DNA double strand break repair in Escherichia coli perturbs cell division and chromosome dynamics
Autoři:
Martin A. White aff001; Elise Darmon aff001; Manuel A. Lopez-Vernaza aff001; David R. F. Leach aff001
Působiště autorů:
Institute of Cell Biology, School of Biological Sciences, University of Edinburgh, The King’s Buildings, Edinburgh, United Kingdom
aff001; Department of Molecular and Cellular Biology, Harvard University, Cambridge MA, United States of America
aff002
Vyšlo v časopise:
DNA double strand break repair in Escherichia coli perturbs cell division and chromosome dynamics. PLoS Genet 16(1): e32767. doi:10.1371/journal.pgen.1008473
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1008473
Souhrn
To prevent the transmission of damaged genomic material between generations, cells require a system for accommodating DNA repair within their cell cycles. We have previously shown that Escherichia coli cells subject to a single, repairable site-specific DNA double-strand break (DSB) per DNA replication cycle reach a new average cell length, with a negligible effect on population growth rate. We show here that this new cell size distribution is caused by a DSB repair-dependent delay in completion of cell division. This delay occurs despite unperturbed cell size regulated initiation of both chromosomal DNA replication and cell division. Furthermore, despite DSB repair altering the profile of DNA replication across the genome, the time required to complete chromosomal duplication is invariant. The delay in completion of cell division is accompanied by a DSB repair-dependent delay in individualization of sister nucleoids. We suggest that DSB repair events create inter-sister connections that persist until those chromosomes are separated by a closing septum.
Klíčová slova:
DNA replication – Cell cycle and cell division – Genetic loci – Chromosome structure and function – Fluorescence imaging – DNA repair – Chromosomal DNA – Cytokinesis
Zdroje
1. Eykelenboom JK, Blackwood JK, Okely E, Leach DR. SbcCD causes a double-strand break at a DNA palindrome in the Escherichia coli chromosome. Mol Cell. 2008;29(5):644–51. Epub 2008/03/18. doi: 10.1016/j.molcel.2007.12.020 18342610.
2. Darmon E, Eykelenboom JK, Lopez-Vernaza MA, White MA, Leach DR. Repair on the Go: E. coli Maintains a High Proliferation Rate while Repairing a Chronic DNA Double-Strand Break. PLoS One. 2014;9(10):e110784. Epub 2014/10/30. doi: 10.1371/journal.pone.0110784 25353327.
3. Sinha AK, Possoz C, Durand A, Desfontaines JM, Barre FX, Leach DRF, et al. Broken replication forks trigger heritable DNA breaks in the terminus of a circular chromosome. PLoS Genet. 2018;14(3):e1007256. Epub 2018/03/10. doi: 10.1371/journal.pgen.1007256 29522563; PubMed Central PMCID: PMCPMC5862497.
4. White MA, Eykelenboom JK, Lopez-Vernaza MA, Wilson E, Leach DR. Non-random segregation of sister chromosomes in Escherichia coli. Nature. 2008;455(7217):1248–50. Epub 2008/10/31. doi: 10.1038/nature07282 18972020.
5. Cooper S, Helmstetter CE. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol. 1968;31(3):519–40. Epub 1968/02/14. doi: 10.1016/0022-2836(68)90425-7 4866337.
6. Donachie WD. Relationship between cell size and time of initiation of DNA replication. Nature. 1968;219(5158):1077–9. Epub 1968/09/07. doi: 10.1038/2191077a0 4876941.
7. Wold S, Skarstad K, Steen HB, Stokke T, Boye E. The initiation mass for DNA replication in Escherichia coli K-12 is dependent on growth rate. Embo J. 1994;13(9):2097–102. Epub 1994/05/01. 8187762; PubMed Central PMCID: PMC395061.
8. Zheng H, Ho PY, Jiang M, Tang B, Liu W, Li D, et al. Interrogating the Escherichia coli cell cycle by cell dimension perturbations. Proc Natl Acad Sci U S A. 2016;113(52):15000–5. Epub 2016/12/14. doi: 10.1073/pnas.1617932114 27956612; PubMed Central PMCID: PMCPMC5206551.
