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Journal of Biosciences

, Volume 36, Issue 4, pp 587–601 | Cite as

Analysis of phage Mu DNA transposition by whole-genome Escherichia coli tiling arrays reveals a complex relationship to distribution of target selection protein B, transcription and chromosome architectural elements

  • Jun Ge
  • Zheng Lou
  • Hong Cui
  • Lei Shang
  • Rasika M Harshey
Article

Abstract

Of all known transposable elements, phage Mu exhibits the highest transposition efficiency and the lowest target specificity. In vitro, MuB protein is responsible for target choice. In this work, we provide a comprehensive assessment of the genome-wide distribution of MuB and its relationship to Mu target selection using high-resolution Escherichia coli tiling DNA arrays. We have also assessed how MuB binding and Mu transposition are influenced by chromosome-organizing elements such as AT-rich DNA signatures, or the binding of the nucleoid-associated protein Fis, or processes such as transcription. The results confirm and extend previous biochemical and lower resolution in vivo data. Despite the generally random nature of Mu transposition and MuB binding, there were hot and cold insertion sites and MuB binding sites in the genome, and differences between the hottest and coldest sites were large. The new data also suggest that MuB distribution and subsequent Mu integration is responsive to DNA sequences that contribute to the structural organization of the chromosome.

Keywords

A-tracts MuB Mu DNA transposition Fis nucleoid-associated proteins target site selection 

Notes

Acknowledgements

This work was supported by National Institutes of Health grant GM 33247 and in part by the Robert Welch Foundation Grant F-1351.

Supplementary material

12038_2011_9108_MOESM1_ESM.pdf (827 kb)
ESM 1 (PDF 827 kb)

