Intricate SUMO-based control of the homologous recombination machinery

The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair, recombination enzymes can cleave, pair, and unwind DNA molecules, and collaborate with regulatory proteins to execute multiple DNA processing...

Full description

Saved in:
Bibliographic Details
Published inGenes & development Vol. 33; no. 19-20; pp. 1346 - 1354
Main Authors Dhingra, Nalini, Zhao, Xiaolan
Format Journal Article
LanguageEnglish
Published United States Cold Spring Harbor Laboratory Press 01.10.2019
Subjects
Animals
Gene Expression Regulation - genetics
Homologous Recombination - genetics
Humans
Rad51 Recombinase - metabolism
Review
SUMO-1 Protein - metabolism
Sumoylation
genome maintenance
sumoylation
homologous recombination
double-strand break repair
Online AccessGet full text

Cover

Abstract The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair, recombination enzymes can cleave, pair, and unwind DNA molecules, and collaborate with regulatory proteins to execute multiple DNA processing steps before generating specific repair products. HR proteins also help to cope with problems arising from DNA replication, modulating impaired replication forks or filling DNA gaps. Given these important roles, it is not surprising that each HR step is subject to complex regulation to adjust repair efficiency and outcomes as well as to limit toxic intermediates. Recent studies have revealed intricate regulation of all steps of HR by the protein modifier SUMO, which has been increasingly recognized for its broad influence in nuclear functions. This review aims to connect established roles of SUMO with its newly identified effects on recombinational repair and stimulate further thought on many unanswered questions.
AbstractList The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair, recombination enzymes can cleave, pair, and unwind DNA molecules, and collaborate with regulatory proteins to execute multiple DNA processing steps before generating specific repair products. HR proteins also help to cope with problems arising from DNA replication, modulating impaired replication forks or filling DNA gaps. Given these important roles, it is not surprising that each HR step is subject to complex regulation to adjust repair efficiency and outcomes as well as to limit toxic intermediates. Recent studies have revealed intricate regulation of all steps of HR by the protein modifier SUMO, which has been increasingly recognized for its broad influence in nuclear functions. This review aims to connect established roles of SUMO with its newly identified effects on recombinational repair and stimulate further thought on many unanswered questions.
The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair, recombination enzymes can cleave, pair, and unwind DNA molecules, and collaborate with regulatory proteins to execute multiple DNA processing steps before generating specific repair products. HR proteins also help to cope with problems arising from DNA replication, modulating impaired replication forks or filling DNA gaps. Given these important roles, it is not surprising that each HR step is subject to complex regulation to adjust repair efficiency and outcomes as well as to limit toxic intermediates. Recent studies have revealed intricate regulation of all steps of HR by the protein modifier SUMO, which has been increasingly recognized for its broad influence in nuclear functions. This review aims to connect established roles of SUMO with its newly identified effects on recombinational repair and stimulate further thought on many unanswered questions.The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair, recombination enzymes can cleave, pair, and unwind DNA molecules, and collaborate with regulatory proteins to execute multiple DNA processing steps before generating specific repair products. HR proteins also help to cope with problems arising from DNA replication, modulating impaired replication forks or filling DNA gaps. Given these important roles, it is not surprising that each HR step is subject to complex regulation to adjust repair efficiency and outcomes as well as to limit toxic intermediates. Recent studies have revealed intricate regulation of all steps of HR by the protein modifier SUMO, which has been increasingly recognized for its broad influence in nuclear functions. This review aims to connect established roles of SUMO with its newly identified effects on recombinational repair and stimulate further thought on many unanswered questions.
In this review, Dhingra et al. discuss the roles of SUMO in light of its newly identified effects on recombinational repair, and present further thoughts on many unanswered questions. The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair, recombination enzymes can cleave, pair, and unwind DNA molecules, and collaborate with regulatory proteins to execute multiple DNA processing steps before generating specific repair products. HR proteins also help to cope with problems arising from DNA replication, modulating impaired replication forks or filling DNA gaps. Given these important roles, it is not surprising that each HR step is subject to complex regulation to adjust repair efficiency and outcomes as well as to limit toxic intermediates. Recent studies have revealed intricate regulation of all steps of HR by the protein modifier SUMO, which has been increasingly recognized for its broad influence in nuclear functions. This review aims to connect established roles of SUMO with its newly identified effects on recombinational repair and stimulate further thought on many unanswered questions.
