Critical amino acid residues within the φc31 integrase DNA-binding domain affect recombination activities in mammalian cells

Human Gene Therapy

Volumn 21, Issue 9, 2010, Pages 1104-1118

  Liesner, Raphael ^a   Zhang, Wenli ^a   Noske, Nadja ^a   Ehrhardt, Anja ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; BLOOD CLOTTING FACTOR 9; PHI C31 INTEGRASE; RECOMBINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HCT116; CELL STRAIN HEK293; DNA BINDING MOTIF; FEMALE; GENETIC RECOMBINATION; HELA CELL; HUMAN; HUMAN CELL; MAMMAL CELL; MAMMALIAN GENETICS; MOUSE; NONHUMAN; POINT MUTATION; SITE DIRECTED MUTAGENESIS;

AMINO ACIDS; ANIMALS; ATTACHMENT SITES, MICROBIOLOGICAL; BACTERIOPHAGES; BIOCATALYSIS; BIOLOGICAL ASSAY; CELL LINE, TUMOR; FACTOR IX; HUMANS; INTEGRASES; LIVER; MAMMALS; MICE; MUTANT PROTEINS; PLASMIDS; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; STRUCTURE-ACTIVITY RELATIONSHIP; VIRUS INTEGRATION;

MAMMALIA;

EID: 77957843252     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2010.034     Document Type: Article

References (42)

