Spatial organization of transcription machinery and its segregation from the replisome in fast-growing bacterial cells

Nucleic Acids Research

Volumn 42, Issue 22, 2014, Pages 13696-13705

  Cagliero, Cedric ^a   Zhou, Yan Ning ^a   Jin, Ding Jun ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; NUSA PROTEIN; NUSB PROTEIN; RIBOSOME RNA; RNA POLYMERASE; UNCLASSIFIED DRUG; ANTITERMINATOR PROTEINS, BACTERIA; DNA DIRECTED DNA POLYMERASE; DNA SYNTHESOME; ELONGATION FACTOR; ESCHERICHIA COLI PROTEIN; MULTIENZYME COMPLEX; NUSA PROTEIN, E COLI; NUSB PROTEIN, E COLI; RNA BINDING PROTEIN; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL CELL; BACTERIAL CHROMOSOME; CELL COMPARTMENTALIZATION; CELL FUNCTION; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA REPLICATION; ESCHERICHIA COLI; GENE DUPLICATION; GENE SEGREGATION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; REPLISOME; RNA SYNTHESIS; TRANSCRIPTION MACHINERY; GENETICS; GROWTH, DEVELOPMENT AND AGING; RNA GENE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

BACTERIAL PROTEINS; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENES, RRNA; MULTIENZYME COMPLEXES; PEPTIDE ELONGATION FACTORS; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 84928796748     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1103     Document Type: Article

References (56)

