Global analysis of double-strand break processing reveals in vivo properties of the helicase-nuclease complex AddAB

In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of DNA ends by a helicase-nuclease complex such as AddAB. The activity of AddAB has been well-studied in vitro, with translocation speeds between...

Full description

Saved in:
Bibliographic Details
Published inPLoS genetics Vol. 13; no. 5; p. e1006783
Main Authors Badrinarayanan, Anjana, Le, Tung B. K., Spille, Jan-Hendrik, Cisse, Ibrahim I., Laub, Michael T.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 10.05.2017
Public Library of Science (PLoS)
Subjects
Online AccessGet full text
ISSN1553-7404
1553-7390
1553-7404
DOI10.1371/journal.pgen.1006783

Cover

Abstract In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of DNA ends by a helicase-nuclease complex such as AddAB. The activity of AddAB has been well-studied in vitro, with translocation speeds between 400-2000 bp/s on linear DNA suggesting that a large section of DNA around a break site is processed for repair. However, the translocation rate and activity of AddAB in vivo is not known, and how AddAB is regulated to prevent excessive DNA degradation around a break site is unclear. To examine the functions and mechanistic regulation of AddAB inside bacterial cells, we developed a next-generation sequencing-based approach to assay DNA processing after a site-specific DSB was introduced on the chromosome of Caulobacter crescentus. Using this assay we determined the in vivo rates of DSB processing by AddAB and found that putative chi sites attenuate processing in a RecA-dependent manner. This RecA-mediated regulation of AddAB prevents the excessive loss of DNA around a break site, limiting the effects of DSB processing on transcription. In sum, our results, taken together with prior studies, support a mechanism for regulating AddAB that couples two key events of DSB repair-the attenuation of DNA-end processing and the initiation of homology search by RecA-thereby helping to ensure that genomic integrity is maintained during DSB repair.
AbstractList In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of DNA ends by a helicase-nuclease complex such as AddAB. The activity of AddAB has been well-studied in vitro, with translocation speeds between 400-2000 bp/s on linear DNA suggesting that a large section of DNA around a break site is processed for repair. However, the translocation rate and activity of AddAB in vivo is not known, and how AddAB is regulated to prevent excessive DNA degradation around a break site is unclear. To examine the functions and mechanistic regulation of AddAB inside bacterial cells, we developed a next-generation sequencing-based approach to assay DNA processing after a site-specific DSB was introduced on the chromosome of Caulobacter crescentus. Using this assay we determined the in vivo rates of DSB processing by AddAB and found that putative chi sites attenuate processing in a RecA-dependent manner. This RecA-mediated regulation of AddAB prevents the excessive loss of DNA around a break site, limiting the effects of DSB processing on transcription. In sum, our results, taken together with prior studies, support a mechanism for regulating AddAB that couples two key events of DSB repair-the attenuation of DNA-end processing and the initiation of homology search by RecA-thereby helping to ensure that genomic integrity is maintained during DSB repair.
In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of DNA ends by a helicase-nuclease complex such as AddAB. The activity of AddAB has been well-studied in vitro, with translocation speeds between 400-2000 bp/s on linear DNA suggesting that a large section of DNA around a break site is processed for repair. However, the translocation rate and activity of AddAB in vivo is not known, and how AddAB is regulated to prevent excessive DNA degradation around a break site is unclear. To examine the functions and mechanistic regulation of AddAB inside bacterial cells, we developed a next-generation sequencing-based approach to assay DNA processing after a site-specific DSB was introduced on the chromosome of Caulobacter crescentus. Using this assay we determined the in vivo rates of DSB processing by AddAB and found that putative chi sites attenuate processing in a RecA-dependent manner. This RecA-mediated regulation of AddAB prevents the excessive loss of DNA around a break site, limiting the effects of DSB processing on transcription. In sum, our results, taken together with prior studies, support a mechanism for regulating AddAB that couples two key events of DSB repair-the attenuation of DNA-end processing and the initiation of homology search by RecA-thereby helping to ensure that genomic integrity is maintained during DSB repair.In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of DNA ends by a helicase-nuclease complex such as AddAB. The activity of AddAB has been well-studied in vitro, with translocation speeds between 400-2000 bp/s on linear DNA suggesting that a large section of DNA around a break site is processed for repair. However, the translocation rate and activity of AddAB in vivo is not known, and how AddAB is regulated to prevent excessive DNA degradation around a break site is unclear. To examine the functions and mechanistic regulation of AddAB inside bacterial cells, we developed a next-generation sequencing-based approach to assay DNA processing after a site-specific DSB was introduced on the chromosome of Caulobacter crescentus. Using this assay we determined the in vivo rates of DSB processing by AddAB and found that putative chi sites attenuate processing in a RecA-dependent manner. This RecA-mediated regulation of AddAB prevents the excessive loss of DNA around a break site, limiting the effects of DSB processing on transcription. In sum, our results, taken together with prior studies, support a mechanism for regulating AddAB that couples two key events of DSB repair-the attenuation of DNA-end processing and the initiation of homology search by RecA-thereby helping to ensure that genomic integrity is maintained during DSB repair.
In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of DNA ends by a helicase-nuclease complex such as AddAB. The activity of AddAB has been well-studied in vitro , with translocation speeds between 400–2000 bp/s on linear DNA suggesting that a large section of DNA around a break site is processed for repair. However, the translocation rate and activity of AddAB in vivo is not known, and how AddAB is regulated to prevent excessive DNA degradation around a break site is unclear. To examine the functions and mechanistic regulation of AddAB inside bacterial cells, we developed a next-generation sequencing-based approach to assay DNA processing after a site-specific DSB was introduced on the chromosome of Caulobacter crescentus . Using this assay we determined the in vivo rates of DSB processing by AddAB and found that putative chi sites attenuate processing in a RecA-dependent manner. This RecA-mediated regulation of AddAB prevents the excessive loss of DNA around a break site, limiting the effects of DSB processing on transcription. In sum, our results, taken together with prior studies, support a mechanism for regulating AddAB that couples two key events of DSB repair–the attenuation of DNA-end processing and the initiation of homology search by RecA–thereby helping to ensure that genomic integrity is maintained during DSB repair. Double-strand breaks (DSBs) are a threat to genome integrity and are faithfully repaired via homologous recombination. The initial processing of DSB ends that prepares them for recombination has been well-studied in vitro , but is less well characterized in vivo . We describe a deep sequencing-based assay for assessing the early steps of DSB processing in bacterial cells by the helicase-nuclease complex AddAB. We find that a combination of chi site recognition and RecA loading is required to attenuate AddAB activity. In the absence of RecA, the chromosome is excessively degraded with a concomitant loss in transcription. Our results, along with prior studies, support a model for how chi recognition and RecA together regulate AddAB to maintain genome integrity and facilitate recombination.
Audience Academic
Author Laub, Michael T.
Badrinarayanan, Anjana
Spille, Jan-Hendrik
Le, Tung B. K.
Cisse, Ibrahim I.
AuthorAffiliation 4 Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, United States of America
5 Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA, United States of America
3 Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
2 National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research, Bangalore, India
1 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, United States of America
National Cancer Institute, UNITED STATES
AuthorAffiliation_xml – name: 1 Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, United States of America
– name: 4 Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, United States of America
– name: 3 Department of Molecular Microbiology, John Innes Centre, Norwich, United Kingdom
– name: 5 Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA, United States of America
– name: 2 National Centre for Biological Sciences (NCBS), Tata Institute of Fundamental Research, Bangalore, India
– name: National Cancer Institute, UNITED STATES
Author_xml – sequence: 1
  givenname: Anjana
  surname: Badrinarayanan
  fullname: Badrinarayanan, Anjana
– sequence: 2
  givenname: Tung B. K.
  orcidid: 0000-0003-4764-8851
  surname: Le
  fullname: Le, Tung B. K.
– sequence: 3
  givenname: Jan-Hendrik
  orcidid: 0000-0001-8493-4721
  surname: Spille
  fullname: Spille, Jan-Hendrik
– sequence: 4
  givenname: Ibrahim I.
  surname: Cisse
  fullname: Cisse, Ibrahim I.
