Target-specific variants of Flp recombinase mediate genome engineering reactions in mammalian cells

FEBS Journal

Volumn 282, Issue 17, 2015, Pages 3323-3333

  Shah, Riddhi ^a   Li, Feng ^a   Voziyanova, Eugenia ^a   Voziyanov, Yuri ^a  

^a LOUISIANA TECH UNIVERSITY   (United States)

Author keywords

Flp; gene targeting; genome engineering; RMCE; site specific recombination

Indexed keywords

INTERLEUKIN 10; RECOMBINASE; CODON; CRE RECOMBINASE; DNA POLYMERASE; ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCENT PROTEIN 583; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; IL10 PROTEIN, HUMAN; INTEGRASE; PHOTOPROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHO CELL LINE; CODON; CONTROLLED STUDY; EMBRYO; FEMALE; GENE CASSETTE; GENETIC ENGINEERING; GENETIC MANIPULATION; GENETIC VARIABILITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; INTERLEUKIN 10 GENE; MAMMAL CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; RECOMBINASE GENE; ANIMAL; CHEMISTRY; CRICETULUS; GENE EXPRESSION; GENETIC RECOMBINATION; GENETICS; GENOME; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLASMID; PROCEDURES; REPORTER GENE; SACCHAROMYCES CEREVISIAE;

ANIMALS; BASE SEQUENCE; CHO CELLS; CODON; CRICETULUS; DNA NUCLEOTIDYLTRANSFERASES; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, REPORTER; GENETIC ENGINEERING; GENOME; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; INTEGRASES; INTERLEUKIN-10; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; PLASMIDS; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE;

EID: 84940722801     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13345     Document Type: Article

References (46)

