The Nucleoid Binding Protein H-NS Acts as an Anti-Channeling Factor to Favor Intermolecular Tn10 Transposition and Dissemination

Journal of Molecular Biology

Volumn 376, Issue 4, 2008, Pages 950-962

  Singh, Randeep K ^a   Liburd, Janine ^a   Wardle, Simon J ^a   Haniford, David B ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

DNA transposition; H NS; IHF; target site selection; Tn10

Indexed keywords

HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; INTEGRATION HOST FACTOR;

ARTICLE; DNA SEQUENCE; DNA STRAND; DNA STRUCTURE; DNA SUPERCOILING; DNA TRANSPOSITION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; TRANSPOSON;

BACTERIA (MICROORGANISMS);

EID: 39049123030     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.12.035     Document Type: Article

References (44)

1. Nagy Z., and Chandler M. Regulation of transposition in bacteria. Res. Microbiol. 155 (2004) 387-398
2. Maxwell P.H., and Curcio M.J. Host factors that control long terminal repeat retrotransposons in Saccharomyces cerevisiae: implications for regulation of mammalian retroviruses. Eukaryot. Cell 6 (2007) 1069-1080
3. Horak R., Ilves H., Pruunsild P., Kuljus M., and Kivisaar M. The ColR-ColS two-component signal transduction system is involved in regulation of Tn4652 transposition in Pseudomonas putida under starvation conditions. Mol. Microbiol. 54 (2004) 795-807
4. Twiss E., Coros A.M., Tavakoli N.P., and Derbyshire K.M. Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol. Microbiol. 57 (2005) 1593-1607
5. Raleigh E.A., and Kleckner N. Quantitation of insertion sequence IS10 transposase gene expression by a method generally applicable to any rarely expressed gene. Proc. Natl Acad. Sci. USA 83 (1986) 1787-1791
6. Kleckner N. Transposon Tn10. In: Berg D.E., and Howe M.M. (Eds). Mobile DNA (1989), American Society for Microbiology, Washington, DC 225-267
7. Benjamin H.W., and Kleckner N. Intramolecular transposition by Tn10. Cell 59 (1989) 373-383
8. Signon L., and Kleckner N. Negative and positive regulation of Tn10/IS10-promoted recombination by IHF: two distinguishable processes inhibit transposition off of multicopy plasmid replicons and activate chromosomal events that favor evolution of new transposons. Genes Dev. 9 (1995) 1123-1136
9. Wardle S.J., O'Carroll M., Derbyshire K.M., and Haniford D.B. The global regulator H-NS acts directly on the transpososome to promote Tn10 transposition. Genes Dev. 19 (2005) 2224-2235
10. Ward C.M., Wardle S.J., Singh R.K., and Haniford D.B. The global regulator H-NS binds to two distinct classes of sites within the Tn10 transpososome to promote transposition. Mol. Microbiol. 64 (2007) 1000-1013
11. Dorman C.J. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2 (2004) 391-400
12. Gal-Mor O., and Finlay B.B. Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell. Microbiol. 8 (2006) 1707-1719
13. Navarre W.W., McClelland M., Libby S.J., and Fang F.C. Silencing of xenogeneic DNA by H-NS-facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev. 21 (2007) 1456-1471
14. Swingle B., O'Carroll M., Haniford D., and Derbyshire K.M. The effect of host-encoded nucleoid proteins on transposition: H-NS influences targeting of both IS903 and Tn10. Mol. Microbiol. 52 (2004) 1055-1067
15. Rouquette C., Serre M.C., and Lane D. Protective role for H-NS protein in IS1 transposition. J. Bacteriol. 186 (2004) 2091-2098
16. Chalmers R., Sewitz S., Lipkow K., and Crellin P. Complete nucleotide sequence of Tn10. J. Bacteriol. 182 (2000) 2970-2972
17. Haniford D.B. Transpososome dynamics and regulation in Tn10 transposition. Crit. Rev. Biochem. Mol. Biol. 41 (2006) 407-424
18. Chalmers R., Guhathakurta A., Benjamin H., and Kleckner N. IHF modulation of Tn10 transposition: sensory transduction of supercoiling status via a proposed protein/DNA molecular spring. Cell 93 (1998) 897-908
19. Crellin P., Sewitz S., and Chalmers R. DNA looping and catalysis; the IHF-folded arm of Tn10 promotes conformational changes and hairpin resolution. Mol. Cell 13 (2004) 537-547
20. Humayun S., Wardle S.J., Shilton B.H., Pribil P.A., Liburd J., and Haniford D.B. Tn10 transposase mutants with altered transpososome unfolding properties are defective in hairpin formation. J. Mol. Biol. 346 (2005) 703-716
