Precise Editing at DNA Replication Forks Enables Multiplex Genome Engineering in Eukaryotes

Cell

Volumn 171, Issue 6, 2017, Pages 1453-1467.e13

  Barbieri, Edward M ^a   Muir, Paul ^a   Akhuetie Oni, Benjamin O ^a   Yellman, Christopher M ^a,b   Isaacs, Farren J ^a  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

DNA replication; genome editing; homologous recombination; metabolic engineering; multiplex genome engineering; natural products; Rad51; ssDNA oligodeoxynucleotides

Indexed keywords

BETA CAROTENE; CAROTENOID; DNA; OLIGONUCLEOTIDE;

ARTICLE; CHROMOSOME; CONTROLLED STUDY; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ELECTROPORATION; FUNGAL GENOME; FUNGAL STRAIN; GENE EDITING; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENETIC ENGINEERING; GENETIC VARIABILITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH THROUGHPUT SEQUENCING; HOMOLOGOUS RECOMBINATION; HYBRIDIZATION; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SACCHAROMYCES CEREVISIAE; ULTRAVIOLET IRRADIATION; CHEMISTRY; ESCHERICHIA COLI; GENETICS; PROCEDURES;

DNA REPLICATION; ESCHERICHIA COLI; GENE EDITING; GENETIC ENGINEERING; OLIGONUCLEOTIDES; SACCHAROMYCES CEREVISIAE;

EID: 85034447094     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.10.034     Document Type: Article

References (60)

