Drosophila P-element transposase is a novel site-specific endonuclease

Genes and Development

Volumn 11, Issue 16, 1997, Pages 2137-2151

  Beall, Eileen L ^a   Rio, Donald C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cleavage site; P transposon; Recombinase; Transposition

Indexed keywords

DNA; ENDONUCLEASE; TRANSPOSASE;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DROSOPHILA MELANOGASTER; NONHUMAN; PRIORITY JOURNAL; TRANSPOSON;

DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 0030847553     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.16.2137     Document Type: Article

References (91)

1. Agrawal, A. and D.G. Schatz. 1997. RAG1 and RAG2 form a stable postcleavage synaptic complex with DNA containing signal ends in V(D)J recombination. Cell 89: 43-53.
2. Anderson, C.W. and S.P. Lees-Miller. 1992. The nuclear serine/threonine protein kinase DNA-PK. Crit. Rev. Eukaryot. Gene Expression 2: 283-314.
3. Bainton, R., P. Gamas, and N.L. Craig. 1991. Tn7 transposition in vitro proceeds through an excised transposon intermediate generated by staggered breaks in DNA. Cell 65: 805-816.
4. Bainton, R.J., K.M. Kubo, J.N. Feng, and N.L. Craig. 1993. Tn7 transposition: Target DNA recognition is mediated by multiple Tn7-encoded proteins in a purified in vitro system. Cell 72: 931-943.
5. Beall, E.L. and D.C. Rio. 1996. Drosophila IRBP/Ku p70 corresponds to the mutagen-sensitive mus309 gene and is involved in P-element excision in vivo. Genes & Dev. 10: 921-933.
6. Beall, E.L., A. Admon, and D.C. Rio. 1994. A Drosophila protein homologous to the human p70 Ku autoimmune antigen interacts with the P transposable element inverted repeats. Proc Natl. Acad. Sci. 91: 12681-12685.
7. Benjamin, H.W. and N. Kleckner. 1992. Excision of Tn10 from the donor site during transposition occurs by flush double-strand cleavages at the transposon termini. Proc. Natl. Acad. Sci. 89: 4648-4652.
8. Blunt, T., N.J. Finnie, G.E. Taccioli, G.C. Smith, J. Demengeot, T.M. Gottlieb, R. Mizuta, A.J. Varghese, F.W. Alt, P.A. Jeggo et al. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80: 813-823.
9. Boubnov, N.V. and D.T. Weaver. 1995. scid cells are deficient in Ku and replication protein A phosphorylation by the DN8A-dependent protein kinase. Mol. Cell. Biol. 15: 5700-5706.
10. Boubnov, N.V., K.T. Hall, Z. Wills, S.E. Lee, D.M. He, D.M. Benjamin, C.R. Pulaski, H. Band, W. Reeves, E.A. Hendrickson et al. 1995. Complementation of the ionizing radiation sensitivity, DNA end binding, and V(D)J recombination defects of double-strand break repair mutants by the p86 Ku autoantigen. Proc. Natl. Acad. Sci. 92: 890-894.
11. Chalmers, R.M. and N. Kleckner. 1996. IS10/Tn10 transposition efficiently accommodates diverse transposon end configurations. EMBO J. 15: 5112-5122.
12. Chen, J.L., L.D. Attardi, C.P. Verrijzer, K. Yokomori, and R. Tijan. 1994. Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators. Cell 79: 93-105.
13. Craig, N.L. 1996. V(D)J recombination and transposition: Closer than expected. Science 271: 1512.
14. Craigie, R. and K. Mizuuchi. 1985. Mechanism of transposition of bacteriophage Mu: Structure of a transposition intermediate. Cell 41: 867-876.
15. _. 1987. Transposition of Mu DNA: Joining of Mu to target DNA can be uncoupled from cleavage at the ends of Mu. Cell 51: 493-501.
16. Cuomo, C.A., C.L. Mundy, and M.A. Oettinger. 1996. DNA sequence and structure requirements for cleavage of V(D)J recombination signal sequences. Mol. Cell. Biol. 16: 5683-5690.
17. Difilippantonio, M.J., C.J. McMahan, Q.M. Eastman, E. Spanopoulou, and D.G. Schatz. 1996. RAG1 mediates signal sequence recognition and recruitment of RAG2 in V(D)J recombination. Cell 87: 253-262.
18. Eastman, Q.M., T.M. Leu, and D.G. Schatz. 1996. Initiation of V(D)J recombination in vitro obeying the 12/23 rule. Nature 380: 85-88.
19. Engelman, A., K. Mizuuchi, and R. Craigie. 1991. HIV-1 DNA integration: Mechanism of viral DNA cleavage and DNA strand transfer. Cell 67: 1211-1221.
