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

Journal of Biosciences

Volumn 36, Issue 4, 2011, Pages 587-601

  Ge, Jun ^a   Lou, Zheng ^a   Cui, Hong ^a   Shang, Lei ^a   Harshey, Rasika M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

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

Indexed keywords

BACTERIAL PROTEIN; PROTEIN MUB; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CHROMOSOME; COLIFORM BACTERIUM; DNA; GENOME; PROTEIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIOPHAGE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA DETERMINATION; DNA EXTRACTION; DNA TRANSPOSITION; ESCHERICHIA COLI; GENE AMPLIFICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

BACTERIOPHAGE MU; BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME MAPPING; CHROMOSOMES; DNA; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FACTOR FOR INVERSION STIMULATION PROTEIN; LAB-ON-A-CHIP DEVICES; MUTAGENESIS, INSERTIONAL; NUCLEIC ACID AMPLIFICATION TECHNIQUES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMIDS; PROTEIN BINDING; SEQUENCE DELETION;

ENTEROBACTERIA PHAGE MU; ESCHERICHIA COLI;

EID: 80055010605     PISSN: 02505991     EISSN: 09737138     Source Type: Journal    
DOI: 10.1007/s12038-011-9108-z     Document Type: Article

References (54)

1. K Adzuma K Mizuuchi 1988 Target immunity of Mu transposition reflects a differential distribution of Mu B protein Cell 53 257 266 2965985 10.1016/0092-8674(88)90387-X 1:CAS:528:DyaL1cXktlaru7k%3D
2. K Adzuma K Mizuuchi 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 1826105 1:CAS:528: DyaK3MXhvVWiu7w%3D (Pubitemid 21906198)
3. AI Alexandrov NR Cozzarelli VF Holmes AB Khodursky BJ Peter L Postow V Rybenkov AV Vologodskii 1999 Mechanisms of separation of the complementary strands of DNA during replication Genetica 106 131 140 10710719 10.1023/A:1003749416449 1:CAS:528:DC%2BD3cXpt1yrug%3D%3D (Pubitemid 30049241)
4. TK Au P Agrawal RM Harshey 2006 Chromosomal integration mechanism of infecting mu virion DNA J. Bacteriol. 188 1829 1834 16484193 10.1128/JB.188.5.1829-1834.2006 1:CAS:528:DC%2BD28XisVWhs7k%3D (Pubitemid 43346861)
5. TA Azam A Ishihama 1999 Twelve species of the nucleoid-associated protein from Escherichia coli. Sequence recognition specificity and DNA binding affinity J. Biol. Chem. 274 33105 33113 10551881 10.1074/jbc.274.46.33105 1:CAS:528:DyaK1MXntlygu7c%3D (Pubitemid 129535353)
6. A Beauregard MJ Curcio M Belfort 2008 The take and give between retrotransposable elements and their hosts Annu. Rev. Genet. 42 587 617 18680436 10.1146/annurev.genet.42.110807.091549 1:CAS:528:DC%2BD1cXhsFemtbvP
7. C Berry S Hannenhalli J Leipzig FD Bushman 2006 Selection of target sites for mobile DNA integration in the human genome PLoS Comput. Biol. 2 e157 17166054 10.1371/journal.pcbi.0020157 (Pubitemid 44819930)
8. N Blot R Mavathur M Geertz A Travers G Muskhelishvili 2006 Homeostatic regulation of supercoiling sensitivity coordinates transcription of the bacterial genome EMBO Rep. 7 710 715 16799466 10.1038/sj.embor.7400729 1:CAS:528:DC%2BD28XmsVanuro%3D (Pubitemid 43986268)
