Site-specific recombinases: From tag-and-target- to tag-and-exchange-based genomic modifications

FASEB Journal

Volumn 25, Issue 12, 2011, Pages 4088-4107

  Turan, Soeren ^a   Bode, Juergen ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cre; F1p; PhiC31; Ser Tyr dependent integrases

Indexed keywords

PROTEIN SERINE KINASE; PROTEIN TYROSINE KINASE; RECOMBINASE;

BINDING SITE; CELL NUCLEUS TRANSPLANTATION; DNA MODIFICATION; GENE CASSETTE; GENE LOCUS; GENE TARGETING; GENE THERAPY; GENETIC RECOMBINATION; GENOMICS; HOMOLOGOUS RECOMBINATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; RECOMBINASE MEDIATED CASSETTE EXCHANGE; REVIEW;

ANIMALS; DNA; DNA NUCLEOTIDYLTRANSFERASES; FEMALE; GENE THERAPY; GENOMICS; HUMANS; MALE; MODELS, ANIMAL; MODELS, GENETIC; RECOMBINATION, GENETIC;

EID: 82655181514     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-186940     Document Type: Review

References (87)

1. Bode, J., Goetze, S., Ernst, E., Huesemann, Y., Baer, A., Seibler, J., and Mielke, C. (2003) Architecture and utilization of highly expressed genomic sites. New Compr. Biochem. 38, pp 551-572
2. Goetze, S., Baer, A., Winkelmann, S., Nehlsen, K., Seibler, J., Maass, K., and Bode, J. (2005) Performance of genomic bordering elements at predefined genomic loci. Mol. Cell. Biol. 25, 2260-2272 (Pubitemid 40354623)
3. Grandjean, M., Girod, P. A., Calabrese, D., Kostyrko, K., Wicht, M., Yerly, F., Mazza, C., Beckman, J. S., Martinet, D., and Mermod, N. (2011) High-level transgene expression by homologous recombination-mediated gene transfer. Nucleic Acids Res. doi:10.1093/nar/gkr436
4. Qiao, J., Oumard, A., Wegloehner, W., and Bode, J. (2009) Novel tag-and-exchange (RMCE) strategies generate master cell clones with predictable and stable transgene expression properties. J. Mol. Biol. 390, 579-594
5. Schleef, M., Blaesen, M., Schmeer, M., Baier, R., Marie, C., Dickson, G., and Scherman, D. (2010) Production of non viral DNA vectors. Curr. Gene Ther. 10, 487-507
6. Broll, S., Oumard, A., Hahn, K., Schambach, A., and Bode, J. (2010) Minicircle performance depending on S/MAR-nuclear matrix interactions. J. Mol. Biol. 395, 950-965
7. Sung, P., and Klein, H. (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell. Biol. 7, 739-750 (Pubitemid 44450458)
8. Connelly, J. P., Barker, J. C., Pruett-Miller, S., and Porteus, M. H. (2010) Gene correction by homologous recombination with zinc finger nucleases in primary cells from a mouse model of a generic recessive genetic disease. Mol. Ther. 18, 1103-1110
9. Pâques, F., and Duchateau, P. (2007) Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr. Gene Ther. 7, 49-66 (Pubitemid 46322288)
10. 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
11. Sangiorgi, E., Shuhua, Z., and Capecchi, M. R. (2008) In vivo evaluation of PhiC31 recombinase activity using a self-excision cassette. Nucleic Acids Res. 36, e134-e134
12. Turan, S., Kuehle, J., Schambach, A., Baum, C., and Bode, J. (2010) Multiplexing RMCE: versatile extensions of the Flp-recombinase- mediated cassette-exchange technology. J. Mol. Biol. 402, 52-69
13. Akopian, A., and Marshall Stark, W. (2005) Site-specific DNA recombinases as instruments for genomic surgery. Adv. Genet. 55, 1-23 (Pubitemid 43583921)
14. Burgin, A. B., Jr., and Nash, H. A. (1995) Suicide substrates reveal properties of the homology-dependent steps during integrative recombination of bacteriophage lambda. Curr. Biol. 5, 1312-1321
