for DNA repair determinants of PARP inhibitor sensitivity,” DNA Repair, vol. 7, no. 12, pp. 2010–2019, 2008. View at Publisher · View at Google Scholar · View at PubMed
  54. M. Słabicki, M. Theis, D. B. Krastev et al., “A genome-scale DNA repair RNAi screen identifies SPG48 as a novel gene associated with hereditary spastic paraplegia,” PLoS Biology, vol. 8, no. 6, Article ID e1000408, 2010. View at Publisher · View at Google Scholar
  55. S. Grizot, J. Smith, F. Daboussi et al., “Efficient targeting of a SCID gene by an engineered single-chain homing endonuclease,” Nucleic Acids Research, vol. 37, no. 16, Article ID gkp548, pp. 5405–5419, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Fujita, S. Watanabe, T. Ichimura et al., “MCAF mediates MBD1-dependent transcriptional repression,” Molecular and Cellular Biology, vol. 23, no. 8, pp. 2834–2843, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Wang, W. An, R. Cao et al., “mAM facilitates conversion by ESET of dimethyl to trimethyl lysine 9 of histone H3 to cause transcriptional repression,” Molecular Cell, vol. 12, no. 2, pp. 475–487, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Ichimura, S. Watanabe, Y. Sakamoto, T. Aoto, N. Pujita, and M. Nakao, “Transcriptional repression and heterochromatin formation by MBD1 and MCAF/AM family proteins,” Journal of Biological Chemistry, vol. 280, no. 14, pp. 13928–13935, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. A. K. Ghosh and J. Varga, “The transcriptional coactivator and acetyltransferase p300 in fibroblast biology and fibrosis,” Journal of Cellular Physiology, vol. 213, no. 3, pp. 663–671, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. S. Arnould, C. Perez, J. P. Cabaniols et al., “Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells,” Journal of Molecular Biology, vol. 371, no. 1, pp. 49–65, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. R. Terada, H. Urawa, Y. Inagaki, K. Tsugane, and S. Iida, “Efficient gene targeting by homologous recombination in rice,” Nature Biotechnology, vol. 20, no. 10, pp. 1030–1034, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. D. Hockemeyer, F. Soldner, C. Beard et al., “Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases,” Nature Biotechnology, vol. 27, no. 9, pp. 851–857, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. V. V. Ogryzko, R. L. Schiltz, V. Russanova, B. H. Howard, and Y. Nakatani, “The transcriptional coactivators p300 and CBP are histone acetyltransferases,” Cell, vol. 87, no. 5, pp. 953–959, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. Z. Arany, W. R. Sellers, D. M. Livingston, and R. Eckner, “E1A-associated p300 and CREB-associated CBP belong to a conserved family of coactivators,” Cell, vol. 77, no. 6, pp. 799–800, 1994. View at Publisher · View at Google Scholar · View at Scopus