9. F Boccard E Esnault M Valens 2005 Spatial arrangement and macrodomain organization of bacterial chromosomes Mol. Microbiol. 57 9 16 15948945 10.1111/j.1365-2958.2005.04651.x 1:CAS:528:DC%2BD2MXmtVemsb8%3D (Pubitemid 40896593)
10. T Brady YN Lee K Ronen N Malani CC Berry PD Bieniasz FD Bushman 2009 Integration target site selection by a resurrected human endogenous retrovirus Genes Dev. 23 633 642 19270161 10.1101/gad.1762309 1:CAS:528: DC%2BD1MXjsVals7c%3D
11. AI Bukhari AL Taylor 1975 Influence of insertions on packaging of host sequences covalently linked to bacteriophage Mu DNA Proc. Natl. Acad. Sci. USA 72 4399 4403 1060118 10.1073/pnas.72.11.4399 1:CAS:528:DyaE28Xisl2ntQ%3D%3D
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 384-402
13. BK Cho EM Knight CL Barrett BO Palsson 2008 Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts Genome Res. 18 900 910 18340041 10.1101/gr.070276.107 1:CAS:528:DC%2BD1cXnsVygsb8%3D (Pubitemid 351793062)
14. C Condon J Philips ZY Fu C Squires CL Squires 1992 Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli EMBO J. 11 4175 4185 1396599 1:CAS:528:DyaK38Xmt1Olu7w%3D
15. C Condon C Squires CL Squires 1995 Control of rRNA transcription in Escherichia coli Microbiol. Rev. 59 623 645 8531889 1:CAS:528: DyaK28XmvFWiuw%3D%3D
16. NL Craig 1997 Target site selection in transposition Annu. Rev. Biochem. 66 437 474 9242914 10.1146/annurev.biochem.66.1.437 1:CAS:528:DyaK2sXktFOntLg%3D (Pubitemid 27274664)
17. RT Dame 2005 The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin Mol. Microbiol. 56 858 870 15853876 10.1111/j.1365-2958.2005.04598.x 1:CAS:528:DC%2BD2MXktlyns7c%3D (Pubitemid 40646761)
18. KA Datsenko BL Wanner 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. USA 97 6640 6645 10829079 10.1073/pnas.120163297 1:CAS:528:DC%2BD3cXktFais7c%3D (Pubitemid 30412767)
19. S Deng RA Stein NP Higgins 2005 Organization of supercoil domains and their reorganization by transcription Mol. Microbiol. 57 1511 1521 16135220 10.1111/j.1365-2958.2005.04796.x 1:CAS:528:DC%2BD2MXhtVKqsrzF (Pubitemid 41337382)
20. SC Dillon CJ Dorman 2010 Bacterial nucleoid-associated proteins, nucleoid structure and gene expression Nat. Rev. Microbiol. 8 185 195 20140026 10.1038/nrmicro2261 1:CAS:528:DC%2BC3cXhs1Omtbc%3D
21. CJ Dorman P Deighan 2003 Regulation of gene expression by histone-like proteins in bacteria Curr. Opin. Genet. Dev 13 179 184 12672495 10.1016/S0959-437X(03)00025-X 1:CAS:528:DC%2BD3sXisV2rtbg%3D (Pubitemid 36369742)
22. O Espeli R Mercier F Boccard 2008 DNA dynamics vary according to macrodomain topography in the E. coli chromosome Mol. Microbiol. 68 1418 1427 18410497 10.1111/j.1365-2958.2008.06239.x 1:CAS:528:DC%2BD1cXntlWjsbs%3D (Pubitemid 351725253)
23. J Ge RM Harshey 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. 380 598 607 18556020 10.1016/j.jmb.2008.05.032 1:CAS:528:DC%2BD1cXnvVKgtrc%3D
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. EC Greene K Mizuuchi 2004 Visualizing the assembly and disassembly mechanisms of the MuB transposition targeting complex J. Biol. Chem. 279 16736 16743 14871890 10.1074/jbc.M311883200 1:CAS:528:DC%2BD2cXivF2qu7s%3D (Pubitemid 38509376)