20. Engels, W.R., D.M. Johnson-Schlitz, W.B. Eggleston, and J. Sved. 1990. High-frequency P element loss in Drosophila is homolog dependent. Cell 62: 515-525.
21. Errami, A., V. Smider, W.K. Rathmell, D.M. He, E.A. Hendrickson, M.Z. Zdzienicka and G. Chu. 1996. Ku86 defines the genetic defect and restores X-ray resistance and V(D)J recombination to complementation group 5 hamster cell mutants. Mol. Cell. Biol. 16: 1519-1526.
22. Falzon, M., J.W. Fewell, and E.L. Kuff. 1993. EBP-80, a transcription factor closely resembling the human autoantigen Ku, recognizes single-to double-strand transitions in DNA. J. Biol. Chem. 268: 10546-10552.
23. Formosa, T. and B.M. Alberts. 1986. DNA synthesis dependent on genetic recombination: Characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell 47: 793-806.
24. Gary, P.A., M.C. Biery, R.J. Bainton, and N.L. Craig. 1996. Multiple DNA processing reactions underlie Tn7 transposition. J. Mol. Biol. 257: 301-316.
25. Gottlieb, T.M. and S.P. Jackson. 1993. The DNA-dependent protein kinase: Requirement for DNA ends and association with Ku antigen. Cell 72: 131-142.
26. Gray, Y.H.M., M.M. Tanaka, and J.A. Sved. 1996. P element-induced recombination in Drosophila melanogaster: Hybrid element insertion. Genetics 144: 1601-1610.
27. Haniford, D.B., H.W. Benjamin, and N. Kleckner. 1991. Kinetic and structural analysis of a cleaved donor intermediate and a strand transfer intermediate in Tn10 transposition. Cell 64: 171-179.
28. Harlow, E. and D. Lane. 1989. Antibodies: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Hiom, K. and M. Gellert. 1997. A stable RAG1-RAG2-DNA complex that is active in V(D)J cleavage. Cell 88: 65-72.
30. Jacoby, D.B. and P.C. Wensink. 1994. Yolk protein factor 1 is a Drosophila homolog of Ku, the DNA-binding subunit of a DNA-dependent protein kinase from humans. J. Biol. Chem. 269: 11484-11491
31. Kaufman, P.D. and D.C. Rio. 1992. P element transposition in vitro proceeds by a cut-and-paste mechanism and uses GTP as a cofactor. Cell 69: 27-39.
32. Kaufman, P.D., R.F. Doll, and D.C. Rio. 1989. Drosophila P element transposase recognizes internal P element DNA sequences. Cell 59: 359-371.
33. Keeler, K.J. and G.B. Gloor. 1997. Efficient gap repair in Drosophila melanogaster requires a maximum of 31 nucleotides of homologous sequence at the searching ends. Mol. Cell. Biol. 17: 627-634.
34. Kirchgessner, C.U., C.K. Patil, J.W. Evans, C.A. Cuomo, L.M. Fried, T. Carter, M.A. Oettinger, and J.M. Brown. 1995. DNA-dependent kinase (p350) as a candidate gene for the murine SCID detect. Science 267: 1178-1183.
35. Kleckner, N., R.M. Chalmers, D. Kwon, J. Sakai, and S. Bolland. 1996. Tn10 and IS10 transposition and chromosome rearrangements: Mechanism and regulation in vivo and in vitro. Curr. Top. Microbiol. Immunol. 204: 49-82.
36. Kruklitis, R., D.J. Welty, and H. Nakai. 1996. ClpX protein of Escherichia coli activates bacteriophage Mu transposase in the strand transfer complex for initiation of Mu DNA synthesis. EMBO J. 15: 935-944.
37. Laski, F.A., D.C. Rio, and G.M. Rubin. 1986. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell 44: 7-19.
38. Lavoie, B.D. and G. Chaconas. 1993. Site-specific HU binding in the Mu transpososome: Conversion of a sequence-independent DNA-binding protein into a chemical nuclease. Genes & Dev. 7: 2510-2519.
39. _. 1996. Transposition of phage Mu DNA. Curr. Top. Microbiol. Immunol. 204: 83-102.
40. Lee, C.C., Y.M. Mul, and D.C. Rio. 1996. The Diosophila P-element KP repressor protein dimerizes and interacts with multiple sites on P-element DNA. Mol. Cell. Biol. 16: 5616-5622.
41. Lee, M.S. and R. Craigie. 1994. Protection of retroviral DNA from autointegration: Involvement of a cellular factor. Proc. Natl. Acad. Sci. 91: 9823-9827.
42. Lees-Miller, S.P., Y.R. Chen, and C.W. Anderson. 1990. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell. Biol. 10: 6472-6481.
43. Lees-Miller, S.P., K. Sakaguchi, S.J. Ullrich, E. Appella, and C.W. Anderson. 1992. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12: 5041-5049.