– sequence: 5
  givenname: Michael T.
  orcidid: 0000-0002-8288-7607
  surname: Laub
  fullname: Laub, Michael T.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28489851$$D View this record in MEDLINE/PubMed
BookMark eNqVk11v0zAUhiM0xD7gHyCIhITgosWOk9jZBVKZYFSamMTXreU4x62La4c4qbZ_z-naTe00IVAuYvk873t8jn2OkwMfPCTJc0rGlHH6bhGGzis3bmfgx5SQkgv2KDmiRcFGPCf5wc76MDmOcUEIK0TFnySHmchFJQp6lMRzF2rlUoVW19HGNJi0CUPtYBT7TvkmrTtQv9K2CxpitH6WdrAC5WJqfbqyq7AOtdD1Fm7E_RzSOTirVYSRH7QDXKQ6LFsHV-mkaSYfniaPDRrAs-3_JPnx6eP3s8-ji8vz6dnkYqR5VvYjkTPVlEXOK1HVteZKNxUpTUkySjGiS1OwEnhFjVHaEJYLgm3gDa254MQYdpK83Pi2LkS57VeUtKIkL1lJCiSmG6IJaiHbzi5Vdy2DsvJmI3QzqbAyLELWwoiirIqsVlkuNKszASajXFGWGVEq9Hq_zTbUS2g0eOyf2zPdj3g7l7OwkkWeM6wEDd5sDbrwe4DYy6WNGpxTHsKA58a7E6TIqjX66h76cHVbaqawAOtNwLx6bSonecU4Y0xUSI0foPBrYGk1vjljcX9P8HZPgEwPV_1MDTHK6bev_8F--Xf28uc--3qHneN77OcxuKG3wcd98MXurdxdx-0EIJBvAN2FGDswdwglcj1ot62V60GT20FD2ek9mba9WqfH7ln3d_Efsa0t2Q
CitedBy_id crossref_primary_10_1371_journal_pbio_3002540
crossref_primary_10_1093_nar_gkad1198
crossref_primary_10_1093_nar_gky1132
crossref_primary_10_1002_2211_5463_13292
crossref_primary_10_1016_j_dnarep_2022_103389
crossref_primary_10_1091_mbc_E20_08_0547
crossref_primary_10_1007_s00253_020_10589_w
crossref_primary_10_1128_jb_00571_21
crossref_primary_10_1073_pnas_2209304119
crossref_primary_10_1093_nar_gkx1290
Cites_doi 10.1016/S0092-8674(00)80315-3
10.1111/j.1365-2958.2006.05346.x
10.1371/journal.pgen.1002244
10.1128/JB.100.1.231-239.1969
10.1093/nar/gku188
10.1016/j.molcel.2013.10.014
10.1006/jmbi.2000.3556
10.1128/jb.179.3.880-888.1997
10.1073/pnas.1424269112
10.1128/JB.00330-06
10.1093/bioinformatics/btq033
10.1016/j.dnarep.2014.02.002
10.1128/MMBR.58.3.401-465.1994
10.1128/JB.01877-07
10.4161/15384101.2014.950892
10.1016/j.molcel.2011.04.012
10.1073/pnas.81.24.7850
10.1093/genetics/115.1.11
10.1128/jb.175.17.5505-5509.1993
10.1016/j.molcel.2006.04.027
10.1038/nrmicro2917
10.1101/gad.2038911
10.1128/jb.176.16.5093-5100.1994
10.1016/S0021-9258(19)69000-9
10.1128/MMBR.05026-11
10.1038/nature13037
10.1128/MMBR.00020-08
10.1111/j.1574-6976.2007.00082.x
10.1016/j.dnarep.2009.12.016
10.1093/nar/gkv1543
10.1099/00221287-147-4-949
10.1111/j.1365-2958.1993.tb01182.x
10.1016/0022-2836(85)90414-0
10.1111/j.1365-2958.2003.03970.x
10.1186/gb-2009-10-3-r25
10.1046/j.1365-2958.1997.1991570.x
10.1371/journal.pgen.1002622
10.1074/jbc.270.27.16360
10.1016/j.cell.2006.05.038
10.1038/nature10782
10.1002/j.1460-2075.1994.tb06570.x
10.1111/j.1432-1033.1980.tb04480.x
10.1038/emboj.2012.9
10.1016/S0092-8674(03)00681-0
10.1128/JB.01052-07
10.1016/0092-8674(81)90333-0
10.1046/j.1365-2958.1998.01018.x
10.1093/nar/18.6.1407
10.1073/pnas.89.24.12073
10.1016/S0923-2508(99)00132-1
10.1016/j.molcel.2015.09.009
10.1128/jb.179.4.1219-1229.1997
10.1073/pnas.1415025111
10.1016/j.dnarep.2012.12.005
10.1186/1471-2180-7-17
10.1111/j.1365-2958.2008.06130.x
10.1080/10409230390242489
10.1016/j.cell.2007.09.023
10.1016/j.jmb.2014.07.017
10.1073/pnas.92.14.6249
10.1073/pnas.1303035110
10.1093/nar/gkq1124
10.1016/j.molcel.2006.01.007
10.1093/nar/gkm818
10.1093/nar/16.14.6883
10.1083/jcb.201505019
10.1128/JB.181.19.6220-6221.1999
10.1073/pnas.95.10.5752
10.1038/nature12868
10.1101/cshperspect.a016436
10.1371/journal.pbio.1001977
10.7554/eLife.08942
ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: properties of the helicase-nuclease complex AddAB. PLoS Genet 13(5): e1006783. https://doi.org/10.1371/journal.pgen.1006783
2017 Badrinarayanan et al 2017 Badrinarayanan et al
2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: properties of the helicase-nuclease complex AddAB. PLoS Genet 13(5): e1006783. https://doi.org/10.1371/journal.pgen.1006783
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: properties of the helicase-nuclease complex AddAB. PLoS Genet 13(5): e1006783. https://doi.org/10.1371/journal.pgen.1006783
– notice: 2017 Badrinarayanan et al 2017 Badrinarayanan et al
– notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: properties of the helicase-nuclease complex AddAB. PLoS Genet 13(5): e1006783. https://doi.org/10.1371/journal.pgen.1006783
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
IOV
ISN
ISR
3V.
7QP
7QR
7SS
7TK
7TM
7TO
7X7
7XB
88E
8FD
8FE
8FH
8FI
8FJ
8FK
ABUWG
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
CCPQU
DWQXO
FR3
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7P
P64
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
RC3
7X8
5PM
DOA
DOI 10.1371/journal.pgen.1006783
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Gale In Context: Opposing Viewpoints
Gale In Context: Canada
Gale In Context: Science
ProQuest Central (Corporate)
Calcium & Calcified Tissue Abstracts
Chemoreception Abstracts
Entomology Abstracts (Full archive)
Neurosciences Abstracts
Nucleic Acids Abstracts
Oncogenes and Growth Factors Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Technology Research Database
ProQuest SciTech Collection
ProQuest Natural Science Journals
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central Essentials - QC
Biological Science Collection
ProQuest Central
Natural Science Collection
ProQuest One Community College
ProQuest Central Korea
Engineering Research Database
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
ProQuest Health & Medical Collection
Medical Database (ProQuest)
Biological Science Database
Biotechnology and BioEngineering Abstracts
Proquest Central Premium
ProQuest One Academic (New)
ProQuest Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
Genetics Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
Oncogenes and Growth Factors Abstracts
Technology Research Database
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
Nucleic Acids Abstracts
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central China
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest Health & Medical Research Collection
Genetics Abstracts
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Health & Medical Research Collection
Biological Science Collection
AIDS and Cancer Research Abstracts
Chemoreception Abstracts
ProQuest Central (New)
ProQuest Medical Library (Alumni)
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
Neurosciences Abstracts
ProQuest Hospital Collection (Alumni)
Biotechnology and BioEngineering Abstracts
Entomology Abstracts
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
Engineering Research Database
ProQuest One Academic
Calcium & Calcified Tissue Abstracts
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList Publicly Available Content Database
MEDLINE - Academic


MEDLINE



Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central
  url: http://www.proquest.com/pqcentral?accountid=15518
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate Global analysis of double-strand break processing in vivo
EISSN 1553-7404
ExternalDocumentID 1910463605
oai_doaj_org_article_b8f856952ba248c3b28ef217a132f86a
PMC5443536
A493733389
28489851
10_1371_journal_pgen_1006783
Genre Journal Article
GeographicLocations United States--US
GeographicLocations_xml – name: United States--US
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: R01 GM082899
– fundername: ;
– fundername: ;
  grantid: 5R01GM082899
– fundername: ;
  grantid: 2654055
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8FE
8FH
8FI
8FJ
AAFWJ
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACGFO
ACIHN
ACIWK
ACPRK
ACUHS
ADBBV
ADRAZ
AEAQA
AENEX
AFKRA
AFPKN
AHMBA
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AOIJS
B0M
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EAP
EAS
EBD
EBS
EJD
EMK
EMOBN
ESX
F5P
FPL
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IGS
IHR
IHW
INH
INR
IOV
ISN
ISR
ITC
KQ8
LK8
M1P
M48
M7P
O5R
O5S
OK1
OVT
P2P
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
PV9
QF4
QN7
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
WOW
XSB
~8M
C1A
CGR
CUY
CVF
ECM
EIF
H13
IPNFZ
NPM
PJZUB
PPXIY
PQGLB
RIG
WOQ
PMFND
3V.