1. Amiram, M., Haimovich, A.D., Fan, C., Wang, Y.S., Aerni, H.R., Ntai, I., Moonan, D.W., Ma, N.J., Rovner, A.J., Hong, S.H., et al. Evolution of translation machinery in recoded bacteria enables multi-site incorporation of nonstandard amino acids. Nat. Biotechnol. 33 (2015), 1272–1279.
2. Anand, R., Beach, A., Li, K., Haber, J., Rad51-mediated double-strand break repair and mismatch correction of divergent substrates. Nature 544 (2017), 377–380.
3. Annaluru, N., Muller, H., Mitchell, L.A., Ramalingam, S., Stracquadanio, G., Richardson, S.M., Dymond, J.S., Kuang, Z., Scheifele, L.Z., Cooper, E.M., et al. Total synthesis of a functional designer eukaryotic chromosome. Science 344 (2014), 55–58.
4. Boeke, J.D., Church, G., Hessel, A., Kelley, N.J., Arkin, A., Cai, Y., Carlson, R., Chakravarti, A., Cornish, V.W., Holt, L., et al. The genome project-write. Science 353 (2016), 126–127.
5. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30 (2014), 2114–2120.
6. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., Boeke, J.D., Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14 (1998), 115–132.
7. Branzei, D., Foiani, M., Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11 (2010), 208–219.
8. Carr, P.A., Wang, H.H., Sterling, B., Isaacs, F.J., Lajoie, M.J., Xu, G., Church, G.M., Jacobson, J.M., Enhanced multiplex genome engineering through co-operative oligonucleotide co-selection. Nucleic Acids Res., 40, 2012, e132.
9. Chandrasegaran, S., Carroll, D., Origins of programmable nucleases for genome engineering. J. Mol. Biol. 428:5 Pt B (2016), 963–989.
10. Collonnier, C., Epert, A., Mara, K., Maclot, F., Guyon-Debast, A., Charlot, F., White, C., Schaefer, D.G., Nogué F., CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss Physcomitrella patens. Plant Biotechnol. J. 15 (2017), 122–131.
11. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., Zhang, F., Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
12. Costantino, N., Court, D.L., Enhanced levels of lambda red-mediated recombinants in mismatch repair mutants. Proc. Natl. Acad. Sci. USA 100 (2003), 15748–15753.
13. Costanzo, M., VanderSluis, B., Koch, E.N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S.D., et al. A global genetic interaction network maps a wiring diagram of cellular function. Science, 353, 2016, 353.
14. Detloff, P., Sieber, J., Petes, T.D., Repair of specific base pair mismatches formed during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 11 (1991), 737–745.
15. DiCarlo, J.E., Conley, A.J., Penttilä M., Jäntti, J., Wang, H.H., Church, G.M., Yeast oligo-mediated genome engineering (YOGE). ACS Synth. Biol. 2 (2013), 741–749.
16. Doudna, J.A., Charpentier, E., Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science, 346, 2014, 1258096.
17. Erler, A., Wegmann, S., Elie-Caille, C., Bradshaw, C.R., Maresca, M., Seidel, R., Habermann, B., Muller, D.J., Stewart, A.F., Conformational adaptability of Redbeta during DNA annealing and implications for its structural relationship with Rad52. J. Mol. Biol. 391 (2009), 586–598.
18. Farzadfard, F., Perli, S.D., Lu, T.K., Tunable and multifunctional eukaryotic transcription factors based on CRISPR/Cas. ACS Synth. Biol. 2 (2013), 604–613.
19. Friedman, K.L., Brewer, B.J., Fangman, W.L., Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2 (1997), 667–678.
20. Fu, Y., Foden, J.A., Khayter, C., Maeder, M.L., Reyon, D., Joung, J.K., Sander, J.D., High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 31 (2013), 822–826.
21. Gibson, D.G., Enzymatic assembly of overlapping DNA fragments. Methods Enzymol. 498 (2011), 349–361.
22. Gietz, R.D., Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol. Biol. 1205 (2014), 1–12.
23. Horwitz, A.A., Walter, J.M., Schubert, M.G., Kung, S.H., Hawkins, K., Platt, D.M., Hernday, A.D., Mahatdejkul-Meadows, T., Szeto, W., Chandran, S.S., Newman, J.D., Efficient multiplexed integration of synergistic alleles and metabolic pathways in yeasts via CRISPR-Cas. Cell Syst. 1 (2015), 88–96.
24. Inui, M., Miyado, M., Igarashi, M., Tamano, M., Kubo, A., Yamashita, S., Asahara, H., Fukami, M., Takada, S., Rapid generation of mouse models with defined point mutations by the CRISPR/Cas9 system. Sci. Rep., 4, 2014, 5396.
25. Jakočiūnas, T., Bonde, I., Herrgård, M., Harrison, S.J., Kristensen, M., Pedersen, L.E., Jensen, M.K., Keasling, J.D., Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae. Metab. Eng. 28 (2015), 213–222.
26. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
27. Komor, A.C., Kim, Y.B., Packer, M.S., Zuris, J.A., Liu, D.R., Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533 (2016), 420–424.
28. Kow, Y.W., Bao, G., Reeves, J.W., Jinks-Robertson, S., Crouse, G.F., Oligonucleotide transformation of yeast reveals mismatch repair complexes to be differentially active on DNA replication strands. Proc. Natl. Acad. Sci. USA 104 (2007), 11352–11357.
29. Krivoruchko, A., Nielsen, J., Production of natural products through metabolic engineering of Saccharomyces cerevisiae. Curr. Opin. Biotechnol. 35 (2015), 7–15.
30. Lajoie, M.J., Rovner, A.J., Goodman, D.B., Aerni, H.R., Haimovich, A.D., Kuznetsov, G., Mercer, J.A., Wang, H.H., Carr, P.A., Mosberg, J.A., et al. Genomically recoded organisms expand biological functions. Science 342 (2013), 357–360.