Author Dhingra, Nalini
Zhao, Xiaolan
AuthorAffiliation Molecular Biology Department, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA
AuthorAffiliation_xml – name: Molecular Biology Department, Memorial Sloan Kettering Cancer Center, New York, New York 10065, USA
Author_xml – sequence: 1
  givenname: Nalini
  surname: Dhingra
  fullname: Dhingra, Nalini
– sequence: 2
  givenname: Xiaolan
  surname: Zhao
  fullname: Zhao, Xiaolan
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31575678$$D View this record in MEDLINE/PubMed
BookMark eNp1UU1PAjEQbYxGQL16NHv0stjSdtteTAwRJdFwUM5NvxZqdre4XUz49xYBoyaeJvPx3puZNwDHTWgcAJcIDhGC6Gah7BCPOMUk5eII9BElIqeEsWPQh1zAXOBC9MAgxjcIYQGL4hT0MKKMFoz3wWTadK03qnPZy_x5lmsVnc1MSNVQZaHMuqXLlqEOVViEdcxaZ0KtfaM6H5qsVmbpG9duzsFJqaroLvbxDMwn96_jx_xp9jAd3z3lBjMkci2UYhwbrDktuFAFtZRoQqHCGruyRNpwNrIltRojTUpmiDHWWsqRQoQgfAZud7yrta6dNS7tqSq5an2t2o0MysvfncYv5SJ8yIIxhPkoEVzvCdrwvnaxk7WPxlWValy6T44whIhxTrdaVz-1vkUOz0sDZDdg2hBj60ppfPf1mCTtK4mg3Hokk0dy51HKRYIN_8AOzP8APgEz5JTo
CitedBy_id crossref_primary_10_1016_j_molcel_2025_02_004
crossref_primary_10_7554_eLife_57720
crossref_primary_10_1016_j_gde_2021_07_007
crossref_primary_10_3389_fgene_2021_671392
crossref_primary_10_1089_crispr_2021_0039
crossref_primary_10_1016_j_jbc_2021_101200
crossref_primary_10_3389_fendo_2024_1393111
crossref_primary_10_1016_j_bbrc_2021_12_099
crossref_primary_10_3390_molecules26040828
crossref_primary_10_1016_j_devcel_2021_06_012
crossref_primary_10_31857_S0026898424040029
crossref_primary_10_1002_1873_3468_14751
crossref_primary_10_1134_S0026893324700201
crossref_primary_10_1016_j_jbc_2023_105547
Cites_doi 10.1101/gad.278275.116
10.1038/nature08593
10.1093/nar/gks484
10.1098/rstb.2016.0282
10.1016/j.molcel.2019.01.005
10.1073/pnas.1303111110
10.1038/sj.emboj.7601158
10.1093/nar/gkp1008
10.1038/nrm3478
10.1016/j.molcel.2010.08.028
10.1128/JVI.01273-12
10.1016/j.molcel.2017.04.017
10.1038/s41467-018-07364-x
10.1371/journal.pgen.1000858
10.1007/s00412-017-0658-1
10.1038/emboj.2013.24
10.1371/journal.pgen.1007942
10.1016/j.tibs.2015.02.006
10.1016/j.molcel.2014.11.014
10.15252/embr.201440017
10.1016/j.celrep.2016.06.015
10.1016/j.molcel.2015.01.022
10.1101/gad.238535.114
10.1074/mcp.O114.044792
10.1038/s41467-017-00183-6
10.1534/genetics.114.166140
10.1038/nature08657
10.1083/jcb.201010117
10.1074/jbc.M512757200
10.1074/jbc.RA118.006006
10.1016/j.molcel.2005.06.001
10.1080/10409238.2018.1488803
10.1016/j.cell.2006.08.050
10.1093/nar/gks270
10.1016/j.molcel.2012.02.017
10.1101/sqb.2015.80.027649
10.1534/genetics.116.196568
10.1093/nar/gkv1523
10.1371/journal.pone.0051540
10.1242/jcs.133744
10.1093/nar/gkq195
10.1038/nature01965
10.1038/nrm.2016.58
10.1038/nature03665
10.1038/ncb2729
10.1101/gad.265058.115
10.1038/nature19071
10.3390/biom6010014
10.1038/sj.emboj.7600394
10.1371/journal.pone.0214102
10.1016/j.molcel.2011.11.010
10.1038/ncb1619
10.1074/jbc.M115.685891
10.1038/nature00991
10.1016/j.celrep.2014.08.054
10.7554/eLife.22195
10.1074/jbc.M009476200
10.1038/emboj.2013.9
10.1016/j.dnarep.2016.04.001
10.1080/15384101.2017.1302628
10.1146/annurev.biochem.73.011303.074118
10.1016/j.celrep.2016.05.007
10.1074/jbc.M100006200
10.1016/j.gde.2016.10.005
10.1146/annurev-biochem-061909-093311
10.1101/gad.265629.115
10.3109/10409238.2016.1172552
10.1016/j.molcel.2011.11.028
10.1016/j.molcel.2010.07.021
10.1371/journal.pgen.1003833
10.1038/ncb1488
10.1073/pnas.0500537102
10.1093/hmg/ddp478
10.1016/j.molcel.2014.11.015
10.1016/j.ceb.2016.02.018
10.1515/bmc-2016-0030
10.1098/rstb.2016.0281
10.1080/15384101.2015.1060381
10.3389/fgene.2013.00167
10.1371/journal.pone.0080442
10.1146/annurev-genet-120215-035043
10.1093/nar/gkn441
10.1371/journal.pgen.1004899
10.1016/j.cell.2012.10.021
10.1073/pnas.0403498101
10.1101/cshperspect.a016501
ContentType Journal Article
Copyright 2019 Dhingra and Zhao; Published by Cold Spring Harbor Laboratory Press.