9. Amir A. Cell Size Regulation in Bacteria. Phys Rev Lett. 2014;112(20). Artn 208102 doi: 10.1103/Physrevlett.112.208102 ISI:000336914800011.
10. Wallden M, Fange D, Lundius EG, Baltekin O, Elf J. The Synchronization of Replication and Division Cycles in Individual E. coli Cells. Cell. 2016;166(3):729–39. Epub 2016/07/30. doi: 10.1016/j.cell.2016.06.052 27471967.
11. Bates D, Kleckner N. Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell. 2005;121(6):899–911. Epub 2005/06/18. doi: 10.1016/j.cell.2005.04.013 15960977; PubMed Central PMCID: PMC2973560.
12. Kleckner NE, Chatzi K, White MA, Fisher JK, Stouf M. Coordination of Growth, Chromosome Replication/Segregation, and Cell Division in E. coli. Front Microbiol. 2018;9:1469. Epub 2018/07/25. doi: 10.3389/fmicb.2018.01469 30038602; PubMed Central PMCID: PMCPMC6046412.
13. Si F, Le Treut G, Sauls JT, Vadia S, Levin PA, Jun S. Mechanistic Origin of Cell-Size Control and Homeostasis in Bacteria. Curr Biol. 2019;29(11):1760–70 e7. Epub 2019/05/21. doi: 10.1016/j.cub.2019.04.062 31104932; PubMed Central PMCID: PMCPMC6548602.
14. Micali G, Grilli J, Marchi J, Osella M, Cosentino Lagomarsino M. Dissecting the Control Mechanisms for DNA Replication and Cell Division in E. coli. Cell Rep. 2018;25(3):761–71 e4. Epub 2018/10/18. doi: 10.1016/j.celrep.2018.09.061 30332654.
15. Powell EO. Growth rate and generation time of bacteria, with special reference to continuous culture. J Gen Microbiol. 1956;15(3):492–511. Epub 1956/12/01. doi: 10.1099/00221287-15-3-492 13385433.
16. Kumar P, Yadav A, Fishov I, Feingold M. Z-ring Structure and Constriction Dynamics in E. coli. Front Microbiol. 2017;8:1670. Epub 2017/09/30. doi: 10.3389/fmicb.2017.01670 28959238; PubMed Central PMCID: PMCPMC5603902.
17. Bremer H, Churchward G. Control of cyclic chromosome replication in Escherichia coli. Microbiol Rev. 1991;55(3):459–75. Epub 1991/09/01. 1943997; PubMed Central PMCID: PMC372830.
18. Skovgaard O, Bak M, Lobner-Olesen A, Tommerup N. Genome-wide detection of chromosomal rearrangements, indels, and mutations in circular chromosomes by short read sequencing. Genome Res. 2011;21(8):1388–93. Epub 2011/05/11. doi: 10.1101/gr.117416.110 21555365; PubMed Central PMCID: PMC3149504.
19. Kogoma T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol Biol Rev. 1997;61(2):212–38. 9184011; PubMed Central PMCID: PMCPMC232608.
20. Rudolph CJ, Upton AL, Stockum A, Nieduszynski CA, Lloyd RG. Avoiding chromosome pathology when replication forks collide. Nature. 2013;500(7464):608–11. doi: 10.1038/nature12312 23892781; PubMed Central PMCID: PMCPMC3819906.
21. Wendel BM, Courcelle CT, Courcelle J. Completion of DNA replication in Escherichia coli. Proc Natl Acad Sci U S A. 2014;111(46):16454–9. doi: 10.1073/pnas.1415025111 25368150; PubMed Central PMCID: PMCPMC4246274.
22. Hendrickson H, Lawrence JG. Mutational bias suggests that replication termination occurs near the dif site, not at Ter sites. Mol Microbiol. 2007;64(1):42–56. doi: 10.1111/j.1365-2958.2007.05596.x 17376071.