1. Allen, B.G., and Weeks, D.L. (2009). Bacteriophage fC31 in-tegrase mediated transgenesis in Xenopus laevis for protein expression at endogenous levels. Methods Mol. Biol. 518, 113-122.
2. Andreas, S., Schwenk, F., Kuter-Luks, B., Faust, N., and Kuhn, R. (2002). Enhanced efficiency through nuclear localization signal fusion on phage fC31-integrase: Activity comparison with Cre and FLPe recombinase in mammalian cells. Nucleic Acids Res. 30, 2299-2306.
3. Belteki, G., Gertsenstein, M., Ow, D.W., and Nagy, A. (2003). Site-specific cassette exchange and germline transmission with mouse ES cells expressing fC31 integrase. Nat. Biotechnol. 21, 321-324.
4. Blaas, L., Musteanu, M., Zenz, R., Eferl, R., and Casanova, E. (2007). fC31-mediated cassette exchange into a bacterial artificial chromosome. Biotechniques 43, 659-660, 662, 664.
5. Cathomen, T., and Joung, J.K. (2008). Zinc-finger nucleases: The next generation emerges. Mol. Ther. 16, 1200-1207.
6. Chalberg, T.W., Portlock, J.L., Olivares, E.C., Thyagarajan, B., Kirby, P.J., Hillman, R.T., Hoelters, J., and Calos, M.P. (2006). Integration specificity of phage fC31 integrase in the human genome. J. Mol. Biol. 357, 28-48.
7. Chen, J.Z., Ji, C.N., Xu, G.L., Pang, R.Y., Yao, J.H., Zhu, H.Z., Xue, J.L., and Jia, W. (2006). DAXX interacts with phage fC31 integrase and inhibits recombination. Nucleic Acids Res. 34, 6298-6304.
8. Cuff, J.A., and Barton, G.J. (2000). Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins 40, 502-511.
9. Ehrhardt, A., Xu, H., Huang, Z., Engler, J.A., and Kay, M.A. (2005). A direct comparison of two nonviral gene therapy vectors for somatic integration: In vivo evaluation of the bac-teriophage integrase fC31 and the Sleeping Beauty transpo-sase. Mol. Ther. 11, 695-706.
10. Ehrhardt, A., Engler, J.A., Xu, H., Cherry, A.M., and Kay, M.A. (2006). Molecular analysis of chromosomal rearrangements in mammalian cells after fC31-mediated integration. Hum. Gene Ther. 17, 1077-1094.
11. Ehrhardt, A., Yant, S.R., Giering, J.C., Xu, H., Engler, J.A., and Kay, M.A. (2007). Somatic integration from an adenoviral hybrid vector into a hot spot in mouse liver results in persistent transgene expression levels in vivo. Mol. Ther. 15, 146-156.
12. Geurts, A.M., Yang, Y., Clark, K.J., Liu, G., Cui, Z., Dupuy, A.J., Bell, J.B., Largaespada, D.A., and Hackett, P.B. (2003). Gene transfer into genomes of human cells by the Sleeping Beauty transposon system. Mol. Ther. 8, 108-117.
13. Groth, A.C., Olivares, E.C., Thyagarajan, B., and Calos, M.P. (2000). A phage integrase directs efficient site-specific integration in human cells. Proc. Natl. Acad. Sci. U.S.A. 97, 5995-6000.
14. Ivics, Z., Katzer, A., Stuwe, E.E., Fiedler, D., Knespel, S., and Izsvak, Z. (2007). Targeted Sleeping Beauty transposition in human cells. Mol. Ther. 15, 1137-1144.
15. Kalderon, D., Roberts, B.L., Richardson, W.D., and Smith, A.E. (1984). A short amino acid sequence able to specify nuclear location. Cell 39, 499-509.
16. Keravala, A., Lee, S., Thyagarajan, B., Olivares, E.C., Gabrovsky, V.E., Woodard, L.E., and Calos, M.P. (2009). Mutational derivatives of fC31 integrase with increased efficiency and specificity. Mol. Ther. 17, 112-120.
17. Liu, F., Song, Y., and Liu, D. (1999). Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6, 1258-1266.
18. Liu, J., Jeppesen, I., Nielsen, K., and Jensen, T.G. (2006). fc31 integrase induces chromosomal aberrations in primary human fibroblasts. Gene Ther. 13, 1188-1190.
19. Liu, S., Ma, J., Wang, W., Zhang, M., Xin, Q., Peng, S., Li, R., and Zhu, H. (2010). Mutational analysis of highly conserved residues in the phage fC31 integrase reveals key amino acids necessary for the DNA recombination. PLoS One 5, e8863.
20. Mates, L., Chuah, M.K., Belay, E., Jerchow, B., Manoj, N., Costa-Sanchez, A., Grzela, D.P., Schmitt, A., Becker, K., Matrai, J., Ma, L., Samara-Kuko, E., Gysemans, C., Pryputniewicz, D., Miskey, C., Fletcher, B., Vandendriessche, T., Ivics, Z., and Izsvak, Z. (2009). Molecular evolution of a novel hyperactive Sleeping Beauty transposase enables robust stable gene transfer in vertebrates. Nat. Genet. 41, 753-761.
