Tn7: Smarter than we thought

Nature Reviews Molecular Cell Biology

Volumn 2, Issue 11, 2001, Pages 806-814

  Peters, Joseph E ^a   Craig, Nancy L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS);

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DNA; DNA BINDING PROTEIN; DNA BINDING PROTEINS; TNSA PROTEIN; TNSB PROTEIN; TNSC PROTEIN;

BIOLOGICAL MODEL; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; REVIEW; TRANSPOSON;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; DNA; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; MODELS, BIOLOGICAL; MODELS, GENETIC; SUPPORT, NON-U.S. GOV'T; SUPPORT, U.S. GOV'T, NON-P.H.S.;

EID: 0035512769     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/35099006     Document Type: Article

References (55)

1. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001).
2. Venter, J. C. et al. The sequence of the human genome. Science 291, 1304-1351 (2001).
3. Craig, N. L. Target site selection in transposition. Annu. Rev. Biochem. 66, 437-474 (1997).
4. Craig, N. L. Transposon Tn7. Curr. Top. Microblol. Immunol. 204, 27-48 (1996).
5. Hall, R. M., Brookes, D. E. & Stokes, H. W. Site-specific insertion of genes into integrons: role of the 59-base element and determination of the recombination cross-over point. Mol. Microbiol. 5, 1941-1959 (1991).
6. Hauer, B. & Shapiro, J. A. Control of Tn7 transposition. Mol. Gen. Genet. 194, 149-158 (1984).
7. Rogers, M., Ekaterinaki, N., Nimmo, E. & Sherratt, D. Analysis of Tn7 transposition. Mol. Gen. Genet. 205, 550-556 (1986).
8. Waddell, C. S. & Craig, N. L. Tn7 transposition: two transposition pathways directed by five Tn7-encoded genes. Genes Dev. 2, 137-149 (1988).
9. Samovsky, R., May, E. W. & Craig, N. L. 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 (1996). Together with reference 20, this study provided the first evidence that the Tn7 transposase was heteromeric.
10. Biery, M., Lopata, M. & Craig, N. L. A minimal system for Tn7 transposition: the transposon-encoded proteins TnsA and TnsB can execute DNA breakage and joining reactions that generate circularized Tn7 species. J. Mol. Biol. 297, 25-37 (2000).
11. Lu, F. & Craig, N. L. Isolation and characterization of Tn7 transposase gain-of-function mutants: a model for transposase activation. EMBO J. 19, 3446-3457 (2000).
12. Mizuuchi, K. Transpositional recombination: mechanistic insights from studies of Mu and other elements. Annu. Rev. Biochem. 61, 1011-1051 (1992).
13. Haren, L., Ton-Hoang, B. & Chandler, M. Integrating DNA: transposases and retroviral integrases. Annu. Rev. Microbiol. 53, 245-281 (1999).
14. Dyda, F. et al. Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucteotidyl transferases. Science 266, 1981-1986 (1994).
15. Rice, P. & Mizuuchi, K. Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration. Cell 82, 209-220 (1995).
16. Davies, D. R., Braam, L. M., Reznikoff, W. S. & Rayment, I. The three-dimensional structure of a Tn5 transposase-related protein determined to 2.9-Å resolution. J. Biol. Chem. 274, 11904-11913 (1999).
17. Reznikoff, W. S. The TnS transposon. Annu. Rev. Microbiol. 47, 945-963 (1993).
18. Kleckner, N., Chalmers, R., Kwon, D., Sakai, J. & Bolland, S. Tn10 and IS10 transposition and chromosome rearrangements: mechanism and regulation in vivo and in vitro. Curr. Top. Microbiol. Immunol. 204, 49-82 (1996).
19. Arciszewska, L. K., Drake, D. & Craig, N. L. Transposon Tn7 cis-acting sequences in transposition and transposition immunity. J. Mol. Biol. 207, 35-52 (1989).
20. May, E. W. & Craig, N. L. Switching from cut-and-paste to replicative Tn7 transposition. Science 272, 401-404 (1996).
21. Hickman, A. B. et al. Unexpected structural diversity in DNA recombination: the restriction endonuclease connection. Mol. Cell 5, 1025-1034 (2000). The structure of TnsA shows that one of the proteins of the heteromeric Tn7 transposase is actually a restriction enzyme that is used for transposition.
22. Bainton, R. J., Kubo, K. M., Feng, J.-N. & Craig, N. L. Tn7 transposition: target DNA recognition is mediated by multiple Tn7-encoded proteins in a purified in vitro system. Cell 72, 931-943 (1993). This study provides the first description of the complete TnsABC+D in vitro transposition reaction from purified proteins.
23. Stellwagen, A. E. Analysis of gain of function mutants of an ATP-dependent regulator of Tn7 transposition. J. Mol. Biol. 305, 633-642 (2001).
24. Stellwagen, A. & Craig, N. L. Gain-of-function mutations in TnsC, an ATP-dependent transposition protein which activates the bacterial transposon Tn7. Genetics 145, 573-585 (1997).
25. Wolkow, C. A., DeBoy, R. T. & Craig, N. L. Conjugating plasmids are preferred targets for Tn7. Genes Dev. 10, 2145-2157 (1996).
26. Barth, P. & Grinter, N. Map of plasmid RP4 derived by insertion of transposon C. J. Mol. Biol. 113, 455-474 (1977).
27. Peters, J. E. & Craig, N. L. Tn7 recognizes target structures associated with DNA replication using the DNA binding protein TnsE. Genes Dev. 15, 737-747 (2001). Together with reference 28, this study showed that TnsE-mediated transposition recognizes structures associated with DNA replication.