2019
Copyright_xml – notice: 2019 Dhingra and Zhao; Published by Cold Spring Harbor Laboratory Press.
– notice: 2019
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
7X8
5PM
DOI 10.1101/gad.328534.119
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE
CrossRef
MEDLINE - Academic
Database_xml – sequence: 1
  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: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate Dhingra and Zhao
EISSN 1549-5477
EndPage 1354
ExternalDocumentID PMC6771382
31575678
10_1101_gad_328534_119
Genre Journal Article
Review
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: R01 GM080670
– fundername: NCI NIH HHS
  grantid: P30 CA008748
– fundername: ;
  grantid: GM080670
GroupedDBID ---
-DZ
-~X
.55
18M
29H
2WC
39C
4.4
53G
5RE
5VS
85S
AAYXX
ABCQX
ABDIX
ACGFO
ACLKE
ACNCT
ADBBV
ADIYS
ADXHL
AECCQ
AENEX
AETEA
AFFNX
AFOSN
AHPUY
ALMA_UNASSIGNED_HOLDINGS
BAWUL
BTFSW
CITATION
CS3
DIK
DU5
E3Z
EBS
EJD
F5P
FRP
GX1
H13
HYE
H~9
IH2
KQ8
L7B
MV1
N9A
OK1
P2P
R.V
RCX
RHI
RPM
SJN
TAE
TN5
TR2
UHB
W8F
WH7
WOQ
X7M
XSW
YBU
YHG
YKV
YSK
CGR
CUY
CVF
ECM
EIF
NPM
RHF
VQA
7X8
5PM
ID FETCH-LOGICAL-c3719-b9aa783c3b85689a65d54b450a3b3eff1bc872df5db31b4f7c4ccddd581a14413
ISSN 0890-9369
1549-5477
IngestDate Thu Aug 21 14:09:02 EDT 2025
Fri Jul 11 04:17:03 EDT 2025
Wed Feb 19 02:30:57 EST 2025
Tue Jul 01 01:12:09 EDT 2025
Thu Apr 24 22:51:20 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 19-20
Keywords genome maintenance
sumoylation
homologous recombination
double-strand break repair
Language English
License 2019 Dhingra and Zhao; Published by Cold Spring Harbor Laboratory Press.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c3719-b9aa783c3b85689a65d54b450a3b3eff1bc872df5db31b4f7c4ccddd581a14413
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
ObjectType-Review-3
content type line 23
OpenAccessLink https://pubmed.ncbi.nlm.nih.gov/PMC6771382
PMID 31575678
PQID 2300178851
PQPubID 23479
PageCount 9
ParticipantIDs pubmedcentral_primary_oai_pubmedcentral_nih_gov_6771382
proquest_miscellaneous_2300178851
pubmed_primary_31575678
crossref_citationtrail_10_1101_gad_328534_119
crossref_primary_10_1101_gad_328534_119
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2019-10-01
20191001
PublicationDateYYYYMMDD 2019-10-01
PublicationDate_xml – month: 10
  year: 2019
  text: 2019-10-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Genes & development
PublicationTitleAlternate Genes Dev
PublicationYear 2019
Publisher Cold Spring Harbor Laboratory Press
Publisher_xml – name: Cold Spring Harbor Laboratory Press
References 2021111620145409000_33.19-20.1346.17
2021111620145409000_33.19-20.1346.16
2021111620145409000_33.19-20.1346.19
2021111620145409000_33.19-20.1346.18
2021111620145409000_33.19-20.1346.53
2021111620145409000_33.19-20.1346.52
2021111620145409000_33.19-20.1346.11
2021111620145409000_33.19-20.1346.55
2021111620145409000_33.19-20.1346.10
2021111620145409000_33.19-20.1346.54
2021111620145409000_33.19-20.1346.13
2021111620145409000_33.19-20.1346.57
2021111620145409000_33.19-20.1346.12
2021111620145409000_33.19-20.1346.56
2021111620145409000_33.19-20.1346.15
2021111620145409000_33.19-20.1346.59
2021111620145409000_33.19-20.1346.14
2021111620145409000_33.19-20.1346.58
2021111620145409000_33.19-20.1346.51
2021111620145409000_33.19-20.1346.50
