Chromosomal Macrodomains and Associated Proteins: Implications for DNA Organization and Replication in Gram Negative Bacteria
The Escherichia coli chromosome is organized into four macrodomains, the function and organisation of which are poorly understood. In this review we focus on the MatP, SeqA, and SlmA proteins that have recently been identified as the first examples of factors with macrodomain-specific DNA-binding properties. In particular, we review the evidence that these factors contribute towards the control of chromosome replication and segregation by specifically targeting subregions of the genome and contributing towards their unique properties. Genome sequence analysis of multiple related bacteria, including pathogenic species, reveals that macrodomain-specific distribution of SeqA, SlmA, and MatP is conserved, suggesting common principles of chromosome organisation in these organisms. This discovery of proteins with macrodomain-specific binding properties hints that there are other proteins with similar specificity yet to be unveiled. We discuss the roles of the proteins identified to date as well as strategies that may be employed to discover new factors.
Vyšlo v časopise:
Chromosomal Macrodomains and Associated Proteins: Implications for DNA Organization and Replication in Gram Negative Bacteria. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002123
Kategorie:
Review
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002123
Souhrn
The Escherichia coli chromosome is organized into four macrodomains, the function and organisation of which are poorly understood. In this review we focus on the MatP, SeqA, and SlmA proteins that have recently been identified as the first examples of factors with macrodomain-specific DNA-binding properties. In particular, we review the evidence that these factors contribute towards the control of chromosome replication and segregation by specifically targeting subregions of the genome and contributing towards their unique properties. Genome sequence analysis of multiple related bacteria, including pathogenic species, reveals that macrodomain-specific distribution of SeqA, SlmA, and MatP is conserved, suggesting common principles of chromosome organisation in these organisms. This discovery of proteins with macrodomain-specific binding properties hints that there are other proteins with similar specificity yet to be unveiled. We discuss the roles of the proteins identified to date as well as strategies that may be employed to discover new factors.
Zdroje
1. MisteliT 2010 Higher-order genome organization in human disease. Cold Spring Harb Perspect Biol 2 a000794
2. LugerKMäderAWRichmondRKSargentDFRichmondTJ 1997 Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 251 260
3. DillonSCDormanCJ 2010 Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat Rev Microbiol 8 185 195
4. DameRTNoomMCWuiteGJ 2006 Bacterial chromatin organization by H-NS protein unravelled using dual DNA manipulation. Nature 444 387 390
5. van NoortJVerbruggeSGoosenNDekkerCDameRT 2004 Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci U S A 101 6969 6974
6. CosgriffSChintakayalaKChimYTChenXAllenS 2010 Dimerization and DNA-dependent aggregation of the Escherichia coli nucleoid protein and chaperone CbpA. Mol Microbiol 77 1289 1300
7. ChoBKKnightEMBarrettCLPalssonBØ 2008 Genome-wide analysis of Fis binding in Escherichia coli indicates a causative role for A-/AT-tracts. Genome Res 18 900 910
8. NoomMCNavarreWWOshimaTWuiteGJDameRT 2007 H-NS promotes looped domain formation in the bacterial chromosome. Curr Biol 17 R913 R914
9. BoccardFEsnaultEValensM 2005 Spatial arrangement and macrodomain organization of bacterial chromosomes. Mol Microbiol 57 9 16
10. NikiHYamaichiYHiragaS 2000 Dynamic organisation of chromosomal DNA in Escherichia coli. Genes Dev 14 212 223
11. NielsenHJOttensenJRYoungrenBAustinSJHansenFG 2006 The Escherichia coli chromosome is organised with the left and right chromosome arms in separate cell halves. Mol Microbiol 62 331 338
12. WangXLiuXPossozCSherattDJ 2006 The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev 20 1727 1731
13. ValensMPenaudSRossignolMCornetFBoccardF 2004 Macrodomain organization of the Escherichia coli chromosome. EMBO J 23 4330 4341
