Rapid and precise engineering of the caenorhabditis elegans genome with lethal mutation co-conversion and inactivation of NHEJ repair

Genetics

Volumn 199, Issue 2, 2014, Pages 363-377

  Ward, Jordan D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Co Conversion; CRISPR Cas9; Nonhomologous end joining; Oligonucleotide mediated homologous recombination; Pha 1

Indexed keywords

EPITOPE; HELMINTH RNA;

ANIMAL EXPERIMENT; ARTICLE; BODY SIZE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA END JOINING REPAIR; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; FEMALE; GENE; GENE CONVERSION; GENE INSERTION; GENE TARGETING; GENETIC ENGINEERING; GENOME; GENOTYPE; HOMOLOGOUS RECOMBINATION; MALE; METHODOLOGY; NONHUMAN; PHA 1 GENE; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; RESTRICTION SITE; ANIMAL; GENE DELETION; GENETICS; LETHAL GENE; MUTATION; PROCEDURES; RECOMBINATION REPAIR; RNA EDITING; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; GENE CONVERSION; GENE DELETION; GENE KNOCK-IN TECHNIQUES; GENE TARGETING; GENES, HELMINTH; GENES, LETHAL; GENETIC ENGINEERING; GENOME, HELMINTH; MALE; MUTATION; RECOMBINATIONAL DNA REPAIR; RNA EDITING; RNA INTERFERENCE; RNA, HELMINTH;

EID: 84926451490     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.172361     Document Type: Article

References (69)