23. White MA, Azeroglu B, Lopez-Vernaza MA, Hasan AMM, Leach DRF. RecBCD coordinates repair of two ends at a DNA double-strand break, preventing aberrant chromosome amplification. Nucleic Acids Res. 2018;46(13):6670–82. Epub 2018/06/15. doi: 10.1093/nar/gky463 29901759; PubMed Central PMCID: PMCPMC6061781.
24. Amarh V, White MA, Leach DRF. Dynamics of RecA-mediated repair of replication-dependent DNA breaks. J Cell Biol. 2018;217(7):2299–307. Epub 2018/05/24. doi: 10.1083/jcb.201803020 29789437; PubMed Central PMCID: PMCPMC6028544.
25. Hasan AMM, Azeroglu B, Leach DRF. Genomic Analysis of DNA Double-Strand Break Repair in Escherichia coli. Methods Enzymol. 2018;612:523–54. Epub 2018/12/07. doi: 10.1016/bs.mie.2018.09.001 30502957.
26. Cockram CA, Filatenkova M, Danos V, El Karoui M, Leach DR. Quantitative genomic analysis of RecA protein binding during DNA double-strand break repair reveals RecBCD action in vivo. Proc Natl Acad Sci U S A. 2015;112(34):E4735–42. doi: 10.1073/pnas.1424269112 26261330; PubMed Central PMCID: PMCPMC4553759.
27. Manwaring JD, Fuchs JA. Relationship between deoxyribonucleoside triphosphate pools and deoxyribonucleic acid synthesis in an nrdA mutant of Escherichia coli. J Bacteriol. 1979;138(1):245–8. Epub 1979/04/01. 374367; PubMed Central PMCID: PMC218263.
28. Morigen M, Flatten I, Skarstad K. The Escherichia coli datA site promotes proper regulation of cell division. Microbiology. 2014;160(Pt 4):703–10. doi: 10.1099/mic.0.074898-0 24574433.
29. Odsbu I, Morigen, Skarstad K. A reduction in ribonucleotide reductase activity slows down the chromosome replication fork but does not change its localization. PLoS One. 2009;4(10):e7617. Epub 2009/11/10. doi: 10.1371/journal.pone.0007617 19898675; PubMed Central PMCID: PMC2773459.
30. Herrick J, Sclavi B. Ribonucleotide reductase and the regulation of DNA replication: an old story and an ancient heritage. Mol Microbiol. 2007;63(1):22–34. Epub 2007/01/19. doi: 10.1111/j.1365-2958.2006.05493.x 17229208.
31. Azeroglu B, Mawer JS, Cockram CA, White MA, Hasan AM, Filatenkova M, et al. RecG Directs DNA Synthesis during Double-Strand Break Repair. PLoS Genet. 2016;12(2):e1005799. doi: 10.1371/journal.pgen.1005799 26872352; PubMed Central PMCID: PMCPMC4752480.
32. Stouf M, Meile JC, Cornet F. FtsK actively segregates sister chromosomes in Escherichia coli. Proc Natl Acad Sci U S A. 2013;110(27):11157–62. Epub 2013/06/20. doi: 10.1073/pnas.1304080110 23781109; PubMed Central PMCID: PMCPMC3704039.
33. Fisher JK, Bourniquel A, Witz G, Weiner B, Prentiss M, Kleckner N. Four-dimensional imaging of E. coli nucleoid organization and dynamics in living cells. Cell. 2013;153(4):882–95. Epub 2013/04/30. doi: 10.1016/j.cell.2013.04.006 23623305; PubMed Central PMCID: PMCPMC3670778.
34. Kleckner N, Fisher JK, Stouf M, White MA, Bates D, Witz G. The bacterial nucleoid: nature, dynamics and sister segregation. Curr Opin Microbiol. 2014;22:127–37. Epub 2014/12/03. doi: 10.1016/j.mib.2014.10.001 25460806; PubMed Central PMCID: PMCPMC4359759.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2020 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Dynamic and regulated TAF gene expression during mouse embryonic germ cell development
- Autophagy gene haploinsufficiency drives chromosome instability, increases migration, and promotes early ovarian tumors
- Genomic profiling of human vascular cells identifies TWIST1 as a causal gene for common vascular diseases
- Ligand dependent gene regulation by transient ERα clustered enhancers