7QP
7QR
7SS
7TK
7TM
7TO
7XB
8FD
8FK
AZQEC
DWQXO
FR3
GNUQQ
H94
K9.
P64
PKEHL
PQEST
PQUKI
PRINS
RC3
7X8
PUEGO
5PM
AAPBV
ABPTK
M~E
UMP
ID FETCH-LOGICAL-c726t-843ad6547989bbc7acd906f602113adc6f536e791ffacf034801007d1b7870ff3
IEDL.DBID M48
ISSN 1553-7404
1553-7390
IngestDate Sun May 07 16:29:04 EDT 2023
Wed Aug 27 01:27:09 EDT 2025
Thu Aug 21 14:36:15 EDT 2025
Fri Sep 05 00:07:44 EDT 2025
Fri Jul 25 12:21:52 EDT 2025
Tue Jun 17 21:46:59 EDT 2025
Tue Jun 10 20:36:46 EDT 2025
Fri Jun 27 04:10:11 EDT 2025
Fri Jun 27 04:17:00 EDT 2025
Fri Jun 27 03:32:16 EDT 2025
Thu May 22 21:19:23 EDT 2025
Mon Jul 21 06:05:06 EDT 2025
Thu Apr 24 22:59:41 EDT 2025
Tue Jul 01 03:55:37 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 5
Language English
License This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c726t-843ad6547989bbc7acd906f602113adc6f536e791ffacf034801007d1b7870ff3
Notes new_version
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
Conceptualization: AB MTL.Data curation: AB TBKL JHS.Formal analysis: AB TBKL JHS MTL.Funding acquisition: AB TBKL IIC MTL.Investigation: AB TBKL JHS.Methodology: AB TBKL JHS IIC MTL.Project administration: MTL.Resources: AB TBKL JHS.Software: JHS.Supervision: MTL.Validation: AB TBKL JHS IIC MTL.Visualization: AB TBKL MTL.Writing – original draft: AB MTL.Writing – review & editing: AB TBKL MTL.
The authors have declared that no competing interests exist.
ORCID 0000-0003-4764-8851
0000-0002-8288-7607
0000-0001-8493-4721
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.1371/journal.pgen.1006783
PMID 28489851
PQID 1910463605
PQPubID 1436339
ParticipantIDs plos_journals_1910463605
doaj_primary_oai_doaj_org_article_b8f856952ba248c3b28ef217a132f86a
pubmedcentral_primary_oai_pubmedcentral_nih_gov_5443536
proquest_miscellaneous_1897805296
proquest_journals_1910463605
gale_infotracmisc_A493733389
gale_infotracacademiconefile_A493733389
gale_incontextgauss_ISR_A493733389
gale_incontextgauss_ISN_A493733389
gale_incontextgauss_IOV_A493733389
gale_healthsolutions_A493733389
pubmed_primary_28489851
crossref_primary_10_1371_journal_pgen_1006783
crossref_citationtrail_10_1371_journal_pgen_1006783
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 20170510
PublicationDateYYYYMMDD 2017-05-10
PublicationDate_xml – month: 5
  year: 2017
  text: 20170510
  day: 10
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS genetics
PublicationTitleAlternate PLoS Genet
PublicationYear 2017
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References A Kuzminov (ref26) 1997; 179
A Köppen (ref58) 1995; 92
J Kooistra (ref28) 1993; 7
M Martins-Pinheiro (ref38) 2007; 7
CA Cockram (ref36) 2015; 112
DA McGrew (ref50) 2003; 38
AL Forget (ref55) 2012; 482
JTP Yeeles (ref23) 2011; 39
JW Modell (ref45) 2011; 25
F Chédin (ref18) 2000; 298
TR Meddows (ref32) 2004; 52
HJ Nielsen (ref53) 2006; 62
JC Alonso (ref1) 2013; 12
C Carrasco (ref15) 2014; 20
DA Dixon (ref10) 1995; 270
M Seigneur (ref66) 1999; 181
F Chédin (ref29) 1998; 29
WW Krajewski (ref14) 2014; 508
M Thanbichler (ref52) 2006; 126
JW Modell (ref46) 2014; 12
AF Taylor (ref9) 2014; 426
P Dabert (ref56) 1992; 89
JG Williams (ref60) 1981; 256
K Zahradka (ref61) 2009; 191
A Badrinarayanan (ref37) 2015; 210
B Thoms (ref63) 2008; 190
M Rajendram (ref67) 2015; 60
DG Ennis (ref57) 1987; 115
JTP Yeeles (ref24) 2011; 42
M Spies (ref20) 2006; 21
LS Symington (ref3) 2014; 6
M Wilkinson (ref5) 2014; 13
MS Dillingham (ref8) 2008; 72
N Renzette (ref49) 2008; 67
A Prell (ref64) 1980; 105
KE McGinness (ref68) 2006; 22
SC Kowalczykowski (ref2) 1994; 58
RB Jensen (ref43) 2006; 188
DB Wigley (ref4) 2013; 11
NS Gilhooly (ref16) 2014; 42
G Karimova (ref47) 1998; 95
B Langmead (ref71) 2009; 10
BM Wendel (ref35) 2014; 111
J Kooistra (ref30) 1997; 23
M Thanbichler (ref40) 2007; 35
KD Vernick (ref70) 1988; 16
C Monteilhet (ref34) 1990; 18
M Spies (ref13) 2003; 114
GR Smith (ref11) 1981; 24
I Erill (ref44) 2007; 31
M Spies (ref7) 2007; 131
AM Chaudhury (ref12) 1984; 81
ALD Septenville (ref33) 2012; 8
K Saikrishnan (ref19) 2012; 31
SE Jones (ref41) 2001; 147
DG Anderson (ref21) 1997; 90
NS Gilhooly (ref39) 2016; 44
M El Karoui (ref42) 1999; 150
GR Smith (ref6) 2012; 76
C Carrasco (ref22) 2013; 110
R Meima (ref27) 1997; 179
MM Zaman (ref62) 1994; 176
AR Quinlan (ref72) 2010; 26
K Skarstad (ref59) 1993; 175
JTP Yeeles (ref17) 2010; 9
NS Willetts (ref31) 1969; 100
AK Adikesavan (ref51) 2011; 7
CD Aakre (ref69) 2013; 52
N Manfrini (ref54) 2015; 4
A Kuzminov (ref25) 1994; 13
C Lesterlin (ref48) 2014; 506
AF Taylor (ref65) 1985; 185
16885470 - J Bacteriol. 2006 Aug;188(16):6016-9
21700225 - Mol Cell. 2011 Jun 24;42(6):806-16
17965170 - J Bacteriol. 2008 Jan;190(1):179-92
9230304 - Cell. 1997 Jul 11;90(1):77-86
9781875 - Mol Microbiol. 1998 Sep;29(6):1369-77
7541534 - Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6249-53
7608206 - J Biol Chem. 1995 Jul 7;270(27):16360-70
17959646 - Nucleic Acids Res. 2007;35(20):e137
9576956 - Proc Natl Acad Sci U S A. 1998 May 12;95(10):5752-6
26231041 - Elife. 2015 Jul 31;4:null
10672998 - Res Microbiol. 1999 Nov-Dec;150(9-10):579-87
22688812 - Microbiol Mol Biol Rev. 2012 Jun;76(2):217-28
13678587 - Cell. 2003 Sep 5;114(5):647-54
21685367 - Genes Dev. 2011 Jun 15;25(12):1328-43
20116346 - DNA Repair (Amst). 2010 Mar 2;9(3):276-85
2951295 - Genetics. 1987 Jan;115(1):11-24
25486468 - Cell Cycle. 2014;13(18):2812-20
15049815 - Mol Microbiol. 2004 Apr;52(1):119-32
8026461 - EMBO J. 1994 Jun 15;13(12):2764-76
26481664 - Mol Cell. 2015 Nov 5;60(3):374-84
22318518 - Nature. 2012 Feb 08;482(7385):423-7
17883408 - FEMS Microbiol Rev. 2007 Nov;31(6):637-56
24670664 - Nature. 2014 Apr 17;508(7496):416-9
25350732 - PLoS Biol. 2014 Oct 28;12(10):e1001977
6245875 - Eur J Biochem. 1980 Mar;105(1):109-16
19074388 - J Bacteriol. 2009 Mar;191(5):1677-87
6265452 - J Biol Chem. 1981 Jul 25;256(14):7573-82
24239291 - Mol Cell. 2013 Dec 12;52(5):617-28
7968921 - Microbiol Rev. 1994 Sep;58(3):401-65
4898990 - J Bacteriol. 1969 Oct;100(1):231-9
20110278 - Bioinformatics. 2010 Mar 15;26(6):841-2
