Spatially Directed Assembly of a Heterotetrameric Cre-Lox Synapse Restricts Recombination Specificity

Journal of Molecular Biology

Volumn 378, Issue 3, 2008, Pages 653-665

  Gelato, Kathy A ^a   Martin, Shelley S ^a   Liu, Patty H ^a   Saunders, April A ^a   Baldwin, Enoch P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cre LoxP site specific recombination; directed subunit assembly; library screening selection; orthogonal protein protein interface; protein engineering

Indexed keywords

CRE RECOMBINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; PROTEIN SUBUNIT; TETRAMER;

ARTICLE; DNA RECOMBINATION; DNA SEQUENCE; LOXP SITE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION;

EID: 42249107316     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.02.058     Document Type: Article

References (58)

1. Wolberger C. Multiprotein-DNA complexes in transcriptional regulation. Annu. Rev. Biophys. Biomol. Struct. 28 (1999) 29-56
2. Remenyi A., Scholer H.R., and Wilmanns M. Combinatorial control of gene expression. Nat. Struct. Mol. Biol. 11 (2004) 812-815
3. Calkhoven C.F., and Ab G. Multiple steps in the regulation of transcription-factor level and activity. Biochem. J. 317 (1996) 329-342
4. Chen F.E., and Ghosh G. Regulation of DNA binding by Rel/NF-kappaB transcription factors: structural views. Oncogene 18 (1999) 6845-6852
5. Kewley R.J., Whitelaw M.L., and Chapman-Smith A. The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int. J. Biochem. Cell Biol. 36 (2004) 189-204
6. Mann R.S. The specificity of homeotic gene function. Bioessays 17 (1995) 855-863
7. Landy A. Mechanistic and structural complexity in the site-specific recombination pathways of Int and FLP. Curr. Opin. Genet. Dev. 3 (1993) 699-707
8. Sadowski P.D. Site-specific genetic recombination: hops, flips, and flops. FASEB J. 7 (1993) 760-767
9. Sherratt D.J., Arciszewska L.K., Blakely G., Colloms S., Grant K., Leslie N., and McCulloch R. Site-specific recombination and circular chromosome segregation. Philos. Trans. R. Soc. London, Ser. B 347 (1995) 37-42
10. Jayaram M., Mehta S., Uzri D., Voziyanov Y., and Velmurugan S. Site-specific recombination and partitioning systems in the stable high copy propagation of the 2-micron yeast plasmid. Prog. Nucleic. Acid Res. Mol. Biol. 77 (2004) 127-172
11. Ow D.W. Recombinase-directed plant transformation for the post-genomic era. Plant Mol. Biol. 48 (2002) 183-200
12. Branda C.S., and Dymecki S.M. Talking about a revolution: the impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 6 (2004) 7-28
13. Jones J.R., Shelton K.D., and Magnuson M.A. Strategies for the use of site-specific recombinases in genome engineering. Methods Mol. Med. 103 (2005) 245-257
14. Oberstein A., Pare A., Kaplan L., and Small S. Site-specific transgenesis by Cre-mediated recombination in Drosophila. Nat. Methods 2 (2005) 583-585
15. Garcia-Otin A.L., and Guillou F. Mammalian genome targeting using site-specific recombinases. Front. Biosci. 11 (2006) 1108-1136
16. Sarkar I., Hauber I., Hauber J., and Buchholz F. HIV-1 proviral DNA excision using an evolved recombinase. Science 316 (2007) 1912-1915
17. Schmidt-Supprian M., and Rajewsky K. Vagaries of conditional gene targeting. Nat. Immunol. 8 (2007) 665-668
18. Sternberg N., Hamilton D., Austin S., Yarmolinsky M., and Hoess R. Site-specific recombination and its role in the life cycle of bacteriophage P1. Cold Spring Harbor Symp. Quant. Biol. 45 (1981) 297-309