15. Turan, S., Galla, M., Ernst, E., Qiao, J., Voelkel, C., Schiedlmeier, B., Zehe, C., and Bode, J. (2011) Recombinase-mediated cassette exchange (RMCE): traditional concepts and current challenges. J. Mol. Biol. 407, 193-221
16. Ringrose, L., Lounnas, V., Ehrlich, L., Buchholz, F., Wade, R., and Stewart, A. F. (1998) Comparative kinetic analysis of FLP and cre recombinases: mathematical models for DNA binding and recombination. J. Mol. Biol. 284, 363-384 (Pubitemid 28542460)
17. Baer, A., and Bode, J. (2001) Coping with kinetic and thermodynamic barriers: RMCE, an efficient strategy for the targeted integration of transgenes. Curr. Opin. Biotechnol. 12, 473-480 (Pubitemid 32972172)
18. Grindley, N. D. F., Whiteson, K. L., and Rice, P. A. (2006) Mechanisms of site-specific recombination. Annu. Rev. Biochem. 75, 567-605 (Pubitemid 44118044)
19. Raymond, C. S., and Soriano, P. (2007) High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PLoS One 2, e162
20. 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 (Pubitemid 24352862)
21. Seibler, J., and Bode, J. (1997) Double-reciprocal crossover mediated by FLP-recombinase: a concept and an assay. Biochemistry 36, 1740-1747 (Pubitemid 27086269)
22. 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 (Pubitemid 27473401)
23. Feng, Y. Q., Seibler, J., Alami, R., Eisen, A., Westerman, K. A., Leboulch, P., Fiering, S., and Bouhassira, E. E. (1999) Site-specific chromosomal integration in mammalian cells: highly efficient CRE recombinase-mediated cassette exchange. J. Mol. Biol. 292, 779-785 (Pubitemid 29465473)
24. 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 (Pubitemid 36314819)
25. Bateman, J. R., Lee, A. M., and Wu, C.-T. (2006) Site-specific transformation of Drosophila via ΦC31 integrase-mediated cassette exchange. Genetics 173, 769-777 (Pubitemid 43945895)
26. Rubera, I., Meier, E., Vuagniaux, G., Mérillat, A.-M., Beermann, F., Rossier, B. C., and Hummler, E. (2002) A conditional allele at the mouse channel activating protease 1 (Prss8) gene locus. Genesis 32, 173-176 (Pubitemid 34211731)
27. Lyznik, L. A., Mitchell, J. C., Hirayama, L., and Hodges, T. K. (1993) Activity of yeast FLP recombinase in maize and rice protoplasts. Nucleic Acids Res. 21, 969-975 (Pubitemid 23153006)
28. Landy, A. (1989) Dynamic, structural, and regulatory aspects of lambda site-specific recombination. Annu. Rev. Biochem. 58, 913-949
29. Dröge, P., Hatfull, G. F., Grindley, N. D., and Cozzarelli, N. R. (1990) The two functional domains of γδ resolvase act on the same recombination site: implications for the mechanism of strand exchange. Proc. Natl. Acad. Sci. U. S. A. 87, 5336-5340
30. Stoll, S. M., Ginsburg, D. S., and Calos, M. P. (2002) Phage TP901-1 site-specific integrase functions in human cells. J. Bacteriol. 184, 3657-3663 (Pubitemid 34625675)
31. Smith, M. C. M., Brown, W. R. A., McEwan, A. R., and Rowley, P. A. (2010) Site-specific recombination by phiC31 integrase and other large serine recombinases. Biochem. Soc. Trans. 38, 388-394
32. Khaleel, T., Younger, E., McEwan, A. R., Varghese, A. S., and Smith, M. C. M. (2011) A phage protein that binds φC31 integrase to switch its directionality. Mol. Microbiol. 80, 1450-1463
33. Li, Z., Fang, Y., Wang, R., Xue, J., and Chen, J. (2011) Preliminary study on the DNA-binding properties of phage ΦC31 integrase. Gene 484, 47-51
