Integration specificity of phage φC31 integrase in the human genome

Journal of Molecular Biology

Volumn 357, Issue 1, 2006, Pages 28-48

  Chalberg, Thomas W ^a   Portlock, Joylette L ^a   Olivares, Eric C ^b   Thyagarajan, Bhaskar ^b   Kirby, Patrick J ^a   Hillman, Robert T ^a   Hoelters, Juergen ^c   Calos, Michele P ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Poetic Genetics   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

Gene therapy; Genome engineering; Pseudo site; Site specific integration; C31 integrase

Indexed keywords

DNA; INTEGRASE; PHI C31 INTEGRASE; UNCLASSIFIED DRUG;

ARTICLE; BIOINFORMATICS; CHROMOSOME 19Q; CHROMOSOME DELETION; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA INTEGRATION; DNA SEQUENCE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN GENOME; NUCLEOTIDE REPEAT; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; TISSUE SPECIFICITY;

MAMMALIA;

EID: 33644767178     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.11.098     Document Type: Article

References (55)

1. S. Kuhstoss, and R.N. Rao Analysis of the integration function of the Streptomycete bacteriophage ΦC31 J. Mol. Biol. 222 1991 897 908
2. H.M. Thorpe, and M.C.M. Smith In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family Proc. Natl Acad. Sci. USA 95 1998 5505 5510
3. H. Rausch, and M. Lehmann Structural analysis of the actinophage ΦC31 attachment site Nucl. Acids Res. 19 1991 5187 5189
4. A.C. Groth, E.C. Olivares, B. Thyagarajan, and M.P. Calos A phage integrase directs efficient site-specific integration in human cells Proc. Natl Acad. Sci. USA 97 2000 5995 6000
5. B. Thyagarajan, E.C. Olivares, R.P. Hollis, D.S. Ginsburg, and M.P. Calos Site-specific genomic integration in mammalian cells mediated by phage φC31 integrase Mol. Cell. Biol. 21 2001 3926 3934
6. A.C. Groth, and M.P. Calos Phage integrases: biology and applications J. Mol. Biol. 335 2004 667 678
7. B. Thyagarajan, and M.P. Calos Site-specific integration for high-level protein production in mammalian cells C.M. Smales D.C. James Therapeutic Proteins: Methods and Protocols vol. 308 2005 Humana Press Totowa, NJ 99 106
8. G. Belteki, M. Gertsenstein, D.W. Ow, and A. Nagy Site-specific cassette exchange and germline transmission with mouse ES cells expressing the φC31 integrase Nature Biotechnol. 21 2003 321 324
9. R.P. Hollis, S.M. Stoll, C.R. Sclimenti, J. Lin, Y. Chen-Tsai, and M.P. Calos Phage integrases for the construction and manipulation of transgenic mammals Reproduct. Biol. Endocrinol. 1 2003 79
10. A.C. Groth, M. Fish, R. Nusse, and M.P. Calos Creation of transgenic Drosophila by using the site-specific integrase from phage φC31 Genetics 166 2004 1775 1782
11. S. Ortiz-Urda, B. Thyagarajan, D. Keene, Q. Lin, M. Fang, M.P. Calos, and P.A. Khavari Stable nonviral genetic correction of inherited human skin disease Nature Med. 8 2002 1166 1170
12. S. Ortiz-Urda, D. Keene, Q. Lin, M.P. Calos, and P. Khavari φC31 integrase-mediated nonviral genetic correction of junctional epidermolysis bullosa Hum. Gene Ther. 14 2003 923 928
13. S. Ortiz-Urda, Q. Lin, C.L. Green, D.R. Keene, M.P. Marinkovich, and P. Khavari Injection of genetically engineered fibroblasts corrects regenerated human epidermolysis bullosa skin tissue J. Clin. Invest. 111 2003 251 255