1. Holt N, Wang J, Kim K, Friedman G, Wang X, Taupin V, Crooks GM, Kohn DB, Gregory PD, Holmes MC, 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.
2. Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, et al,. (2011) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29, 143-148.
3. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG 2nd, Tan W, Penheiter SG, Ma AC, Leung AY, et al,. (2012) In vivo genome editing using a high-efficiency TALEN system. Nature 491, 114-118.
4. Carlson DF, Tan W, Lillico SG, Stverakova D, Proudfoot C, Christian M, Voytas DF, Long CR, Whitelaw CB, &, Fahrenkrug SC, (2012) Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci USA 109, 17382-17387.
5. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, et al,. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823.
6. Gaj T, Gersbach CA, &, Barbas CF, 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31, 397-405.
7. Mali P, Yang L, Esvelt KM, Aach J, Guell M, Dicarlo JE, Norville JE, &, Church GM, (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826.
8. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, &, Jaenisch R, (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918.
9. Niu Y, Shen B, Cui Y, Chen Y, Wang J, Wang L, Kang Y, Zhao X, Si W, Li W, et al,. (2014) Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156, 836-843.
10. Kilby NJ, Snaith MR, &, Murray JA, (1993) Site-specific recombinases: tools for genome engineering. Trends Genet 9, 413-421.
11. Buchholz F, Refaeli Y, Trumpp A, &, Bishop JM, (2000) Inducible chromosomal translocation of AML1 and ETO genes through Cre/loxP-mediated recombination in the mouse. EMBO Rep 1, 133-139.
12. Mills AA, &, Bradley A, (2001) From mouse to man: generating megabase chromosome rearrangements. Trends Genet 17, 331-339.
13. Glaser S, Anastassiadis K, &, Stewart AF, (2005) Current issues in mouse genome engineering. Nat Genet 37, 1187-1193.
14. Calos MP, (2006) The phiC31 integrase system for gene therapy. Curr Gene Ther 6, 633-645.
15. Wirth D, Gama-Norton L, Riemer P, Sandhu U, Schucht R, &, Hauser H, (2007) Road to precision: recombinase-based targeting technologies for genome engineering. Curr Opin Biotechnol 18, 411-419.
16. Osterwalder M, Galli A, Rosen B, Skarnes WC, Zeller R, &, Lopez-Rios J, (2010) Dual RMCE for efficient re-engineering of mouse mutant alleles. Nat Methods 7, 893-895.
17. Turan S, Galla M, Ernst E, Qiao J, Voelkel C, Schiedlmeier B, Zehe C, &, Bode J, (2011) Recombinase-mediated cassette exchange (RMCE): traditional concepts and current challenges. J Mol Biol 407, 193-221.
18. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, Mujica AO, Thomas M, Harrow J, Cox T, et al,. (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342.
19. Gaj T, Sirk SJ, &, Barbas CF 3rd, (2014) Expanding the scope of site-specific recombinases for genetic and metabolic engineering. Biotechnol Bioeng 111, 1-15.
20. Zhu F, Gamboa M, Farruggio AP, Hippenmeyer S, Tasic B, Schule B, Chen-Tsai Y, &, Calos MP, (2014) DICE, an efficient system for iterative genomic editing in human pluripotent stem cells. Nucleic Acids Res 42, e34.
21. Yagil E, Dorgai L, &, Weisberg RA, (1995) Identifying determinants of recombination specificity: construction and characterization of chimeric bacteriophage integrases. J Mol Biol 252, 163-177.
22. Dorgai L, Yagil E, &, Weisberg RA, (1995) Identifying determinants of recombination specificity: construction and characterization of mutant bacteriophage integrases. J Mol Biol 252, 178-188.
23. Stemmer WP, (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370, 389-391.
24. Lorimer IA, &, Pastan I, (1995) Random recombination of antibody single chain Fv sequences after fragmentation with DNaseI in the presence of Mn2 +. Nucleic Acids Res 23, 3067-3068.
25. Zhao H, &, Arnold FH, (1997) Optimization of DNA shuffling for high fidelity recombination. Nucleic Acids Res 25, 1307-1308.
26. Guo F, Gopaul DN, &, Van Duyne GD, (1997) Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389, 40-46.
27. Chen Y, Narendra U, Iype LE, Cox MM, &, Rice PA, (2000) Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Mol Cell 6, 885-897.
28. Buchholz F, &, Stewart AF, (2001) Alteration of Cre recombinase site specificity by substrate-linked protein evolution. Nat Biotechnol 19, 1047-1052.
29. Santoro SW, &, Schultz PG, (2002) Directed evolution of the site specificity of Cre recombinase. Proc Natl Acad Sci USA 99, 4185-4190.
30. Rufer AW, &, Sauer B, (2002) Non-contact positions impose site selectivity on Cre recombinase. Nucleic Acids Res 30, 2764-2771.
31. Sarkar I, Hauber I, Hauber J, &, Buchholz F, (2007) HIV-1 proviral DNA excision using an evolved recombinase. Science 316, 1912-1915.
32. Voziyanov Y, Stewart AF, &, Jayaram M, (2002) A dual reporter screening system identifies the amino acid at position 82 in Flp site-specific recombinase as a determinant for target specificity. Nucleic Acids Res 30, 1656-1663.
33. Voziyanov Y, Konieczka JH, Stewart AF, &, Jayaram M, (2003) Stepwise manipulation of DNA specificity in Flp recombinase: progressively adapting Flp to individual and combinatorial mutations in its target site. J Mol Biol 326, 65-76.
34. Konieczka JH, Paek A, Jayaram M, &, Voziyanov Y, (2004) Recombination of hybrid target sites by binary combinations of Flp variants: mutations that foster interprotomer collaboration and enlarge substrate tolerance. J Mol Biol 339, 365-378.
35. Bolusani S, Ma CH, Paek A, Konieczka JH, Jayaram M, &, Voziyanov Y, (2006) Evolution of variants of yeast site-specific recombinase Flp that utilize native genomic sequences as recombination target sites. Nucleic Acids Res 34, 5259-5269.
36. Shultz JL, Voziyanova E, Konieczka JH, &, Voziyanov Y, (2011) A genome-wide analysis of FRT-like sequences in the human genome. PLoS One 6, e18077.
37. Schlake T, &, Bode J, (1994) Use of mutated FLP recognition target (FRT) sites for the exchange of expression cassettes at defined chromosomal loci. Biochemistry 33, 12746-12751.
38. Turan S, Zehe C, Kuehle J, Qiao J, &, Bode J, (2013) Recombinase-mediated cassette exchange (RMCE)-a rapidly-expanding toolbox for targeted genomic modifications. Gene 515, 1-27.
39. Lauth M, Spreafico F, Dethleffsen K, &, Meyer M, (2002) Stable and efficient cassette exchange under non-selectable conditions by combined use of two site-specific recombinases. Nucleic Acids Res 30, e115.
40. Anderson RP, Voziyanova E, &, Voziyanov Y, (2012) Flp and Cre expressed from Flp-2A-Cre and Flp-IRES-Cre transcription units mediate the highest level of dual recombinase-mediated cassette exchange. Nucleic Acids Res 40, e62.
41. Voziyanova E, Malchin N, Anderson RP, Yagil E, Kolot M, &, Voziyanov Y, (2013) Efficient Flp-Int HK022 dual RMCE in mammalian cells. Nucleic Acids Res 41, e125.
42. Raymond CS, &, Soriano P, (2007) High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PLoS One 2, e162.
43. Shimshek DR, Kim J, Hubner MR, Spergel DJ, Buchholz F, Casanova E, Stewart AF, Seeburg PH, &, Sprengel R, (2002) Codon-improved Cre recombinase (iCre) expression in the mouse. Genesis 32, 19-26.
44. Baubonis W, &, Sauer B, (1993) Genomic targeting with purified Cre recombinase. Nucleic Acids Res 21, 2025-2029.
45. Logie C, &, Stewart AF, (1995) Ligand-regulated site-specific recombination. Proc Natl Acad Sci USA 92, 5940-5944.
46. Blaisonneau J, Sor F, Cheret G, Yarrow D, &, Fukuhara H, (1997) A circular plasmid from the yeast Torulaspora delbrueckii. Plasmid 38, 202-209.