Homologous recombination contributes to the repair of zinc-finger-nuclease induced double strand breaks in pig primary cells and facilitates recombination with exogenous DNA

Journal of Biotechnology

Volumn 177, Issue 1, 2014, Pages 74-81

  Klymiuk, Nikolai ^a   Fezert, Pauline ^a   Wünsch, Annegret ^a   Kurome, Mayuko ^a   Kessler, Barbara ^a   Wolf, Eckhard ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Double strand break repair; Homologous recombination; Large animal models; Site specific nucleases; Somatic cells

Indexed keywords

CELLS; DNA; FREE RADICALS; GENES; JOINING; REPAIR; TOOLS; VECTORS; ZINC;

ANIMAL MODEL; DOUBLE STRAND BREAK REPAIR; HOMOLOGOUS RECOMBINATION; SITE-SPECIFIC; SOMATIC CELLS;

MOLECULAR BIOLOGY;

ZINC FINGER NUCLEASE; DEOXYRIBONUCLEASE; DNA; ZINC FINGER PROTEIN;

ALLELE; ANIMAL CELL; ARTICLE; CELL CLONE; CONTROLLED STUDY; DNA MODIFICATION; DNA RECOMBINATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENE TARGETING; GENETIC TRANSFECTION; HOMOLOGOUS RECOMBINATION; MALE; NONHUMAN; PLASMID; POINT MUTATION; PRIORITY JOURNAL; SOMATIC CELL; SWINE; ANIMAL; ANIMAL EMBRYO; CELL LINE; CELL NUCLEUS TRANSPLANTATION; CHEMISTRY; CYTOLOGY; DNA END JOINING REPAIR; GENETICS; METABOLISM; RECOMBINATION REPAIR;

ANIMALS; CELL LINE; DEOXYRIBONUCLEASES; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; EMBRYO, MAMMALIAN; MALE; NUCLEAR TRANSFER TECHNIQUES; RECOMBINATIONAL DNA REPAIR; SWINE; ZINC FINGERS;

EID: 84896598312     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2014.01.018     Document Type: Article

References (34)