1. Adamo, A., S. J. Collis, C. A. Adelman, N. Silva, Z. Horejsi et al., 2010 Preventing nonhomologous end joining suppresses DNA repair defects of Fanconi anemia. Mol. Cell 39: 25–35.
2. Arribere, J. A., R. T. Bell, B. X. H. Fu, K. L. Artiles, P. S. Hartman et al., 2014 Efficient marker-free recovery of custom genetic modifications with CRISPR/Cas9 in Caenorhabditis elegans. Genetics 198: 837–846.
3. Asahina, M., T. Ishihara, M. Jindra, Y. Kohara, I. Katsura et al., 2000 The conserved nuclear receptor Ftz-F1 is required for embryogenesis, moulting and reproduction in Caenorhabditis elegans. Genes Cells 5: 711–723.
4. Asahina, M., T. Valenta, M. Silhánková, V. Korinek, and M. Jindra, 2006 Crosstalk between a nuclear receptor and beta-catenin signaling decides cell fates in the C. elegans somatic gonad. Dev. Cell 11: 203–211.
5. Bassik, M. C., R. J. Lebbink, L. S. Churchman, N. T. Ingolia, W. Patena et al., 2009 Rapid creation and quantitative monitoring of high coverage shRNA libraries. Nat. Methods 6: 443–445.
6. Bedell, V. M., Y. Wang, J. M. Campbell, T. L. Poshusta, C. G. Starker et al., 2012 In vivo genome editing using a high-efficiency TALEN system. Nature 490: 114–118.
7. Beumer, K. J., J. K. Trautman, A. Bozas, J.-L. Liu, J. Rutter et al., 2008 Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases. Proc. Natl. Acad. Sci. USA 105: 19821–19826.
8. Bottcher, R., M. Hollmann, K. Merk, V. Nitschko, C. Obermaier et al., 2014 Efficient chromosomal gene modification with CRISPR/cas9 and PCR-based homologous recombination donors in cultured Drosophila cells. Nucleic Acids Res. 42: e89.
9. Brenner, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71–94.
10. Broday, L., I. Kolotuev, C. Didier, A. Bhoumik, B. P. Gupta et al., 2004 The small ubiquitin-like modifier (SUMO) is required for gonadal and uterine-vulval morphogenesis in Caenorhabditis elegans. Genes Dev. 18: 2380–2391.
11. Brooks, D. R., P. J. Appleford, L. Murray, and R. E. Isaac, 2003 An essential role in molting and morphogenesis of Caenorhabditis elegans for ACN-1, a novel member of the angiotensin-converting enzyme family that lacks a metallopeptidase active site. J. Biol. Chem. 278: 52340–52346.
12. Chen, B., L. A. Gilbert, B. A. Cimini, J. Schnitzbauer, W. Zhang et al., 2013a Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479–1491.
13. Chen, C., L. A. Fenk, and M. de Bono, 2013b Efficient genome editing in Caenorhabditis elegans by CRISPR-targeted homologous recombination. Nucleic Acids Res. 41: e193.
14. Chen, F., S. M. Pruett-Miller, Y. Huang, M. Gjoka, K. Duda et al., 2011 High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases. Nat. Methods 8: 753753.
15. Chen, Z., D. J. Eastburn, and M. Han, 2004 The Caenorhabditis elegans nuclear receptor gene nhr-25 regulates epidermal cell development. Mol. Cell. Biol. 24: 7345–7358.
16. Chiu, H., H. T. Schwartz, I. Antoshechkin, and P. W. Sternberg, 2013 Transgene-free genome editing in Caenorhabditis elegans using CRISPR-Cas. Genetics 195: 1167–1171.
17. Cho, S. W., J. Lee, D. Carroll, J.-S. Kim, and J. Lee, 2013 Heritable gene knockout in Caenorhabditis elegans by direct injection of Cas9-sgRNA ribonucleoproteins. Genetics 195: 1177–1180.
18. Clejan, I., J. Boerckel, and S. Ahmed, 2006 Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173: 1301–1317.
19. Cong, L., F. A. Ran, D. Cox, S. Lin, R. Barretto et al., 2013 Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819–823.
20. DiCarlo, J. E., J. E. Norville, P. Mali, X. Rios, J. Aach et al., 2013 Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 41: 4336–4343.
21. Dickinson, D. J., J. D. Ward, D. J. Reiner, and B. Goldstein, 2013 Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat. Methods 10: 1028–1034.
22. Dmitrieva, N. I., A. Celeste, A. Nussenzweig, and M. B. Burg, 2005 Ku86 preserves chromatin integrity in cells adapted to high NaCl. Proc. Natl. Acad. Sci. USA 102: 10730–10735.
