Repair at single targeted DNA double-strand breaks in pluripotent and differentiated human cells

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Fung, Hua ^a   Weinstock, David M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASTOGEN; ZINC FINGER PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ASSAY; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINE; CONTROLLED STUDY; DNA MODIFICATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENVIRONMENTAL FACTOR; EX VIVO STUDY; GENETIC MANIPULATION; GENOME; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MAMMAL CELL; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PROGENY; REPORTER GENE; SOMATIC CELL; BINDING SITE; CELL CULTURE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL STRAIN HCT116; CELL STRAIN HEK293; COMET ASSAY; DNA DAMAGE; EMBRYONIC STEM CELL; FLUORESCENCE MICROSCOPY; GENETIC RECOMBINATION; GENETICS; HELA CELL; METABOLISM; METHODOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

MAMMALIA; MURINAE;

ASTROCYTES; BINDING SITES; BLOTTING, WESTERN; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELLS, CULTURED; COMET ASSAY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; EMBRYONIC STEM CELLS; G0 PHASE; G1 PHASE; GREEN FLUORESCENT PROTEINS; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; PLURIPOTENT STEM CELLS; POLYMERASE CHAIN REACTION; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC;

EID: 79957501495     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0020514     Document Type: Article

References (49)

1. Dudley DD, Chaudhuri J, Bassing CH, Alt FW, (2005) Mechanism and Control of V(D)J Recombination versus Class Switch Recombination: Similarities and Differences. Adv Immunol 86: 43-112.
2. Lieber MR, Ma Y, Pannicke U, Schwarz K, (2003) Mechanism and regulation of human non-homologous DNA end-joining. Nat Rev Mol Cell Biol 4: 712-720.
3. Symington LS, (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 66: 630-670, table of contents.
4. Johnson RD, Jasin M, (2000) Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. Embo J 19: 3398-3407.
5. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M, (2004) Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol 24: 9305-9316.
6. Mao Z, Bozzella M, Seluanov A, Gorbunova V, (2008) DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells. Cell Cycle 7: 2902-2906.
7. Pierce AJ, Hu P, Han M, Ellis N, Jasin M, (2001) Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 15: 3237-3242.
8. Adamo A, Collis SJ, Adelman CA, Silva N, Horejsi Z, et al. (2010) Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol Cell 39: 25-35.
9. Pace P, Mosedale G, Hodskinson MR, Rosado IV, Sivasubramaniam M, et al. (2010) Ku70 corrupts DNA repair in the absence of the Fanconi anemia pathway. Science 329: 219-223.
10. Bunting SF, Callen E, Wong N, Chen HT, Polato F, et al. (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243-254.
11. Weinstock DM, Nakanishi K, Helgadottir HR, Jasin M, (2006) Assaying double-strand break repair pathway choice in mammalian cells using a targeted endonuclease or the RAG recombinase. Methods Enzymol 409: 524-540.
12. Maynard S, Swistowska AM, Lee JW, Liu Y, Liu ST, et al. (2008) Human embryonic stem cells have enhanced repair of multiple forms of DNA damage. Stem Cells 26: 2266-2274.
13. Hong Y, Cervantes RB, Tichy E, Tischfield JA, Stambrook PJ, (2007) Protecting genomic integrity in somatic cells and embryonic stem cells. Mutat Res 614: 48-55.
14. Filion TM, Qiao M, Ghule PN, Mandeville M, van Wijnen AJ, et al. (2009) Survival responses of human embryonic stem cells to DNA damage. J Cell Physiol 220: 586-592.
15. Milyavsky M, Gan OI, Trottier M, Komosa M, Tabach O, et al. (2010) A distinctive DNA damage response in human hematopoietic stem cells reveals an apoptosis-independent role for p53 in self-renewal. Cell Stem Cell 7: 186-197.
16. Momcilovic O, Choi S, Varum S, Bakkenist C, Schatten G, et al. (2009) Ionizing radiation induces ataxia telangiectasia mutated-dependent checkpoint signaling and G(2) but not G(1) cell cycle arrest in pluripotent human embryonic stem cells. Stem Cells 27: 1822-1835.
17. Van Hoof D, Braam SR, Dormeyer W, Ward-van Oostwaard D, Heck AJ, et al. (2008) Feeder-free monolayer cultures of human embryonic stem cells express an epithelial plasma membrane protein profile. Stem Cells 26: 2777-2781.
18. Chen HF, Kuo HC, Lin SP, Chien CL, Chiang MS, et al. (2010) Hypoxic culture maintains self-renewal and enhances embryoid body formation of human embryonic stem cells. Tissue Eng Part A 16: 2901-2913.