26. Y Guo HL Levin 2010 High-throughput sequencing of retrotransposon integration provides a saturated profile of target activity in Schizosaccharomyces pombe Genome Res. 20 239 248 20040583 10.1101/gr.099648.109 1:CAS:528:DC%2BC3cXhs1Ghtbw%3D
27. S Haapa-Paananen H Rita H Savilahti 2002 DNA transposition of bacteriophage Mu. A quantitative analysis of target site selection in vitro J. Biol. Chem. 277 2843 2851 11700310 10.1074/jbc.M108044200 1:CAS:528: DC%2BD38XhtVSgt7w%3D (Pubitemid 34953317)
28. TE Haran JD Kahn DM Crothers 1994 Sequence elements responsible for DNA curvature J. Mol. Biol. 244 135 143 7966325 10.1006/jmbi.1994.1713 1:CAS:528:DyaK2MXitl2htr4%3D (Pubitemid 24366032)
29. A Hillebrand R Wurm A Menzel R Wagner 2005 The seven E. coli ribosomal RNA operon upstream regulatory regions differ in structure and transcription factor binding efficiencies Biol. Chem. 386 523 534 16006239 10.1515/BC.2005.062 1:CAS:528:DC%2BD2MXlvFCqtr0%3D (Pubitemid 41447574)
30. Y Hodges-Garcia PJ Hagerman DE Pettijohn 1989 DNA ring closure mediated by protein HU J. Biol. Chem. 264 14621 14623 2768236 1:CAS:528: DyaL1MXls12ltrs%3D
31. CH Laundon JD Griffith 1988 Curved helix segments can uniquely orient the topology of supertwisted DNA Cell 52 545 549 2830027 10.1016/0092-8674(88) 90467-9 1:STN:280:DyaL1c7jsFOluw%3D%3D
32. I Lee RM Harshey 2001 Importance of the conserved CA dinucleotide at Mu termini J. Mol. Biol. 314 433 444 11846557 10.1006/jmbi.2001.5177 1:CAS:528:DC%2BD38XivFGksQ%3D%3D (Pubitemid 33131847)
33. MK Lewinski M Yamashita M Emerman A Ciuffi H Marshall G Crawford F Collins P Shinn, et al. 2006 Retroviral DNA integration: viral and cellular determinants of target-site selection PLoS Pathog. 2 e60 16789841 10.1371/journal.ppat.0020060 (Pubitemid 43998856)
34. D Manna AM Breier NP Higgins 2004 Microarray analysis of transposition targets in Escherichia coli: the impact of transcription Proc. Natl. Acad. Sci. USA 101 9780 9785 15210965 10.1073/pnas.0400745101 1:CAS:528: DC%2BD2cXlvVaht7k%3D (Pubitemid 38869313)
35. D Manna S Deng AM Breier NP Higgins 2005 Bacteriophage Mu targets the trinucleotide sequence CGG J. Bacteriol. 187 3586 3588 15866949 10.1128/JB.187.10.3586-3588.2005 1:CAS:528:DC%2BD2MXkt1Cksbc%3D (Pubitemid 40628718)
36. M Mizuuchi K Mizuuchi 1993 Target site selection in transposition of phage Mu Cold Spring Harb. Symp. Quant. Biol. 58 515 523 7956065 1:CAS:528:DyaK2MXmtFyltw%3D%3D (Pubitemid 24219513)
37. LD Murphy SB Zimmerman 1997 Isolation and characterization of spermidine nucleoids from Escherichia coli J. Struct. Biol. 119 321 335 9245770 10.1006/jsbi.1997.3883 1:CAS:528:DyaK2sXls1Sls7k%3D (Pubitemid 27357280)
38. H Niki Y Yamaichi S Hiraga 2000 Dynamic organization of chromosomal DNA in Escherichia coli Genes Dev. 14 212 223 10652275 1:CAS:528: DC%2BD3cXhtVSht7w%3D (Pubitemid 30070986)
39. M Nomura 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 1822 10051551 10.1073/pnas.96.5.1820 1:CAS:528:DyaK1MXhvVSrtb4%3D (Pubitemid 29117824)
40. T Oshima S Ishikawa K Kurokawa H Aiba N Ogasawara 2006 Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase DNA Res 13 141 153 17046956 10.1093/dnares/ dsl009 1:CAS:528:DC%2BD28Xht1GktLnK (Pubitemid 44726365)
