The interwoven architecture of the Mu transposase couples DNA synapsis to catalysis

Cell

Volumn 85, Issue 2, 1996, Pages 257-269

  Aldaz, Hector ^a   Schuster, Eugene ^a   Baker, Tania A ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; TRANSPOSASE;

ARTICLE; BACTERIOPHAGE; BINDING SITE; CHROMOSOME PAIRING; DNA CROSS LINKING; DNA TRANSPOSITION; ENZYME STRUCTURE; GENETIC RECOMBINATION; PRIORITY JOURNAL; PROTEIN DNA BINDING;

EID: 0029871975     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81102-2     Document Type: Article

References (66)

1. Adzuma, K., and Mizuuchi, K. (1991). Steady-state kinetic analysis of ATP hydrolysis by the B protein of bacteriophage Mu. J. Biol. Chem. 266, 6159-6167.
2. Allison, R.G., and Chaconas, G. (1992). Role of the A protein-binding sites in the in vitro transposition of Mu DNA: a complex circuit of interaction involving the Mu ends and the transpositional enhancer. J. Biol. Chem. 267, 19963-19970.
3. Arciszewska, L.K., and Sherratt, D.J. (1995). Xer site-specific recombination in vitro. EMBO J. 14, 2112-2120.
4. Bainton, R., Gamas, P., and Craig, N.L. (1991). Tn7 transposition in vitro proceeds through an excised transposon intermediate generated by staggered breaks in DNA. Cell 65, 805-816.
5. Baker, T.A., and Mizuuchi, K. (1992). DNA-promoted assembly of the active tetramer of the Mu transposase. Genes Dev. 6, 2221-2232.
6. 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.
7. Baker, T.A., Mizuuchi, M., and Mizuuchi, K. (1991). Mu B protein allosterically activates strand transfer by the transposase of phage Mu. Cell 65, 1003-1013.
8. Baker, T.A., Mizuuchi, M., Savilahti, H., and Mizuuchi, K. (1993). Division of labor among monomers within the Mu transposase tetramer. Cell 74, 723-733.
9. Baker, T.A., Kremenstova, E., and Luo, L. (1994). Complete transposition requires four active monomers in the Mu transposase tetramer. Genes Dev. 8, 2416-2428.
10. Benjamin, H.W., and Kleckner, N. (1992). Tn10 transposase excises Tn10 from flanking donor DNA by flush double - strand cleavages at the transposon termini. Proc. Natl. Acad. Sci. USA 89, 4648-4652.
11. Berg, D.E., and Howe, M.M. (1989). Mobile DNA (Washington, D.C.: American Society for Microbiology).
12. Boocock, M.R., Zhu, X., and Grindley, N.D. (1995). Catalytic residues of gamma delta resolvase act in cis. EMBO J. 14, 5129-5140.
13. Bujacz, G., Jaskolski, M., Alexandratos, J., Wlodawer, A., Merkel, G., Katz, R.A., and Skalka, A.M. (1995). High-resolution structure of the catalytic domain of avian sarcoma virus integrase. J. Mol. Biol. 253, 333-346.
14. 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.
15. Chen, J.W., Lee, J., and Jayaram, M. (1992). DNA cleavage in trans by the active site tyrosine during Flp recombination: switching protein partners before exchanging strands. Cell 69, 647-658.
16. Chen, J.W., Yang, S.H., and Jayaram, M. (1993). Tests for the fractional active-site model in Flp site-specific recombination. J. Biol. Chem. 268, 14417-14425.
17. Craig, N.L. (1995). Unity in transposition reactions. Science 270, 253-254.
18. Craigie, R., and Mizuuchi, K. (1986). Role of DNA topology in Mu transposition: mechanism of sensing the relative orientation of two DNA segments. Cell 45, 793-800.
19. 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.
20. Craigie, R., Mizuuchi, M., and Mizuuchi, K. (1984). Site-specific recognition of the bacteriophage Mu ends by the Mu A protein. Cell 39, 387-394.
21. Doak, T.G., Doerder, F.P., Jahn, C.L., and Herrick, G. (1994). A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common "D35E" motif. Proc. Natl. Acad. Sci. USA 91, 942-946.