1. Stokke, C., Flatten, I. and Skarstad, K. (2012) An easy-to-use simulation program demonstrates variations in bacterial cell cycle parameters depending on medium and temperature. PLoS One, 7, e30981.
2. Jin, D.J., Cagliero, C. and Zhou, Y.N. (2012) Growth rate regulation in Escherichia coli. FEMS Microbiol. Rev., 36, 269-287.
3. Jin, D.J., Cagliero, C. and Zhou, Y.N. (2013) Role of RNA polymerase and transcription in the organization of the bacterial nucleoid. Chem. Rev., 113, 8662-8682.
4. Cabrera, J.E. and Jin, D.J. (2003) The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues. Mol. Microbiol., 50, 1493-1505.
5. Nielsen, H.J., Youngren, B., Hansen, F.G. and Austin, S. (2007) Dynamics of Escherichia coli chromosome segregation during multifork replication. J. Bacteriol., 189, 8660-8666.
6. Bremer, H. and Dennis, P.P. (1996) Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt, FC, Curtiss, R III, Ingraham, JL, Lin, ECC, Low, KB, Magasanik, B, Reznikoff, WS, Riley, M, Schaechter, M and Umbarger, HE (eds). Escherichia coli and Salmonella. ASM Press, Washington, DC, 2, pp. 1553-1569.
7. Endesfelder, U., Finan, K., Holden, S.J., Cook, P.R., Kapanidis, A.N. and Heilemann, M. (2013) Multiscale spatial organization of RNA polymerase in Escherichia coli. Biophys. J., 105, 172-181.
8. Quan, S., Zhang, N., French, S. and Squires, C.L. (2005) Transcriptional polarity in rRNA operons of Escherichia coli nusA and nusB mutant strains. J. Bacteriol., 187, 1632-1638.
9. Squires, C.L., Greenblatt, J., Li, J. and Condon, C. (1993) Ribosomal RNA antitermination in vitro: requirement for Nus factors and one or more unidentifed cellular components. Proc. Natl Acad. Sci. U. S. A., 90, 970-974.
10. Morgan, E.A. (1986) Antitermination mechanisms in rRNA operons of Escherichia coli. J. Bacteriol., 168, 1-5.
11. Court, D.L., Oppenheim, A.B. and Adhya, S.L. (2007) A new look at bacteriophage lambda genetic networks. J. Bacteriol., 189, 298-304.
12. Li, S.C., Squires, C.L. and Squires, C. (1984) Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut-like sequences. Cell, 38, 851-860.
13. Torres, M., Balada, J.M., Zellars, M., Squires, C. and Squires, C.L. (2004) In vivo effect of NusB and NusG on rRNA transcription antitermination. J. Bacteriol., 186, 1304-1310.
14. Greenblatt, J. and Li, J. (1981) Interaction of the sigma factor and the nusA gene protein of E. coli with RNA polymerase in the initiation-termination cycle of transcription. Cell, 24, 421-428.
15. Stagno, J.R., Altieri, A.S., Bubunenko, M., Tarasov, S.G., Li, J., Court, D.L., Byrd, R.A. and Ji, X. (2011) Structural basis for RNA recognition by NusB and NusE in the initiation of transcription antitermination. Nucleic Acids Res., 39, 7803-7815.
16. Greive, S.J., Lins, A.F. and von Hippel, P.H. (2005) Assembly of an RNA-protein complex. Binding of NusB and NusE (S10) proteins to boxA RNA nucleates the formation of the antitermination complex involved in controlling rRNA transcription in Escherichia coli. J. Biol. Chem., 280, 36397-36408.
17. Nodwell, J.R. and Greenblatt, J. (1993) Recognition of boxA antiterminator RNA by the E. coli antitermination factors NusB and ribosomal protein S10. Cell, 72, 261-268.
18. Davies, K.M., Dedman, A.J., van Horck, S. and Lewis, P.J. (2005) The NusA:RNA polymerase ratio is increased at sites of rRNA synthesis in Bacillus subtilis. Mol. Microbiol., 57, 366-379.
19. Doherty, G.P., Meredith, D.H. and Lewis, P.J. (2006) Subcellular partitioning of transcription factors in Bacillus subtilis. J. Bacteriol., 188, 4101-4110.
20. Cabrera, J.E., Cagliero, C., Quan, S., Squires, C.L. and Jin, D.J. (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.
21. Jin, D.J. and Cabrera, J.E. (2006) Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J. Struct. Biol., 156, 284-291.
22. Yao, N.Y. and O'Donnell, M. (2010) SnapShot: the replisome. Cell, 141, 1088, 1088.e1.
23. O'Donnell, M. (2006) Replisome architecture and dynamics in Escherichia coli. J. Biol. Chem., 281, 10653-10656.
24. Reyes-Lamothe, R., Possoz, C., Danilova, O. and Sherratt, D.J. (2008) Independent positioning and action of Escherichia coli replisomes in live cells. Cell, 133, 90-102.
25. Marceau, A.H., Bahng, S., Massoni, S.C., George, N.P., Sandler, S.J., Marians, K.J. and Keck, J.L. (2011) Structure of the SSB-DNA polymerase III interface and its role in DNA replication. EMBO J., 30, 4236-4247.
26. Lu, M., Campbell, J.L., Boye, E. and Kleckner, N. (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell, 77, 413-426.
27. Waldminghaus, T. and Skarstad, K. (2009) The Escherichia coli SeqA protein. Plasmid, 61, 141-150.
28. Waldminghaus, T., Weigel, C. and Skarstad, K. (2012) Replication fork movement and methylation govern SeqA binding to the Escherichia coli chromosome. Nucleic Acids Res., 40, 5465-5476.