34. 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 φC31 integrase. Nucleic Acids Res. 39, 6137-6147
35. Zhang, L., Ou, X., Zhao, G., and Ding, X. (2008) Highly efficient in vitro site-specific recombination system based on streptomyces phage ΦBT1 integrase. J. Bacteriol. 190, 6392-6397
36. Woodard, L. E., Hillman, R. T., Keravala, A., Lee, S., and Calos, M. P. (2010) Effect of nuclear localization and hydrodynamic delivery-induced cell division on φC31 integrase activity, NLS addition, cell division, and φC31 integrase. Gene Ther. 17, 217-226
37. Galla, M., Schambach, A., Towers, G. J., and Baum, C. (2008) Cellular restriction of retrovirus particle-mediated mRNA transfer. J. Virol. 82, 3069-3077 (Pubitemid 351329195)
38. Maetzig, T., Galla, M., Baum, C., and Schambach, A. (2011) Gammaretroviral vectors: biology, technology and application. Viruses 3, 677-713
39. Galla, M., Schambach, A., Falk, C. S., Maetzig, T., Kuehle, J., Lange, K., Zychlinski, D., Heinz, N. Brugman, M. H., Göhring, G., Izsvák, Z., Ivics, Z., and Baum., C. (2011) Avoiding cytotoxicity of transposases by dose-controlled mRNA delivery. Nucleic Acids Res. doi:10.1093/nar/gkr384
40. Voelkel, C., Galla, M., Maetzig, T., Warlich, E., Kuehle, J., Zychlinski, D., Bode, J., Cantz, T., Schambach, A., and Baum, C. (2010) Protein transduction from retroviral Gag precursors. Proc. Natl. Acad. Sci. U. S. A. 107, 7805-7810
41. Osterwalder, M., Galli, A., Rosen, B., Skarnes, W. C., Zeller, R., and Lopez-Rios, J. (2010) Dual RMCE for efficient re-engineering of mouse mutant alleles. Nat. Methods 7, 893-895
42. 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
43. Malchin, N., Molotsky, T., Borovok, I., Voziyanov, Y., Kotlyar, A. B., Yagil, E., and Kolot, M. (2010) High efficiency of a sequential recombinase-mediated cassette exchange reaction in Escherichia coli. J. Mol. Microbiol. Biotechnol. 19, 117-122
44. Malchin, N., Tuby, C. N., Yagil, E., and Kolot, M. (2011) Arm site independence of coliphage HK022 integrase in human cells. Mol. Genet. Genomics 285, 403-413
45. Suzuki, E., and Nakayama, M. (2011) VCre/VloxP and SCre/ SloxP: new site-specific recombination systems for genome engineering. Nucleic Acids Res. doi:10.1093/nar/gkq1280
46. 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 (Pubitemid 34065420)
47. 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 φC31 integrase in the human genome. J. Mol. Biol. 357, 28-48 (Pubitemid 43339312)
48. 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 bacteriophage integrase φC31 and the Sleeping Beauty transposase. Mol. Ther. 11, 695-706 (Pubitemid 40567974)
49. 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 φC31 integrase. Mol. Cell. Biol. 21, 3926-3934 (Pubitemid 32476454)
50. Keravala, A., Groth, A. C., Jarrahian, S., Thyagarajan, B., Hoyt, J. J., Kirby, P. J., and Calos, M. P. (2006) A diversity of serine phage integrases mediate site-specific recombination in mammalian cells. Mol. Genet. Genomics 276, 135-146 (Pubitemid 44079953)
51. Ehrhardt, A., Engler, J. A., Xu, H., Cherry, A. M., and Kay, M. A. (2006) Molecular analysis of chromosomal rearrangements in mammalian cells after φC31-mediated integration. Hum. Gene Ther. 17, 1077-1094 (Pubitemid 44749710)
52. Chavez, C. L., and Calos, M. P. (2011) Therapeutic applications of the phiC31-integrase system. Curr. Gene Ther. 11, 375-381