25073102 - J Mol Biol. 2014 Oct 23;426(21):3479-99
16839883 - Cell. 2006 Jul 14;126(1):147-62
2841646 - Nucleic Acids Res. 1988 Jul 25;16(14B):6883-96
26762979 - Nucleic Acids Res. 2016 Apr 7;44(6):2727-41
9004227 - Mol Microbiol. 1997 Jan;23(1):137-49
9023205 - J Bacteriol. 1997 Feb;179(4):1219-29
2997450 - J Mol Biol. 1985 Sep 20;185(2):431-43
10498743 - J Bacteriol. 1999 Oct;181(19):6220-1
9006046 - J Bacteriol. 1997 Feb;179(3):880-8
1465442 - Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12073-7
8366035 - J Bacteriol. 1993 Sep;175(17):5505-9
8387145 - Mol Microbiol. 1993 Mar;7(6):915-23
16762842 - Mol Cell. 2006 Jun 9;22(5):701-7
17352799 - BMC Microbiol. 2007 Mar 12;7:17
8051022 - J Bacteriol. 1994 Aug;176(16):5093-100
10756102 - J Mol Biol. 2000 Apr 21;298(1):7-20
26261330 - Proc Natl Acad Sci U S A. 2015 Aug 25;112(34):E4735-42
14693725 - Crit Rev Biochem Mol Biol. 2003;38(5):385-432
24362571 - Nature. 2014 Feb 13;506(7487):249-53
21071401 - Nucleic Acids Res. 2011 Mar;39(6):2271-85
23380520 - DNA Repair (Amst). 2013 Mar 1;12(3):162-76
6453653 - Cell. 1981 May;24(2):429-36
6393130 - Proc Natl Acad Sci U S A. 1984 Dec;81(24):7850-4
24569169 - DNA Repair (Amst). 2014 Aug;20:119-29
22307084 - EMBO J. 2012 Mar 21;31(6):1568-78
17020576 - Mol Microbiol. 2006 Oct;62(2):331-8
23202527 - Nat Rev Microbiol. 2013 Jan;11(1):9-13
19052323 - Microbiol Mol Biol Rev. 2008 Dec;72(4):642-71, Table of Contents
19261174 - Genome Biol. 2009;10(3):R25
23798400 - Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):E2562-71
25085909 - Cold Spring Harb Perspect Biol. 2014 Aug 01;6(8):null
24682829 - Nucleic Acids Res. 2014 May;42(9):5633-43
25368150 - Proc Natl Acad Sci U S A. 2014 Nov 18;111(46):16454-9
11283290 - Microbiology. 2001 Apr;147(Pt 4):949-58
18022364 - Cell. 2007 Nov 16;131(4):694-705
16483938 - Mol Cell. 2006 Feb 17;21(4):573-80
2183191 - Nucleic Acids Res. 1990 Mar 25;18(6):1407-13
18298444 - Mol Microbiol. 2008 Mar;67(6):1347-59
22496668 - PLoS Genet. 2012;8(4):e1002622
21912525 - PLoS Genet. 2011 Sep;7(9):e1002244
26240183 - J Cell Biol. 2015 Aug 3;210(3):385-400
References_xml – volume: 90
  start-page: 77
  year: 1997
  ident: ref21
  article-title: The translocating RecBCD enzyme stimulates recombination by directing RecA protein onto ssDNA in a χ-regulated manner
  publication-title: Cell
  doi: 10.1016/S0092-8674(00)80315-3
– volume: 62
  start-page: 331
  year: 2006
  ident: ref53
  article-title: The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves
  publication-title: Mol Microbiol
  doi: 10.1111/j.1365-2958.2006.05346.x
– volume: 7
  start-page: e1002244
  year: 2011
  ident: ref51
  article-title: Separation of recombination and SOS response in Escherichia coli RecA suggests LexA interaction sites
  publication-title: PLOS Genet
  doi: 10.1371/journal.pgen.1002244
– volume: 100
  start-page: 231
  year: 1969
  ident: ref31
  article-title: Characteristics of some multiply recombination-deficient strains of Escherichia coli
  publication-title: J Bacteriol
  doi: 10.1128/JB.100.1.231-239.1969
– volume: 42
  start-page: 5633
  year: 2014
  ident: ref16
  article-title: Recombination hotspots attenuate the coupled ATPase and translocase activities of an AddAB-type helicase-nuclease
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gku188
– volume: 52
  start-page: 617
  year: 2013
  ident: ref69
  article-title: A bacterial toxin inhibits DNA replication elongation through a direct interaction with the β sliding clamp
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2013.10.014
– volume: 298
  start-page: 7
  year: 2000
  ident: ref18
  article-title: The Bacillus subtilis AddAB helicase/nuclease is regulated by its cognate Chi sequence in vitro1
  publication-title: J Mol Biol
  doi: 10.1006/jmbi.2000.3556
– volume: 179
  start-page: 880
  year: 1997
  ident: ref26
  article-title: Stability of linear DNA in recA mutant Escherichia coli cells reflects ongoing chromosomal DNA degradation
  publication-title: J Bacteriol
  doi: 10.1128/jb.179.3.880-888.1997
– volume: 112
  start-page: E4735
  year: 2015
  ident: ref36
  article-title: Quantitative genomic analysis of RecA protein binding during DNA double-strand break repair reveals RecBCD action in vivo
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.1424269112
– volume: 188
  start-page: 6016
  year: 2006
  ident: ref43
  article-title: Analysis of the terminus region of the Caulobacter crescentus chromosome and identification of the dif site
  publication-title: J Bacteriol
  doi: 10.1128/JB.00330-06
– volume: 26
  start-page: 841
  year: 2010
  ident: ref72
  article-title: BEDTools: a flexible suite of utilities for comparing genomic features
  publication-title: Bioinforma Oxf Engl
  doi: 10.1093/bioinformatics/btq033
– volume: 20
  start-page: 119
  year: 2014
  ident: ref15
  article-title: Single molecule approaches to monitor the recognition and resection of double-stranded DNA breaks during homologous recombination
  publication-title: DNA Repair
  doi: 10.1016/j.dnarep.2014.02.002
– volume: 58
  start-page: 401
  year: 1994
  ident: ref2
  article-title: Biochemistry of homologous recombination in Escherichia coli
  publication-title: Microbiol Rev
  doi: 10.1128/MMBR.58.3.401-465.1994
– volume: 191
  start-page: 1677
  year: 2009
  ident: ref61
  article-title: Roles of ExoI and SbcCD nucleases in “reckless” DNA degradation in recA mutants of Escherichia coli
  publication-title: J Bacteriol
  doi: 10.1128/JB.01877-07
– volume: 13
  start-page: 2812
  year: 2014
  ident: ref5
  article-title: Structural features of Chi recognition in AddAB with implications for RecBCD
  publication-title: Cell Cycle
  doi: 10.4161/15384101.2014.950892
– volume: 42
  start-page: 806
  year: 2011
  ident: ref24
  article-title: van Aelst K, Dillingham MS, Moreno-Herrero F. Recombination hotspots and single-stranded DNA binding proteins couple DNA translocation to DNA unwinding by the AddAB helicase-nuclease
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2011.04.012