29. Hiraga, S., Ichinose, C., Niki, H. and Yamazoe, M. (1998) Cell cycle-dependent duplication and bidirectional migration of SeqA-associated DNA-protein complexes in E. coli. Mol. Cell, 1, 381-387.
30. Yamazoe, M., Adachi, S., Kanaya, S., Ohsumi, K. and Hiraga, S. (2005) Sequential binding of SeqA protein to nascent DNA segments at replication forks in synchronized cultures of Escherichia coli. Mol. Microbiol., 55, 289-298.
31. Brendler, T., Sawitzke, J., Sergueev, K. and Austin, S. (2000) A case for sliding SeqA tracts at anchored replication forks during Escherichia coli chromosome replication and segregation. EMBO J., 19, 6249-6258.
32. Cagliero, C., Grand, R.S., Jones, M.B., Jin, D.J. and O'Sullivan, J.M. (2013) Genome conformation capture reveals that the Escherichia coli chromosome is organized by replication and transcription. Nucleic Acids Res., 41, 6058-6071.
33. Merrikh, H., Zhang, Y., Grossman, A.D. and Wang, J.D. (2012) Replication-transcription conficts in bacteria. Nat. Rev. Microbiol., 10, 449-458.
34. Carlton, P.M. (2008) Three-dimensional structured illumination microscopy and its application to chromosome structure. Chromosome Res., 16, 351-365.
35. Langhorst, M.F., Schaffer, J. and Goetze, B. (2009) Structure brings clarity: structured illumination microscopy in cell biology. Biotechnol. J., 4, 858-865.
36. Cagliero, C. and Jin, D.J. (2013) Dissociation and re-association of RNA polymerase with DNA during osmotic stress response in Escherichia coli. Nucleic Acids Res., 41, 315-326.
37. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. U.S.A., 97, 6640-6645.
38. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Plainview, NY.
39. Canny, J. (1986) A computational approach to edge-detection. IEEE Trans. Pattern Anal. Mach. Intell., 8, 679-698.
40. Meyer, F. (1994) Topographic distance and watershed lines. Signal Process., 38, 113-125.
41. Bolte, S. and Cordelieres, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc., 224, 213-232.
42. Nicolas, E., Upton, A.L., Uphoff, S., Henry, O., Badrinarayanan, A. and Sherratt, D. (2014) The SMC complex MukBEF recruits topoisomerase IV to the origin of replication region in live Escherichia coli. MBio, 5, e01001-e01013.
43. Bakshi, S., Siryaporn, A., Goulian, M. and Weisshaar, J.C. (2012) Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Mol. Microbiol., 85, 21-38.
44. Spahn, C., Endesfelder, U. and Heilemann, M. (2014) Super-resolution imaging of Escherichia coli nucleoids reveals highly structured and asymmetric segregation during fast growth. J. Struct. Biol., 185, 243-249.
45. Margolin, W. (2012) Imaging the Bacterial Nucleoid. In: Dame, RT and Dorman, CJ (eds). In Bacterial Chromatin. Springer Dordrecht, Heidelberg, pp. 13-30.
46. Onogi, T., Niki, H., Yamazoe, M. and Hiraga, S. (1999) The assembly and migration of SeqA-Gfp fusion in living cells of Escherichia coli. Mol. Microbiol., 31, 1775-1782.
47. Morigen, Odsbu, I. and Skarstad, K. (2009) Growth rate dependent numbers of SeqA structures organize the multiple replication forks in rapidly growing Escherichia coli. Genes Cells, 14, 643-657.
48. Molina, F. and Skarstad, K. (2004) Replication fork and SeqA focus distributions in Escherichia coli suggest a replication hyperstructure dependent on nucleotide metabolism. Mol. Microbiol., 52, 1597-1612.
49. Norris, V., den Blaauwen, T., Cabin-Flaman, A., Doi, R.H., Harshey, R., Janniere, L., Jimenez-Sanchez, A., Jin, D.J., Levin, P.A., Mileykovskaya, E. et al. (2007) Functional taxonomy of bacterial hyperstructures. Microbiol. Mol. Biol. Rev., 71, 230-253.
50. Wang, F., Redding, S., Finkelstein, I.J., Gorman, J., Reichman, D.R. and Greene, E.C. (2013) The promoter-search mechanism of Escherichia coli RNA polymerase is dominated by three-dimensional diffusion. Nat. Struct. Mol. Biol., 20, 174-181.
51. Sanchez-Romero, M.A., Busby, S.J., Dyer, N.P., Ott, S., Millard, A.D. and Grainger, D.C. (2010) Dynamic distribution of seqa protein across the chromosome of escherichia coli K-12. MBio, 1, doi:10.1128/mBio.00012-10.
52. Bates, D., Epstein, J., Boye, E., Fahrner, K., Berg, H. and Kleckner, N. (2005) The Escherichia coli baby cell column: a novel cell synchronization method provides new insight into the bacterial cell cycle. Mol. Microbiol., 57, 380-391.
53. Nielsen, H.J., Li, Y., Youngren, B., Hansen, F.G. and Austin, S. (2006) Progressive segregation of the Escherichia coli chromosome. Mol. Microbiol., 61, 383-393.
54. Meaburn, K.J. and Misteli, T. (2007) Cell biology: chromosome territories. Nature, 445, 379-781.
55. Cremer, T. and Cremer, M. (2010) Chromosome territories. Cold Spring Harb. Perspect. Biol., 2, a003889.
56. Cavalli, G. and Misteli, T. (2013) Functional implications of genome topology. Nat. Struct. Mol. Biol., 20, 290-299.