References

  1. Adzuma K and Mizuuchi K 1988 Target immunity of Mu transposition reflects a differential distribution of Mu B protein. Cell 53 257–266PubMedCrossRefGoogle Scholar
  2. 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 6159–6167PubMedGoogle Scholar
  3. Alexandrov AI, Cozzarelli NR, Holmes VF, Khodursky AB, Peter BJ, Postow L, Rybenkov V and Vologodskii AV 1999 Mechanisms of separation of the complementary strands of DNA during replication. Genetica 106 131–140PubMedCrossRefGoogle Scholar
  4. Au TK, Agrawal P and Harshey RM 2006 Chromosomal integration mechanism of infecting mu virion DNA. J. Bacteriol. 188 1829–1834PubMedCrossRefGoogle Scholar
  5. Azam TA and Ishihama A 1999 Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity. J. Biol. Chem. 274 33105–33113PubMedCrossRefGoogle Scholar
  6. Beauregard A, Curcio MJ and Belfort M 2008 The take and give between retrotransposable elements and their hosts. Annu. Rev. Genet. 42 587–617PubMedCrossRefGoogle Scholar
  7. Berry C, Hannenhalli S, Leipzig J, and Bushman FD 2006 Selection of target sites for mobile DNA integration in the human genome. PLoS Comput. Biol. 2 e157PubMedCrossRefGoogle Scholar
  8. Blot N, Mavathur R, Geertz M, Travers A and Muskhelishvili G 2006 Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome. EMBO Rep. 7 710–715PubMedCrossRefGoogle Scholar
  9. Boccard F, Esnault E and Valens M 2005 Spatial arrangement and macrodomain organization of bacterial chromosomes. Mol. Microbiol. 57 9–16PubMedCrossRefGoogle Scholar
  10. Brady T, Lee YN, Ronen K, Malani N, Berry CC, Bieniasz PD and Bushman FD 2009 Integration target site selection by a resurrected human endogenous retrovirus. Genes Dev. 23 633–642PubMedCrossRefGoogle Scholar
  11. Bukhari AI and Taylor AL 1975 Influence of insertions on packaging of host sequences covalently linked to bacteriophage Mu DNA. Proc. Natl. Acad. Sci. USA 72 4399–4403PubMedCrossRefGoogle Scholar
  12. Chaconas G and Harshey RM 2002 Transposition of phage Mu DNA; in Mobile DNA II eds NL Craig, R Craigie, M Gellert and AM Lambowitz (Washington DC: SM Press) pp 384–402Google Scholar
  13. Cho BK, Knight EM, Barrett CL and Palsson BO 2008 Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res. 18 900–910PubMedCrossRefGoogle Scholar
  14. Condon C, Philips J, Fu ZY, Squires C and Squires CL 1992 Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli. EMBO J. 11 4175–4185PubMedGoogle Scholar
  15. Condon C, Squires C and Squires CL 1995 Control of rRNA transcription in Escherichia coli. Microbiol. Rev. 59 623–645PubMedGoogle Scholar
  16. Craig NL 1997 Target site selection in transposition. Annu. Rev. Biochem. 66 437–474PubMedCrossRefGoogle Scholar
  17. Dame RT 2005 The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol. Microbiol. 56 858–870PubMedCrossRefGoogle Scholar
  18. Datsenko KA and Wanner BL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97 6640–6645PubMedCrossRefGoogle Scholar
  19. Deng S, Stein RA and Higgins NP 2005 Organization of supercoil domains and their reorganization by transcription. Mol. Microbiol. 57 1511–1521PubMedCrossRefGoogle Scholar
  20. Dillon SC and Dorman CJ 2010 Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 8 185–195PubMedCrossRefGoogle Scholar
  21. Dorman CJ and Deighan P 2003 Regulation of gene expression by histone-like proteins in bacteria. Curr. Opin. Genet. Dev. 13 179–184PubMedCrossRefGoogle Scholar
  22. Espeli O, Mercier R and Boccard F 2008 DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol. Microbiol. 68 1418–1427PubMedCrossRefGoogle Scholar
  23. Ge J and Harshey RM 2008 Congruence of in vivo and in vitro insertion patterns in hot E. coli gene targets of transposable element Mu: opposing roles of MuB in target capture and integration. J. Mol. Biol. 380 598–607PubMedCrossRefGoogle Scholar
  24. Ge J, Lou Z and Harshey RM 2010 Immunity of replicating Mu to self-integration: a novel mechanism employing MuB protein. Mobile DNA 1 doi:  10.1186/1759-8753-1-8
  25. Greene EC and Mizuuchi K 2004 Visualizing the assembly and disassembly mechanisms of the MuB transposition targeting complex. J. Biol. Chem. 279 16736–16743PubMedCrossRefGoogle Scholar
  26. Guo Y and Levin HL 2010 High-throughput sequencing of retrotransposon integration provides a saturated profile of target activity in Schizosaccharomyces pombe. Genome Res. 20 239–248PubMedCrossRefGoogle Scholar
  27. Haapa-Paananen 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 2843–2851PubMedCrossRefGoogle Scholar
  28. Haran TE, Kahn JD and Crothers DM 1994 Sequence elements responsible for DNA curvature. J. Mol. Biol. 244 135–143PubMedCrossRefGoogle Scholar
  29. Hillebrand A, Wurm R, Menzel A and Wagner R 2005 The seven E. coli ribosomal RNA operon upstream regulatory regions differ in structure and transcription factor binding efficiencies. Biol. Chem. 386 523–534PubMedCrossRefGoogle Scholar