– volume: 81
  start-page: 7850
  year: 1984
  ident: ref12
  article-title: A new class of Escherichia coli recBC mutants: implications for the role of RecBC enzyme in homologous recombination
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.81.24.7850
– volume: 115
  start-page: 11
  year: 1987
  ident: ref57
  article-title: Genetic functions promoting homologous recombination in Escherichia coli: A study of inversions in Phage Λ
  publication-title: Genetics
  doi: 10.1093/genetics/115.1.11
– volume: 175
  start-page: 5505
  year: 1993
  ident: ref59
  article-title: Degradation of individual chromosomes in recA mutants of Escherichia coli
  publication-title: J Bacteriol
  doi: 10.1128/jb.175.17.5505-5509.1993
– volume: 22
  start-page: 701
  year: 2006
  ident: ref68
  article-title: Engineering controllable protein degradation
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2006.04.027
– volume: 11
  start-page: 9
  year: 2013
  ident: ref4
  article-title: Bacterial DNA repair: recent insights into the mechanism of RecBCD, AddAB and AdnAB
  publication-title: Nat Rev Microbiol
  doi: 10.1038/nrmicro2917
– volume: 25
  start-page: 1328
  year: 2011
  ident: ref45
  article-title: A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW
  publication-title: Genes Dev
  doi: 10.1101/gad.2038911
– volume: 176
  start-page: 5093
  year: 1994
  ident: ref62
  article-title: Chi-dependent formation of linear plasmid DNA in exonuclease-deficient recBCD+ strains of Escherichia coli
  publication-title: J Bacteriol
  doi: 10.1128/jb.176.16.5093-5100.1994
– volume: 256
  start-page: 7573
  year: 1981
  ident: ref60
  article-title: Escherichia coli recA protein protects single-stranded DNA or gapped duplex DNA from degradation by RecBC DNase
  publication-title: J Biol Chem
  doi: 10.1016/S0021-9258(19)69000-9
– volume: 76
  start-page: 217
  year: 2012
  ident: ref6
  article-title: How RecBCD enzyme and Chi promote DNA break repair and recombination: a molecular biologist’s view
  publication-title: Microbiol Mol Biol Rev MMBR
  doi: 10.1128/MMBR.05026-11
– volume: 508
  start-page: 416
  year: 2014
  ident: ref14
  article-title: Structural basis for translocation by AddAB helicase-nuclease and its arrest at χ sites
  publication-title: Nature
  doi: 10.1038/nature13037
– volume: 72
  start-page: 642
  year: 2008
  ident: ref8
  article-title: RecBCD enzyme and the repair of double-stranded DNA breaks
  publication-title: Microbiol Mol Biol Rev
  doi: 10.1128/MMBR.00020-08
– volume: 31
  start-page: 637
  year: 2007
  ident: ref44
  article-title: Aeons of distress: an evolutionary perspective on the bacterial SOS response
  publication-title: FEMS Microbiol Rev
  doi: 10.1111/j.1574-6976.2007.00082.x
– volume: 9
  start-page: 276
  year: 2010
  ident: ref17
  article-title: The processing of double-stranded DNA breaks for recombinational repair by helicase–nuclease complexes
  publication-title: DNA Repair
  doi: 10.1016/j.dnarep.2009.12.016
– volume: 44
  start-page: 2727
  year: 2016
  ident: ref39
  article-title: Chi hotspots trigger a conformational change in the helicase-like domain of AddAB to activate homologous recombination
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkv1543
– volume: 147
  start-page: 949
  year: 2001
  ident: ref41
  article-title: New members of the ctrA regulon: the major chemotaxis operon in Caulobacter is CtrA dependent
  publication-title: Microbiol Read Engl
  doi: 10.1099/00221287-147-4-949
– volume: 7
  start-page: 915
  year: 1993
  ident: ref28
  article-title: The Bacillus subtilis addAB genes are fully functional in Escherichia coli
  publication-title: Mol Microbiol
  doi: 10.1111/j.1365-2958.1993.tb01182.x
– volume: 185
  start-page: 431
  year: 1985
  ident: ref65
  article-title: Substrate specificity of the DNA unwinding activity of the RecBC enzyme of Escherichia coli
  publication-title: J Mol Biol
  doi: 10.1016/0022-2836(85)90414-0
– volume: 52
  start-page: 119
  year: 2004
  ident: ref32
  article-title: RecG helicase promotes DNA double-strand break repair
  publication-title: Mol Microbiol
  doi: 10.1111/j.1365-2958.2003.03970.x
– volume: 10
  start-page: R25
  year: 2009
  ident: ref71
  article-title: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
  publication-title: Genome Biol
  doi: 10.1186/gb-2009-10-3-r25
– volume: 23
  start-page: 137
  year: 1997
  ident: ref30
  article-title: A conserved helicase motif of the AddA subunit of the Bacillus subtilis ATP-dependent nuclease (AddAB) is essential for DNA repair and recombination
  publication-title: Mol Microbiol
  doi: 10.1046/j.1365-2958.1997.1991570.x
– volume: 8
  start-page: e1002622
  year: 2012
  ident: ref33
  article-title: Replication fork reversal after replication–transcription collision
  publication-title: PLOS Genet
  doi: 10.1371/journal.pgen.1002622
– volume: 270
  start-page: 16360
  year: 1995
  ident: ref10
  article-title: Role of the Escherichia coli recombination hotspot, chi, in RecABCD-dependent homologous pairing
  publication-title: J Biol Chem
  doi: 10.1074/jbc.270.27.16360
– volume: 126
  start-page: 147
  year: 2006
  ident: ref52
  article-title: MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter
  publication-title: Cell
  doi: 10.1016/j.cell.2006.05.038
– volume: 482
  start-page: 423
  year: 2012
  ident: ref55
  article-title: Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search
  publication-title: Nature
  doi: 10.1038/nature10782
– volume: 13
  start-page: 2764
  year: 1994
  ident: ref25
  article-title: Chi sites in combination with RecA protein increase the survival of linear DNA in Escherichia coli by inactivating exoV activity of RecBCD nuclease
  publication-title: EMBO J
  doi: 10.1002/j.1460-2075.1994.tb06570.x
– volume: 105
  start-page: 109
  year: 1980
  ident: ref64
  article-title: Degradation of linear and circular DNA with gaps by the recBC enzyme of Escherichia coli
  publication-title: Eur J Biochem
  doi: 10.1111/j.1432-1033.1980.tb04480.x