14. S.P. Quenneville, P. Chapdelaine, J. Rousseau, J. Beaulieu, N.J. Caron, and D. Skuk Nucleofection of muscle-derived stem cells and myoblasts with φC31 integrase: stable expression of a full-length-dystrophin fusion gene by human myoblasts Mol. Ther. 10 2004 679 687
15. E.C. Olivares, R.P. Hollis, T.W. Chalberg, L. Meuse, M.A. Kay, and M.P. Calos Site-specific genomic integration produces therapeutic factor IX levels in mice Nature Biotechnol. 20 2002 1124 1128
16. P.K. Held, E.C. Olivares, C.P. Aguilar, M. Finegold, M.P. Calos, and M. Grompe In vivo correction of murine hereditary tyrosinemia type I by φC31 integrase-mediated gene delivery Mol. Ther. 11 2005 399 408
17. T.C. Chalberg, H.L. Genise, D. Vollrath, and M.P. Calos φC31 integrase confers genomic integration and long-term transgene expression in rat retina Invest. Ophthalmol. Visual Sci. 46 2005 2140 2146
18. A. Ehrhardt, H. Xu, Z. Huang, J.A. Engler, and M.A. Kary A direct comparison of two nonviral gene therapy vectors for somatic integration: in vivo evaluation of the bacteriophage integase φC31 and the Sleeping Beauty transposase Mol. Ther. 11 2005 695 706
19. S. Hacein-Bey-Abina, C. Von Kalle, M. Schmidt, M.P. McCormack, N. Wulffratt, and P. Leboulch LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1 Science 302 2003 415 419
20. R.S. Mitchell, B.F. Beitzel, A.R. Schroder, P. Shinn, H. Chen, and C.C. Berry Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences PLoS Biol. 2 2004 E234
21. A. Narezkina, K.D. Taganov, S. Litwin, R. Stoyanova, J. Hayashi, and C. Seeger Genome-wide analyses of avian sarcoma virus integration sites J. Virol. 78 2004 11656 11663
22. J.B. Weidhaus, E.L. Angelichio, S. Fenner, and J.M. Coffin Relationship between retroviral integration and gene expression J. Virol. 74 2000 8382 8389
23. A.R. Schroder, P. Shinn, H. Chen, C. Berry, J.R. Ecker, and F. Bushman HIV-1 integration in the human genome favors active genes and local hotspots Cell 110 2002 521 529
24. X. Wu, Y. Li, B. Crise, and S.M. Burgess Transcription start regions in the human genome are favored targets for MLV integration Science 300 2003 1749 1752
25. H. Nakai, E. Montini, S. Fuess, T.A. Storm, M. Grompe, and M.A. Kay AAV serotype 2 vectors preferentially integrate into active genes in mice Nature Genet. 34 2003 241 242
26. T.J. Vigdal, C.D. Kaufman, Z. Izsvak, D.F. Voytas, and Z. Ivics Common physical properties of DNA affecting target site selection of Sleeping Beauty and other Tc1/mariner transposable elements J. Mol. Biol. 323 2002 441 452
27. S.R. Yant, X. Wu, Y. Huang, B. Garrison, S.M. Burgess, and M.A. Kay High-resolution genome-wide mapping of transposon integration in mammals Mol. Cell. Biol. 25 2005 2085 2094
28. F.D. Bushman Targeting survival: integration site selection by retroviruses and LTR-retrotransposons Cell 115 2003 135 138
29. W.J. Kent BLAT - the BLAST-like alignment tool Genome Res. 12 2002 656 664
30. W.J. Kent, C.W. Sugnet, T.S. Furey, K.M. Roskin, T.H. Pringle, A.M. Zahler, and D. Haussler The human genome browser at UCSC Genome Res. 12 2002 996 1006
31. M.C.M. Smith, and H.M. Thorpe Diversity in the serine recombinases Mol. Microbiol. 44 2002 299 307
32. T.L. Bailey, and C. Elkan Fitting a mixture model by expectation maximization to discover motifs in biopolymers Proc. Int. Conf. Intell. Syst. Mol. Biol. 2 1994 28 36
33. T.L. Bailey, and M. Gribskov Combining evidence using p-values: application to sequence homology searches Bioinformatics 14 1998 48 54