22. Dröge, P., Hatfull, G.F., Grindley, N.D., and Cozzarelli, N.R. (1990). The two functional domains of gamma delta resolvase act on the same recombination site: implications for the mechanism of strand exchange. Proc. Natl. Acad. Sci. USA 87, 5336-5340.
23. Dyda, F., Hickman, A.B., Jenkins, T.M., Engleman, A., Craigie, R., and Davies, D.R. (1994). Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266, 1981-1986.
24. Fayet, O., Ramond, P., Polard, P., Prere, M.F., and Chandler, M. (1990). Functional similarities between retroviruses and the IS3 family of bacterial insertion sequences? Mol. Microbiol. 4, 1771-1777.
25. Grindley, N.D.F., and Leschziner, A.E. (1995). DNA transposition: from a black box to a color monitor. Cell 83, 1063-1066.
26. Groenen, M.A., Kokke, M., and van de Putte, P. (1986). Transposition of mini-Mu containing only one of the ends of bacteriophage Mu. EMBO. J. 5, 3687-3690.
27. Kaufman, P.D., and Rio, D.C. (1992). P element transposition in vitro proceeds by a cut-and-paste mechanism and uses GTP as a cofactor. Cell 69, 27-39.
28. Kim, K., and Harshey, R.M. (1995). Mutational analysis of the att DNA-binding domain of phage Mu transposase. Nucl. Acids Res. 23, 3937-3943.
29. 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.
30. Kim, S., and Landy, A. (1992). Lambda Int protein bridges between higher-order complexes at two distant chromosomal loci attL and attR. Science 256, 198-203.
31. Kulkosky, J., Jones, K.S., Katz, R.A., Mack, J.P.G., and Skalka, A.M. (1992). Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol. Cell. Biol. 12, 2331-2388.
32. 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.
33. Lee, J., Whang, I., Lee, J., and Jayaram, M. (1994). Directed protein replacement in recombination full sites reveals trans-horizontal DNA cleavage by Flp recombinase. EMBO. J. 13, 5346-5354.
34. Leung, P.C., Teplow, D.B., and Harshey, R.M. (1989). Interaction of distinct domains in Mu transposase with Mu DNA ends and an internal transpositional enhancer. Nature 338, 656-658.
35. Levchenko, I., Luo, L., and Baker, T.A. (1995). Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 9, 2399-2408.
36. Mizuuchi, K. (1992a). Polynucleotidyl transfer reaction in transpositional DNA recombination. J. Biol. Chem. 267, 21273-21276.
37. Mizuuchi, K. (1992b). Transpositional recombination: mechanistic insights from studies of Mu and other elements. Annu. Rev. Biochem. 61, 1011-1051.
38. Mizuuchi, M., and Mizuuchi, K. (1989). Efficient Mu transposition requires interaction of transposase with a DNA sequence at the Mu operator: implication for regulation. Cell 58, 399-408.
39. Mizuuchi, K., and Adzuma, K. (1991). Inversion of the phosphate chirality at the target site of Mu DNA strand transfer: evidence for a one-step transesterification mechanism. Cell 66, 129-140.
40. Mizuuchi, M., Baker, T.A., and Mizuuchi, K. (1991). DNase protection analysis of the stable synaptic complexes involved in Mu transposition. Proc. Natl. Acad. Sci. USA 88, 9031-9035.
41. Mizuuchi, M., Baker, T.A., and Mizuuchi, K. (1992). Assembly of the active form of the transposase-Mu DNA complex: a critical control point in Mu transposition. Cell 70, 303-311.
42. Mizuuchi, M., Baker, T.A., and Mizuuchi, K. (1995). Assembly of phage Mu transpososomes: cooperative transitions assisted by protein and DNA scaffolds. Cell 83, 375-385.
43. Nakayama, C., Teplow, D.B., and Harshey, R.M. (1987). Structural domains in phage Mu transposase: identification of the site-specific DNA-binding domain. Proc. Natl. Acad. Sci. USA 94, 1809-1813.
44. Nünes-Duby, S.E., Tirumalai, R.S., Dorgai, L., Yagil, E., Weisberg, R.A., and Landy, A. (1994). λ integrase cleaves DNA in cis. EMBO J. 18, 4421-4430.