19. Buecker C, Chen HH, Polo JM, Daheron L, Bu L, et al. (2010) A murine ESC-like state facilitates transgenesis and homologous recombination in human pluripotent stem cells. Cell Stem Cell 6: 535-546.
20. Gauthaman K, Fong CY, Bongso A, (2010) Effect of ROCK inhibitor Y-27632 on normal and variant human embryonic stem cells (hESCs) in vitro: its benefits in hESC expansion. Stem Cell Rev 6: 86-95.
21. Braam SR, Denning C, Matsa E, Young LE, Passier R, et al. (2008) Feeder-free culture of human embryonic stem cells in conditioned medium for efficient genetic modification. Nat Protoc 3: 1435-1443.
22. Pierce AJ, Jasin M, (2005) Measuring recombination proficiency in mouse embryonic stem cells. Methods Mol Biol 291: 373-384.
23. Bennardo N, Gunn A, Cheng A, Hasty P, Stark JM, (2009) Limiting the persistence of a chromosome break diminishes its mutagenic potential. PLoS Genet 5: e1000683.
24. Chandrasegaran S, Smith J, (1999) Chimeric restriction enzymes: what is next? Biol Chem 380: 841-848.
25. Carroll D, (2004) Using nucleases to stimulate homologous recombination. Methods Mol Biol 262: 195-207.
26. Moehle EA, Rock JM, Lee YL, Jouvenot Y, DeKelver RC, et al. (2007) Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases. Proc Natl Acad Sci U S A 104: 3055-3060.
27. DeKelver RC, Choi VM, Moehle EA, Paschon DE, Hockemeyer D, et al. (2010) 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 Res 20: 1133-1142.
28. Kotin RM, Linden RM, Berns KI, (1992) Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination. Embo J 11: 5071-5078.
29. Smith JR, Maguire S, Davis LA, Alexander M, Yang F, et al. (2008) Robust, Persistent Transgene Expression in Human Embryonic Stem Cells Is Achieved with AAVS1-Targeted Integration. Stem Cells 26: 496-504.
30. Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, et al. (2009) Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 27: 851-857.
31. Brunet E, Simsek D, Tomishima M, DeKelver R, Choi VM, et al. (2009) Chromosomal translocations induced at specified loci in human stem cells. Proc Natl Acad Sci U S A 106: 10620-10625.
32. Moynahan ME, Pierce AJ, Jasin M, (2001) BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell 7: 263-272.
33. Banuelos CA, Banath JP, MacPhail SH, Zhao J, Eaves CA, et al. (2008) Mouse but not human embryonic stem cells are deficient in rejoining of ionizing radiation-induced DNA double-strand breaks. DNA Repair (Amst) 7: 1471-1483.
34. Willmore E, de Caux S, Sunter NJ, Tilby MJ, Jackson GH, et al. (2004) A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood 103: 4659-4665.
35. Song H, Chung SK, Xu Y, (2010) Modeling disease in human ESCs using an efficient BAC-based homologous recombination system. Cell Stem Cell 6: 80-89.
36. Adams BR, Golding SE, Rao RR, Valerie K, (2010) Dynamic dependence on ATR and ATM for double-strand break repair in human embryonic stem cells and neural descendants. PLoS One 5: e10001.
37. Adams BR, Hawkins AJ, Povirk LF, Valerie K, (2010) ATM-independent, high-fidelity nonhomologous end joining predominates in human embryonic stem cells. Aging (Albany NY) 2: 582-596.
38. Boskovic J, Rivera-Calzada A, Maman JD, Chacon P, Willison KR, et al. (2003) Visualization of DNA-induced conformational changes in the DNA repair kinase DNA-PKcs. Embo J 22: 5875-5882.
39. DeFazio LG, Stansel RM, Griffith JD, Chu G, (2002) Synapsis of DNA ends by DNA-dependent protein kinase. Embo J 21: 3192-3200.
40. Seita J, Rossi DJ, Weissman IL, (2010) Differential DNA damage response in stem and progenitor cells. Cell Stem Cell 7: 145-147.
41. Lane AA, Scadden DT, (2010) Stem cells and DNA damage: persist or perish? Cell 142: 360-362.
42. Mandal PK, Blanpain C, Rossi DJ, (2011) DNA damage response in adult stem cells: pathways and consequences. Nat Rev Mol Cell Biol 12: 198-202.
43. Holt N, Wang J, Kim K, Friedman G, Wang X, et al. (2010) Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 28: 839-847.
44. Perez EE, Wang J, Miller JC, Jouvenot Y, Kim KA, et al. (2008) Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 26: 808-816.
45. Gerrard L, Rodgers L, Cui W, (2005) Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 23: 1234-1241.
46. Wu JQ, Habegger L, Noisa P, Szekely A, Qiu C, et al. (2010) Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing. Proc Natl Acad Sci U S A 107: 5254-5259.
47. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, et al. (2005) CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434: 598-604.
48. Nakanishi K, Yang YG, Pierce AJ, Taniguchi T, Digweed M, et al. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc Natl Acad Sci U S A 102: 1110-1115.
49. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.