1. Bedell V.M., Wang Y., Campbell J.M., Poshusta T.L., Starker C.G., Krug R.G., Tan W., Penheiter S.G., Ma A.C., Leung A.Y., Fahrenkrug S.C., Carlson D.F., Voytas D.F., Clark K.J., Essner J.J., Ekker S.C. In vivo genome editing using a high-efficiency TALEN system. Nature 2012, 491(7422):114-118.
2. Brandsma I., Gent D.C. Pathway choice in DNA double strand break repair: observations of a balancing act. Genome Integr. 2012, 3(1):9.
3. Chang C.J., Bouhassira E.E. Zinc-finger nuclease-mediated correction of alpha-thalassemia in iPS cells. Blood 2012, 120(19):3906-3914.
4. Chapman J.R., Taylor M.R., Boulton S.J. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 2012, 47(4):497-510.
5. Clark K.J., Carlson D.F., Fahrenkrug S.C. Pigs taking wing with transposons and recombinases. Genome Biol. 2007, 8(Suppl. 1):S13.
6. Collin J., Lako M. Concise review: putting a finger on stem cell biology: zinc finger nuclease-driven targeted genetic editing in human pluripotent stem cells. Stem Cells 2011, 29(7):1021-1033.
7. Duranthon V., Beaujean N., Brunner M., Odening K.E., Santos A.N., Kacskovics I., Hiripi L., Weinstein E.J., Bosze Z. On the emerging role of rabbit as human disease model and the instrumental role of novel transgenic tools. Transgenic Res. 2012, 21(4):699-713.
8. Ekker S.C. Zinc finger-based knockout punches for zebrafish genes. Zebrafish 2008, 5(2):121-123.
9. Gantz J.A., Palpant N.J., Welikson R.E., Hauschka S.D., Murry C.E., Laflamme M.A. Targeted genomic integration of a selectable floxed dual fluorescence reporter in human embryonic stem cells. PLoS ONE 2012, 7(10):e46971.
10. Grabarz A., Barascu A., Guirouilh-Barbat J., Lopez B.S. Initiation of DNA double strand break repair: signaling and single-stranded resection dictate the choice between homologous recombination, non-homologous end-joining and alternative end-joining. Am. J. Cancer Res. 2012, 2(3):249-268.
11. Hockemeyer D., Soldner F., Beard C., Gao Q., Mitalipova M., DeKelver R.C., Katibah G.E., Amora R., Boydston E.A., Zeitler B., Meng X., Miller J.C., Zhang L., Rebar E.J., Gregory P.D., Urnov F.D., Jaenisch R. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 2009, 27(9):851-857.
12. Klymiuk N., Aigner B., Brem G., Wolf E. Genetic modification of pigs as organ donors for xenotransplantation. Mol. Reprod. Dev. 2010, 77(3):209-221.
13. Klymiuk N., Blutke A., Graf A., Krause S., Burkhardt K., Wuensch A., Krebs S., Kessler B., Zakhartchenko V., Kurome M., Kemter E., Nagashima H., Schoser B., Herbach N., Blum H., Wanke R., Aartsma-Rus A., Thirion C., Lochmuller H., Walter M.C., Wolf E. Dystrophin-deficient pigs provide new insights into the hierarchy of physiological derangements of dystrophic muscle. Hum. Mol. Genet. 2013, 22:4368-4382.
14. Klymiuk N., Mundhenk L., Kraehe K., Wuensch A., Plog S., Emrich D., Langenmayer M.C., Stehr M., Holzinger A., Kroner C., Richter A., Kessler B., Kurome M., Eddicks M., Nagashima H., Heinritzi K., Gruber A.D., Wolf E. Sequential targeting of CFTR by BAC vectors generates a novel pig model of cystic fibrosis. J. Mol. Med. (Berl.) 2012, 90(5):597-608.
15. Kurome M., Ueda H., Tomii R., Naruse K., Nagashima H. Production of transgenic-clone pigs by the combination of ICSI-mediated gene transfer with somatic cell nuclear transfer. Transgenic Res. 2006, 15(2):229-240.
16. Meyer M., de Angelis M.H., Wurst W., Kuhn R. Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(34):15022-15026.
17. Mladenov E., Iliakis G. Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat. Res. 2011, 711(1-2):61-72.
18. Moehle E.A., Rock J.M., Lee Y.L., Jouvenot Y., DeKelver R.C., Gregory P.D., Urnov F.D., Holmes M.C. Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(9):3055-3060.
19. Nagashima H., Kashiwazaki N., Ashman R.J., Grupen C.G., Nottle M.B. Cryopreservation of porcine embryos. Nature 1995, 374(6521):416.
20. Ou H., Huang Y., Ma Q., Ren Z., Huang S., Zeng F., Zeng Y. A highly efficient site-specific integration strategy using combination of homologous recombination and the PhiC31 integrase. J. Biotechnol. 2013, 167(4):427-432. pii:S0168-1656(13)00340-4.
21. Perez-Pinera P., Ousterout D.G., Brown M.T., Gersbach C.A. Gene targeting to the ROSA26 locus directed by engineered zinc finger nucleases. Nucleic Acids Res. 2012, 40(8):3741-3752.
22. Porteus M.H. Mammalian gene targeting with designed zinc finger nucleases. Mol. Ther. 2006, 13(2):438-446.
23. Richter A., Kurome M., Kessler B., Zakhartchenko V., Klymiuk N., Nagashima H., Wolf E., Wuensch A. Potential of primary kidney cells for somatic cell nuclear transfer mediated transgenesis in pig. BMC Biotechnol. 2012, 12:84. pii:1472-6750-12-84. 10.1186/1472-6750-12-84.
24. Strande N.T., Waters C.A., Ramsden D.A. Resolution of complex ends by nonhomologous end joining - better to be lucky than good?. Genome Integr. 2012, 3(1):10. pii:2041-9414-3-10.
25. Sun N., Abil Z., Zhao H. Recent advances in targeted genome engineering in mammalian systems. Biotechnol. J. 2012, 7(9):1074-1087.
26. Tan W., Carlson D.F., Lancto C.A., Garbe J.R., Webster D.A., Hackett P.B., Fahrenkrug S.C. Efficient nonmeiotic allele introgression in livestock using custom endonucleases. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(41):16526-16531.
27. Tan W.S., Carlson D.F., Walton M.W., Fahrenkrug S.C., Hackett P.B. Precision editing of large animal genomes. Adv. Genet. 2012, 80:37-97. 10.1016/B978-0-12-404742-6.00002-8.
28. Thompson L.H. Recognition, signaling, and repair of DNA double-strand breaks produced by ionizing radiation in mammalian cells: the molecular choreography. Mutat. Res. 2012, 751(2):158-246.
29. Toscano M.G., Anderson P., Munoz P., Lucena G., Cobo M., Benabdellah K., Gregory P.D., Holmes M.C., Martin F. Use of zinc-finger nucleases to knock out the WAS gene in K562 cells: a human cellular model for Wiskott-Aldrich syndrome. Dis. Models Mech. 2013, 6(2):544-554.
30. Valenzuela D.M., Murphy A.J., Frendewey D., Gale N.W., Economides A.N., Auerbach W., Poueymirou W.T., Adams N.C., Rojas J., Yasenchak J., Chernomorsky R., Boucher M., Elsasser A.L., Esau L., Zheng J., Griffiths J.A., Wang X., Su H., Xue Y., Dominguez M.G., Noguera I., Torres R., Macdonald L.E., Stewart A.F., DeChiara T.M., Yancopoulos G.D. High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat. Biotechnol. 2003, 21(6):652-659.
31. Watanabe T., Ochiai H., Sakuma T., Horch H.W., Hamaguchi N., Nakamura T., Bando T., Ohuchi H., Yamamoto T., Noji S., Mito T. Non-transgenic genome modifications in a hemimetabolous insect using zinc-finger and TAL effector nucleases. Nat. Commun. 2012, 3:1017.
32. Whyte J.J., Prather R.S. Genetic modifications of pigs for medicine and agriculture. Mol. Reprod. Dev. 2011, 78(10-11):879-891.
33. Yano A., Guyomard R., Nicol B., Jouanno E., Quillet E., Klopp C., Cabau C., Bouchez O., Fostier A., Guiguen Y. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr. Biol. 2012, 22(15):1423-1428.
34. Young J.J., Harland R.M. Targeted gene disruption with engineered zinc-finger nucleases (ZFNs). Methods Mol. Biol. 2012, 917:129-141.