44. Levchenko, I., L. Luo, and T.A. Baker. 1995. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes & Dev. 9: 2399-2408.
45. Lewis, S.M. and G.E. Wu. 1997. The origins of V(D)J recombination. Cell 88: 159-162.
46. Marchuk, D., M. Drumm, A. Saulino, and F.S. Collins. 1991. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 19: 1154.
47. Mimori, T. and J.A. Hardin. 1986. Mechanism of interaction between Ku protein and DNA. J. Biol. Chem. 261: 10375-10379.
48. Mizuuchi, K. 1992a. Polynucleotidyl transfer reactions in transpositional DNA recombination. J. Biol. Chem. 267: 21273-21276.
49. _. 1992b. Transpositional recombination: Mechanistic insights from studies of mu and other elements. Annu. Rev. Biochem. 61: 1011-1051.
50. Mizuuchi, M. and K. Mizuuchi. 1989. Efficient Mu transposition requires interaction of transposase with a DNA sequence at the Mu operator: Implications for regulation. Cell 58: 399-408.
51. Mizuuchi, M., T.A. Baker, and K. Mizuuchi. 1992. Assembly of the active form of the transposase-Mu DNA complex: A critical control point in Mu transposition. Cell 70: 303-311.
52. Morozov, V.E., M. Falzon, C.W. Anderson, and E.L. Kuff. 1994. DNA-dependent protein kinase is activated by nicks and larger single-stranded gaps. J. Biol. Chem. 269: 16684-16688.
53. Mul, Y.M. and D.C. Rio. 1997. Reprogramming the purine nucleotide cofactor requirement of Drosophila P element transposase in vivo. EMBO J. (in press).
54. Mullins, M.C., D.C. Rio, and G.M. Rubin. 1989. cis-acting DNA sequence requirements for P-element transposition. Genes & Dev. 3: 729-738.
55. Nakai, H. and R. Kruklitis. 1995. Disassembly of the bacteriophage Mu transposase for the initiation of Mu DNA replication. J. Biol. Chem. 270: 19591-19598.
56. Nassif, N., J. Penney, S. Pal, W.R. Engels, and G.B. Gloor. 1994. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14: 1613-1625.
57. Nicolas, A.L., P.L. Munz, and C.S.H. Young. 1995. A modified single-strand annealing model best explains the joining of DNA double-strand breaks in mammalian cells and cell extracts. Nucleic Acids Res. 23: 1036-1043.
58. O'Brochta, D.A., S.P. Gomez, and A.M. Handler. 1991. P element excision in Drosophila melanogaster and related drosophilids. Mol. Gen. Genet. 225: 387-394.
59. O'Hare, K. and G.M. Rubin. 1983. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell 34: 25-35.
60. Oettinger, M.A., D.G. Schatz, C. Gorka, and D. Baltimore. 1990. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248: 1517-1523.
61. Preston, C.R. and W.R. Engels. 1996. P-element-induced male recombination and gene conversion in Drosophila. Genetics 144: 1611-1622.
62. Preston, C.R., J.A. Sved, and W.R. Engels. 1996. Flanking duplications and deletions associated with P-induced male recombination in Drosophila. Genetics 144: 1623-1638.
63. Ramsden, D.A., J.F. McBlane, D.C. van Gent, and M. Gellert. 1996. Distinct DNA sequence and structure requirements for the two steps of V(D)J recombination signal cleavage. EMBO J. 15: 3197-3206.
64. Rio, D.C. and G.M. Rubin. 1988. Identification and purification of a Drosophila protein that binds to the terminal 31-base-pair inverted repeats of the P transposable element. Proc. Natl. Acad. Sci. 85: 8929-8933.
65. Rio, D.C., F.A. Laski, and G.M. Rubin. 1986. Identification and immunochemical analysis of biologically active Drosophila P element transposase. Cell 44: 21-32.
66. Roth, D.B. and J.H. Wilson. 1986. Nonhomologous recombination in mammalian cells: Role for short sequence homologies in the joining reaction. Mol. Cell. Biol. 6: 4295-4304.
67. Roth, D.B., C. Zhu, and M. Gellert. 1993. Characterization of broken DNA molecules associated with V(D)J recombination. Proc. Natl. Acad. Sci. 90: 10788-10792.
68. Sakai, J., R.H. Chalmers, and N. Kleckner. 1995. Identification and characterization of a pre-cleavage synaptic complex that is an early intermediate in Tn10 transposition. EMBO J. 14: 4374-4383.
