Redesign of the monomer-monomer interface of Cre recombinase yields an obligate heterotetrameric complex

Nucleic Acids Research

Volumn 43, Issue 18, 2015, Pages 9076-9085

  Zhang, Chi ^a   Myers, Connie A ^a   Qi, Zongtai ^a   Mitra, Robi D ^b   Corbo, Joseph C ^a   Havranek, James J ^b  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; MONOMER; TETRAMER; DNA; INTEGRASE;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA RECOMBINATION; EMBRYO; ENZYME ENGINEERING; MAMMAL CELL; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; ANIMAL; CELL CULTURE; CHEMISTRY; GENETIC RECOMBINATION; GENETICS; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION;

ANIMALS; CELLS, CULTURED; DNA; INTEGRASES; MICE; MODELS, MOLECULAR; MUTATION; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; RECOMBINATION, GENETIC;

EID: 84984685505     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv901     Document Type: Article

References (40)

1. Sternberg, N. and Hamilton, D. (1981) Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J. Mol. Biol., 150, 467-486.
2. Gu, H., Zou, Y.R. and Rajewsky, K. (1993) Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell, 73, 1155-1164.
3. Saleh-Gohari, N. and Helleday, T. (2004) Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucleic Acids Res., 32, 3683-3688.
4. Rothkamm, K., Kruger, I., Thompson, L.H. and Lobrich, M. (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol., 23, 5706-5715.
5. Bouhassira, E.E., Westerman, K. and Leboulch, P. (1997) Transcriptional behavior of LCR enhancer elements integrated at the same chromosomal locus by recombinase-mediated cassette exchange. Blood, 90, 3332-3344.
6. Schlake, T. and 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.
7. Seibler, J. and Bode, J. (1997) Double-reciprocal crossover mediated by FLP-recombinase: a concept and an assay. Biochemistry, 36, 1740-1747.
8. Bethke, B. and Sauer, B. (1997) Segmental genomic replacement by Cre-mediated recombination: genotoxic stress activation of the p53 promoter in single-copy transformants. Nucleic Acids Res., 25, 2828-2834.
9. Soukharev, S., Miller, J.L. and Sauer, B. (1999) Segmental genomic replacement in embryonic stem cells by double lox targeting. Nucleic Acids Res., 27, e21.
10. Turan, S., Zehe, C., Kuehle, J., Qiao, J. and Bode, J. (2013) Recombinase-mediated cassette exchange (RMCE) - a rapidly-expanding toolbox for targeted genomic modifications. Gene, 515, 1-27.
11. Anderson, R.P., Voziyanova, E. and 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.
12. Buchholz, F. and Stewart, A.F. (2001) Alteration of Cre recombinase site specificity by substrate-linked protein evolution. Nat. Biotechnol., 19, 1047-1052.
13. Santoro, S.W. and Schultz, P.G. (2002) Directed evolution of the site specificity of Cre recombinase. Proc. Natl. Acad. Sci. U.S.A., 99, 4185-4190.
14. Sarkar, I., Hauber, I., Hauber, J. and Buchholz, F. (2007) HIV-1 proviral DNA excision using an evolved recombinase. Science, 316, 1912-1915.
15. Bolusani, S., Ma, C.H., Paek, A., Konieczka, J.H., Jayaram, M. and 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, 5259-5262.
16. Saraf-Levy, T., Santoro, S.W., Volpin, H., Kushnirsky, T., Eyal, Y., Schultz, P.G., Gidoni, D. and Carmi, N. (2006) Site-specific recombination of asymmetric lox sites mediated by a heterotetrameric Cre recombinase complex. Bioorg. Med. Chem., 14, 3081-3089.
17. Loonstra, A., Vooijs, M., Beverloo, H.B., Allak, B.A., van Drunen, E., Kanaar, R., Berns, A. and Jonkers, J. (2001) Growth inhibition and DNA damage induced by Cre recombinase in mammalian cells. Proc. Natl. Acad. Sci. U.S.A., 98, 9209-9214.
18. Szczepek, M., Brondani, V., Buchel, J., Serrano, L., Segal, D.J. and Cathomen, T. (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat. Biotechnol., 25, 786-793.
19. Gelato, K.A., Martin, S.S., Liu, P.H., Saunders, A.A. and Baldwin, E.P. (2008) Spatially directed assembly of a heterotetrameric Cre-Lox synapse restricts recombination specificity. J. Mol. Biol., 378, 653-665.