41. AR Parks Z Li Q Shi RM Owens MM Jin JE Peters 2009 Transposition into replicating DNA occurs through interaction with the processivity factor Cell 138 685 695 19703395 10.1016/j.cell.2009.06.011 1:CAS:528:DC%2BD1MXhsVCjs7rN
42. B Ren F Robert JJ Wyrick O Aparicio EG Jennings I Simon J Zeitlinger J Schreiber, et al. 2000 Genome-wide location and function of DNA binding proteins Science 290 2306 2309 11125145 10.1126/science.290.5500.2306 1:CAS:528:DC%2BD3cXptFSmsL8%3D (Pubitemid 32041573)
43. CP Ren RR Chaudhuri A Fivian CM Bailey M Antonio WM Barnes MJ Pallen 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 3560 15150243 10.1128/JB.186.11.3547-3560.2004 1:CAS:528:DC%2BD2cXks1Cqt7o%3D (Pubitemid 38661553)
44. K Rippe PH von Hippel J Langowski 1995 Action at a distance: DNA-looping and initiation of transcription Trends Biochem. Sci. 20 500 506 8571451 10.1016/S0968-0004(00)89117-3 1:CAS:528:DyaK2MXhtVSjsLbK
45. R Schneider R Lurz G Luder C Tolksdorf A Travers G Muskhelishvili 2001 An architectural role of the Escherichia coli chromatin protein FIS in organising DNA Nucleic Acids Res. 29 5107 5114 11812843 10.1093/nar/29.24.5107 1:CAS:528:DC%2BD38Xmslantw%3D%3D (Pubitemid 34065428)
46. RR Sinden DE Pettijohn 1981 Chromosomes in living Escherichia coli cells are segregated into domains of supercoiling Proc. Natl. Acad. Sci. USA 78 224 228 6165987 10.1073/pnas.78.1.224 1:CAS:528:DyaL3MXhtFOlt70%3D (Pubitemid 11131269)
47. RA Stein S Deng NP Higgins 2005 Measuring chromosome dynamics on different time scales using resolvases with varying half-lives Mol. Microbiol. 56 1049 1061 15853889 10.1111/j.1365-2958.2005.04588.x 1:CAS:528: DC%2BD2MXktlynsbw%3D (Pubitemid 40646774)
48. Symonds N, Toussaint A, Van de Putte P and Howe MM 1987 Phage Mu (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory)
49. X Tan M Mizuuchi K Mizuuchi 2007 DNA transposition target immunity and the determinants of the MuB distribution patterns on DNA Proc. Natl. Acad. Sci. USA 104 13925 13929 17709741 10.1073/pnas.0706564104 1:CAS:528: DC%2BD2sXhtVWisr3K (Pubitemid 350003314)
50. MY Tolstorukov KM Virnik S Adhya VB Zhurkin 2005 A-tract clusters may facilitate DNA packaging in bacterial nucleoid Nucleic Acids Res. 33 3907 3918 16024741 10.1093/nar/gki699 1:CAS:528:DC%2BD2MXmsV2hsb8%3D (Pubitemid 41418559)
51. D Ussery TS Larsen KT Wilkes C Friis P Worning A Krogh S Brunak 2001 Genome organisation and chromatin structure in Escherichia coli Biochimie 83 201 212 11278070 10.1016/S0300-9084(00)01225-6 1:CAS:528:DC%2BD3MXitlWjtrk%3D (Pubitemid 32243565)
52. T Vora AK Hottes S Tavazoie 2009 Protein occupancy landscape of a bacterial genome Mol. Cell 35 247 253 19647521 10.1016/j.molcel.2009.06.035 1:CAS:528:DC%2BD1MXhtVKqt7%2FM
53. Y Wei JM Lee C Richmond FR Blattner JA Rafalski RA LaRossa 2001 High-density microarray-mediated gene expression profiling of Escherichia coli J. Bacteriol. 183 545 556 11133948 10.1128/JB.183.2.545-556.2001 1:CAS:528:DC%2BD3MXktVOksQ%3D%3D (Pubitemid 32048113)
54. X Wu SM Burgess 2004 Integration target site selection for retroviruses and transposable elements Cell Mol. Life Sci. 61 2588 2596 15526164 10.1007/s00018-004-4206-9 1:CAS:528:DC%2BD2cXhtVOmt7bN (Pubitemid 39586519)