21. Maucksch, C., Aneja, M.K., Hennen, E., Bohla, A., Hoffmann, F., Elfinger, M., Rosenecker, J., and Rudolph, C. (2008). Cell type differences in activity of the Streptomyces bacteriophage fC31 integrase. Nucleic Acids Res. 36, 5462-5471.
22. McEwan, A.R., Rowley, P.A., and Smith, M.C. (2009). DNA binding and synapsis by the large C-terminal domain of fC31 integrase. Nucleic Acids Res. 37, 4764-4773.
23. Miao, C.H., Ohashi, K., Patijn, G.A., Meuse, L., Ye, X., Thompson, A.R., and Kay, M.A. (2000). Inclusion of the hepatic locus control region, an intron, and untranslated region increases and stabilizes hepatic factor IX gene expression in vivo but not in vitro. Mol. Ther. 1, 522-532.
24. Olivares, E.C., Hollis, R.P., Chalberg, T.W., Meuse, L., Kay, M.A., and Calos, M.P. (2002). Site-specific genomic integration produces therapeutic factor IX levels in mice. Nat. Biotechnol. 20, 1124-1128.
25. Ortiz-Urda, S., Thyagarajan, B., Keene, D.R., Lin, Q., Fang, M., Ca-los, M.P., and Khavari, P.A. (2002). Stable nonviral genetic correction of inherited human skin disease. Nat. Med. 8, 1166-1170.
26. Porteus, M. H., and Carroll, D. (2005). Gene targeting using zinc finger nucleases. Nat. Biotechnol. 23, 967-973.
27. Raymond, C.S., and Soriano, P. (2007). High-efficiency FLP and fC31 site-specific recombination in mammalian cells. PLoS One 2, e162.
28. Recchia, A., Parks, R.J., Lamartina, S., Toniatti, C., Pieroni, L., Palombo, F., Ciliberto, G., Graham, F.L., Cortese, R., La Monica, N., and Colloca, S. (1999). Site-specific integration mediated by a hybrid adenovirus/adeno-associated virus vector. Proc. Natl. Acad. Sci. U.S.A. 96, 2615-2620. (Pubitemid 29148766)
29. Rowley, P.A., and Smith, M.C. (2008). Role of the N-terminal domain of fC31 integrase in attB-attP synapsis. J. Bacteriol. 190, 6918-6921.
30. Rowley, P.A., Smith, M.C., Younger, E., and Smith, M.C. (2008). A motif in the C-terminal domain of fC31 integrase controls the directionality of recombination. Nucleic Acids Res. 36, 3879-3891.
31. Satoh, W., Hirai, Y., Tamayose, K., and Shimada, T. (2000). Site-specific integration of an adeno-associated virus vector plasmid mediated by regulated expression of rep based on Cre-loxP recombination. J. Virol. 74, 10631-10638.
32. 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.
33. Sharma, N., Moldt, B., Dalsgaard, T., Jensen, T.G., and Mikkel-sen, J.G. (2008). Regulated gene insertion by steroid-induced fC31 integrase. Nucleic Acids Res. 36, e67.
34. Smith, M.C., and Thorpe, H.M. (2002). Diversity in the serine recombinases. Mol. Microbiol. 44, 299-307.
35. Tan, W., Dong, Z., Wilkinson, T.A., Barbas, C.F., III, and Chow, S.A. (2006). Human immunodeficiency virus type 1 incorporated with fusion proteins consisting of integrase and the designed polydactyl zinc finger protein E2C can bias integration of viral DNA into a predetermined chromosomal region in human cells. J. Virol. 80, 1939-1948.
36. Thorpe, H.M., and Smith, M.C. (1998). In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc. Natl. Acad. Sci. U.S.A. 95, 5505-5510.
37. Thyagarajan, B., Olivares, E.C., Hollis, R.P., Ginsburg, D.S., and Calos, M.P. (2001). Site-specific genomic integration in mammalian cells mediated by phage fC31 integrase. Mol. Cell. Biol. 21, 3926-3934.
38. Thyagarajan, B., Liu, Y., Shin, S., Lakshmipathy, U., Scheyhing, K., Xue, H., Ellerstrom, C., Strehl, R., Hyllner, J., Rao, M.S., and Chesnut, J.D. (2008). Creation of engineered human embryonic stem cell lines using fC31 integrase. Stem Cells 26, 119-126.
39. Weber, L.W., Boll, M., and Stampfl, A. (2003). Hepatotoxicity and mechanism of action of haloalkanes: Carbon tetrachloride as a toxicological model. Crit. Rev. Toxicol. 33, 105-136.
40. Yant, S.R., Huang, Y., Akache, B., and Kay, M.A. (2007). Site-directed transposon integration in human cells. Nucleic Acids Res. 35, e50.
41. Yuan, P., Gupta, K., and Van Duyne, G.D. (2008). Tetrameric structure of a serine integrase catalytic domain. Structure 16, 1275-1286.
42. Zayed, H., Izsvak, Z., Walisko, O., and Ivics, Z. (2004). Development of hyperactive Sleeping Beauty transposon vectors by mutational analysis. Mol. Ther. 9, 292-304.