Characteristics of MuA transposase-catalyzed processing of model transposon end DNA hairpin substrates

Nucleic Acids Research

Volumn 34, Issue 10, 2006, Pages 3139-3149

  Saariaho, Anna Helena ^a   Savilahti, Harri ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CALCIUM ION; MAGNESIUM ION; MANGANESE; TRANSPOSASE; DIVALENT CATION; DNA; METAL;

3' UNTRANSLATED REGION; ARTICLE; BACTERIOPHAGE MU; BIOCHEMISTRY; CATALYSIS; CHEMICAL REACTION; CONTROLLED STUDY; DNA CLEAVAGE; DNA SEQUENCE; DNA STRUCTURE; DNA TRANSPOSITION; ENZYME SUBSTRATE; ESCHERICHIA COLI; HOST PATHOGEN INTERACTION; IN VITRO STUDY; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; STRUCTURE ANALYSIS; TRANSPOSON; CHEMISTRY; CONFORMATION; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM;

ENTEROBACTERIA PHAGE MU;

BACTERIOPHAGE MU; CATALYSIS; CATIONS, DIVALENT; DNA; DNA TRANSPOSABLE ELEMENTS; METALS; NUCLEIC ACID CONFORMATION; SUBSTRATE SPECIFICITY; TRANSPOSASES;

EID: 33745160049     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl405     Document Type: Article

References (59)