31. Lang, G.I., Parsons, L., Gammie, A.E., Mutation rates, spectra, and genome-wide distribution of spontaneous mutations in mismatch repair deficient yeast. G3 (Bethesda) 3 (2013), 1453–1465.
32. Lee, M., Lee, C.H., Demin, A.A., Munashingha, P.R., Amangyeld, T., Kwon, B., Formosa, T., Seo, Y.S., Rad52/Rad59-dependent recombination as a means to rectify faulty Okazaki fragment processing. J. Biol. Chem. 289 (2014), 15064–15079.
33. Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv, arXiv:13033997v1 [q-bioGN], https://arxiv.org/abs/1303.3997.
34. Liu, L., Maguire, K.K., Kmiec, E.B., Genetic re-engineering of Saccharomyces cerevisiae RAD51 leads to a significant increase in the frequency of gene repair in vivo. Nucleic Acids Res. 32 (2004), 2093–2101.
35. Lubliner, S., Keren, L., Segal, E., Sequence features of yeast and human core promoters that are predictive of maximal promoter activity. Nucleic Acids Res. 41 (2013), 5569–5581.
36. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M., RNA-guided human genome engineering via Cas9. Science 339 (2013), 823–826.
37. Markham, N.R., Zuker, M., UNAFold: software for nucleic acid folding and hybridization. Methods Mol. Biol. 453 (2008), 3–31.
38. Mitchell, L.A., Chuang, J., Agmon, N., Khunsriraksakul, C., Phillips, N.A., Cai, Y., Truong, D.M., Veerakumar, A., Wang, Y., Mayorga, M., et al. Versatile genetic assembly system (VEGAS) to assemble pathways for expression in S. cerevisiae. Nucleic Acids Res. 43 (2015), 6620–6630.
39. Paquet, D., Kwart, D., Chen, A., Sproul, A., Jacob, S., Teo, S., Olsen, K.M., Gregg, A., Noggle, S., Tessier-Lavigne, M., Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature 533 (2016), 125–129.
40. Rivera-Torres, N., Kmiec, E.B., Genetic spell-checking: gene editing using single-stranded DNA oligonucleotides. Plant Biotechnol. J. 14 (2016), 463–470.
41. Rodriguez, G.P., Song, J.B., Crouse, G.F., Transformation with oligonucleotides creating clustered changes in the yeast genome. PLoS ONE, 7, 2012, e42905.
42. San Filippo, J., Sung, P., Klein, H., Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77 (2008), 229–257.
43. Schmittgen, T.D., Livak, K.J., Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3 (2008), 1101–1108.
44. Smanski, M.J., Bhatia, S., Zhao, D., Park, Y., B A Woodruff, L., Giannoukos, G., Ciulla, D., Busby, M., Calderon, J., Nicol, R., et al. Functional optimization of gene clusters by combinatorial design and assembly. Nat. Biotechnol. 32 (2014), 1241–1249.
45. Smith, D.J., Whitehouse, I., Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483 (2012), 434–438.
46. Song, B., Sung, P., Functional interactions among yeast Rad51 recombinase, Rad52 mediator, and replication protein A in DNA strand exchange. J. Biol. Chem. 275 (2000), 15895–15904.
47. Storici, F., Resnick, M.A., Delitto perfetto targeted mutagenesis in yeast with oligonucleotides. Genet. Eng. (N. Y.) 25 (2003), 189–207.
48. Sung, P., Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272 (1997), 28194–28197.
49. Szpiech, Z.A., Jakobsson, M., Rosenberg, N.A., ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24 (2008), 2498–2504.
50. Tsai, S.Q., Joung, J.K., Defining and improving the genome-wide specificities of CRISPR-Cas9 nucleases. Nat. Rev. Genet. 17 (2016), 300–312.
51. Van der Auwera, G.A., Carneiro, M.O., Hartl, C., Poplin, R., Del Angel, G., Levy-Moonshine, A., Jordan, T., Shakir, K., Roazen, D., Thibault, J., et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinformatics 43 (2013), 11.10.1–11.10.33.
52. Wang, H.H., Isaacs, F.J., Carr, P.A., Sun, Z.Z., Xu, G., Forest, C.R., Church, G.M., Programming cells by multiplex genome engineering and accelerated evolution. Nature 460 (2009), 894–898.
53. Wingler, L.M., Cornish, V.W., Reiterative recombination for the in vivo assembly of libraries of multigene pathways. Proc. Natl. Acad. Sci. USA 108 (2011), 15135–15140.
54. Winzeler, E.A., Shoemaker, D.D., Astromoff, A., Liang, H., Anderson, K., Andre, B., Bangham, R., Benito, R., Boeke, J.D., Bussey, H., et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 (1999), 901–906.
55. Wu, C.A., Zechner, E.L., Marians, K.J., Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. I. Multiple effectors act to modulate Okazaki fragment size. J. Biol. Chem. 267 (1992), 4030–4044.
56. Xie, W., Lv, X., Ye, L., Zhou, P., Yu, H., Construction of lycopene-overproducing Saccharomyces cerevisiae by combining directed evolution and metabolic engineering. Metab. Eng. 30 (2015), 69–78.
57. Xu, W., Aparicio, J.G., Aparicio, O.M., Tavaré S., Genome-wide mapping of ORC and Mcm2p binding sites on tiling arrays and identification of essential ARS consensus sequences in S. cerevisiae. BMC Genomics, 7, 2006, 276.
58. Yamamoto, T., Moerschell, R.P., Wakem, L.P., Ferguson, D., Sherman, F., Parameters affecting the frequencies of transformation and co-transformation with synthetic oligonucleotides in yeast. Yeast 8 (1992), 935–948.
59. Yang, L., Güell, M., Niu, D., George, H., Lesha, E., Grishin, D., Aach, J., Shrock, E., Xu, W., Poci, J., et al. Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350 (2015), 1101–1104.
60. Zhang, G.C., Kong, I.I., Kim, H., Liu, J.J., Cate, J.H., Jin, Y.S., Construction of a quadruple auxotrophic mutant of an industrial polyploid saccharomyces cerevisiae strain by using RNA-guided Cas9 nuclease. Appl. Environ. Microbiol. 80 (2014), 7694–7701.