Efficient ligase 3-dependent microhomology-mediated end joining repair of DNA double-strand breaks in zebrafish embryos

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 780, Issue , 2015, Pages 86-96

  He, Mu Dan ^a,b   Zhang, Feng Hua ^a,b   Wang, Hua Lin ^a,b   Wang, Hou Peng ^a   Zhu, Zuo Yan ^a   Sun, Yong Hua ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

CRISPR (clustered regularly interspaced short palindromic repeats) Cas9; Double strand breaks repair; Ligase 3; Ligase 4; Microhomology mediated end joining (MMEJ); Transcription activator like effector nuclease (TALEN)

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DOUBLE STRANDED DNA; LIGASE; LIGASE 3; LIGASE 4; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; UNCLASSIFIED DRUG; DNA LIGASE; DNA LIGASE III; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA MICROHOMOLOGY MEDIATED END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; GENOME; IN VITRO STUDY; IN VIVO STUDY; MUTATION; NONHUMAN; PRIORITY JOURNAL; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; EMBRYOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

DANIO RERIO;

ANIMALS; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA LIGASES; EMBRYO, NONMAMMALIAN; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84940032369     PISSN: 00275107     EISSN: 18792871     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2015.08.004     Document Type: Article

References (65)

1. Hiom K. Coping with DNA double strand breaks. DNA Repair 2010, 9:1256-1263.
2. Magwood A.C., Malysewich M.J., Cealic I., Mundia M.M., Knapp J., Baker M.D. Endogenous levels of Rad51 and Brca2 are required for homologous recombination and regulated by homeostatic re-balancing. DNA Repair (Amst.) 2013, 12:1122-1133.
3. Yan H., Toczylowski T., McCane J., Chen C., Liao S. Replication protein A promotes 5'->3' end processing during homology-dependent DNA double-strand break repair. J. Cell. Biol. 2011, 192:251-261.
4. Weterings E., Chen D.J. The endless tale of non-homologous end-joining. Cell Res. 2008, 18:114-124.
5. Deriano L., Roth D.B. Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu. Rev. Genet. 2013, 47:433-455.
6. McVey M., Lee S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 2008, 24:529-538.
7. Liang L., Deng L., Nguyen S.C., Zhao X., Maulion C.D., Shao C., Tischfield J.A. Human DNA ligases I and III, but not ligase IV, are required for microhomology-mediated end joining of DNA double-strand breaks. Nucleic Acids Res. 2008, 36:3297-3310.
8. Symington L.S., Gautier J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 2011, 45:247-271.
9. Roth D.B., Wilson J.H. Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol. Cell. Biol. 1986, 6:4295-4304.
10. Zhang Y., Jasin M. An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat. Struct. Mol. Biol. 2011, 18:80.
11. Lee-Theilen M., Matthews A.J., Kelly D., Zheng S., Chaudhuri J. CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat. Struct. Mol. Biol. 2011, 18:75-79.
12. Ma J.L., Kim E.M., Haber J.E., Lee S.E. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 2003, 23:8820-8828.
13. Fattah F., Lee E.H., Weisensel N., Wang Y., Lichter N., Hendrickson E.A. Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet. 2010, 6:e1000855.
14. Feldmann E., Schmiemann V., Goedecke W., Reichenberger S., Pfeiffer P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res. 2000, 28:2585-2596.
15. Bentley J., Diggle C.P., Harnden P., Knowles M.A., Kiltie A.E. DNA double strand break repair in human bladder cancer is error prone and involves microhomology-associated end-joining. Nucleic Acids Res. 2004, 32:5249-5259.
16. Corneo B., Wendland R.L., Deriano L., Cui X., Klein I.A., Wong S.Y., Arnal S., Holub A.J., Weller G.R., Pancake B.A., Shah S., Brandt V.L., Meek K., Roth D.B. Rag mutations reveal robust alternative end joining. Nature 2007, 449:483-486.
17. Ma Y., Lu H., Schwarz K., Lieber M.R. Repair of double-strand DNA breaks by the human nonhomologous DNA end joining pathway: the iterative processing model. Cell Cycle 2005, 4:1193-1200.