34. W.N. Grundy, T.L. Bailey, C.P. Elkan, and M.E. Baker Meta-MEME: motif-based hidden Markov models of protein families Comput. Appl. Biosci. 13 1997 397 406
35. The ENCODE Project Consortium. (2004). The ENCODE (ENCyclopedia Of DNA Elements) Project. Science, 306, 636-640.
36. J.C. Venter, M.D. Adams, E.W. Myers, P.W. Li, R.J. Mural, and G.G. Sutton The sequence of the human genome Science 291 2001 1304 1351
37. International Human Genome Sequencing Consortium Finishing the euchromatic sequence of the human genome Nature 431 2004 931 945
38. E.S. Lander, L.M. Linton, B. Birren, C. Nusbaum, M.C. Zody, and J. Baldwin Initial sequencing and analysis of the human genome Nature 409 2001 860 921
39. J. Jurka Repbase update: a database and an electronic journal of repetitive elements Trends Genet. 16 2000 418 420
40. R. Gifford, P. Kabat, J. Martin, C. Lynch, and M. Tristem Evolution and distribution of class II-related endogenous retroviruses J. Virol. 79 2005 6478 6486
41. R. Gifford, and M. Tristem The evolution, distribution and diversity of endogenous retroviruses Virus Genes 26 2003 291 315
42. A.F. Smit, G. Toth, A.D. Riggs, and J. Jurka Ancestral, mammalian-wide subfamilies of LINE-1 repetitive sequences J. Mol. Biol. 246 1995 401 417
43. P.A. Futreal, L. Coin, M. Marshall, T. Down, T. Hubbard, R. Wooster, and N. Rahman A census of human cancer genes Nature Rev. Cancer 4 2004 177 183
44. F. Mitelman, B. Johansson, and F. Mertens Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer Nature Genet. 36 2004 331 334
45. R. Versteeg, B.D. van Schaik, M.F. van Batenburg, M. Roos, R. Monajemi, and H. Caron The human transcriptome map reveals extremes in gene density, intron length, GC content, and repeat pattern for domains of highly and weakly expressed genes Genome Res. 1998 2003 1998 2004
46. H. Hamilton, J. Gomos, K.I. Berns, and E. Falck-Pedersen Adeno-associated virus site-specific integration and AAVS1 disruption J. Virol. 78 2004 7874 7882
47. T.H. Kim, Y.J. Jeon, J.M. Yi, D.S. Kim, J.W. Huh, C.G. Hur, and H.S. Kim The distribution and expression of HERV families in the human genome Mol. Cells 18 2004 87 93
48. B.G. Allen, and D.L. Weeks Transgenic Xenopus laevis embryos can be generated using phiC31 integrase Nature Methods 2 2005 975 979
49. C.R. Sclimenti, B. Thyagarajan, and M.P. Calos Directed evolution of a recombinase for improved genomic integration at a native human sequence Nucl. Acids Res. 29 2001 5044 5051
50. F.L. Graham, J. Smiley, W.C. Russell, and R. Nairn Characteristics of a human cell line transformed by DNA from human adenovirus type 5 J. Gen. Virol. 36 1977 59 72
51. L. Marinari, C.M. Lenich, and A.C. Ross Production and secretion of retinol-binding protein by a human hepatoma cell line HepG2 J. Lipid Res. 28 1987 941 948
52. A.A. Davis, P.S. Bernstein, D. Bok, J. Turner, M. Nachtigal, and R.C. Hunt A human retinal pigment epithelial cell line that retains epithelial characteristics after prolonged culture Invest. Ophthalmol. Vis. Sci. 36 1995 955 964
53. E.C. Olivares, R.P. Hollis, and M.P. Calos Phage R4 integrase mediates efficient integration in mammalian cells Gene 278 2001 167 176
54. D.A. Benson, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell, and D.L. Wheeler GenBank: update Nucl. Acids Res. 32 2004 D23 D26
55. W. Schempp, and B. Meer Cytologic evidence for three human X-chromosomal segments escaping inactivation Hum. Genet. 63 1983 171 174