Early intermediates of mariner transposition: Catalysis without synapsis of the transposon ends suggests a novel architecture of the synaptic complex

Molecular and Cellular Biology

Volumn 24, Issue 18, 2004, Pages 8301-8311

  Lipkow, Karen ^a,c   Buisine, Nicolas ^a   Lampe, David J ^b   Chalmers, Ronald ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b DUQUESNE UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HIMAR1 TRANSPOSASE; MONOMER; TRANSPOSASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYST; CHROMOSOME PAIRING; DIMERIZATION; DNA CLEAVAGE; DNA FOOTPRINTING; DNA RECOMBINATION; DNA TRANSPOSITION; EUKARYOTE; GENE INSERTION; MARINER TRANSPOSON; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TITRIMETRY; TRANSPOSON;

ANIMALS; BASE SEQUENCE; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENES, INSECT; MUTATION; RECOMBINANT FUSION PROTEINS; TRANSPOSASES;

BACTERIA (MICROORGANISMS); EUKARYOTA; INSERTION SEQUENCES; TRANSPOSONS;

EID: 4444295114     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.18.8301-8311.2004     Document Type: Article

References (61)

1. Akerley, B. J., and D. J. Lampe. 2002. Analysis of gene function in bacterial pathogens by GAMBIT. Methods Enzymol. 358:100-108.
2. Akerley, B. J., E. J. Rubin, A. Camilli, D. J. Lampe, H. M. Robertson, and J. J. Mekalanos. 1998. Systematic identification of essential genes by in vitro mariner mutagenesis. Proc. Natl. Acad. Sci. USA 95:8927-8932.
3. Aldaz, H., E. Schuster, and T. A. Baker. 1996. The interwoven architecture of the Mu transposase couples DNA synapsis to catalysis. Cell 85:257-269.
4. Anxolabehere, D., M. G. Kidwell, and G. Periquet. 1988. Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Mol. Biol. Evol. 5:252-269.
5. Augé-Gouillou, C., M. H. Hamelin, M. V. Demattei, G. Periquet, and Y. Bigot. 2001. The ITR binding domain of the mariner Mos-1 transposase. Mol. Genet. Genomics 265:58-65.
6. Barry, E. G., D. J. Witherspoon, and D. J. Lampe. 2004. A bacterial genetic screen identifies functional coding sequences of the insect mariner transposable element Famar1 amplified from the genome of the earwig, Forficula auricularia. Genetics 166:823-833.
7. Bhasin, A., I. Y. Goryshin, and W. S. Reznikoff. 1999. Hairpin formation in Tn5 transposition. J. Biol. Chem. 274:37021-37029.
8. Bhasin, A., I. Y. Goryshin, M. Steiniger-White, D. York, and W. S. Reznikoff. 2000. Characterization of a Tn5 pre-cleavage synaptic complex. J. Mol. Biol. 302:49-63.
9. Chaconas, G., and R. M. Harshey. 2002. Transposition of phage Mu DNA, p. 384-402. In N. L. Craig, R. Craigie, M. Gellert, and A. M. Lambowitz (ed.), Mobile DNA II. American Society for Microbiology, Washington, D.C.
10. Chalmers, R., A. Guhathakurta, H. Benjamin, and N. Kleckner. 1998. IHF modulation of Tn10 transposition: sensory transduction of supercoiling status via a proposed protein/DNA molecular spring. Cell 93:897-908.
11. Chalmers, R. M., and N. Kleckner. 1996. IS10/Tn10 transposition efficiently accommodates diverse transposon end configurations. EMBO J. 15:5112-5122.
12. Chalmers, R. M., and N. Kleckner. 1994. Tn10/IS10 transposase purification, activation, and in vitro reaction. J. Biol. Chem. 269:8029-8035.
13. Coen, E. S., T. P. Robbins, J. Almeida, A. Hudson, and R. Carpenter. 1989. Consequences and mechanisms of transposition in Antirrhinum majus, p. 413-436. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
14. Craig, N. L. 2002. Tn7, p. 423-456, In N. L. Craig, R. Craigie, M. Gellert, and A. M. Lambowitz (ed.), Mobile DNA II. American Society for Microbiology, Washington, D.C.