18. Pfeiffer P., Goedecke W., Kuhfittig-Kulle S., Obe G. Pathways of DNA double-strand break repair and their impact on the prevention and formation of chromosomal aberrations. Cytogenet. Genome Res. 2004, 104:7-13.
19. Sugawara N., Ira G., Haber J.E. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell. Biol. 2000, 20:5300-5309.
20. Wang H., Zeng Z.C., Bui T.A., Sonoda E., Takata M., Takeda S., Iliakis G. Efficient rejoining of radiation-induced DNA double-strand breaks in vertebrate cells deficient in genes of the RAD52 epistasis group. Oncogene 2001, 20:2212-2224.
21. Wang H.C., Rosidi B., Perrault R., Wang M.L., Zhang L.H., Windhofer F., Iliakis G. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 2005, 65:4020-4030.
22. Oh S., Harvey A., Zimbric J., Wang Y., Nguyen T., Jackson P.J., Hendrickson E.A. DNA ligase III and DNA ligase IV carry out genetically distinct forms of end joining in human somatic cells. DNA Repair 2014, 21:97-110.
23. Truong L.N., Li Y., Shi L.Z., Hwang P.Y., He J., Wang H., Razavian N., Berns M.W., Wu X. Microhomology-mediated End Joining and Homologous Recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7720-7725.
24. Audebert M., Salles B., Calsou P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J. Biol. Chem. 2004, 279:55117-55126.
25. Sonoda E., Takata M., Yamashita Y.M., Morrison C., Takeda S. Homologous DNA recombination in vertebrate cells. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:8388-8394.
26. Tauchi H., Kobayashi J., Morishima K., van Gent D.C., Shiraishi T., Verkaik N.S., vanHeems D., Ito E., Nakamura A., Sonodo E., Takata M., Takeda S., Matsuura S., Komatsu K. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 2002, 420:93-98.
27. Bladen C.L., Lam W.K., Dynan W.S., Kozlowski D.J. DNA damage response and Ku80 function in the vertebrate embryo. Nucleic Acids Res. 2005, 33:3002-3010.
28. Sandrini J.Z., Trindade G.S., Nery L.E., Marins L.F. Time-course expression of DNA repair-related genes in hepatocytes of zebrafish (Danio rerio) after UV-B exposure. Photochem. Photobiol. 2009, 85:220-226.
29. Pei D.S., Strauss P.R. Zebrafish as a model system to study DNA damage and repair. Mutat. Res. Fund. Mol. 2013, 743:151-159.
30. Liu J., Gong L., Chang C., Liu C., Peng J., Chen J. Development of novel visual-plus quantitative analysis systems for studying DNA double-strand break repairs in zebrafish. J. Genet. Genomics 2012, 39:489-502.
31. Ye D., Zhu Z., Sun Y. Fish genome manipulation and directional breeding. Sci. China Life Sci. 2015, 58:170-177.
32. Auer T.O., Del Bene F. CRISPR/Cas9 and TALEN-mediated knock-in approaches in zebrafish. Methods 2014, 69:142-150.
33. Huang P., Xiao A., Zhou M.G., Zhu Z.Y., Lin S., Zhang B. Heritable gene targeting in zebrafish using customized TALENs. Nat. Biotechnol. 2011, 29:699-700.
34. Chang N., Sun C., Gao L., Zhu D., Xu X., Zhu X., Xiong J.W., Xi J.J. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res. 2013, 23:465-472.
35. Xiong F., Wei Z.Q., Zhu Z.Y., Sun Y.H. Targeted expression in zebrafish primordial germ cells by Cre/loxP and Gal4/UAS systems. Mar Biotechnol. (N.Y.) 2013, 15:526-539.
36. Ochiai H., Sakamoto N., Fujita K., Nishikawa M., Suzuki K., Matsuura S., Miyamoto T., Sakuma T., Shibata T., Yamamoto T. Zinc-finger nuclease-mediated targeted insertion of reporter genes for quantitative imaging of gene expression in sea urchin embryos. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10915-10920.
37. Wei C.-Y., Wang H.-P., Zhu Z.-Y., Sun Y.-H. Transcriptional factors Smad1 and Smad9 act redundantly to mediate zebrafish ventral specification downstream of Smad5. J. Biol. Chem. 2014.
38. Shih J., Fraser S.E. Characterizing the zebrafish organizer: microsurgical analysis at the early-shield stage. Development 1996, 122:1313-1322.
39. -δδC(T) method. Methods 2001, 25:402-408.
40. Zhu Z.Y., Sun Y.H. Embryonic and genetic manipulation in fish. Cell Res. 2000, 10:17-27.
41. Sun Y.H., Chen S.P., Wang Y.P., Hu W., Zhu Z.Y. Cytoplasmic impact on cross-genus cloned fish derived from transgenic common carp (Cyprinus carpio) nuclei and goldfish (Carassius auratus) enucleated eggs. Biol. Reprod. 2005, 72:510-515.