14. EspeliOMercierRBoccardF 2008 DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol Microbiol 68 1418 1427
15. LovettSTSegallAM 2004 New views of the bacterial chromosome. EMBO Rep 5 860 864
16. WigginsPACheverallsKCMartinJSLintnerRKondevJ 2010 Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament. Proc Natl Acad Sci 107 4991 4995
17. Sánchez-RomeroMABusbySJDyerNPOttSMillardAD 2010 Dynamic distribution of SeqA protein across the chromosome of Escherichia coli K-12. mBio 1 e00012 10
18. WaldminghausTSkarstadK 2010 ChIP on Chip: surprising results are often artefacts. BMC Genomics 11 414
19. TonthatNKAroldSTPickeringBFVan DykeMWLiangS 2011 Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30 154 164
20. MercierRPetitMASchbathSRobinSEl KarouiM 2008 The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135 475 485
21. ChoHMcManusHRDoveSLBernhardtTG 2011 Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerisation antagonist. Proc Natl Acad Sci U S A 108 3773 3778
22. LuMCampbellJLBoyeEKlecknerN 1994 SeqA: a negative modulator of replication initiation in E. coli. Cell 77 413 426
23. von FreieslebenURasmussenKVSchaechterM 1994 SeqA limits DnaA activity in replication from oriC in Escherichia coli. Mol Microbiol 14 763 772
24. BachTKreklingMASkarstadK 2003 Excess SeqA prolongs sequestration of oriC and delays nucleoid segregation and cell division. EMBO J 22 315 323
25. BernhardtTGde BoerPA 2005 SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol. Cell 18 555 564
26. LiYYoungrenBSergueevKAustinS 2003 Segregation of the Escherichia coli chromosome terminus. Mol Microbiol 50 825 834
27. MargolinW 2005 FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6 862 871
28. WuLJIshiwakaSKawaiYOshimaTOgasawaraN 2009 Noc protein binds to specific DNA sequences to co-ordinate cell division with chromosome segregation. EMBO J 28 1940 1952
29. ThanbichlerMShapiroL 2006 MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126 147 162
30. ZhouPBoganJAWelchKPickettSRWangHJ 1997 Gene transcription and chromosome replication in Escherichia coli. J Bacteriol 179 163 169
31. BoganJAHelmstetterCE 1996 mioC transcription, initiation of replication, and the eclipse in Escherichia coli. J Bacteriol 178 3201 3206
32. ZhouPHelmstetterCE 1994 Relationship between ftsZ gene expression and chromosome replication in Escherichia coli. J Bacteriol 176 6100 6106
33. Løbner-OlesenAMarinusMGHansenFG 2003 Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci U S A 100 4672 4677
34. ButalaMBusbySJLeeDJ 2009 DNA sampling: a method for probing protein binding at specific loci on bacterial chromosomes. Nucleic Acids Res 37 e37
35. ZimmermanSB 2006 Cooperative transitions of isolated Escherichia coli nucleoids: implications for the nucleoid as a cellular phase. J Struct Biol 153 160 175
36. van BerkumNLDekkerJ 2009 Determining spatial chromatin organization of large genomic regions using 5C technology. Methods Mol Biol 567 189 213
37. GitaiZ 2009 New fluorescence microscopy methods for microbiology: sharper, faster, and quantitative. Curr Opin Microbiol 12 341 346
38. XieXSChoiPJLiG-WLeeNKLiaG 2008 Single-molecule approach to molecular biology in living bacterial cells. Ann Rev Biophys 37 417 444
39. OhniwaRLMorikawaKKimJOhtaTIshihamaA 2006 Dynamic state of DNA topology is essential for genome condensation in bacteria. EMBO J 25 5591 5602
40. CabreraJECaglieroCQuanSSquiresCLJinDJ 2009 Active transcription of rRNA operons condenses the nucleoid in Escherichia coli: examining the effect of transcription on nucleoid structure in the absence of transertion. J Bacteriol 191 4180 4185
41. GraingerDCHurdDGoldbergMDBusbySJ 2006 Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res 34 4642 4652
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 6
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Statistical Inference on the Mechanisms of Genome Evolution
- Recurrent Chromosome 16p13.1 Duplications Are a Risk Factor for Aortic Dissections
- Chromosomal Macrodomains and Associated Proteins: Implications for DNA Organization and Replication in Gram Negative Bacteria
- Maps of Open Chromatin Guide the Functional Follow-Up of Genome-Wide Association Signals: Application to Hematological Traits