21. Madrid C., Nieto J.M., Paytubi S., Falconi M., Gualerzi C.O., and Juarez A. Temperature- and H-NS-dependent regulation of a plasmid-encoded virulence operon expressing Escherichia coli hemolysin. J. Bacteriol. 184 (2002) 5058-5066
22. Prosseda G., Falconi M., Giangrossi M., Gualerzi C.O., Micheli G., and Colonna B. The virF promoter in Shigella: more than just a curved DNA stretch. Mol. Microbiol. 51 (2004) 523-537
23. Sakai J., Chalmers R.M., and Kleckner N. Identification and characterization of a pre-cleavage synaptic complex that is an early intermediate in Tn10 transposition. EMBO J. 14 (1995) 4374-4383
24. Haniford D.B., Chelouche A.R., and Kleckner N. A specific class of IS10 transposase mutants are blocked for target site interactions and promote formation of an excised transposon fragment. Cell 59 (1989) 385-394
25. Sakai J.S., Kleckner N., Yang X., and Guhathakurta A. Tn10 transpososome assembly involves a folded intermediate that must be unfolded for target capture and strand transfer. EMBO J. 19 (2000) 776-785
26. Crellin P., and Chalmers R. Protein-DNA contacts and conformational changes in the Tn10 transpososome during assembly and activation for cleavage. EMBO J. 20 (2001) 3882-3891
27. Spurio R., Falconi M., Brandi A., Pon C.L., and Gualerzi C.O. The oligomeric structure of nucleoid protein H-NS is necessary for recognition of intrinsically curved DNA and for DNA bending. EMBO J. 16 (1997) 1795-1805
28. Badaut C., Williams R., Arluison V., Bouffartigues E., Robert B., Buc H., and Rimsky S. The degree of oligomerization of the H-NS nucleoid structuring protein is related to specific binding to DNA. J. Biol. Chem. 277 (2002) 41657-41666
29. Chalmers R.M., and Kleckner N. IS10/Tn10 transposition efficiently accommodates diverse transposon end configurations. EMBO J. 15 (1996) 5112-5122
30. Tupper A.E., Owen-Hughes T.A., Ussery D.W., Santos D.S., Ferguson D.J., Sidebotham J.M., et al. The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J. 13 (1994) 258-268
31. Bliska J.B., and Cozzarelli N.R. Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J. Mol. Biol. 194 (1987) 205-218
32. Haniford D.B., Benjamin H.W., and Kleckner N. Kinetic and structural analysis of a cleaved donor intermediate and a strand transfer intermediate in Tn10 transposition. Cell 64 (1991) 171-179
33. Yang S.W., and Nash H.A. Comparison of protein binding to DNA in vivo and in vitro: defining an effective intracellular target. EMBO J. 14 (1995) 6292-6300
34. Chen H., and Engelman A. The barrier-to-autointegration protein is a host factor for HIV type 1 integration. Proc. Natl Acad. Sci. USA 95 (1998) 15270-15274
35. Lee M.S., and Craigie R. A previously unidentified host protein protects retroviral DNA from autointegration. Proc. Natl Acad. Sci. USA 95 (1998) 1528-1533
36. Zheng R., Ghirlando R., Lee M.S., Mizuuchi K., Krause M., and Craigie R. Barrier-to-autointegration factor (BAF) bridges DNA in a discrete, higher-order nucleoprotein complex. Proc. Natl Acad. Sci. USA 97 (2000) 8997-9002
37. Morisato D., and Kleckner N. Tn10 transposition and circle formation in vitro. Cell 51 (1987) 101-111
38. Morisato D., and Kleckner N. Transposase promotes double strand breaks and single strand joints at Tn10 termini in vivo. Cell 39 (1984) 181-190
39. Pribil P.A., Wardle S.J., and Haniford D.B. Enhancement and rescue of target capture in Tn10 transposition by site-specific modifications in target DNA. Mol. Microbiol. 52 (2004) 1173-1186
40. Chalmers R.M., and Kleckner N. Tn10/IS10 transposase purification, activation, and in vitro reaction. J. Biol. Chem. 269 (1994) 8029-8035
41. Surette M.G., and Chaconas G. A protein factor which reduces the negative supercoiling requirement in the Mu DNA strand transfer reaction is Escherichia coli integration host factor. J. Biol. Chem. 264 (1989) 3028-3034
42. Zhang A., Rimsky S., Reaban M.E., Buc H., and Belfort M. Escherichia coli protein analogs StpA and H-NS: regulatory loops, similar and disparate effects on nucleic acid dynamics. EMBO J. 15 (1996) 1340-1349
43. Krogh B.O., and Shuman S. A poxvirus-like type IB topoisomerase family in bacteria. Proc. Natl Acad. Sci. USA 99 (2002) 1853-1858
44. Ansari A., and Gartenberg M.R. The yeast silent information regulator Sir4p anchors and partitions plasmids. Mol. Cell. Biol. 17 (1997) 7061-7068