The B. subtilis Accessory Helicase PcrA Facilitates DNA Replication through Transcription Units

PLoS Genetics

Volumn 11, Issue 6, 2015, Pages

  Merrikh, Christopher N ^a   Brewer, Bonita J ^a   Merrikh, Houra ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; PROTEIN PCRA; RIBOSOME RNA; TRANSFER RNA; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DNA HELICASE; PCRA PROTEIN, BACTERIA;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BINDING SITE; CELL DEATH; CELL SURVIVAL; DNA REPLICATION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; GENE LOCUS; GENE REPLICATION; HISC GENE; LACZ GENE; NONHUMAN; PCRA GENE; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN DEPLETION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; OPERON;

BACILLUS SUBTILIS; ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA;

ADENOSINE TRIPHOSPHATE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA HELICASES; DNA REPLICATION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; OPERON; RNA, RIBOSOMAL; RNA, TRANSFER; TRANSCRIPTION, GENETIC;

EID: 84937793079     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005289     Document Type: Article

References (52)

1. French S, (1992) Consequences of replication fork movement through transcription units in vivo. Science 258: 1362–1365. 1455232
2. Mirkin EV, Mirkin SM, (2005) Mechanisms of transcription-replication collisions in bacteria. Mol Cell Biol 25: 888–895. 15657418
3. Wang JD, Berkmen MB, Grossman AD, (2007) Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis. Proc Natl Acad Sci U S A 104: 5608–5613. 17372224
4. Rudolph CJ, Dhillon P, Moore T, Lloyd RG, (2007) Avoiding and resolving conflicts between DNA replication and transcription. DNA Repair (Amst) 6: 981–993. 17400034
5. Merrikh H, Machon C, Grainger WH, Grossman AD, Soultanas P, (2011) Co-directional replication-transcription conflicts lead to replication restart. Nature 470: 554–557. doi: 10.1038/nature09758 21350489
6. Dutta D, Shatalin K, Epshtein V, Gottesman ME, Nudler E, (2011) Linking RNA polymerase backtracking to genome instability in E. coli. Cell 146: 533–543. doi: 10.1016/j.cell.2011.07.034 21854980
7. Rocha EP, Danchin A, (2003) Gene essentiality determines chromosome organisation in bacteria. Nucleic Acids Res 31: 6570–6577. 14602916
8. Rocha EP, Danchin A, (2003) Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet 34: 377–378. 12847524
9. Rocha EP, (2004) The replication-related organization of bacterial genomes. Microbiology 150: 1609–1627. 15184548
10. Rocha EP, Touchon M, Feil EJ, (2006) Similar compositional biases are caused by very different mutational effects. Genome Res 16: 1537–1547. 17068325
11. Brewer BJ, (1988) When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53: 679–686. 3286014
12. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390: 249–256. 9384377
13. McLean MJ, Wolfe KH, Devine KM, (1998) Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. J Mol Evol 47: 691–696. 9847411
14. Guy L, Roten CA, (2004) Genometric analyses of the organization of circular chromosomes: a universal pressure determines the direction of ribosomal RNA genes transcription relative to chromosome replication. Gene 340: 45–52. 15556293
15. Price MN, Alm EJ, Arkin AP, (2005) Interruptions in gene expression drive highly expressed operons to the leading strand of DNA replication. Nucleic Acids Res 33: 3224–3234. 15942025
16. Merrikh H, Zhang Y, Grossman AD, Wang JD, (2012) Replication-transcription conflicts in bacteria. Nat Rev Microbiol 10: 449–458. doi: 10.1038/nrmicro2800 22669220
17. Boubakri H, de Septenville AL, Viguera E, Michel B, (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29: 145–157. doi: 10.1038/emboj.2009.308 19851282
18. Baharoglu Z, Lestini R, Duigou S, Michel B, (2010) RNA polymerase mutations that facilitate replication progression in the rep uvrD recF mutant lacking two accessory replicative helicases. Mol Microbiol 77: 324–336. doi: 10.1111/j.1365-2958.2010.07208.x 20497334
19. Condon C, Putzer H, (2002) The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res 30: 5339–5346. 12490701
20. Petit MA, Dervyn E, Rose M, Entian KD, McGovern S, et al. (1998) PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol Microbiol 29: 261–273. 9701819
21. Petit MA, Ehrlich D, (2002) Essential bacterial helicases that counteract the toxicity of recombination proteins. EMBO J 21: 3137–3147. 12065426
22. Cox MM, (1999) Recombinational DNA repair in bacteria and the RecA protein. Prog Nucleic Acid Res Mol Biol 63: 311–366. 10506835
23. Lenhart JS, Schroeder JW, Walsh BW, Simmons LA, (2012) DNA repair and genome maintenance in Bacillus subtilis. Microbiol Mol Biol Rev 76: 530–564. doi: 10.1128/MMBR.05020-11 22933559
24. Anand SP, Zheng H, Bianco PR, Leuba SH, Khan SA, (2007) DNA helicase activity of PcrA is not required for the displacement of RecA protein from DNA or inhibition of RecA-mediated strand exchange. J Bacteriol 189: 4502–4509. 17449621
25. Gwynn EJ, Smith AJ, Guy CP, Savery NJ, McGlynn P, et al. (2013) The conserved C-terminus of the PcrA/UvrD helicase interacts directly with RNA polymerase. PLoS One 8: e78141. doi: 10.1371/journal.pone.0078141 24147116