28. Peters, J. E. & Craig, N. L. Tn7 transposes proximal to DNA double-strand breaks and into regions where chromosomal DNA replication terminates. Mol. Cell 6, 573-582 (2000).
29. Cox, M. M. et al. The importance of repairing stalled replication forks. Nature 404, 37-41 (2000).
30. Gay, N. J., Tybulewica, V. L. J. & Walker, J. E. Insertion of transposon Tn7 into the Escherichia coli glmS transcriptional terminator. Biochem. J. 234, 111-117 (1986).
31. Lichtenstein, C. & Brenner, S. Unique insertion site of Tn7 in E. coli chromosome. Nature 297, 601-603 (1982).
32. Walker, J. E., Gay, N. J., Saraste, M. & Eberle, A. N. DNA sequence around the Escherichia coli unc operon. Completion of the sequence of a 17 kilobase segment containing asnA, oriC, unc, glmS and phoS. Biochem. J. 224, 799-815 (1984).
33. Gringauz, E., Orle, K., Orle, A., Waddell, C. S. & Craig, N. L. Recognition of Escherichia coli attTn7 by transposon Tn7: lack of specific sequence requirements at the point of Tn7 insertion. J. Bacteriol. 170, 2832-2840 (1988).
34. Cleaver, S. H. & Wickstrom, E. Transposon Tn7 gene insertion into an evolutionarily conserved human homolog of Escherichia coli attTn7. Gene 254, 37-44 (2000).
35. Bainton, R., Gamas, P. & Craig, N. L. Tn7 transposition in vitro proceeds through an excised transposon intermediate generated by staggered breaks in DNA. Cell 65, 805-816 (1991).
36. Rao, J. E., Miller, R S. & Craig, N. L. Recognition of triple-helical DNA structures by transposon Tn7. Proc. Natl Acad. Sci. USA 97, 3936-3941 (2000).
37. Kuduvalli, P., Rao, J. & Craig, N. L. Target DNA structure plays a critical role in Tn7 transposition. EMBO J. 20, 1-10 (2001). Together with reference 36, this study shows that an induced DNA structure is of key importance in recruiting TnsC and the core transposition machinery.
38. Pryciak, P. M. & Varmus, H. E. Nucleosomes, DNA-binding proteins, and DNA sequence modulate retroviral integration target site selection. Cell 69, 769-780 (1992).
39. Katz, R. A., Gravuer, K. & Skalka, A. M. A preferred target DNA structure for retroviral integrase in vitro. J. Biol. Chem. 273, 24190-24195 (1998).
40. Rao, J. E. & Craig, N. L. Selective recognition of pyrimidine motif triplexes by a protein encoded by the bacterial transposon Tn7. J. Mol. Biol. 307, 1161-1170 (2001).
41. Sharpe, P. & Craig, N. L. Host proteins can stimulate Tn7 transposition: a novel role for the ribosomal protein L29 and the acyl carrier protein. EMBO J. 17, 5822-5831 (1998).
42. Gamas, P. & Craig, N. L. Purification and characterization of TnsC, a Tn7 transposition protein that binds ATP and DNA. Nucleic Acids Res. 20, 2525-2532 (1992).
43. Oppon, J. C., Sarnovsky, R. J., Craig, N. L. & Rawlings, D. E. A Tn7-like transposon is present in the glmUS region of the obligately hemoautolithotrophic bacterium Thiobacillus ferrooxidans. J. Bacteriol. 180, 3007-3012 (1998).
44. Lee, C.-H., Bhagwhat, A. & Heffron, F. Identification of a transposon Tn3 sequence required for transposition immunity, Proc. Natl Acad. Sci. USA 80, 6765-6769 (1983).
45. Adzuma, K. & Mizuuchi, K. Interaction of proteins located at a distance along DNA: mechanism of target immunity in the Mu DNA strand-transfer reaction. Cell 57, 41-47 (1989).
46. Reyes, I., Beyou, A., Mignotte-Vieux, C. & Richaud, F. Mini-Mu transduction: cis-inhibition of the insertion of Mud transposons. Plasmid 18, 183-192 (1987).
47. DeBoy, R. & Craig, N. L. Tn7 transposition as a probe of cis interactions between widely separated (190 kilobases apart) DNA sites in the Escherichia coli chromosome. J. Bacteriol. 178, 6184-6191 (1996).
48. Stellwagen, A. & Craig, N. L. Avoiding self: two Tn7-encoded proteins mediate target immunity in Tn7 transposition. EMBO J. 16, 6823-6834 (1997).
49. Bourne, H. R., Sanders, D. A. & McCormick, F. The GTPase superfamily: a conserved switch for diverse cell functions. Nature 348, 125-132 (1990).
50. Maxwell, A., Craigie, R. & Mizuuchi, K. B protein of bacteriophage Mu is an ATPase that preferentially stimulates intermolecular DNA strand transfer. Proc. Natl Acad. Sci. USA 84, 699-703 (1987).
51. Baker, T. A., Mizuuchi, M. & Mizuuchi, K. MuB protein allosterically activates strand transfer by the transposase of phage Mu. Cell 65, 1003-1013 (1991).
52. Surette, M. G. & Chaconas, G. Stimulation of the Mu DNA strand cleavage and intramolecular strand transfer reactions by the MuB protein is independent of stable binding of the MuB protein to DNA. J. Biol. Chem. 266, 17306-17313 (1991).
53. Stellwagen, A. & Craig, N. L. Mobile DNA elements: controlling transposition with ATP-dependent molecular switches. Trends Biochem. Sci. 23, 486-490 (1998).
54. Lowy, D. R. & Willumsen, B. M. Function and regulation of Ras. Annu. Rev. Biochem. 62, 851-891 (1993).
55. Sprang, S. R. G protein mechanisms: insights from structural analysis. Annu. Rev. Biochem. 66, 639-678 (1997).