– volume: 31
  start-page: 1568
  year: 2012
  ident: ref19
  article-title: Insights into Chi recognition from the structure of an AddAB-type helicase-nuclease complex
  publication-title: EMBO J
  doi: 10.1038/emboj.2012.9
– volume: 114
  start-page: 647
  year: 2003
  ident: ref13
  article-title: A molecular throttle: the recombination hotspot chi controls DNA translocation by the RecBCD helicase
  publication-title: Cell
  doi: 10.1016/S0092-8674(03)00681-0
– volume: 190
  start-page: 179
  year: 2008
  ident: ref63
  article-title: Effects of single-strand DNases ExoI, RecJ, ExoVII, and SbcCD on homologous recombination of recBCD+ strains of Escherichia coli and roles of SbcB15 and XonA2 ExoI mutant enzymes
  publication-title: J Bacteriol
  doi: 10.1128/JB.01052-07
– volume: 24
  start-page: 429
  year: 1981
  ident: ref11
  article-title: Structure of chi hotspots of generalized recombination
  publication-title: Cell
  doi: 10.1016/0092-8674(81)90333-0
– volume: 29
  start-page: 1369
  year: 1998
  ident: ref29
  article-title: A five-nucleotide sequence protects DNA from exonucleolytic degradation by AddAB, the RecBCD analogue of Bacillus subtilis
  publication-title: Mol Microbiol
  doi: 10.1046/j.1365-2958.1998.01018.x
– volume: 18
  start-page: 1407
  year: 1990
  ident: ref34
  article-title: Purification and characterization of the in vitro activity of I-Sce I, a novel and highly specific endonuclease encoded by a group I intron
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/18.6.1407
– volume: 89
  start-page: 12073
  year: 1992
  ident: ref56
  article-title: Chi sequence protects against RecBCD degradation of DNA in vivo
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.89.24.12073
– volume: 150
  start-page: 579
  year: 1999
  ident: ref42
  article-title: Characteristics of Chi distribution on different bacterial genomes
  publication-title: Res Microbiol
  doi: 10.1016/S0923-2508(99)00132-1
– volume: 60
  start-page: 374
  year: 2015
  ident: ref67
  article-title: Anionic phospholipids stabilize RecA filament bundles in Escherichia coli
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2015.09.009
– volume: 179
  start-page: 1219
  year: 1997
  ident: ref27
  article-title: Role of enzymes of homologous recombination in illegitimate plasmid recombination in Bacillus subtilis
  publication-title: J Bacteriol
  doi: 10.1128/jb.179.4.1219-1229.1997
– volume: 111
  start-page: 16454
  year: 2014
  ident: ref35
  article-title: Completion of DNA replication in Escherichia coli
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.1415025111
– volume: 12
  start-page: 162
  year: 2013
  ident: ref1
  article-title: Early steps of double-strand break repair in Bacillus subtilis
  publication-title: DNA Repair
  doi: 10.1016/j.dnarep.2012.12.005
– volume: 7
  start-page: 17
  year: 2007
  ident: ref38
  article-title: Genome analysis of DNA repair genes in the alpha proteobacterium Caulobacter crescentus
  publication-title: BMC Microbiol
  doi: 10.1186/1471-2180-7-17
– volume: 67
  start-page: 1347
  year: 2008
  ident: ref49
  article-title: Requirements for ATP binding and hydrolysis in RecA function in Escherichia coli
  publication-title: Mol Microbiol
  doi: 10.1111/j.1365-2958.2008.06130.x
– volume: 38
  start-page: 385
  year: 2003
  ident: ref50
  article-title: Molecular design and functional organization of the RecA protein
  publication-title: Crit Rev Biochem Mol Biol
  doi: 10.1080/10409230390242489
– volume: 131
  start-page: 694
  year: 2007
  ident: ref7
  article-title: RecBCD enzyme switches lead motor subunits in response to chi recognition
  publication-title: Cell
  doi: 10.1016/j.cell.2007.09.023
– volume: 426
  start-page: 3479
  year: 2014
  ident: ref9
  article-title: Control of RecBCD enzyme activity by DNA binding- and Chi hotspot-dependent conformational changes
  publication-title: J Mol Biol
  doi: 10.1016/j.jmb.2014.07.017
– volume: 92
  start-page: 6249
  year: 1995
  ident: ref58
  article-title: Interaction with the recombination hot spot chi in vivo converts the RecBCD enzyme of Escherichia coli into a chi-independent recombinase by inactivation of the RecD subunit
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.92.14.6249
– volume: 110
  start-page: E2562
  year: 2013
  ident: ref22
  article-title: On the mechanism of recombination hotspot scanning during double-stranded DNA break resection
  publication-title: Proc Natl Acad Sci
  doi: 10.1073/pnas.1303035110
– volume: 39
  start-page: 2271
  year: 2011
  ident: ref23
  article-title: The AddAB helicase-nuclease catalyses rapid and processive DNA unwinding using a single Superfamily 1A motor domain
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkq1124
– volume: 21
  start-page: 573
  year: 2006
  ident: ref20
  article-title: The RecA binding locus of RecBCD is a general domain for recruitment of DNA strand exchange proteins
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2006.01.007
– volume: 35
  start-page: e137
  year: 2007
  ident: ref40
  article-title: A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkm818
– volume: 16
  start-page: 6883
  year: 1988
  ident: ref70
  article-title: Mung bean nuclease exhibits a generalized gene-excision activity upon purified Plasmodium falciparum genomic DNA
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/16.14.6883
– volume: 210
  start-page: 385
  year: 2015
  ident: ref37
  article-title: Rapid pairing and resegregation of distant homologous loci enables double-strand break repair in bacteria
  publication-title: J Cell Biol
  doi: 10.1083/jcb.201505019
– volume: 181
  start-page: 6220
  year: 1999
  ident: ref66
  article-title: recD sbcB sbcD mutants are deficient in recombinational repair of UV lesions by RecBC
  publication-title: J Bacteriol
  doi: 10.1128/JB.181.19.6220-6221.1999
– volume: 95
  start-page: 5752
  year: 1998
  ident: ref47
  article-title: A bacterial two-hybrid system based on a reconstituted signal transduction pathway