26. Noirot-Gros MF, Dervyn E, Wu LJ, Mervelet P, Errington J, et al. (2002) An expanded view of bacterial DNA replication. Proc Natl Acad Sci U S A 99: 8342–8347. 12060778
27. Epshtein V, Kamarthapu V, McGary K, Svetlov V, Ueberheide B, et al. (2014) UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 505: 372–377. doi: 10.1038/nature12928 24402227
28. Park J, Myong S, Niedziela-Majka A, Lee KS, Yu J, et al. (2010) PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell 142: 544–555. doi: 10.1016/j.cell.2010.07.016 20723756
29. Fagerburg MV, Schauer GD, Thickman KR, Bianco PR, Khan SA, et al. (2012) PcrA-mediated disruption of RecA nucleoprotein filaments—essential role of the ATPase activity of RecA. Nucleic Acids Res 40: 8416–8424. 22743269
30. Griffith KL, Grossman AD, (2008) Inducible protein degradation in Bacillus subtilis using heterologous peptide tags and adaptor proteins to target substrates to the protease ClpXP. Mol Microbiol 70: 1012–1025. doi: 10.1111/j.1365-2958.2008.06467.x 18811726
31. Merrikh H, Grossman AD, (2011) Control of the replication initiator DnaA by an anti-cooperativity factor. Mol Microbiol 82: 434–446. doi: 10.1111/j.1365-2958.2011.07821.x 21895792
32. Rahn-Lee L, Merrikh H, Grossman AD, Losick R, (2011) The sporulation protein SirA inhibits the binding of DnaA to the origin of replication by contacting a patch of clustered amino acids. J Bacteriol 193: 1302–1307. doi: 10.1128/JB.01390-10 21239581
33. Smits WK, Merrikh H, Bonilla CY, Grossman AD, (2011) Primosomal proteins DnaD and DnaB are recruited to chromosomal regions bound by DnaA in Bacillus subtilis. J Bacteriol 193: 640–648. doi: 10.1128/JB.01253-10 21097613
34. Million-Weaver S, Samadpour AN, Moreno-Habel DA, Nugent P, Brittnacher MJ, et al. (2015) An underlying mechanism for the increased mutagenesis of lagging-strand genes in Bacillus subtilis. Proc Natl Acad Sci U S A 112: E1096–1105. doi: 10.1073/pnas.1416651112 25713353
35. Waldminghaus T, Skarstad K, (2010) ChIP on Chip: surprising results are often artifacts. BMC Genomics 11: 414. doi: 10.1186/1471-2164-11-414 20602746
36. Teytelman L, Thurtle DM, Rine J, van Oudenaarden A, (2013) Highly expressed loci are vulnerable to misleading ChIP localization of multiple unrelated proteins. Proc Natl Acad Sci U S A 110: 18602–18607. doi: 10.1073/pnas.1316064110 24173036
37. Wright GE, Brown NC, (1974) Synthesis of 6-(phenylhydrazino)uracils and their inhibition of a replication-specific deoxyribonucleic acid polymerase. J Med Chem 17: 1277–1282. 4473549
38. Brewer BJ, Fangman WL, (1987) The localization of replication origins on ARS plasmids in S. cerevisiae. Cell 51: 463–471. 2822257
39. Harriott K (2012) The characterisation of the interaction between PcrA and RNA polymerase [University of Newcastle Research Higher Degree Thesis].
40. Bjornson KP, Wong I, Lohman TM, (1996) ATP hydrolysis stimulates binding and release of single stranded DNA from alternating subunits of the dimeric E. coli Rep helicase: implications for ATP-driven helicase translocation. J Mol Biol 263: 411–422. 8918597
41. Guy CP, Atkinson J, Gupta MK, Mahdi AA, Gwynn EJ, et al. (2009) Rep provides a second motor at the replisome to promote duplication of protein-bound DNA. Mol Cell 36: 654–666. doi: 10.1016/j.molcel.2009.11.009 19941825
42. Pomerantz RT, O'Donnell M, (2010) Direct restart of a replication fork stalled by a head-on RNA polymerase. Science 327: 590–592. doi: 10.1126/science.1179595 20110508
43. Srivatsan A, Tehranchi A, MacAlpine DM, Wang JD, (2010) Co-orientation of replication and transcription preserves genome integrity. PLoS Genet 6: e1000810. doi: 10.1371/journal.pgen.1000810 20090829
44. Esnault E, Valens M, Espeli O, Boccard F, (2007) Chromosome structuring limits genome plasticity in Escherichia coli. PLoS Genet 3: e226. 18085828
45. Argueso JL, Westmoreland J, Mieczkowski PA, Gawel M, Petes TD, et al. (2008) Double-strand breaks associated with repetitive DNA can reshape the genome. Proc Natl Acad Sci U S A 105: 11845–11850. doi: 10.1073/pnas.0804529105 18701715
46. Friedman KL, Brewer BJ, (1995) Analysis of replication intermediates by two-dimensional agarose gel electrophoresis. Methods Enzymol 262: 613–627. 8594382
47. Bose B, Grossman AD, (2011) Regulation of horizontal gene transfer in Bacillus subtilis by activation of a conserved site-specific protease. J Bacteriol 193: 22–29. doi: 10.1128/JB.01143-10 21036995
48. Smits WK, Goranov AI, Grossman AD, (2010) Ordered association of helicase loader proteins with the Bacillus subtilis origin of replication in vivo. Mol Microbiol 75: 452–461. doi: 10.1111/j.1365-2958.2009.06999.x 19968790
49. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359. doi: 10.1038/nmeth.1923 22388286
50. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943
51. Lee CA, Babic A, Grossman AD, (2010) Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol 75: 268–279. doi: 10.1111/j.1365-2958.2009.06985.x 19943900
52. Doherty GP, Fogg MJ, Wilkinson AJ, Lewis PJ, (2010) Small subunits of RNA polymerase: localization, levels and implications for core enzyme composition. Microbiology 156: 3532–3543. doi: 10.1099/mic.0.041566-0 20724389