Serine integrase chimeras with activity in E. coli and HeLa cells

Biology Open

Volumn 3, Issue 10, 2014, Pages 895-903

  Farruggio, Alfonso P ^a   Calos, Michele P ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chimeric recombinase; Genome engineering; Hybrid protein; Phage integrase; Sequence specific recombination

Indexed keywords

EID: 84979233519     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20148748     Document Type: Article

References (65)

1. 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.
2. Avila, P., Ackroyd, A. J. and Halford, S. E. (1990). DNA binding by mutants of Tn21 resolvase with DNA recognition functions from Tn3 resolvase. J. Mol. Biol. 216, 645-655.
3. Bateman, J. R., Lee, A. M. and Wu, C.-t. (2006). Site-specific transformation of Drosophila via phiC31 integrase-mediated cassette exchange. Genetics 173, 769-777.
4. Belteki, G., Gertsenstein, M., Ow, D. W. and Nagy, A. (2003). Site-specific cassette exchange and germline transmission with mouse ES cells expressing phiC31 integrase. Nat. Biotechnol. 21, 321-324.
5. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
6. Brown, W. R. A., Lee, N. C. O., Xu, Z. and Smith, M. C. M. (2011). Serine recombinases as tools for genome engineering. Methods 53, 372-379.
7. Campbell, M., Corisdeo, S., McGee, C. and Kraichely, D. (2010). Utilization of site-specific recombination for generating therapeutic protein producing cell lines. Mol. Biotechnol. 45, 199-202.
8. 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 phiC31 integrase in the human genome. J. Mol. Biol. 357, 28-48.
9. Chompoosri, J., Fraser, T., Rongsriyam, Y., Komalamisra, N., Siriyasatien, P., Thavara, U., Tawatsin, A. and Fraser, M. J., Jr. (2009). Intramolecular integration assay validates integrase phi C31 and R4 potential in a variety of insect cells. Southeast Asian J. Trop. Med. Public Health 40, 1235-1253.
10. Christian, M., Cermak, T., Doyle, E. L., Schmidt, C., Zhang, F., Hummel, A., Bogdanove, A. J. and Voytas, D. F. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186, 757-761.
11. Cole, C., Barber, J. D. and Barton, G. J. (2008). The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201.
12. 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.
13. DeSantis, M. E. and Shorter, J. (2012). The elusive middle domain of Hsp104 and ClpB: location and function. Biochim. Biophys. Acta 1823, 29-39.
14. Farruggio, A. P., Chavez, C. L., Mikell, C. L. and Calos, M. P. (2012). Efficient reversal of phiC31 integrase recombination in mammalian cells. Biotechnol. J. 7, 1332-1336.
15. Ghosh, P., Pannunzio, N. R. and Hatfull, G. F. (2005). Synapsis in phage Bxb1 integration: selection mechanism for the correct pair of recombination sites. J. Mol. Biol. 349, 331-348.
16. Gordley, R. M., Smith, J. D., Gräslund, T. and Barbas, C. F., III. (2007). Evolution of programmable zinc finger-recombinases with activity in human cells. J. Mol. Biol. 367, 802-813.
17. Gregory, M. A., Till, R. and Smith, M. C. M. (2003). Integration site for Streptomyces phage phiBT1 and development of site-specific integrating vectors. J. Bacteriol. 185, 5320-5323.
18. 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. USA 97, 5995-6000.
19. Groth, A. C., Fish, M., Nusse, R. and Calos, M. P. (2004). Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775-1782.
20. Huang, J., Ghosh, P., Hatfull, G. F. and Hong, Y. (2011). Successive and targeted DNA integrations in the Drosophila genome by Bxb1 and phiC31 integrases. Genetics 189, 391-395.
21. Hunter, S., Jones, P., Mitchell, A., Apweiler, R., Attwood, T. K., Bateman, A., Bernard, T., Binns, D., Bork, P., Burge, S. et al. (2012). InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res. 40, D306-D312.
22. 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.