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.95.10.5752
– volume: 506
  start-page: 249
  year: 2014
  ident: ref48
  article-title: RecA bundles mediate homology pairing between distant sisters during DNA break repair
  publication-title: Nature
  doi: 10.1038/nature12868
– volume: 6
  start-page: a016436
  year: 2014
  ident: ref3
  article-title: End resection at double-strand breaks: mechanism and regulation
  publication-title: Cold Spring Harb Perspect Biol
  doi: 10.1101/cshperspect.a016436
– volume: 12
  start-page: e1001977
  year: 2014
  ident: ref46
  article-title: A DNA damage-induced, SOS-independent checkpoint regulates cell division in Caulobacter crescentus
  publication-title: PLoS Biol
  doi: 10.1371/journal.pbio.1001977
– volume: 4
  year: 2015
  ident: ref54
  article-title: Resection is responsible for loss of transcription around a double-strand break in Saccharomyces cerevisiae
  publication-title: eLife
  doi: 10.7554/eLife.08942
– reference: 2841646 - Nucleic Acids Res. 1988 Jul 25;16(14B):6883-96
– reference: 24670664 - Nature. 2014 Apr 17;508(7496):416-9
– reference: 9230304 - Cell. 1997 Jul 11;90(1):77-86
– reference: 23798400 - Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):E2562-71
– reference: 20116346 - DNA Repair (Amst). 2010 Mar 2;9(3):276-85
– reference: 26231041 - Elife. 2015 Jul 31;4:null
– reference: 23380520 - DNA Repair (Amst). 2013 Mar 1;12(3):162-76
– reference: 25486468 - Cell Cycle. 2014;13(18):2812-20
– reference: 16762842 - Mol Cell. 2006 Jun 9;22(5):701-7
– reference: 22318518 - Nature. 2012 Feb 08;482(7385):423-7
– reference: 22307084 - EMBO J. 2012 Mar 21;31(6):1568-78
– reference: 10756102 - J Mol Biol. 2000 Apr 21;298(1):7-20
– reference: 25073102 - J Mol Biol. 2014 Oct 23;426(21):3479-99
– reference: 21071401 - Nucleic Acids Res. 2011 Mar;39(6):2271-85
– reference: 9006046 - J Bacteriol. 1997 Feb;179(3):880-8
– reference: 17959646 - Nucleic Acids Res. 2007;35(20):e137
– reference: 18022364 - Cell. 2007 Nov 16;131(4):694-705
– reference: 7541534 - Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6249-53
– reference: 6245875 - Eur J Biochem. 1980 Mar;105(1):109-16
– reference: 24569169 - DNA Repair (Amst). 2014 Aug;20:119-29
– reference: 1465442 - Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12073-7
– reference: 26261330 - Proc Natl Acad Sci U S A. 2015 Aug 25;112(34):E4735-42
– reference: 2997450 - J Mol Biol. 1985 Sep 20;185(2):431-43
– reference: 8366035 - J Bacteriol. 1993 Sep;175(17):5505-9
– reference: 2951295 - Genetics. 1987 Jan;115(1):11-24
– reference: 22688812 - Microbiol Mol Biol Rev. 2012 Jun;76(2):217-28
– reference: 18298444 - Mol Microbiol. 2008 Mar;67(6):1347-59
– reference: 6393130 - Proc Natl Acad Sci U S A. 1984 Dec;81(24):7850-4
– reference: 20110278 - Bioinformatics. 2010 Mar 15;26(6):841-2
– reference: 17883408 - FEMS Microbiol Rev. 2007 Nov;31(6):637-56
– reference: 11283290 - Microbiology. 2001 Apr;147(Pt 4):949-58
– reference: 26762979 - Nucleic Acids Res. 2016 Apr 7;44(6):2727-41
– reference: 19261174 - Genome Biol. 2009;10(3):R25
– reference: 17965170 - J Bacteriol. 2008 Jan;190(1):179-92
– reference: 26481664 - Mol Cell. 2015 Nov 5;60(3):374-84
– reference: 17352799 - BMC Microbiol. 2007 Mar 12;7:17
– reference: 8387145 - Mol Microbiol. 1993 Mar;7(6):915-23
– reference: 7968921 - Microbiol Rev. 1994 Sep;58(3):401-65
– reference: 19074388 - J Bacteriol. 2009 Mar;191(5):1677-87
– reference: 6265452 - J Biol Chem. 1981 Jul 25;256(14):7573-82
– reference: 16483938 - Mol Cell. 2006 Feb 17;21(4):573-80
– reference: 9004227 - Mol Microbiol. 1997 Jan;23(1):137-49
– reference: 17020576 - Mol Microbiol. 2006 Oct;62(2):331-8
– reference: 22496668 - PLoS Genet. 2012;8(4):e1002622
– reference: 25350732 - PLoS Biol. 2014 Oct 28;12(10):e1001977
– reference: 8051022 - J Bacteriol. 1994 Aug;176(16):5093-100
– reference: 6453653 - Cell. 1981 May;24(2):429-36
– reference: 9576956 - Proc Natl Acad Sci U S A. 1998 May 12;95(10):5752-6
– reference: 24362571 - Nature. 2014 Feb 13;506(7487):249-53
– reference: 19052323 - Microbiol Mol Biol Rev. 2008 Dec;72(4):642-71, Table of Contents
– reference: 13678587 - Cell. 2003 Sep 5;114(5):647-54
– reference: 25085909 - Cold Spring Harb Perspect Biol. 2014 Aug 01;6(8):null
– reference: 10672998 - Res Microbiol. 1999 Nov-Dec;150(9-10):579-87
– reference: 2183191 - Nucleic Acids Res. 1990 Mar 25;18(6):1407-13
– reference: 21912525 - PLoS Genet. 2011 Sep;7(9):e1002244
– reference: 9781875 - Mol Microbiol. 1998 Sep;29(6):1369-77
– reference: 8026461 - EMBO J. 1994 Jun 15;13(12):2764-76
– reference: 21685367 - Genes Dev. 2011 Jun 15;25(12):1328-43
– reference: 16885470 - J Bacteriol. 2006 Aug;188(16):6016-9
– reference: 10498743 - J Bacteriol. 1999 Oct;181(19):6220-1
– reference: 14693725 - Crit Rev Biochem Mol Biol. 2003;38(5):385-432
– reference: 4898990 - J Bacteriol. 1969 Oct;100(1):231-9
– reference: 24682829 - Nucleic Acids Res. 2014 May;42(9):5633-43
– reference: 15049815 - Mol Microbiol. 2004 Apr;52(1):119-32
– reference: 26240183 - J Cell Biol. 2015 Aug 3;210(3):385-400
– reference: 24239291 - Mol Cell. 2013 Dec 12;52(5):617-28
– reference: 7608206 - J Biol Chem. 1995 Jul 7;270(27):16360-70
– reference: 16839883 - Cell. 2006 Jul 14;126(1):147-62
– reference: 21700225 - Mol Cell. 2011 Jun 24;42(6):806-16
– reference: 25368150 - Proc Natl Acad Sci U S A. 2014 Nov 18;111(46):16454-9
– reference: 23202527 - Nat Rev Microbiol. 2013 Jan;11(1):9-13
– reference: 9023205 - J Bacteriol. 1997 Feb;179(4):1219-29
SSID ssj0035897
Score 2.294887
Snippet In bacteria, double-strand break (DSB) repair via homologous recombination is thought to be initiated through the bi-directional degradation and resection of...
SourceID plos
doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1006783
SubjectTerms Assaying
Bacteria
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biodegradation
Biology
Biology and life sciences
Bismuth
Caulobacter
Caulobacter crescentus - genetics
Chromosomes
Couples
Deoxyribonucleic acid
DNA
DNA Breaks, Double-Stranded
DNA damage