23. Friedland, A. E., Y. B. Tzur, K. M. Esvelt, M. P. Colaiácovo, G. M. Church et al., 2013 Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat. Methods 10: 741–743.
24. Frøkjaer-Jensen, C., M. W. Davis, C. E. Hopkins, B. J. Newman, J. M. Thummel et al., 2008 Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40: 1375–1383.
25. Frøkjær-Jensen, C., M. W. Davis, G. Hollopeter, J. Taylor, T. W. Harris et al., 2010 Targeted gene deletions in C. elegans using transposon excision. Nat. Methods 7: 451–453.
26. Frøkjær-Jensen, C., M. W. Davis, M. Ailion, and E. M. Jorgensen, 2012 Improved Mos1-mediated transgenesis in C. elegans. Nat. Methods 9: 117–118.
27. Gilbert, L. A., M. A. Horlbeck, B. Adamson, J. E. Villalta, Y. Chen et al., 2014 Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159: 647–661.
28. Giordano-Santini, R., S. Milstein, N. Svrzikapa, D. Tu, R. Johnsen et al., 2010 An antibiotic selection marker for nematode transgenesis. Nat. Methods 7: 721–723.
29. Gissendanner, C. R., and A. E. Sluder, 2000 nhr-25, the Caenorhabditis elegans ortholog of ftz-f1, is required for epidermal and somatic gonad development. Dev. Biol. 221: 259–272.
30. Granato, M., H. Schnabel, and R. Schnabel, 1994 pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res. 22: 1762–1763.
31. Gratz, S. J., A. M. Cummings, J. N. Nguyen, D. C. Hamm, L. K. Donohue et al., 2013 Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 194: 1029–1035.
32. Gratz, S. J., F. P. Ukken, C. D. Rubinstein, G. Thiede, L. K. Donohue et al., 2014 Highly specific and efficient CRISPR/Cas9catalyzed homology-directed repair in Drosophila. Genetics 196: 961–971.
33. Hobert, O., 2002 PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32: 728–730.
34. Hwang, W. Y., Y. Fu, D. Reyon, M. L. Maeder, S. Q. Tsai et al., 2013 Efficient genome editing in zebrafish using a CRISPRCas system. Nat. Biotechnol. 31: 227–229.
35. Igoucheva, O., V. Alexeev, and K. Yoon, 2001 Targeted gene correction by small single-stranded oligonucleotides in mammalian cells. Gene Ther. 8: 391–399.
36. Jinek, M., K. Chylinski, I. Fonfara, M. Hauer, J. A. Doudna et al., 2012 A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337: 816–821.
37. Kamath, R. S., A. G. Fraser, Y. Dong, G. Poulin, R. Durbin et al., 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231–237.
38. Kamath R. S., M. Martinez-Campos, P. Zipperlen, A. G. Fraser, and J. Ahringer, 2001 Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.
39. Kaminsky, R., C. Denison, U. Bening-Abu-Shach, A. D. Chisholm, S. P. Gygi et al., 2009 SUMO regulates the assembly and function of a cytoplasmic intermediate filament protein in C. elegans. Dev. Cell 17: 724–735.
40. Katic, I., and H. Grosshans, 2013 Targeted heritable mutation and gene conversion by Cas9-CRISPR in Caenorhabditis elegans. Genetics 195: 1173–1176.
41. Kim, H., T. Ishidate, K. S. Ghanta, M. Seth, D. Conte et al., 2014 A Co-CRISPR strategy for efficient genome editing in Caenorhabditis elegans. Genetics 197: 1069–1080.
42. Kostrouchova, M., M. Krause, Z. Kostrouch, and J. E. Rall, 1998 CHR3: a Caenorhabditis elegans orphan nuclear hormone receptor required for proper epidermal development and molting. Development 125: 1617–1626.
43. Kostrouchova, M., M. Krause, Z. Kostrouch, and J. E. Rall, 2001 Nuclear hormone receptor CHR3 is a critical regulator of all four larval molts of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98: 7360–7365.
44. Li, J.-F., J. E. Norville, J. Aach, M. McCormack, D. Zhang et al., 2013 Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat. Biotechnol. 31: 688–691.
45. Lo, T.-W., C. S. Pickle, S. Lin, E. J. Ralston, M. Gurling et al., 2013 Precise and heritable genome editing in evolutionarily diverse nematodes using TALENs and CRISPR/Cas9 to engineer insertions and deletions. Genetics 195: 331–348.
46. Mali, P., K. M. Esvelt, and G. M. Church, 2013 Cas9 as a versatile tool for engineering biology. Nat. Methods 10: 957–963.