19. Hoess R.H., Ziese M., and Sternberg N. P1 site-specific recombination: nucleotide sequence of the recombining sites. Proc. Natl Acad. Sci. USA 79 (1982) 3398-3402
20. Hoess R.H., and Abremski K. Mechanism of strand cleavage and exchange in the Cre-lox site-specific recombination system. J. Mol. Biol. 181 (1985) 351-362
21. Hoess R., Wierzbicki A., and Abremski K. Isolation and characterization of intermediates in site-specific recombination. Proc. Natl Acad. Sci. USA 84 (1987) 6840-6844
22. Van Duyne G.D. A structural view of cre-loxp site-specific recombination. Annu. Rev. Biophys. Biomol. Struct. 30 (2001) 87-104
23. Grindley N.D., Whiteson K.L., and Rice P.A. Mechanisms of site-specific recombination. Annu. Rev. Biochem. 75 (2006) 567-605
24. Guo F., Gopaul D.N., and van Duyne G.D. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389 (1997) 40-46
25. Santoro S.W., and Schultz P.G. Directed evolution of the site specificity of Cre recombinase. Proc. Natl Acad. Sci. USA 99 (2002) 4185-4190
26. Saraf-Levy T., Santoro S.W., Volpin H., Kushnirsky T., Eyal Y., Schultz P.G., et al. Site-specific recombination of asymmetric lox sites mediated by a heterotetrameric Cre recombinase complex. Bioorg. Med. Chem. 14 (2006) 3081-3089
27. Lee L., and Sadowski P.D. Sequence of the loxP site determines the order of strand exchange by the Cre recombinase. J. Mol. Biol. 326 (2003) 397-412
28. Lee L., and Sadowski P.D. Strand selection by the tyrosine recombinases. In: Moldave K. (Ed). Prog. Nucleic. Acid Res. Mol. Biol. vol. 80 (2005), Academic Press, New York 1-42
29. Gelato K.A., Martin S.S., and Baldwin E.P. Reversed DNA strand cleavage specificity in initiation of Cre-LoxP recombination induced by the His289Ala active-site substitution. J. Mol. Biol. 354 (2005) 233-245
30. Ghosh K., Guo F., and Van Duyne G.D. Synapsis of loxP sites by Cre recombinase. J. Biol. Chem. 282 (2007) 24004-24016
31. Hartung M., and Kisters-Woike B. Cre mutants with altered DNA binding properties. J. Biol. Chem. 273 (1998) 22884-22891
32. Rufer A.W., and Sauer B. Non-contact positions impose site selectivity on Cre recombinase. Nucleic Acids Res. 30 (2002) 2764-2771
33. Gelato K.A., Martin S.S., Wong S., and Baldwin E.P. Multiple levels of affinity-dependent DNA discrimination in Cre-LoxP recombination. Biochemistry 45 (2006) 12216-12226
34. Buchholz F., and Stewart A.F. Alteration of Cre recombinase site specificity by substrate-linked protein evolution. Nat. Biotechnol. 19 (2001) 1047-1052
35. Bolusani S., Ma C.H., Paek A., Konieczka J.H., Jayaram M., and Voziyanov Y. Evolution of variants of yeast site-specific recombinase Flp that utilize native genomic sequences as recombination target sites. Nucleic Acids Res. 34 (2006) 5259-5269
36. Martin S.S., Chu V.C., and Baldwin E. Modulation of the active complex assembly and turnover rate by protein-DNA interactions in Cre-LoxP recombination. Biochemistry 42 (2003) 6814-6826
37. Porteus M.H., and Baltimore D. Chimeric nucleases stimulate gene targeting in human cells. Science 300 (2003) 763
38. Alwin S., Gere M.B., Guhl E., Effertz K., Barbas III C.F., Segal D.J., et al. Custom zinc-finger nucleases for use in human cells. Mol. Ther. 12 (2005) 610-617
39. Chevalier B.S., Kortemme T., Chadsey M.S., Baker D., Monnat R.J., and Stoddard B.L. Design, activity, and structure of a highly specific artificial endonuclease. Mol. Cell 10 (2002) 895-905
40. Nautiyal S., Woolfson D.N., King D.S., and Alber T. A designed heterotrimeric coiled coil. Biochemistry 34 (1995) 11645-11651