1. Craig,N.L., Craigie,R., Gellert,M. and Lambowitz,A.M. (eds) (2002) Mobile DNA II. American Society for Microbiology, Washington DC.
2. Curcio,J.M. and Derbyshire,K.M. (2003) The outs and ins of transposition: From Mu to kangaroo. Mol. Cell. Biol., 4, 1-13.
3. Craig,N. (1995) Unity in transposition reactions. Science, 270, 253-254.
4. Gueguen,E., Rousseau,P., Duval-Valentin,G. and Chandler,M. (2005) The transpososome: Control of transposition at the level of catalysis. Trends Microbiol., 13, 543-549.
5. Rice,P. and Mizuuchi,K. (1995) Structure of the bacteriophage Mu transposase core: A common structural motif for DNA transposition. Cell, 82, 209-220.
6. Haren,L., Ton-Hoang,B. and Chandler,M. (1999) Integrating DNA: transposases and retroviral integrases. Annu. Rev. Microbiol., 53, 245-281.
7. Mizuuchi,K. and Baker,T.A. (2002) Chemical mechanisms for mobilizing DNA. In Craig,N.L., Craigie,R., Gellert,M. and Lambowitz,A.M. (eds), Mobile DNA II. American Society for Microbiology, Washington DC, pp. 12-23.
8. Savilahti,H. and Mizuuchi,K. (1996) Mu transpositional recombination: donor DNA cleavage and strand transfer in trans by the Mu transposase. Cell, 85, 271-280.
9. Namgoong,S.Y. and Harshey,R.M. (1998) The same two monomers within a MuA tetramer provide the DDE domains for the strand cleavage and strand transfer steps of transposition. EMBO J., 17, 3775-3785.
10. Williams,T.L., Jackson,E.L., Carritte,A. and Baker,T.A. (1999) Organization and dynamics of the Mu transpososome: Recombination by communication between two active sites. Genes Dev., 13, 2725-2737.
11. Naumann,T.A. and Reznikoff,W.S. (2000) Trans catalysis in Tn5 transposition. Proc. Natl Acad. Sci. USA, 97, 8944-8949.
12. Davies,D.R.,.Goryshin,I.Y., Reznikoff,W.S. and Rayment,I. (2000) Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science, 289, 77-83.
13. Yuan,J.F., Beniac,D.R., Chaconas,G. and Ottensmeyer,F.P. (2005) 3D reconstruction of the Mu transposase and the Type 1 transpososome: A structural framework for Mu DNA transposition. Genes Dev., 19, 840-852.
14. Chaconas,G. and Harshey,R.M. (2002) Transposition of phage Mu DNA. In Craig,N.L., Craigie,R., Gellert,M. and Lambowitz,A.M. (eds), Mobile DNA II. American Society for Microbiology. Washington DC, pp. 384-402.
15. Chaconas,G., Harshey,R.M., Sarvetnick,N. and Bukhari,A.I. (1981) Predominant end-products of prophage Mu DNA transposition during the lytic cycle are replicon fusions. J. Mol. Biol., 150, 341-359.
16. Liebart,J.C., Ghelardini,P. and Paolozzi,L. (1982) Conservative integration of bacteriophage Mu DNA into pBR322 plasmid. Proc. Natl Acad. Sci. USA, 79, 4362-4366.
17. Akroyd,J.E. and Symonds,N. (1983) Evidence for a conservative pathway of transposition of bacteriophage Mu. Nature, 303, 84-86.
18. Chaconas,G., Kennedy,D.L. and Evans,D. (1983) Predominant integration end products of infecting bacteriophage Mu DNA are simple insertions with no preference for integration of either Mu DNA strand. Virology, 128, 48-59.
19. Harshey,R.M. (1984) Transposition without duplication of infecting bacteriophage Mu DNA. Nature, 311, 580-581.
20. Surette,M.G., Buch,S.J. and Chaconas,G. (1987) Transpososomes: Stable protein-DNA complexes involved in the in vitro transposition of bacteriophage Mu DNA. Cell, 49, 253-262.
21. Craigie,R. and Mizuuchi,K. (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.
22. Savilahti,H., Rice,P.A. and Mizuuchi,K. (1995) The phage Mu transpososome core: DNA requirements for assembly and function. EMBO J., 14, 4893-4903.
23. Lee,I. and Harshey,R.M. (2001) Importance of the conserved CA dinucleotide at Mu termini. J. Mol. Biol., 314, 433-444.
24. Goldhaber-Gordon,I., Williams,T.L. and Baker,T.A. (2002b) DNA recognition sites activate MuA transposase to perform transposition of non-Mu DNA. J. Biol. Chem., 277, 7694-7702.
25. Goldhaber-Gordon,I., Early,M.H., Gray,M.K. and Baker,T.A. (2002a) Sequence and positional requirements for DNA sites in a Mu transpososome. J. Biol. Chem., 277, 7703-7712.
26. Lee,I. and Harshey,R M. (2003) The conserved CA/TG motif at Mu termini: T specifies stable transpososome assembly. J. Mol. Biol., 330, 261-275.
27. Saariaho,A.-H., Lamberg,A., Elo, S. and Savilahti,H. (2005) Functional comparison of the transposition core machineries of phage Mu and Haemophilus influenzae Mu like prophage Hin-Mu reveals interchangeable components. Virology, 331, 6-19.
28. Kennedy,A.K., Guhathakurta,A., Kleckner,N. and Haniford,D.B. (1998) Tn10 transposition via a DNA hairpin intermediate. Cell, 95, 125-134.
29. Bhasin,A., Goryshin,I.Y. and Reznikoff,W.S. (1999) Hairpin formation in Tn5 transposition. J. Biol. Chem., 52, 37021-37029.
30. McBlane,J.F., van Gent,D.C., Ramsden,D.A., Romeo,C., Cuomo,C.A., Gellert,M. and Oettinger,M.A. (1995) Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell, 83, 387-395.