20. Martin, S.S., Pulido, E., Chu, V.C., Lechner, T.S. and Baldwin, E.P. (2002) The order of strand exchanges in Cre-LoxP recombination and its basis suggested by the crystal structure of a Cre-LoxP Holliday junction complex. J. Mol. Biol., 319, 107-127.
21. Leaver-Fay, A., Tyka, M., Lewis, S.M., Lange, O.F., Thompson, J., Jacak, R., Kaufman, K., Renfrew, P.D., Smith, C.A., Sheffler, W. et al. (2011) ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol., 487, 545-574.
22. Shapovalov, M.V. and Dunbrack, R.L. (2011) A smoothed backbone-dependent rotamer library for proteins derived from adaptive kernel density estimates and regressions. Structure, 19, 844-858.
23. Dantas, G., Corrent, C., Reichow, S.L., Havranek, J.J., Eletr, Z.M., Isern, N.G., Kuhlman, B., Varani, G., Merritt, E.A. and Baker, D. (2007) High-resolution structural and thermodynamic analysis of extreme stabilization of human procarboxypeptidase by computational protein design. J. Mol. Biol., 366, 1209-1221.
24. Studier, F.W. (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expr. Purif., 41, 207-234.
25. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R. et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci., 13, 133-140.
26. Hsiau, T.H., Diaconu, C., Myers, C.A., Lee, J., Cepko, C.L. and Corbo, J.C. (2007) The cis-regulatory logic of the mammalian photoreceptor transcriptional network. PLoS One, 2, e643.
27. Akimoto, M., Cheng, H., Zhu, D., Brzezinski, J.A., Khanna, R., Filippova, E., Oh, E.C., Jing, Y., Linares, J.L., Brooks, M. et al. (2006) Targeting of GFP to newborn rods by Nrl promoter and temporal expression profiling of flow-sorted photoreceptors. Proc. Natl. Acad. Sci. U.S.A., 103, 3890-3895.
28. Montana, C.L., Myers, C.A. and Corbo, J.C. (2013) Quantifying the activity of cis-regulatory elements in the mouse retina by explant electroporation. Methods Mol. Biol., 935, 329-340.
29. Sheren, J., Langer, S.J. and Leinwand, L.A. (2007) A randomized library approach to identifying functional lox site domains for the Cre recombinase. Nucleic Acids Res., 35, 5464-5473.
30. Hirrlinger, J., Scheller, A., Hirrlinger, P.G., Kellert, B., Tang, W., Wehr, M.C., Goebbels, S., Reichenbach, A., Sprengel, R., Rossner, M.J. et al. (2009) Split-cre complementation indicates coincident activity of different genes in vivo. PLoS One, 4, e4286.
31. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A. et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science, 339, 819-823.
32. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A. and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 337, 816-821.
33. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E. and Church, G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
34. Hsu, P.D., Lander, E.S. and Zhang, F. (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell, 157, 1262-1278.
35. Elliott, B., Richardson, C., Winderbaum, J., Nickoloff, J.A. and Jasin, M. (1998) Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol., 18, 93-101.
36. Wallace, H.A., Marques-Kranc, F., Richardson, M., Luna-Crespo, F., Sharpe, J.A., Hughes, J., Wood, W.G., Higgs, D.R. and Smith, A.J.H. (2007) Manipulating the mouse genome to engineer precise functional syntenic replacements with human sequence. Cell, 128, 197-209.
37. Karimova, M., Abi-Ghanem, J., Berger, N., Surendranath, V., Pisabarro, M.T. and Buchholz, F. (2013) Vika/vox, a novel efficient and specific Cre/loxP-like site-specific recombination system. Nucleic Acids Res., 41, e37.
38. Sauer, B. and McDermott, J. (2004) DNA recombination with a heterospecific Cre homolog identified from comparison of the pac-c1 regions of P1-related phages. Nucleic Acids Res., 32, 6086-6095.
39. Suzuki, E. and Nakayama, M. (2011) VCre/VloxP and SCre/SloxP: new site-specific recombination systems for genome engineering. Nucleic Acids Res., 39, e49.
40. Nunes-Duby, S.E., Kwon, H.J., Tirumalai, R.S., Ellenberger, T. and Landy, A. (1998) Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res., 26, 391-406.