53. Keravala, A., Chavez, C. L., Hu, G., Woodard, L. E., Monahan, P. E., and Calos, M. P. (2011) Long-term phenotypic correction in factor IX knockout mice by using phiC31 integrase-mediated gene therapy. Gene Ther. 18, 842-848
54. Thomson, J. G., Rucker, E. B., 3rd, and Piedrahita, J. A. (2003) Mutational analysis of loxP sites for efficient Cre-mediated insertion into genomic DNA. Genesis 36, 162-167 (Pubitemid 36959348)
55. Sarkar, I., Hauber, I., Hauber, J., and Buchholz, F. (2007) HIV-1 proviral DNA excision using an evolved recombinase. Science 316, 1912-1915 (Pubitemid 47025793)
56. Shultz, J. L., Voziyanova, E., Konieczka, J. H., and Voziyanov, Y. (2011) A genome-wide analysis of FRT-like sequences in the human genome. PLoS One 6, e18077
57. Reid, L. H., Gregg, R. G., Smithies, O., and Koller, B. H. (1990) Regulatory elements in the introns of the human HPRT gene are necessary for its expression in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 87, 4299-4303
58. Stacey, A., Schnieke, A., McWhir, J., Cooper, J., Colman, A., and Melton, D. W. (1994) Use of double-replacement gene targeting to replace the murine α-lactalbumin gene with its human counterpart in embryonic stem cells and mice. Mol. Cell. Biol. 14, 1009-1016
59. Chen, Y. T., and Bradley, A. (2000) A new positive/negative selectable marker, puΔtk, for use in embryonic stem cells. Genesis 28, 31-35
60. Preuß, E., Treschow, A., Newrzela, S., Bruecher, D., Weber, K., Felldin, U., Alici, E., Gahrton, G., von Laer, D., Dilber, M. S., and Fehse, B. (2010) TK.007: a novel, codon-optimized HSVtk(A168H) mutant for suicide gene therapy. Hum. Gene Ther. 21, 929-941
61. Roebroek, A. J. M., Reekmans, S., Lauwers, A., Feyaerts, N., Smeijers, L., and Hartmann, D. (2006) Mutant Lrp1 knock-in mice generated by recombinase-mediated cassette exchange reveal differential importance of the NPXY motifs in the intracellular domain of LRP1 for normal fetal development. Mol. Cell. Biol. 26, 605-616 (Pubitemid 43089772)
62. Roebroek, A. J. M., Gordts, P. L. S. M., and Reekmans, S. (2011) Generation of a series of knock-in alleles using RMCE in ES cells. Methods Mol. Biol. 693, 277-281
63. Cesari, F., Rennekampff, V., Vintersten, K., Vuong, L. G., Seibler, J., Bode, J., Wiebel, F. F., and Nordheim, A. (2004) Elk-1 knock-out mice engineered by Flp recombinase-mediated cassette exchange. Genesis 38, 87-92 (Pubitemid 38327896)
64. Toledo, F., Liu, C.-W., Lee, C. J., and Wahl, G. M. (2006) RMCE-ASAP: a gene targeting method for ES and somatic cells to accelerate phenotype analyses. Nucleic Acids Res. 34, e92
65. Ramachandra, C. J. A., Shahbazi, M., Kwang, T. W. X., Choudhury, Y., Bak, X. Y., Yang, J., and Wang, S. (2011) Efficient recombinase-mediated cassette exchange at the AAVS1 locus in human embryonic stem cells using baculoviral vectors. [E-pub ahead of print] Nucleic Acids Res. doi:10.1093/nar/gkr409
66. 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
67. Chen, C., Krohn, J., Bhattacharya, S., and Davies, B. (2011) A comparison of exogenous promoter activity at the ROSA26 locus using a PhiC31 integrase mediated cassette exchange approach in mouse ES cells. PLoS ONE 6, e23376
68. Hitz, C., Wurst, W., and Kühn, R. (2007) Conditional brain-specific knockdown of MAPK using Cre/loxP regulated RNA interference. Nucleic Acids Res. 35, e90
69. Spradling, A. C., and Rubin, G. M. (1983) The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell 34, 47-57 (Pubitemid 13045467)