23. Keravala, A., Groth, A. C., Jarrahian, S., Thyagarajan, B., Hoyt, J. J., Kirby, P. J. and Calos, M. P. (2006a). A diversity of serine phage integrases mediate site-specific recombination in mammalian cells. Mol. Genet. Genomics 276, 135-146.
24. Keravala, A., Portlock, J. L., Nash, J. A., Vitrant, D. G., Robbins, P. D. and Calos, M. P. (2006b). PhiC31 integrase mediates integration in cultured synovial cells and enhances gene expression in rabbit joints. J. Gene Med. 8, 1008-1017.
25. Keravala, A., Lee, S., Thyagarajan, B., Olivares, E. C., Gabrovsky, V. E., Woodard, L. E. and Calos, M. P. (2009). Mutational derivatives of PhiC31 integrase with increased efficiency and specificity. Mol. Ther. 17, 112-120.
26. Kichler, A., Leborgne, C. and Danos, O. (2005). Dilution of reporter gene with stuffer DNA does not alter the transfection efficiency of polyethylenimines. J. Gene Med. 7, 1459-1467.
27. Kurtz, S., Phillippy, A., Delcher, A. L., Smoot, M., Shumway, M., Antonescu, C. and Salzberg, S. L. (2004). Versatile and open software for comparing large genomes. Genome Biol. 5, R12.
28. Li, W. and Godzik, A. (2006). Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658-1659.
29. Ma, Q. W., Sheng, H. Q., Yan, J. B., Cheng, S., Huang, Y., Chen-Tsai, Y., Ren, Z. R., Huang, S. Z. and Zeng, Y. T. (2006). Identification of pseudo attP sites for phage phiC31 integrase in bovine genome. Biochem. Biophys. Res. Commun. 345, 984-988.
30. 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.
31. Mandali, S., Dhar, G., Avliyakulov, N. K., Haykinson, M. J. and Johnson, R. C. (2013). The site-specific integration reaction of Listeria phage A118 integrase, a serine recombinase. Mob. DNA 4, 2.
32. McEwan, A. R., Rowley, P. A. and Smith, M. C. M. (2009). DNA binding and synapsis by the large C-terminal domain of phiC31 integrase. Nucleic Acids Res. 37, 4764-4773.
33. McEwan, A. R., Raab, A., Kelly, S. M., Feldmann, J. and Smith, M. C. M. (2011). Zinc is essential for high-affinity DNA binding and recombinase activity of WC31 integrase. Nucleic Acids Res. 39, 6137-6147.
34. Mercer, A. C., Gaj, T., Fuller, R. P. and Barbas, C. F., III. (2012). Chimeric TALE recombinases with programmable DNA sequence specificity. Nucleic Acids Res. 40, 11163-11172.
35. Monetti, C., Nishino, K., Biechele, S., Zhang, P., Baba, T., Woltjen, K. and Nagy, A. (2011). PhiC31 integrase facilitates genetic approaches combining multiple recombinases. Methods 53, 380-385.
36. Morita, K., Yamamoto, T., Fusada, N., Komatsu, M., Ikeda, H., Hirano, N. and Takahashi, H. (2009). The site-specific recombination system of actinophage TG1. FEMS Microbiol. Lett. 297, 234-240.
37. Murray, A. N. and Kelly, J. W. (2012). Hsp104 gives clients the individual attention they need. Cell 151, 695-697.
38. Ni, W., Hu, S., Qiao, J., Wang, Y., Shi, H., Wang, Y., He, Z., Li, G. and Chen, C. (2012). WC31 integrase mediates efficient site-specific integration in sheep fibroblasts. Biosci. Biotechnol. Biochem. 76, 2093-2095.
39. Nkrumah, L. J., Muhle, R. A., Moura, P. A., Ghosh, P., Hatfull, G. F., Jacobs, W. R., Jr and Fidock, D. A. (2006). Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat. Methods 3, 615-621.
40. Nomura, W., Masuda, A., Ohba, K., Urabe, A., Ito, N., Ryo, A., Yamamoto, N. and Tamamura, H. (2012). Effects of DNA binding of the zinc finger and linkers for domain fusion on the catalytic activity of sequence-specific chimeric recombinases determined by a facile fluorescent system. Biochemistry 51, 1510-1517.
41. Olivares, E. C., Hollis, R. P. and Calos, M. P. (2001). Phage R4 integrase mediates site-specific integration in human cells. Gene 278, 167-176.
42. 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.
43. Rausch, H. and Lehmann, M. (1991). Structural analysis of the actinophage phi C31 attachment site. Nucleic Acids Res. 19, 5187-5189.
44. Rice, P., Longden, I. and Bleasby, A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277.