31. Zhou,L., Mitra,R., Atkinson,P.W., Hickman,A.B., Dyda,F. and Craig,N.L (2004) Transposition of hAT elements links transposable elements and V(D)J recombination. Nature, 432, 995-1001.
32. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. Baker,T.A. and Luo,L. (1994) Identification of residues in the Mu transposase essential for catalysis. Proc. Natl Acad. Sci. USA, 91, 6654-6658.
34. Chaconas,G., Gloor,G. and Miller,J.L. (1985) Amplification and purification of the bacteriophage Mu encoded B transposition protein. J. Biol. Chem., 260, 2662-2669.
35. Adzuma,K. and Mizuuchi,K (1991) Steady-state kinetic analysis of ATP hydrolysis by the B protein of bacteriophage Mu. Involvement of protein oligomerization in the ATPase cycle. J. Biol. Chem., 266, 6159-6167.
36. Haapa-Paananeu,S, Rita,H. and Savilahti,H. (2002) DNA transposition of bacteriophage Mu. A quantitative analysis of target site selection in vitro. J. Biol. Chem., 277, 2843-2851.
37. Haapa,S., Taira,S., Heikkinen,E. and Savilahti,H. (1999) An efficient and accurate integration of mini-Mu transposons in vitro: A general methodology for functional genetic analysis and molecular biology applications. Nucleic Acids Res., 27, 2777-2784.
38. Lamberg,A., Nieminen,S., Qiao,M. and Savilahti,H. (2002) Efficient insertion mutagenesis for bacterial genomes involving electroporation of in vitro-assembled DNA transposition complexes of bacteriophage Mu. Appl. Environ. Microbiol., 68, 705-712.
39. Coros,C.J. and Chaconas,G. (2001) Effect of mutations in the Mu-host junction region on transpososome assembly. J. Mol. Biol., 310, 299-309.
40. Lavoie,B.D., Chan,B.S., Allison,R.G. and Chaconas,G. (1991) Structural aspects of a higher order nucleoprotein complex: Induction of an altered DNA structure at the Mu-host junction of the Mu type 1 transpososome. EMBO J., 10, 3051-3059.
41. Kim, K., Namgoong,S.Y., Jayaram,M. and Harshey,R.M. (1995) Step-arrest mutants of phage Mu transposase. Implications in DNA-protein assembly, Mu end cleavage, and strand transfer. J. Biol. Chem., 270, 1472-1479.
42. Namgoong,S.Y., Kim,K., Saxena,P., Yang,J.Y., Jayaram,M., Giedroc,D.P. and Harshey,R.M. (1998) Mutational analysis of domain II beta of bacteriophage Mu transposase: Domains II alpha and II beta belong to different catalytic complementation groups. J. Mol. Biol., 275, 221-232.
43. Baker,T.A. and Mizuuchi,K. (1992) DNA-promoted assembly of the active tetramer of the Mu transposase. Genes Dev., 6, 2221-2232.
44. Rezsohazy,R., Hallet,B., Delcour,J. and Mahillon,J. (1993) The IS4 family of insertion sequences: Evidence for a conserved transposase motif. Mol. Microbiol., 9, 1283-1295.
45. Allingham,J.S., Wardle,S.J. and Haniford,D.B. (2001) Determinants for hairpin formation in Tn10 transposition. EMBO J., 20, 2931-2942.
46. Ason,B. and and Reznikoff,W.S. (2002) Mutational analysis of the base flipping event found in Tn5 transposition. J. Biol. Chem., 277, 11284-11291.
47. Naumann,T.A. and Reznikoff,W.S. (2002) Tn5 transposase active site mutants. J. Biol. Chem., 277, 17623-17629.
48. Reznikoff,W.S. (2003) Tn5 as a model for understanding DNA transposition. Mol. Microbiol., 47, 1199-4206.
49. Polard,P., Prere,M.F., Fayet,O. and Chandler,M. (1992) Transposase-induced excision and circularization of the bacterial insertion sequence IS911. EMBO J., 11, 5079-5090.
50. Biery, M.C., Lopata,M. and Craig,N.L. (2000) 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.
51. Molisato,D. and Kleckner,N. (1984) Transposase promotes double strand breaks and single strand joints at Tn10 termini in vivo. Cell, 39, 181-190.
52. Tavakoli,N.P. and Derbyshire,K.M. (2001) Tipping the balance between replicative and simple transposition. EMBO J., 20, 2923-2930.
53. Craigie,R. and Mizuuchi,K. (1985) Mechanism of transposition of bacteriophage Mu: Structure of a transposition intermediate. Cell. 41. 867-876.
54. Au,T.K., Agrawal,P. and Harshey,R.M. (2006) Chromosomal integration mechanism of infecting Mu virion DNA. J. Bacteriol., 188, 1828-1834.
55. Au,T.K., Pathania,S. and Harshey,R.M. (2004) True reversal of MU integration. EMBO J., 23, 3408-3420.
56. Vipond,I.B. and Halford,S.E. (1993) Structure-function correlation for the EcoRV restriction enzyme: From non-specific binding to specific DNA cleavage. Mol. Microbiol., 9, 225-231.
57. Gimble,F.S. and Wang,J. (1996) Substrate recognition and induced DNA distortion by the PI-SceI endonuclease, an enzyme generated by protein splicing. J. Mol. Biol., 263, 163-180.
58. Mueller,J.E., Smith,D., Bryk,M. and Belfort,M. (1995) Intron-encoded endonuclease I-TevI binds as a monomer to effect sequential cleavage via conformational changes in the td homing site. EMBO J., 14, 5724-5735.
59. Luscombe,N.M., Austin,S.E., Berman,H.M. and Thornton,J.M. (2000) An overview of the structures of protein-DNA complexes. Genome Biol., 1, 1-37.