15. Crellin, P., and R. Chalmers. 2001. Protein-DNA contacts and conformational changes in the Tn10 transpososome during assembly and activation for cleavage. EMBO J. 20:3882-3891.
16. Crellin, P., S. Sewitz, and R. Chalmers. 2004. DNA looping and catalysis; the IHF-folded arm of Tn10 promotes conformational changes and hairpin resolution. Mol. Cell 13:537-547.
17. Davies, D. R., I. Y. Goryshin, W. S. Reznikoff, and I. Rayment. 2000. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289:77-85.
18. Dawson, A., and D. J. Finnegan. 2003. Excision of the Drosophila mariner transposon Mos1. Comparison with bacterial transposition and V(D)J recombination. Mol. Cell 11:225-235.
19. De Aguiar, D., and D. L. Hartl. 1999. Regulatory potential of nonautonomous mariner elements and subfamily crosstalk. Genetica 107:79-85.
20. Engels, W. R. 1997. Invasions of P elements. Genetics 145:11-15.
21. Fischer, S. E., E. Wienholds, and R. H. Plasterk. 2003. Continuous exchange of sequence information between dispersed Tc1 transposons in the Caenorhabditis elegans genome. Genetics 164:127-134.
22. Fugmann, S. D., A. I. Lee, P. E. Shockett, I. J. Villey, and D. G. Schatz. 2000. The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu. Rev. Immunol. 18:495-527.
23. Gellert, M. 2002. V(D)J recombination: Rag proteins, repair factors, and regulation. Annu. Rev. Biochem. 71:101-132.
24. Haniford, D. B. 2002. Transposon Tn10, p. 457-483. In N. L. Craig, R. Craigie, M. Gellert, and A. M. Lambowitz (ed.), Mobile DNA II. American Society for Microbiology, Washington, D.C.
25. Hartl, D. L., A. R. Lohe, and E. R. Lozovskaya. 1997. Modern thoughts on an ancyent marinere: function, evolution, regulation. Annu. Rev. Genet. 31:337-358.
26. Hartl, D. L., E. R. Lozovskaya, D. I. Nurminsky, and A. R. Lohe. 1997. What restricts the activity of mariner-like transposable elements. Trends Genet. 13:197-201.
27. Ivics, Z., P. B. Hackett, R. H. Plasterk, and Z. Izsvak. 1997. Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501-510.
28. Kennedy, A. K., A. Guhathakurta, N. Kleckner, and D. B. Haniford. 1998. Tn10 transposition via a DNA hairpin intermediate. Cell 95:125-134.
29. Lampe, D. J., B. J. Akerley, E. J. Rubin, J. J. Mekalanos, and H. M. Robertson. 1999. Hyperactive transposase mutants of the Himarl mariner transposon. Proc. Natl. Acad. Sci. USA 96:11428-11433.
30. Lampe, D. J., M. E. A. Churchill, and H. M. Robertson. 1996. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J. 15:5470-5479.
31. Lampe, D. J., T. E. Grant, and H. M. Robertson. 1998. Factors affecting transposition of the Himar1 mariner transposon in vitro. Genetics 149:179-187.
32. Lee, C. C., Y. M. Mul, and D. C. Rio. 1996. The Drosophila P-element KP repressor protein dimerizes and interacts with multiple sites on P-element DNA. Mol. Cell. Biol. 16:5616-5622.
33. Lee, G. S., M. B. Neiditch, S. S. Salus, and D. B. Roth. 2004. RAG proteins shepherd double-strand breaks to a specific pathway, suppressing error-prone repair, but RAG nicking initiates homologous recombination. Cell 117:171-184.
34. Lipkow, K. 2003. Molecular analysis of hobo and Himarl transposition. Ph.D. thesis. Oxford University, Oxford, United Kingdom.
35. Lippman, Z., B. May, C. Yordan, T. Singer, and R. Martienssen. 2003. Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone Modification. PLoS Biol. 1:E67.
36. Lohe, A. R., and D. L. Hartl. 1996. Autoregulation of mariner transposase activity by overproduction and dominant-negative complementation. Mol. Biol. Evol. 13:549-555.
37. Lohe, A. R., E. N. Moriyama, D. A. Lidholm, and D. L. Hartl. 1995. Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol. Biol. Evol. 12:62-72.