45. Pan, G., Luetke, K., and Sadowski, P.D. (1993). Mechanism of cleavage and ligation by the FLP recombinase: classification of mutations in the FLP protein using in vitro complementation analysis. Mol. Cell. Biol. 13, 3167-3175.
46. Qian, X., and Cox, M.M. (1995). Asymmetry in active complexes of FLP recombinase. Genes Dev. 9, 2053-2064.
47. Rådström, P., Skold, O., Swedberg, G., Flensburg, J., Roy, P.H., and Sundström, L. (1994). Transposon Tn5090 of plasmid R751, which carries an integron, is related to Tn7, Mu, and the retroelements. J. Bacteriol. 176, 3257-3268.
48. Rice, P.A., and Mizuuchi, K. (1995). Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration. Cell 82, 209-220.
49. Robertson, H.M. (1993). The mariner transposable element is widespread in insects. Nature 362, 241-245.
50. Rowland, S.-J., and Dyke, K.G. (1990). Tn552, a novel transposable element from Staphylococcus aureus. Mol. Microbiol. 4, 961-975.
51. 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.
52. Schumm, J.W., and Howe, M.M. (1981). Mu-specific properties of lambda phages containing both ends of Mu depend on the relative orientation of Mu end DNA fragments. Virology 114, 429-450.
53. Stark, W.M., Boocock M.R., and Sherratt, D.J. (1992). Catalysis by site-specific recombinases. Trends Genet. 8, 432-439.
54. Surette, M.G., and Chaconas, G. (1992). The Mu transpositional enhancer can function in trans: requirement of the enhancer for synapsis but not strand cleavage. Cell 68, 1101-1108.
55. Surette, M.G., Bush, S.M., and Chaconas, G. (1987). Transpososomes: stable protein-DNA complexes involved in the in vitro transposition of bacteriophage Mu DNA. Cell 49, 253-262.
56. Surette, M.G., Harkness, T., and Chaconas, G. (1991). Stimulation of the Mu A protein-mediated strand cleavage reaction by the Mu B protein and the requirement of DNA nicking for stable type 1 transpososome formation: in vitro transposition characteristics of mini-Mu plasmids carrying terminal base pair mutations. J. Biol. Chem. 266, 3118-3124.
57. van Luenen, G.G.A.M., Colloms, S.D., and Plasterk, T. (1994). The mechanism of transposition of Tc3 in C. elegans. Cell 79, 293-301.
58. Willis, M.C., Hicke, B.J., Uhlenbeck, O.C., Cech, T.R., and Koch, T.H. (1993). Photocross-linking of 5-lodouracil-substituted RNA and DNA to proteins. Science 262, 1255-1257.
59. Wu, Z., and Chaconas, G. (1995). A novel DNA binding and nuclease activity in domain III of Mu transposase: evidence for a catalytic region involved in donor cleavage. EMBO J. 14, 3835-3843.
60. Wu, Z.G., and Chaconas, G. (1994). Characterization of a region in phage Mu transposase that is involved in interaction with the Mu B protein. J. Biol. Chem. 269, 28829-28833.
61. Yang, J.Y., Kim, K., Jayaram, M., and Harshey, R.M. (1995). A domain-sharing model for active site assembly within the Mu A tetramer during transposition: the enhancer may specify domain contributions. EMBO J. 14, 2374-2384.
62. Yang, S.H., and Jayaram, M. (1994). Generality of the shared active site among yeast family site-specific recombinases. The ARg site-specific recombinase follows the Flp paradigm. J. Biol. Chem. 269, 12789-12796.
63. Yang W., and Steitz, T.A. (1995a). Crystal structure of the site-specific recombinase gamma delta resolvase complexed with a 34 bp cleavage site. Cell 82, 193-207.
64. Yang, W., and Steitz, T.A. (1995b). Recombining the structures of HIV integrase, RuvC, and RNase H. Structure 3 131-134.
65. Zou, A.H., Jayaram, M., Getzoff, E., and Harshey, R. (1991a). DNA-protein complexes during attachment-site synapsis in Mu DNA transposition. EMBO J. 10, 1585-1591.
66. Zou, A.H., Leung, P.C, and Harshey, R.M. (1991b). Transposase contacts with Mu ends. J. Biol. Chem. 266, 20476-20482.