DNA helicase
DNA repair
DNA sequencing
Double-strand break repair
E coli
Enzymes
Exodeoxyribonucleases - genetics
Exodeoxyribonucleases - metabolism
Genetic aspects
Genome, Bacterial
Genomes
Genomic Instability
Helicases
Homologous recombination
Homology
Medicine and Health Sciences
Nuclease
Rec A Recombinases - genetics
Rec A Recombinases - metabolism
RecA protein
Research and analysis methods
Studies
Transcription
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3fi9QwEA6yIPgi_r7qqVEEn-K1TdMmj3vicfpwgnpybyVJE29xaYvdPfS_dybplqsc3D34tmwmCzszmfmmnXxDyJvUeqtlKpnLuGCFqDwz3FimC8jOuZZeuNDle1IenxafzsTZpVFf2BMW6YGj4g6M9FKUSuRG54W03OTSecDRGsooL8sAjVKV7oqpGIO5kHGsihCcVVDWj5fmeJUdjDZ614OBsEcAojWfJaXA3T9F6EW_7oar4Oe_XZSX0tLRPXJ3xJN0Gf_HfXLLtQ_I7Thh8s9DMkROf6pH7hHaedp0W7N2DJ9xtA2Fklj_pH28LwB5jCKnE_gkXbX0YnXR4VKPzdcubAa8SM8dPukbHGuRDBk-0NCY7n7TZdMsDx-R06MP394fs3HOArNVXm6YLLhucAixksoYW2nbqLT0JaT_DFZs6QUvXaUy77X1KUfGGYAWTWbwtHvPH5NF27Vuj1CHZDh5nhnAXZAevc5kUyipjXfKClclhO8UXduRhBxnYazr8GatgmIk6q1G89SjeRLCpl19JOG4Rv4QbTjJIoV2-AIcqx4dq77OsRLyEj2gjvdRp0BQLwtAdBwqe5WQ10ECaTRa7NP5obfDUH_8_P0GQl9PbiL0ZSb0dhTyHejM6vECBWgeObxmkvszSYgYdra8h069U91QQ80eieME7Nw5-tXLr6Zl_FFs0GtdtwUZGadjqDIhT-K5mNQPCEgqQPYJqWYnZmaf-Uq7Og9U58jOCM739H8Y9Bm5kyMmC9S7-2Sx-bV1zwFRbsyLEDz-Agbzco4
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3fb9MwELagCIkXxO8VBhiExJNZE8eJ84Q6xDR4GBIw1LfIduytWpWEpZ3gv-fOdgNBE-yt6l2q6u58_s45f0fIq5lxRsmZZDbhgmWicExzbZjKYHdOlXTC-i7fo_zwOPu4EIt44NbHtsptTvSJum4NnpHvQV0RyK3E2-47w6lR-HY1jtC4Tm4kgERwdEOxGAouLmQYriIEZwUU9_HqHC-SveipNx24CTsFIGfz0dbkGfyHPD3pVm1_GQj9u5fyj83p4A65HVElnYcwuEuu2eYeuRnmTP68T_rA7E9VZCChraN1u9Ery_Cko6kpFMbqjHbh1gDsZhSZnSAy6bKhF8uLFkUdtmBb_zCgRnpq8byvt6xBSmT4QH17uv1B53U9339Ajg_ef313yOK0BWaKNF8zmXFV4yjiUpZam0KZupzlLgcQkIDE5E7w3BZl4pwybsaRdwYARp1oXPPO8Ydk0rSN3SHUIiVOmiYa0Bdskk4lss5KqbSzpRG2mBK-NXRlIhU5TsRYVf79WgElSbBbhe6ponumhA1PdYGK4z_6--jDQReJtP0X7flJFddlpaWTIi9FqlWaScN1Kq2DMk1Ble5krqbkOUZAFW6lDumgmmeA6zjU9-WUvPQaSKbRYLfOidr0ffXh07crKH05uorS55HS66jkWrCZUfEaBVgembxGmrsjTcgbZiTewaDemq6vfq8weHIb6JeLXwxi_FFs02tsuwEdGWZklPmUPArrYjA_4CBZAr6fkmK0Ykb-GUua5aknPEeORgi-x__-W0_IrRQxl6fW3SWT9fnGPgXEuNbPfFr4BTdJajg
  priority: 102
  providerName: ProQuest
Title Global analysis of double-strand break processing reveals in vivo properties of the helicase-nuclease complex AddAB
URI https://www.ncbi.nlm.nih.gov/pubmed/28489851
https://www.proquest.com/docview/1910463605
https://www.proquest.com/docview/1897805296
https://pubmed.ncbi.nlm.nih.gov/PMC5443536
https://doaj.org/article/b8f856952ba248c3b28ef217a132f86a
http://dx.doi.org/10.1371/journal.pgen.1006783
Volume 13
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3db9MwELe2Tki8IL4XGMUgJJ4yNXESOw8ItbBq8FDQoKhvke3YW7UqKU07bf89d04aEdSJPTXqnaPozh-_s8-_I-TdQFstxUD4JmCxH8Xc-oop7csIVudQChsbl-U7SU6n0ddZPNsj25qtjQGrnaEd1pOarhbH179vPsKA_-CqNvBg2-h4CSbHU3-Yf9k-OXAnRpjMF7XnCiwWKW8u0N3WsrNAOR7_drbuLRdltQuK_ptR-dcSNX5IHjTYkg7rzvCI7JniMblXV5u8eUKqmt-fyoaHhJaW5uVGLYyP-x1FTiE8lpd0Wd8dgDWNIr8T2InOC3o1vypRtMREbOMaA3akFwZ3_SrjF0iMDA_UJambazrM8-HoKZmOT35-OvWbmgu-5mGy9kXEZI4FiVORKqW51Hk6SGwCUCAAiU5szBLD08Baqe2AIfsMwIw8UDjyrWXPSK8oC3NIqEFinDAMFGAwcIWVgcijVEhlTapjwz3CtobOdENIjnUxFpk7ZeMQmNR2y9A9WeMej_htq2VNyPEf_RH6sNVFOm33R7k6z5rRmSlhRZykcahkGAnNVCiMhWBNQqxuRSI98hp7QFbfTW0nhWwYAbpjEOWnHnnrNJBSo8CcnXO5qarsy7dfd1D6MbmL0llH6X2jZEuwmZbNZQqwPPJ5dTSPOpowe-iO-BA79dZ0VQbxe00iF0PLbUffLX7TivGlmKxXmHIDOqKulJEmHnlej4vW_ICGRAoo3yO8M2I6_ulKivmFoz1HpkbofC9u_-KX5H6IqMuR6x6R3nq1Ma8AM65Vn-zzGe-Tg-Ho82gMv6OTyfezvtuB6bsp4g8kvnFO
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9MwELdGJwQviO8FBjMIxFNYE8eJ8zChFjZ1bBQ0tmlvwXHsraJKwtIO9s_xt3GXOIWgCfaytyo-R9Xd-T6cu98R8qKvjJKiL1ztMe4GPDJuylLlygC8sy-F4bqu8h2Ho4Pg_RE_WiI_214YLKtsbWJtqLNC4R35OuQVDbgVf1N-c3FqFH5dbUdoSDtaIduoIcZsY8eOPv8OKVy1sf0O5P3S97c299-OXDtlwFWRH85cETCZ4QjeWMRpqiKpsrgfmhCcnwcrKjSchTqKPWOkMn2GeCvgWDMvRV03hsF7r5HlAC9QemR5uDn-tNf6AsZFM96Fc-ZGLO7b5j0WeetWV16XoChYqwBeg3WcYz1DYOEpeuW0qC4Kg_-u5vzDPW7dJrdsXEsHjSLeIUs6v0uuN5Muz--RqpktQKXFQKGFoVkxT6faxbuWPKOQmsuvtGz6FsCfUsSWgrNBJzk9m5wVuFRiEbiuN0PcSk803jhW2s0RlBl-0LpAXv-ggywbDO-TgyuRxAPSy4tcrxCqEZTH970U4j9w00Z6IgtiIVOjY8V15BDWMjpRFgwdZ3JMk_oLXwRJUcO3BMWTWPE4xF3sKhswkP_QD1GGC1qE8q4fFKfHibUMSSqM4GHM_VT6gVAs9YU2kChKj_lGhNIha6gBSdMXuzBIySCAyJIxCDgd8rymQDiPHOuFjuW8qpLtj4eXIPo8vgzRXofolSUyBfBMSdvIAZxHLLEO5WqHEiyX6iyvoFK3rKuS32ccdraKfvHys8UyvhQLBXNdzIFGNFM64tAhD5tzsWA_RGIihgzDIVHnxHTk013JJyc15DqiRILyPfr331ojN0b7H3aT3e3xzmNy08cIsAb6XSW92elcP4H4dZY-tUaCki9XbZd-AZbTrSo
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9MwELdGJxAviO8FBjMIxFNoE-fDeZhQy1atDJVpMLS3YDv2NlElYWkH-xf5q7hLnELQBHvZWxWfo-rufB_O3e8IeTFQRgk-4K72WOgGYWxcyaRyRQDe2RfchLqu8p1GOwfBu8PwcIX8bHthsKyytYm1oc4KhXfkfcgrGnCrsG9sWcTe1vhN-c3FCVL4pbUdpyHsmIVss4Ybs00eu_r8O6Rz1eZkC2T_0vfH25_e7rh24oCrYj-auzxgIsNxvAlPpFSxUFkyiEwEjtCDFRWZkEU6TjxjhDIDhtgr4GQzT6LeG8PgvdfIagxeHxLB1dH2dG-_9Qss5M2olzBkLlAMbCMfi72-1ZvXJSgN1i2AB2EdR1nPE1h6jV45K6qLQuK_Kzv_cJXj2-SWjXHpsFHKO2RF53fJ9Wbq5fk9UjVzBqiweCi0MDQrFnKmXbx3yTMKabr4SsumhwF8K0WcKTgn9CSnZydnBS6VWBCu680Qw9JjjbePlXZzBGiGH7Qultc_6DDLhqP75OBKJPGA9PIi12uEagTo8X1PQiwILtsIj2dBwoU0OlGhjh3CWkanygKj43yOWVp_7YshQWr4lqJ4Uiseh7jLXWUDDPIf-hHKcEmLsN71g-L0KLVWIpXc8DBKQl8KP-CKSZ9rA0mj8JhveCQcsoEakDY9skvjlA4DiDIZg-DTIc9rCoT2yPGQHIlFVaWTD58vQfRxehmi_Q7RK0tkCuCZErapAziPuGIdyvUOJVgx1VleQ6VuWVelv8877GwV_eLlZ8tlfCkWDea6WAANbyZ2JJFDHjbnYsl-iMp4AtmGQ-LOienIp7uSnxzX8OuIGAnK9-jff2uD3AD7lL6fTHcfk5s-BoM15u866c1PF_oJhLJz-dTaCEq-XLVZ-gUi4LFu
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Global+analysis+of+double-strand+break+processing+reveals+in+vivo+properties+of+the+helicase-nuclease+complex+AddAB&rft.jtitle=PLoS+genetics&rft.au=Badrinarayanan%2C+Anjana&rft.au=Le%2C+Tung&rft.au=Jan-Hendrik+Spille&rft.au=Cisse%2C+Ibrahim&rft.date=2017-05-10&rft.pub=Public+Library+of+Science&rft.eissn=1553-7404&rft.volume=13&rft.issue=5&rft_id=info:doi/10.1371%2Fjournal.pgen.1006783&rft.externalDocID=1910463605
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7404&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7404&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7404&client=summon