Selection of bacteriophage λ integrases with altered recombination specificity by in vitro compartmentalization

Nucleic Acids Research

Volumn 38, Issue 4, 2009, Pages

  Tay, Yvonne ^a   Ho, Candice ^a   Drooge, Peter ^b   Ghadessy, Farid J ^a  

^a p53 Laboratory   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; INTEGRASE; BACTERIOPHAGE RECEPTOR;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE LAMBDA; BIOTECHNOLOGY; CELL COMPARTMENTALIZATION; CELL STRAIN HEK293; CONTROLLED STUDY; DNA SEQUENCE; ENZYME REGULATION; ENZYME SPECIFICITY; GENE MUTATION; GENE TARGETING; GENETIC MANIPULATION; GENETIC RECOMBINATION; GENETIC SELECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; CELL LINE; CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; ENZYMOLOGY; EVALUATION; GENETICS; METABOLISM; METHODOLOGY; MUTATION; NUCLEOTIDE SEQUENCE; PLASMID; SEQUENCE ALIGNMENT;

ENTEROBACTERIA PHAGE LAMBDA;

ATTACHMENT SITES, MICROBIOLOGICAL; BACTERIOPHAGE LAMBDA; BASE SEQUENCE; CELL LINE; DIRECTED MOLECULAR EVOLUTION; DNA; HUMANS; INTEGRASES; MUTATION; PLASMIDS; RECOMBINATION, GENETIC; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 77951182287     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1089     Document Type: Article

References (50)