69. Sarnovsky, R.J., E.W. May, and N.L. Craig. 1996. The Tn7 transposase is a heteromeric complex in which DNA breakage and joining activities are distributed between different gene products. EMBO J. 15: 6348-6361.
70. Savilahti, H., P.A. Rice, and K. Mizuuchi. 1995. The phage Mu transpososome core: DNA requirements for assembly and function. EMBO J. 14: 4893-4903.
71. Schatz, D.G., M.A. Oettinger, and D. Baltimore. 1989. The V(D)J recombination activating gene, RAG-1. Cell 59: 1035-1048.
72. Schlissel, M., A. Constantinescu, T. Morrow, M. Baxter, and A. Peng. 1993. Double-strand signal sequence breaks in V(D)J recombination are blunt, 5′-phosphorylated, RAG-dependent, and cell cycle regulated. Genes & Dev. 7: 2520-2532.
73. Scottoline, B.P., S. Chow, V. Ellison, and P.O. Brown. 1997. Disruption of the terminal base pairs of retroviral DNA during integration. Genes & Dev. 11: 371-382.
74. Spanopoulou, E., F. Zaitseva, F.H. Wang, S. Santagata, D. Baltimore, and G. Panayotou. 1996. The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell 87: 263-276.
75. Staveley, B.E., T.R. Heslip, R.B. Hodgetts, and J.B. Bell. 1995. Protected P-element termini suggest a role for inverted-repeat-binding protein in transposase-induced gap repair in Drosophila melanogaster. Genetics 139: 1321-1329.
76. Steen, S.B., L. Gomelsky, S.L. Speidel, and D.B. Roth. 1997. Initiation of V(D)J recombination in vivo: Role of recombination signal sequences in formation of single and paired double-strand breaks. EMBO J. 16: 2656-2664.
77. Surette, M.G. and G. Chaconas. 1992. The Mu transpositional enhancer can function in trans: Requirement of the enhancer for synapsis but not strand cleavage. Cell 68: 1101-1108.
78. Surette, M.G., S.J. Buch, and G. Chaconas. 1987. Transpososomes: Stable protein-DNA complexes involved in the in vitro transposition of bacteriophage Mu DNA. Cell 49: 253-262.
79. Taccioli, G.E., T.M. Gottlieb, T. Blunt, A. Priestley, J. Demengeot, R. Mizuta, A.R. Lehmann, F.W. Alt, S.P. Jackson, and P.A. Jeggo. 1994. Ku80: Product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265: 1442-1445.
80. Takasu-Ishikawa, E., M. Yoshihara, and Y. Hotta. 1992. Extra sequences found at P element excision sites in Drosophila melanogaster. Mol. Gen. Genet. 232: 17-23.
81. Tuteja, N., R. Tuteja, A. Ochem, P. Taneja, N.W. Huang, A. Simoncsits, S. Susie, K. Rahman, L. Marusic, J. Chen et al. 1994. Human DNA helicase II: A novel DNA unwinding enzyme identified as the Ku autoantigen. EMBO J. 13: 4991-5001.
82. van Gent, D.C., J.F. McBlane, D.A. Ramsden, M.J. Sadofsky, J.E. Hesse, and M. Gellert. 1995. Initiation of V(D)J recombination in a cell-free system. Cell 81: 925-934.
83. van Gent, D.C., D.A. Ramsden and M. Gellert. 1996a. The RAG1 and RAG2 proteins establish the 12/23 rule in V(D)J recombination. Cell 85: 107-113.
84. van Gent, D.C., K. Mizuuchi, and M. Gellert. 1996b. Similarities between initiation of V(D)J recombination and retroviral integration. Science 271: 1592-1594.
85. van Gent, D.C., K. Hiom, T.T. Paull, and M. Gellert. 1997. Stimulation of V(D)J cleavage by high mobility group proteins. EMBO J. 16: 2665-26670.
86. van Luenen, H.G., S.D. Colloms and R.H. Plasterk. 1993. Mobilization of quiet, endogenous Tc3 transposons of Caenorhabditis elegans by forced expression of Tc3 transposase. EMBO J. 12: 2513-2520.
87. _. 1994. The mechanism of transposition of Tc3 in C. elegans. Cell 79: 293-301.
88. Vos, J.C. and R.H. Plasterk. 1994. Tc1 transposase of Caenorhabditis elegans is an endonuclease with a bipartite DNA binding domain. EMBO J. 13: 6125-6132.
89. Vos, J.C., I. De Baere, and R.H. Plasterk. 1996. Transposase is the only nematode protein required for in vitro transposition of Tc1. Genes & Dev. 10: 755-761.
90. Watson, M.A. and G. Chaconas. 1996. Three-site synapsis during Mu DNA transposition: A critical intermediate preceding engagement of the active site. Cell 85: 435-445.
91. Zhu, C., M.A. Bogue, D.S. Lim, P. Hasty, and D.B. Roth. 1996. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86: 379-389.