47. McColl, G., M. C. Vantipalli, and G. J. Lithgow, 2005 The C. elegans ortholog of mammalian Ku70, interacts with insulin-like signaling to modulate stress resistance and life span. FASEB J. 19: 1716–1718.
48. Moerman, D. G., and D. L. Baillie, 1979 Genetic organization in Caenorhabditis elegans: fine-structure analysis of the unc-22 gene. Genetics 91: 95–103.
49. Mullaney, B. C., R. D. Blind, G. A. Lemieux, C. L. Perez, I. C. Elle et al., 2010 Regulation of C. elegans fat uptake and storage by acyl-CoA synthase-3 is dependent on NR5A family nuclear hormone receptor nhr-25. Cell Metab. 12: 398–410.
50. Nakanishi, T., Y. Kato, T. Matsuura, and H. Watanabe, 2014 CRISPR/Cas-mediated targeted mutagenesis in Daphnia magna. PLoS ONE 9: e98363.
51. Paix, A., Y. Wang, H. E. Smith, C.-Y. S. Lee, D. Calidas et al., 2014 Scalable and versatile genome editing using linear DNAs with microhomology to Cas9 sites in Caenorhabditis elegans. Genetics 198: 1347–1356.
52. Plasterk, R. H., and J. T. Groenen, 1992 Targeted alterations of the Caenorhabditis elegans genome by transgene instructed DNA double strand break repair following Tc1 excision. EMBO J. 11: 287–290.
53. Posch, A., J. Kohn, K. Oh, M. Hammond, and N. Liu, 2013 V3 stain-free workflow for a practical, convenient, and reliable total protein loading control in western blotting. J. Vis. Exp. 30: 50948.
54. Ran, F. A., P. D. Hsu, J. Wright, V. Agarwala, D. A. Scott et al., 2013 Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8: 2281–2308.
55. Robert, V., and J.-L. Bessereau, 2007 Targeted engineering of the Caenorhabditis elegans genome following Mos1-triggered chromosomal breaks. EMBO J. 26: 170–183.
56. Schnabel, H., G. Bauer, and R. Schnabel, 1991 Suppressors of the organ-specific differentiation gene pha-1 of Caenorhabditis elegans. Genetics 129: 69–77.
57. Shtonda, B. B., and L. Avery, 2006 Dietary choice behavior in Caenorhabditis elegans. J. Exp. Biol. 209: 89–102.
58. Storici, F., C. L. Durham, D. A. Gordenin, and M. A. Resnick, 2003 Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc. Natl. Acad. Sci. USA 100: 14994–14999.
59. Tzur, Y. B., A. E. Friedland, S. Nadarajan, G. M. Church, J. A. Calarco et al., 2013 Heritable custom genomic modifications in Caenorhabditis elegans via a CRISPR-Cas9 system. Genetics 195: 1181–1185.
60. Waaijers, S., and M. Boxem, 2014 Engineering the Caenorhabditis elegans genome with CRISPR/Cas9. Methods 68: 381–388.
61. Waaijers, S., V. Portegijs, J. Kerver, B. B. L. G. Lemmens, M. Tijsterman et al., 2013 CRISPR/Cas9-targeted mutagenesis in Caenorhabditis elegans. Genetics 195: 1187–1191.
62. Ward, J. D., N. Bojanala, T. Bernal, K. Ashrafi, M. Asahina et al., 2013 Sumoylated NHR-25/NR5A regulates cell fate during C. elegans vulval development. PLoS Genet. 9: e1003992.
63. Ward, J. D., B. Mullaney, B. J. Schiller, L. D. He, S. E. Petnic et al., 2014 Defects in the C. elegans acyl-CoA synthase, acs-3, and nuclear hormone receptor, nhr-25, cause sensitivity to distinct, but overlapping stresses. PLoS ONE 9: e92552.
64. Wood, A. J., T.-W. Lo, B. Zeitler, C. S. Pickle, E. J. Ralston et al., 2011 Targeted genome editing across species using ZFNs and TALENs. Science 333: 307.
65. Yang, B., X. Wen, N. S. Kodali, C. A. Oleykowski, C. G. Miller et al., 2000 Purification, cloning, and characterization of the CEL I nuclease. Biochemistry 39: 3533–3541.
66. Zhao, P., Z. Zhang, H. Ke, Y. Yue, and D. Xue, 2014 Oligonucleotidebased targeted gene editing in C. elegans via the CRISPR/Cas9 system. Cell Res. 24: 247–250.
67. FRIEDLAND A. E., TZUR Y. B., ESVELT K. M., COLAIÁCOVO M. P., CHURCH G. M., CALARCO J. A., 2013 Heritable genome editing in C. elegans via a CRISPR‐Cas9 system. Nat Meth 10: 741–743.
68. KIM H., ISHIDATE T., GHANTA K. S., SETH M., CONTE D., SHIRAYAMA M., MELLO C. C., 2014 A Co‐CRISPR Strategy for Efficient Genome Editing in Caenorhabditis elegans. Genetics 197: 1069–1080.
69. ZHAO P., ZHANG Z., KE H., YUE Y., XUE D., 2014 Oligonucleotide‐based targeted gene editing in C. elegans via the CRISPR/Cas9 system. Cell Research 24: 247–250.