1. Metzger, D. and Feil, R. (1999) Engineering the mouse genome by site-specific recombination. Curr. Opin. Biotechnol., 10, 470-476.
2. Nagy, A. (2000) Cre recombinase: the universal reagent for genome tailoring. Genesis, 26, 99-109.
3. Seibler, J., Schubeler, D., Fiering, S., Groudine, M. and Bode, J. (1998) DNA cassette exchange in ES cells mediated by Flp recombinase: an efficient strategy for repeated modification of tagged loci by marker-free constructs. Biochemistry, 37, 6229-6234.
4. Birling, M.C., Gofflot, F. and Warot, X. (2009) Site-specific recombinases for manipulation of the mouse genome. Methods Mol. Biol., 561, 245-263.
5. Irion, S., Luche, H., Gadue, P., Fehling, H.J., Kennedy, M. and Keller, G. (2007) Identification and targeting of the ROSA26 locus in human embryonic stem cells. Nat. Biotechnol., 25, 1477-1482.
6. Coates, C.J., Kaminski, J.M., Summers, J.B., Segal, D.J., Miller, A.D. and Kolb, A.F. (2005) Site-directed genome modification: derivatives of DNA-modifying enzymes as targeting tools. Trends Biotechnol., 23, 407-419.
7. Collins, C.H., Yokobayashi, Y., Umeno, D. and Arnold, F.H. (2003) Engineering proteins that bind, move, make and break DNA. Curr. Opin. Biotechnol., 14, 665.
8. Zhou, R. and Droge, P. (2006) High-precision surgery in the genome of human stem cells. Curr. Genomics, 7, 427-433.
9. Sarkar, I., Hauber, I., Hauber, J. and Buchholz, F. (2007) HIV-1 proviral DNA excision using an evolved recombinase. Science, 316, 1912-1915.
10. Buchholz, F. and Stewart, A.F. (2001) Alteration of Cre recombinase site specificity by substrate-linked protein evolution. Nat. Biotechnol., 19, 1047-1052.
11. Sclimenti, C.R., Thyagarajan, B. and Calos, M.P. (2001) Directed evolution of a recombinase for improved genomic integration at a native human sequence. Nucleic Acids Res., 29, 5044-5051.
12. 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, 5259-5269.
13. Akopian, A., He, J., Boocock, M.R. and Stark, W.M. (2003) Chimeric recombinases with designed DNA sequence recognition. Proc. Natl Acad. Sci. USA, 100, 8688-8691.
14. Gordley, R.M., Gersbach, C.A. and Barbas, C.F. III. (2009) Synthesis of programmable integrases. Proc. Natl Acad. Sci. USA, 106, 5053-5058.
15. Porteus, M.H. (2006) Mammalian gene targeting with designed zinc finger nucleases. Mol. Ther., 13, 438-446.
16. Porteus, M.H. and Carroll, D. (2005) Gene targeting using zinc finger nucleases. Nat. Biotechnol., 23, 967-973.
17. Dorgai, L., Yagil, E. and Weisberg, R.A. (1995) Identifying determinants of recombination specificity: construction and characterization of mutant bacteriophage integrases. J. Mol. Biol., 252, 178-188.
18. Yagil, E., Dorgai, L. and Weisberg, R.A. (1995) Identifying determinants of recombination specificity: construction and characterization of chimeric bacteriophage integrases. J. Mol. Biol., 252, 163-177.
19. Cheng, Q., Swalla, B.M., Beck, M., Alcaraz, R. Jr, Gumport, R.I. and Gardner, J.F. (2000) Specificity determinants for bacteriophage Hong Kong 022 integrase: analysis of mutants with relaxed core-binding specificities. Mol. Microbiol., 36, 424-436.
20. Buchholz, F., Angrand, P.O. and Stewart, A.F. (1998) Improved properties of FLP recombinase evolved by cycling mutagenesis. Nat. Biotechnol., 16, 657-662.
21. Calmels, C., de Soultrait, V.R., Caumont, A., Desjobert, C., Faure, A., Fournier, M., Tarrago-Litvak, L. and Parissi, V. (2004) Biochemical and random mutagenesis analysis of the region carrying the catalytic E152 amino acid of HIV-1 integrase. Nucleic Acids Res., 32, 1527-1538.
22. Griffiths, A.D. and Tawfik, D.S. (2006) Miniaturising the laboratory in emulsion droplets. Trends Biotechnol., 24, 395-402.
23. Tawfik, D.S. and Griffiths, A.D. (1998) Man-made cell-like compartments for molecular evolution. Nat. Biotechnol., 16, 652-656.
24. Cohen, H.M., Tawfik, D.S. and Griffiths, A.D. (2004) Altering the sequence specificity of HaeIII methyltransferase by directed evolution using in vitro compartmentalization. Protein Eng. Des. Sel., 17, 3-11.
25. Fen, C.X., Coomber, D.W., Lane, D.P. and Ghadessy, F.J. (2007) Directed evolution of p53 variants with altered DNA-binding specificities by in vitro compartmentalization. J. Mol. Biol., 371, 1238-1248.