70. Pfeiffer, B. D., Ngo, T.-T. B., Hibbard, K. L., Murphy, C., Jenett, A., Truman, J. W., and Rubin, G. M. (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735-755
71. Siegal, M. L., and Hartl, D. L. (1996) Transgene coplacement and high efficiency site-specific recombination with the Cre/ loxP system in Drosophila. Genetics 144, 715-726 (Pubitemid 26325862)
72. Groth, A. C., Fish, M., Nusse, R., and Calos, M. P. (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage φC31. Genetics 166, 1775-1782 (Pubitemid 38621059)
73. Ohtsuka, M., Ogiwara, S., Miura, H., Mizutani, A., Warita, T., Sato, M., Imai, K., Hozumi, K., Sato, T., Tanaka, M., Kimura, M., and Inoko, H. (2010) Pronuclear injection-based mouse targeted transgenesis for reproducible and highly efficient transgene expression. Nucleic Acids Res. 38, e198
74. 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. U. S. A. 108, 7902-7907
75. Iqbal, K., Barg-Kues, B., Broll, S., Bode, J., Niemann, H., and Kues, W. (2009) Cytoplasmic injection of circular plasmids allows targeted expression in mammalian embryos. BioTechniques 47, 959-968
76. Friedrich, G., and Soriano, P. (1991) Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5, 1513-1523 (Pubitemid 21906058)
77. Schnuetgen, F., Ehrmann, F., Ruiz-Noppinger, P., and von Melchner, H. (2011) High throughput gene trapping and postinsertional modifications of gene trap alleles. Methods 53, 347-355
78. Schebelle, L., Wolf, C., Stribl, C., Javaheri, T., Schnütgen, F., Ettinger, A., Ivics, Z., Hansen, J., Ruiz, P., von Melchner, H., Wurst, W., and Floss, T. (2010) Efficient conditional and promoter-specific in vivo expression of cDNAs of choice by taking advantage of recombinase-mediated cassette exchange using FlEx gene traps. Nucleic Acids Res. 38, e106
79. Rajewsky, K. (2007) From a dream to reality. Eur. J. Immunol. 37(Suppl. 1), S134-S137
80. Schnuetgen, F., Ehrmann, F., Poser, I., Hubner, N. C., Hansen, J., Floss,T., deVries, I., Wurst, W., Hyman, A., Mann, M., and von Melchner, H. (2011) Resources for proteomics in mouse embryonic stem cells. Nat. Methods 8, 103-104
81. Gordley, R. M., Gersbach, C. A., and Barbas, C. F., 3rd (2009) Synthesis of programmable integrases. Proc. Natl. Acad. Sci. U. S. A. 106, 5053-5058
82. Silver, D. P., and Livingston, D. M. (2001) Self-excising retroviral vectors encoding the Cre recombinase overcome Cre-mediated cellular toxicity. Mol. Cell 8, 233-243 (Pubitemid 32772921)
83. Torres, R., García, A., Payá, M., and Ramirez, J. C. (2011) Non-integrative lentivirus drives high-frequency cre-mediated cassette exchange in human cells. PLoS One 6, e19794
84. Mielke, C., Maass, K., Tümmler, M., and Bode, J. (1996) Anatomy of highly expressing chromosomal sites targeted by retroviral vectors. Biochemistry 35, 2239-2252 (Pubitemid 26071657)
85. McEwan, A. R., Rowley, P. A., and Smith, M. C. M. (2009) DNA binding and synapsis by the large C-terminal domain of ΦC31 integrase. Nucleic Acids Res. 37, 4764-4773
86. Marshall Stark, W., Boocock, M. R., Olorunniji, F. J., and Rowland, S.-J. (2011) Intermediates in serine recombinase-mediated site-specific recombination. Biochem. Soc. Trans. 39, 617-622
87. Yang, W., and Steitz, T. A. (1995) Crystal structure of the site-specific recombinase γδ resolvase complexed with a 34 bp cleavage site. Cell 82, 193-207