41. Arndt K.M., Pelletier J.N., Muller K.M., Alber T., Michnick S.W., and Pluckthun A. A heterodimeric coiled-coil peptide pair selected in vivo from a designed library-versus-library ensemble. J. Mol. Biol. 295 (2000) 627-639
42. Ali M.H., Taylor C.M., Grigoryan G., Allen K.N., Imperiali B., and Keating A.E. Design of a heterospecific, tetrameric, 21-residue miniprotein with mixed alpha/beta structure. Structure 13 (2005) 225-234
43. Kortemme T., Joachimiak L.A., Bullock A.N., Schuler A.D., Stoddard B.L., and Baker D. Computational redesign of protein-protein interaction specificity. Nat. Struct. Mol. Biol. 11 (2004) 371-379
44. Baldwin E.P., Martin S.S., Abel J., Gelato K.A., Kim H., Schultz P.G., and Santoro S.W. A specificity switch in selected cre recombinase variants is mediated by macromolecular plasticity and water. Chem. Biol. 10 (2003) 1085-1094
45. Ringrose L., Lounnas V., Ehrlich L., Buchholz F., Wade R., and Stewart A.F. Comparative kinetic analysis of FLP and cre recombinases: mathematical models for DNA binding and recombination. J. Mol. Biol. 284 (1998) 363-384
46. Thyagarajan B., Guimaraes M.J., Groth A.C., and Calos M.P. Mammalian genomes contain active recombinase recognition sites. Gene 244 (2000) 47-54
47. Semprini S., Troup T.J., Kotelevtseva N., King K., Davis J.R., Mullins L.J., et al. Cryptic loxP sites in mammalian genomes: genome-wide distribution and relevance for the efficiency of BAC/PAC recombineering techniques. Nucleic Acids Res. 35 (2007) 1402-1410
48. Miller J.C., Holmes M.C., Wang J., Guschin D.Y., Lee Y.L., Rupniewski I., et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat. Biotechnol. 25 (2007) 778-785
49. Szczepek M., Brondani V., Buchel J., Serrano L., Segal D.J., and Cathomen T. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat. Biotechnol. 25 (2007) 786-793
50. Blakely G., May G., McCulloch R., Arciszewska L.K., Burke M., Lovett S.T., and Sherratt D.J. Two related recombinases are required for site-specific recombination at dif and cer in E. coli K12. Cell 75 (1993) 351-361
51. Hayes F., and Sherratt D.J. Recombinase binding specificity at the chromosome dimer resolution site dif of Escherichia coli. J. Mol. Biol. 266 (1997) 525-537
52. Blakely G.W., and Sherratt D.J. Interactions of the site-specific recombinases XerC and XerD with the recombination site dif. Nucleic Acids Res. 22 (1994) 5613-5620
53. Hallet B., Arciszewska L.K., and Sherratt D.J. Reciprocal control of catalysis by the tyrosine recombinases XerC and XerD: an enzymatic switch in site-specific recombination. Mol. Cell 4 (1999) 949-959
54. Baldwin E., Xu J., Hajiseyedjavadi O., Baase W.A., and Matthews B.W. Thermodynamic and structural compensation in "size-switch" core repacking variants of bacteriophage T4 lysozyme. J. Mol. Biol. 259 (1996) 542-559
55. Baldwin E.P., and Matthews B.W. Core-packing constraints, hydrophobicity and protein design. Curr. Opin. Biotechnol. 5 (1994) 396-402
56. Woods K.C., Martin S.S., Chu V.C., and Baldwin E.P. Quasi-equivalence in site-specific recombinase structure and function: crystal structure and activity of trimeric Cre recombinase bound to a three-way Lox DNA junction. J. Mol. Biol. 313 (2001) 49-69
57. Russell C.B., and Dahlquist F.W. Exchange of chromosomal and plasmid alleles in Escherichia coli by selection for loss of a dominant antibiotic sensitivity marker. J. Bacteriol. 171 (1989) 2614-2618
58. Kunkel T.A., Bebenek K., and McClary J. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204 (1991) 125-139