  30. Hodges-Garcia Y, Hagerman PJ and Pettijohn DE 1989 DNA ring closure mediated by protein HU. J. Biol. Chem. 264 14621–14623PubMedGoogle Scholar
  31. Laundon CH and Griffith JD 1988 Curved helix segments can uniquely orient the topology of supertwisted DNA. Cell 52 545–549PubMedCrossRefGoogle Scholar
  32. Lee I and Harshey RM 2001 Importance of the conserved CA dinucleotide at Mu termini. J. Mol. Biol. 314 433–444PubMedCrossRefGoogle Scholar
  33. Lewinski MK, Yamashita M, Emerman M, Ciuffi A, Marshall H, Crawford G, Collins F, Shinn P, et al. 2006 Retroviral DNA integration: viral and cellular determinants of target-site selection. PLoS Pathog. 2 e60PubMedCrossRefGoogle Scholar
  34. Manna D, Breier AM and Higgins NP 2004 Microarray analysis of transposition targets in Escherichia coli: the impact of transcription. Proc. Natl. Acad. Sci. USA 101 9780–9785PubMedCrossRefGoogle Scholar
  35. Manna D, Deng S, Breier AM and Higgins NP 2005 Bacteriophage Mu targets the trinucleotide sequence CGG. J. Bacteriol. 187 3586–3588PubMedCrossRefGoogle Scholar
  36. Mizuuchi M and Mizuuchi K 1993 Target site selection in transposition of phage Mu. Cold Spring Harb. Symp. Quant. Biol. 58 515–523PubMedCrossRefGoogle Scholar
  37. Murphy LD and Zimmerman SB 1997 Isolation and characterization of spermidine nucleoids from Escherichia coli. J. Struct. Biol. 119 321–335PubMedCrossRefGoogle Scholar
  38. Niki H, Yamaichi Y and Hiraga S 2000 Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 14 212–223PubMedGoogle Scholar
  39. Nomura M 1999 Engineering of bacterial ribosomes: replacement of all seven Escherichia coli rRNA operons by a single plasmid-encoded operon. Proc. Natl. Acad. Sci. USA 96 1820–1822PubMedCrossRefGoogle Scholar
  40. Oshima T, Ishikawa S, Kurokawa K, Aiba H and Ogasawara N 2006 Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res. 13 141–153PubMedCrossRefGoogle Scholar
  41. Parks AR, Li Z, Shi Q, Owens RM, Jin MM and Peters JE 2009 Transposition into replicating DNA occurs through interaction with the processivity factor. Cell 138 685–695PubMedCrossRefGoogle Scholar
  42. Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, Simon I, Zeitlinger J, Schreiber J, et al. 2000 Genome-wide location and function of DNA binding proteins. Science 290 2306–2309PubMedCrossRefGoogle Scholar
  43. Ren CP, Chaudhuri RR, Fivian A, Bailey CM, Antonio M, Barnes WM and Pallen MJ 2004 The ETT2 gene cluster, encoding a second type III secretion system from Escherichia coli, is present in the majority of strains but has undergone widespread mutational attrition. J. Bacteriol. 186 3547–3560PubMedCrossRefGoogle Scholar
  44. Rippe K, von Hippel PH and Langowski J 1995 Action at a distance: DNA-looping and initiation of transcription. Trends Biochem. Sci. 20 500–506PubMedCrossRefGoogle Scholar
  45. Schneider R, Lurz R, Luder G, Tolksdorf C, Travers A and Muskhelishvili G 2001 An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids Res. 29 5107–5114PubMedCrossRefGoogle Scholar
  46. Sinden RR and Pettijohn DE 1981 Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling. Proc. Natl. Acad. Sci. USA 78 224–228PubMedCrossRefGoogle Scholar
  47. Stein RA, Deng S and Higgins NP 2005 Measuring chromosome dynamics on different time scales using resolvases with varying half-lives. Mol. Microbiol. 56 1049–1061PubMedCrossRefGoogle Scholar
  48. Symonds N, Toussaint A, Van de Putte P and Howe MM 1987 Phage Mu (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory)Google Scholar
  49. Tan X, Mizuuchi M and Mizuuchi K 2007 DNA transposition target immunity and the determinants of the MuB distribution patterns on DNA. Proc. Natl. Acad. Sci. USA 104 13925–13929PubMedCrossRefGoogle Scholar
  50. Tolstorukov MY, Virnik KM, Adhya S and Zhurkin VB 2005 A-tract clusters may facilitate DNA packaging in bacterial nucleoid. Nucleic Acids Res. 33 3907–3918PubMedCrossRefGoogle Scholar
  51. Ussery D, Larsen TS, Wilkes KT, Friis C, Worning P, Krogh A and Brunak S 2001 Genome organisation and chromatin structure in Escherichia coli. Biochimie 83 201–212PubMedCrossRefGoogle Scholar
  52. Vora T, Hottes AK and Tavazoie S 2009 Protein occupancy landscape of a bacterial genome. Mol. Cell 35 247–253PubMedCrossRefGoogle Scholar
  53. Wei Y, Lee JM, Richmond C, Blattner FR, Rafalski JA and LaRossa RA 2001 High-density microarray-mediated gene expression profiling of Escherichia coli. J. Bacteriol. 183 545–556PubMedCrossRefGoogle Scholar
  54. Wu X and Burgess SM 2004 Integration target site selection for retroviruses and transposable elements. Cell Mol. Life Sci. 61 2588–2596PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2011

Authors and Affiliations

  • Jun Ge
    • 1
  • Zheng Lou
    • 1
  • Hong Cui
    • 1
  • Lei Shang
    • 1
  • Rasika M Harshey
    • 1
  1. 1.Section of Molecular Genetics and Microbiology & Institute of Cellular and Molecular BiologyUniversity of Texas at AustinAustinUSA

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