Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication

John Atkinson, Milind Kumar Gupta, Christian J. Rudolph, Hazel Bell, Robert G. Lloyd, Peter McGlynn

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Genome duplication requires accessory helicases to displace proteins ahead of advancing replication forks. E. coli contains three helicases, Rep, UvrD and DinG, that might promote replication of protein-bound DNA. One of these helicases, Rep, also interacts with the replicative helicase DnaB. We demonstrate that Rep is the only putative accessory helicase whose absence results in an increased chromosome duplication time. We show also that the interaction between Rep and DnaB is required for Rep to maintain rapid genome duplication. Furthermore, this Rep-DnaB interaction is critical in minimising the need for both recombinational processing of blocked replication forks and replisome reassembly, indicating that colocalisation of Rep and DnaB minimises stalling and subsequent inactivation of replication forks. These data indicate that E. coli contains only one helicase that acts as an accessory motor at the fork in wild type cells, that such an activity is critical for the maintenance of rapid genome duplication and that colocalisation with the replisome is crucial for this function. Given that the only other characterised accessory motor, S. cerevisiae Rrm3p, physically associates with the replisome, our demonstration of the functional importance of such an association indicates that colocalisation may be a conserved feature of accessory replicative motors.
Original languageEnglish
Pages (from-to)949-957
Number of pages9
JournalNucleic Acids Research
Volume39
Issue number3
Early online date4 Oct 2010
DOIs
Publication statusPublished - Feb 2011

Fingerprint

Genome
DnaB Helicases
Chromosome Duplication
Escherichia coli
Saccharomyces cerevisiae
Proteins
Maintenance
DNA

Cite this

Atkinson, J., Gupta, M. K., Rudolph, C. J., Bell, H., Lloyd, R. G., & McGlynn, P. (2011). Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication. Nucleic Acids Research, 39(3), 949-957. https://doi.org/10.1093/nar/gkq889

Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication. / Atkinson, John; Gupta, Milind Kumar; Rudolph, Christian J.; Bell, Hazel; Lloyd, Robert G.; McGlynn, Peter.

In: Nucleic Acids Research, Vol. 39, No. 3, 02.2011, p. 949-957.

Research output: Contribution to journalArticle

Atkinson, J, Gupta, MK, Rudolph, CJ, Bell, H, Lloyd, RG & McGlynn, P 2011, 'Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication', Nucleic Acids Research, vol. 39, no. 3, pp. 949-957. https://doi.org/10.1093/nar/gkq889
Atkinson, John ; Gupta, Milind Kumar ; Rudolph, Christian J. ; Bell, Hazel ; Lloyd, Robert G. ; McGlynn, Peter. / Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication. In: Nucleic Acids Research. 2011 ; Vol. 39, No. 3. pp. 949-957.
@article{c019f6c24e5741dfb88433831cef9f9e,
title = "Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication",
abstract = "Genome duplication requires accessory helicases to displace proteins ahead of advancing replication forks. E. coli contains three helicases, Rep, UvrD and DinG, that might promote replication of protein-bound DNA. One of these helicases, Rep, also interacts with the replicative helicase DnaB. We demonstrate that Rep is the only putative accessory helicase whose absence results in an increased chromosome duplication time. We show also that the interaction between Rep and DnaB is required for Rep to maintain rapid genome duplication. Furthermore, this Rep-DnaB interaction is critical in minimising the need for both recombinational processing of blocked replication forks and replisome reassembly, indicating that colocalisation of Rep and DnaB minimises stalling and subsequent inactivation of replication forks. These data indicate that E. coli contains only one helicase that acts as an accessory motor at the fork in wild type cells, that such an activity is critical for the maintenance of rapid genome duplication and that colocalisation with the replisome is crucial for this function. Given that the only other characterised accessory motor, S. cerevisiae Rrm3p, physically associates with the replisome, our demonstration of the functional importance of such an association indicates that colocalisation may be a conserved feature of accessory replicative motors.",
author = "John Atkinson and Gupta, {Milind Kumar} and Rudolph, {Christian J.} and Hazel Bell and Lloyd, {Robert G.} and Peter McGlynn",
year = "2011",
month = "2",
doi = "10.1093/nar/gkq889",
language = "English",
volume = "39",
pages = "949--957",
journal = "Nucleic Acids Research",
issn = "0305-1048",
publisher = "Oxford University Press",
number = "3",

}

TY - JOUR

T1 - Localization of an accessory helicase at the replisome is critical in sustaining efficient genome duplication

AU - Atkinson, John

AU - Gupta, Milind Kumar

AU - Rudolph, Christian J.

AU - Bell, Hazel

AU - Lloyd, Robert G.

AU - McGlynn, Peter

PY - 2011/2

Y1 - 2011/2

N2 - Genome duplication requires accessory helicases to displace proteins ahead of advancing replication forks. E. coli contains three helicases, Rep, UvrD and DinG, that might promote replication of protein-bound DNA. One of these helicases, Rep, also interacts with the replicative helicase DnaB. We demonstrate that Rep is the only putative accessory helicase whose absence results in an increased chromosome duplication time. We show also that the interaction between Rep and DnaB is required for Rep to maintain rapid genome duplication. Furthermore, this Rep-DnaB interaction is critical in minimising the need for both recombinational processing of blocked replication forks and replisome reassembly, indicating that colocalisation of Rep and DnaB minimises stalling and subsequent inactivation of replication forks. These data indicate that E. coli contains only one helicase that acts as an accessory motor at the fork in wild type cells, that such an activity is critical for the maintenance of rapid genome duplication and that colocalisation with the replisome is crucial for this function. Given that the only other characterised accessory motor, S. cerevisiae Rrm3p, physically associates with the replisome, our demonstration of the functional importance of such an association indicates that colocalisation may be a conserved feature of accessory replicative motors.

AB - Genome duplication requires accessory helicases to displace proteins ahead of advancing replication forks. E. coli contains three helicases, Rep, UvrD and DinG, that might promote replication of protein-bound DNA. One of these helicases, Rep, also interacts with the replicative helicase DnaB. We demonstrate that Rep is the only putative accessory helicase whose absence results in an increased chromosome duplication time. We show also that the interaction between Rep and DnaB is required for Rep to maintain rapid genome duplication. Furthermore, this Rep-DnaB interaction is critical in minimising the need for both recombinational processing of blocked replication forks and replisome reassembly, indicating that colocalisation of Rep and DnaB minimises stalling and subsequent inactivation of replication forks. These data indicate that E. coli contains only one helicase that acts as an accessory motor at the fork in wild type cells, that such an activity is critical for the maintenance of rapid genome duplication and that colocalisation with the replisome is crucial for this function. Given that the only other characterised accessory motor, S. cerevisiae Rrm3p, physically associates with the replisome, our demonstration of the functional importance of such an association indicates that colocalisation may be a conserved feature of accessory replicative motors.

U2 - 10.1093/nar/gkq889

DO - 10.1093/nar/gkq889

M3 - Article

VL - 39

SP - 949

EP - 957

JO - Nucleic Acids Research

JF - Nucleic Acids Research

SN - 0305-1048

IS - 3

ER -