38. Lohe, A. R., C. Timmons, I. Beerman, E. R. Lozovskaya, and D. L. Hartl. 2000. Self-inflicted wounds, template-directed gap repair and a recombination hotspot. Effects of the mariner transposase. Genetics 154:647-656.
39. Mahillon, J., and M. Chandler. 1998. Insertion sequences. Microbiol. Mol. Biol. Rev. 62:725-774.
40. Mizuuchi, K. 1992. Polynucleotidyl transfer reactions in transpositional DNA recombination. J. Biol. Chem. 267:21273-21276.
41. 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.
42. Papavassiliou, A. G. 1994. 1,10-Phenanthroline-copper ion nuclease foot-printing of DNA-protein complexes in situ following mobility-shift electrophoresis assays, p. 43-78. In G. G. Kneale (ed.), DNA-protein interactions: principles and protocols. Humana Press, Totowa, N.J.
43. Robertson, H. M., and D. J. Lampe. 1995. Distribution of transposable elements in arthropods. Annu. Rev. Entomol. 40:333-357.
44. Robertson, H. M., and D. J. Lampe. 1995. Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol. Biol. Evol. 12:850-862.
45. Rubin, E. J., B. J. Akerley, V. N. Novik, D. J. Lampe, R. N. Husson, and J. J. Mekalanos. 1999. In vivo transposition of mariner-based elements in enteric bacteria and mycobacteria. Proc. Natl. Acad. Sci. USA 96:1645-1650.
46. Rudenko, G. N., A. Ono, and V. Walbot. 2003. Initiation of silencing of maize MuDR/Mu transposable elements. Plant J. 33:1013-1025.
47. Sakai, J., R. M. 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.
48. Sambrook, J., E. F. Fritsch, and T Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Savilahti, H., and K. Mizuuchi. 1996. Mu transpositional recombination: donor DNA cleavage and strand transfer in trans by the Mu transposase. Cell 85:271-280.
50. Schickor, P., and H. Heumann. 1994. Hydroxyl radical footprinting, p. 21-32. In G. G. Kneale (ed.), DNA-protein interactions: principles and protocols. Humana Press, Totowa, N.J.
51. Sewitz, S., P. Crellin, and R. Chalmers. 2003. The positive and negative regulation of Tn10 transposition by IHF is mediated by structurally asymmetric transposon arms. Nucleic Acids Res. 31:5868-5876.
52. Sijen, T., and R. H. Plasterk. 2003. Transposon silencing in the Caenorhabditis elegans germ line by natural RNAi. Nature 426:310-314.
53. 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.
54. Swanson, P. C. 2001. The DDE motif in RAG-1 is contributed in trans to a single active site that catalyzes the nicking and transesterification steps of V(D)J recombination. Mol. Cell. Biol. 21:449-458.
55. Swanson, P. C. 2002. Fine structure and activity of discrete RAG-HMG complexes on V(D)J recombination signals. Mol. Cell. Biol. 22:1340-1351.
56. Swanson, P. C. 2002. A RAG-1/RAG-2 tetramer supports 12/23-regulated synapsis, cleavage, and transposition of V(D)J recombination signals. Mol. Cell. Biol. 22:7790-7801.
57. Vigdal, T. J., C. D. Kaufman, Z. Izsvak, D. F. Voytas, and Z. Ivics. 2002. Common physical properties of DNA affecting target site selection of Sleeping Beauty and other Tc1/mariner transposable elements. J. Mol. Biol. 323:441-452.
58. Yu, K., and M. R. Lieber. 2000. The nicking step in V(D)J recombination is independent of synapsis: implications for the immune repertoire. Mol. Cell. Biol. 20:7914-7921.
59. Zayed, H., Z. Izsvak, D. Khare, U. Heinemann, and Z. Ivics. 2003. The DNA-bending protein HMGB1 is a cellular cofactor of Sleeping Beauty transposition. Nucleic Acids Res. 31:2313-2322.
60. Zhang, L., A. Dawson, and D. J. Finnegan. 2001. DNA-binding activity and subunit interaction of the mariner transposase. Nucleic Acids Res. 29:3566-3575.
61. Zou, A. H., P. C. Leung, and R. M. Harshey. 1991. Transposase contacts with Mu DNA ends. J. Biol. Chem. 266:20476-20482.