26. Zheng, Y. and Roberts, R.J. (2007) Selection of restriction endonucleases using artificial cells. Nucleic Acids Res., 35, e83.
27. Ghadessy, F.J., Ong, J.L. and Holliger, P. (2001) Directed evolution of polymerase function by compartmentalized self-replication. Proc. Natl Acad. Sci. USA, 98, 4552-4557.
28. Ghadessy, F.J., Ramsay, N., Boudsocq, F., Loakes, D., Brown, A., Iwai, S., Vaisman, A., Woodgate, R. and Holliger, P. (2004) Generic expansion of the substrate spectrum of a DNA polymerase by directed evolution. Nat. Biotechnol., 22, 755-759.
29. Campbell, A.M. (ed.) (1962), Episomes. Academic Press, New York.
30. Nash, H.A. (1974) Purification of bacteriophage ( Int protein. Nature, 247, 923-929.
31. Suttie, J.L., Chilton, M. and Que, Q. (2008) US patent no. 7351877.
32. Christ, N., Corona, T. and Droge, P. (2002) Site-specific recombination in eukaryotic cells mediated by mutant lambda integrases: implications for synaptic complex formation and the reactivity of episomal DNA segments. J. Mol. Biol., 319, 305-314.
33. Droge, P. and Enenkel, B. (2005) EP patent no.1565562 (A1).
34. Landy, A. (1989) Dynamic, structural, and regulatory aspects of lambda site-specific recombination. Annu. Rev. Biochem., 58, 913-949.
35. Radman-Livaja, M., Biswas, T., Ellenberger, T., Landy, A. and Aihara, H. (2006) DNA arms do the legwork to ensure the directionality of lambda site-specific recombination. Curr. Opin. Struct. Biol., 16, 42-50.
36. Radman-Livaja, M., Shaw, C., Azaro, M., Biswas, T., Ellenberger, T. and Landy, A. (2003) Arm sequences contribute to the architecture and catalytic function of a lambda integrase-Holliday junction complex. Mol. Cell, 11, 783-794.
37. Christ, N. and Droge, P. (2002) Genetic manipulation of mouse embryonic stem cells by mutant lambda integrase. Genesis, 32, 203-208.
38. Vartanian, J.P., Henry, M. and Wain-Hobson, S. (1996) Hypermutagenic PCR involving all four transitions and a sizeable proportion of transversions. Nucleic Acids Res., 24, 2627-2631.
39. Zaccolo, M. and Gherardi, E. (1999) The effect of high-frequency random mutagenesis on in vitro protein evolution: a study on TEM-1 beta-lactamase. J. Mol. Biol., 285, 775-783.
40. Kazmierczak, R.A., Swalla, B.M., Burgin, A.B., Gumport, R.I. and Gardner, J.F. (2002) Regulation of site-specific recombination by the C-terminus of λ integrase. Nucleic Acids Res., 30, 5193-5204.
41. Zhao, H., Giver, L., Shao, Z., Affholter, J.A. and Arnold, F.H. (1998) Molecular evolution by staggered extension process (StEP) in vitro recombination. Nat. Biotechnol., 16, 258-261.
42. Ross, W. and Landy, A. (1983) Patterns of lambda Int recognition in the regions of strand exchange. Cell, 33, 261-272.
43. Lorbach, E., Christ, N., Schwikardi, M. and Droge, P. (2000) Site-specific recombination in human cells catalyzed by phage lambda integrase mutants. J. Mol. Biol., 296, 1175-1181.
44. Biswas, T., Aihara, H., Radman-Livaja, M., Filman, D., Landy, A. and Ellenberger, T. (2005) A structural basis for allosteric control of DNA recombination by lambda integrase. Nature, 435, 1059-1066.
45. Sarkar, D., Radman-Livaja, M. and Landy, A. (2001) The small DNA binding domain of lambda integrase is a context-sensitive modulator of recombinase functions. EMBO J., 20, 1203-1212.
46. Hazelbaker, D., Azaro, M.A. and Landy, A. (2008) A biotin interference assay highlights two different asymmetric interaction profiles for lambda integrase arm-type binding sites in integrative versus excisive recombination. J. Biol. Chem., 283, 12402-12414.
47. Warren, D., Lee, S.Y. and Landy, A. (2005) Mutations in the amino-terminal domain of lambda-integrase have differential effects on integrative and excisive recombination. Mol. Microbiol., 55, 1104-1112.
48. Tan, S.M. and Droge, P. (2005) Comparative analysis of sequence-specific DNA recombination systems in human embryonic stem cells. Stem Cells, 23, 868-873.
49. Hartley, J.L., Temple, G.F. and Brasch, M.A. (2000) DNA cloning using in vitro site-specific recombination. Genome Res., 10, 1788-1795.
50. Fadeev, E.A., Sam, M.D. and Clubb, R.T. (2009) NMR structure of the amino-terminal domain of the lambda integrase protein in complex with DNA: immobilization of a flexible tail facilitates beta-sheet recognition of the major groove. J. Mol. Biol., 388, 682-690.