42. Sun Y., Chen S., Wang Y., Zhu Z. The onset of foreign gene transcription in nuclear-transferred embryos of fish. Sci. China Life Sci. 2000, 43:597-605.
43. Wang J., Levasseur D.N., Orkin S.H. Requirement of Nanog dimerization for stem cell self-renewal and pluripotency. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:6326-6331.
44. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
45. Kukshal V., Kim I.K., Hura G.L., Tomkinson A.E., Tainer J.A., Ellenberger T. Human DNA ligase III bridges two DNA ends to promote specific intermolecular DNA end joining. Nucleic Acids Res. 2015.
46. Ahnesorg P., Smith P., Jackson S.P. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 2006, 124:301-313.
47. Wilson T.E., Grawunder U., Lieber M.R. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 1997, 388:495-498.
48. Wu P.Y., Frit P., Meesala S., Dauvillier S., Modesti M., Andres S.N., Huang Y., Sekiguchi J., Calsou P., Salles B., Junop M.S. Structural and functional interaction between the human DNA repair proteins DNA ligase IV and XRCC4. Mol. Cell. Biol. 2009, 29:3163-3172.
49. Yu X., Gabriel A. Ku-dependent and Ku-independent end-joining pathways lead to chromosomal rearrangements during double-strand break repair in Saccharomyces cerevisiae. Genetics 2003, 163:843-856.
50. Boulton S.J., Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO. J. 1998, 17:1819-1828.
51. Liang F., Jasin M. Ku80-deficient cells exhibit excess degradation of extrachromosomal DNA. J. Biol. Chem. 1996, 271:14405-14411.
52. McVey M., Radut D., Sekelsky J.J. End-joining repair of double-strand breaks in Drosophila melanogaster is largely DNA ligase IV independent. Genetics 2004, 168:2067-2076.
53. Heacock M., Spangler E., Riha K., Puizina J., Shippen D.E. Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J. 2004, 23:2304-2313.
54. Rai R., Zheng H., He H., Luo Y., Multani A., Carpenter P.B., Chang S. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J. 2010, 29:2598-2610.
55. Yan C.T., Boboila C., Souza E.K., Franco S., Hickernell T.R., Murphy M., Gumaste S., Geyer M., Zarrin A.A., Manis J.P., Rajewsky K., Alt F.W. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007, 449:478-482.
56. Gratz S.J., Cummings A.M., Nguyen J.N., Hamm D.C., Donohue L.K., Harrison M.M., Wildonger J., O'Connor-Giles K.M. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 2013, 194:1029-1035.
57. Yasue A., Mitsui S.N., Watanabe T., Sakuma T., Oyadomari S., Yamamoto T., Noji S., Mito T., Tanaka E. Highly efficient targeted mutagenesis in one-cell mouse embryos mediated by the TALEN and CRISPR/Cas systems. Sci. Rep. 2014, 4:5705.
58. Hisano Y., Sakuma T., Nakade S., Ohga R., Ota S., Okamoto H., Yamamoto T., Kawahara A. Precise in-frame integration of exogenous DNA mediated by CRISPR/Cas9 system in zebrafish. Sci. Rep. 2015, 5:8841.
59. Lee K., Lee S.E. Saccharomyces cerevisiae Sae2- and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 2007, 176:2003-2014.
60. Simsek D., Brunet E., Wong S.Y., Katyal S., Gao Y., McKinnon P.J., Lou J., Zhang L., Li J., Rebar E.J., Gregory P.D., Holmes M.C., Jasin M. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet. 2011, 7:e1002080.
61. Decottignies A. Microhomology-mediated end joining in fission yeast is repressed by pku70 and relies on genes involved in homologous recombination. Genetics 2007, 176:1403-1415.
62. Glover L., Jun J., Horn D. Microhomology-mediated deletion and gene conversion in African trypanosomes. Nucleic Acids Res. 2011, 39:1372-1380.
63. Mattarucchi E., Guerini V., Rambaldi A., Campiotti L., Venco A., Pasquali F., Lo Curto F., Porta G. Microhomologies and interspersed repeat elements at genomic breakpoints in chronic myeloid leukemia. Genes Chromosomes Cancer 2008, 47:625-632.
64. Zhang Y., Rowley J.D. Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair (Amst.) 2006, 5:1282-1297.
65. Ritz K., van Schaik B.D.C., Jakobs M.E., Aronica E., Tijssen M.A., van Kampen A.H.C., Baas F. Looking ultra deep: Short identical sequences and transcriptional slippage. Genomics 2011, 98:90-95.