45. Rowley, P. A., Smith, M. C. A., Younger, E. and Smith, M. C. M. (2008). A motif in the C-terminal domain of phiC31 integrase controls the directionality of recombination. Nucleic Acids Res. 36, 3879-3891.
46. Russell, J. P., Chang, D. W., Tretiakova, A. and Padidam, M. (2006). Phage Bxb1 integrase mediates highly efficient site-specific recombination in mammalian cells. Biotechniques 40, 460, 462, 464.
47. Rutherford, K., Yuan, P., Perry, K., Sharp, R. and Van Duyne, G. D. (2013). Attachment site recognition and regulation of directionality by the serine integrases. Nucleic Acids Res. 41, 8341-8356.
48. Schneider, F., Schwikardi, M., Muskhelishvili, G. and Dröge, P. (2000). A DNAbinding domain swap converts the invertase gin into a resolvase. J. Mol. Biol. 295, 767-775.
49. 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.
50. Siebenkotten, G., Leyendeckers, H., Christine, R. and Radbruch, A. (1995). Isolation of plasmid DNA from mammalian cells with QIAprep. QIAGEN News 2, 11-12.
51. Smith, M. C. M. and Thorpe, H. M. (2002). Diversity in the serine recombinases. Mol. Microbiol. 44, 299-307.
52. Smith, M. C. M., Brown, W. R. A., McEwan, A. R. and Rowley, P. A. (2010). Sitespecific recombination by phiC31 integrase and other large serine recombinases. Biochem. Soc. Trans. 38, 388-394.
53. Tasic, B., Hippenmeyer, S., Wang, C., Gamboa, M., Zong, H., Chen-Tsai, Y. and Luo, L. (2011). Site-specific integrase-mediated transgenesis in mice via pronuclear injection. Proc. Natl. Acad. Sci. USA 108, 7902-7907.
54. Thomson, J. G., Chan, R., Smith, J., Thilmony, R., Yau, Y.-Y., Wang, Y. and Ow, D. W. (2012). The Bxb1 recombination system demonstrates heritable transmission of site-specific excision in Arabidopsis. BMC Biotechnol. 12, 9.
55. Thorpe, H. M. and Smith, M. C. M. (1998). In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc. Natl. Acad. Sci. USA 95, 5505-5510.
56. UniProt Consortium. (2012). Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40, D71-D75.
57. Venken, K. J. T., He, Y., Hoskins, R. A. and Bellen, H. J. (2006). P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751.
58. Wei, Q.-X., Odell, A. F., van der Hoeven, F. and Hollstein, M. (2011). Rapid derivation of genetically related mutants from embryonic cells harboring a recombinase-specific Trp53 platform. Cell Cycle 10, 1261-1270.
59. Woltjen, K., Michael, I. P., Mohseni, P., Desai, R., Mileikovsky, M., Hämäläinen, R., Cowling, R., Wang, W., Liu, P., Gertsenstein, M. et al. (2009). piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458, 766-770.
60. Woltjen, K., Hämäläinen, R., Kibschull, M., Mileikovsky, M. and Nagy, A. (2011). Transgene-free production of pluripotent stem cells using piggyBac transposons. In Human Pluripotent Stem Cells (ed. P. H. Schwartz and R. L. Wesselschmidt), pp. 87-103. New York, NY: Humana Press.
61. Yamaguchi, S., Kazuki, Y., Nakayama, Y., Nanba, E., Oshimura, M. and Ohbayashi, T. (2011). A method for producing transgenic cells using a multiintegrase system on a human artificial chromosome vector. PLoS ONE 6, e17267.
62. Yuan, P., Gupta, K. and Van Duyne, G. D. (2008). Tetrameric structure of a serine integrase catalytic domain. Structure 16, 1275-1286.
63. Zhang, L., Wang, L., Wang, J., Ou, X., Zhao, G. and Ding, X. (2010). DNA cleavage is independent of synapsis during Streptomyces phage phiBT1 integrase-mediated site-specific recombination. J. Mol. Cell Biol. 2, 264-275.
64. Zhao, C., Farruggio, A. P., Bjornson, C. R. R., Chavez, C. L., Geisinger, J. M., Neal, T. L., Karow, M. and Calos, M. P. (2014). Recombinase-mediated reprogramming and dystrophin gene addition in mdx mouse induced pluripotent stem cells. PLoS ONE 9, e96279.
65. Zhu, F., Gamboa, M., Farruggio, A. P., Hippenmeyer, S., Tasic, B., Schüle, B., Chen-Tsai, Y. and Calos, M. P. (2014). DICE, an efficient system for iterative genomic editing in human pluripotent stem cells. Nucleic Acids Res. 42, e34-e34.