2021111620145409000_33.19-20.1346.49
2021111620145409000_33.19-20.1346.42
2021111620145409000_33.19-20.1346.86
2021111620145409000_33.19-20.1346.41
2021111620145409000_33.19-20.1346.85
2021111620145409000_33.19-20.1346.44
2021111620145409000_33.19-20.1346.43
2021111620145409000_33.19-20.1346.46
2021111620145409000_33.19-20.1346.45
2021111620145409000_33.19-20.1346.48
2021111620145409000_33.19-20.1346.47
2021111620145409000_33.19-20.1346.80
2021111620145409000_33.19-20.1346.82
2021111620145409000_33.19-20.1346.81
2021111620145409000_33.19-20.1346.40
2021111620145409000_33.19-20.1346.84
2021111620145409000_33.19-20.1346.83
2021111620145409000_33.19-20.1346.39
2021111620145409000_33.19-20.1346.38
2021111620145409000_33.19-20.1346.31
2021111620145409000_33.19-20.1346.75
2021111620145409000_33.19-20.1346.30
2021111620145409000_33.19-20.1346.74
2021111620145409000_33.19-20.1346.33
2021111620145409000_33.19-20.1346.77
2021111620145409000_33.19-20.1346.32
2021111620145409000_33.19-20.1346.76
2021111620145409000_33.19-20.1346.35
2021111620145409000_33.19-20.1346.79
2021111620145409000_33.19-20.1346.34
2021111620145409000_33.19-20.1346.78
2021111620145409000_33.19-20.1346.37
2021111620145409000_33.19-20.1346.36
2021111620145409000_33.19-20.1346.71
2021111620145409000_33.19-20.1346.70
2021111620145409000_33.19-20.1346.73
2021111620145409000_33.19-20.1346.72
2021111620145409000_33.19-20.1346.28
2021111620145409000_33.19-20.1346.27
2021111620145409000_33.19-20.1346.29
2021111620145409000_33.19-20.1346.2
2021111620145409000_33.19-20.1346.20
2021111620145409000_33.19-20.1346.64
2021111620145409000_33.19-20.1346.1
2021111620145409000_33.19-20.1346.63
2021111620145409000_33.19-20.1346.22
2021111620145409000_33.19-20.1346.66
2021111620145409000_33.19-20.1346.21
2021111620145409000_33.19-20.1346.65
2021111620145409000_33.19-20.1346.24
2021111620145409000_33.19-20.1346.68
2021111620145409000_33.19-20.1346.23
2021111620145409000_33.19-20.1346.67
2021111620145409000_33.19-20.1346.26
2021111620145409000_33.19-20.1346.25
2021111620145409000_33.19-20.1346.69
2021111620145409000_33.19-20.1346.9
2021111620145409000_33.19-20.1346.8
2021111620145409000_33.19-20.1346.7
2021111620145409000_33.19-20.1346.6
2021111620145409000_33.19-20.1346.60
2021111620145409000_33.19-20.1346.5
2021111620145409000_33.19-20.1346.4
2021111620145409000_33.19-20.1346.62
2021111620145409000_33.19-20.1346.3
2021111620145409000_33.19-20.1346.61
References_xml – ident: 2021111620145409000_33.19-20.1346.4
  doi: 10.1101/gad.278275.116
– ident: 2021111620145409000_33.19-20.1346.43
  doi: 10.1038/nature08593
– ident: 2021111620145409000_33.19-20.1346.31
  doi: 10.1093/nar/gks484
– ident: 2021111620145409000_33.19-20.1346.75
  doi: 10.1098/rstb.2016.0282
– ident: 2021111620145409000_33.19-20.1346.49
  doi: 10.1016/j.molcel.2019.01.005
– ident: 2021111620145409000_33.19-20.1346.41
  doi: 10.1073/pnas.1303111110
– ident: 2021111620145409000_33.19-20.1346.54
  doi: 10.1038/sj.emboj.7601158
– ident: 2021111620145409000_33.19-20.1346.40
  doi: 10.1093/nar/gkp1008
– ident: 2021111620145409000_33.19-20.1346.25
  doi: 10.1038/nrm3478
– ident: 2021111620145409000_33.19-20.1346.64
  doi: 10.1016/j.molcel.2010.08.028
– ident: 2021111620145409000_33.19-20.1346.67
  doi: 10.1128/JVI.01273-12
– ident: 2021111620145409000_33.19-20.1346.78
  doi: 10.1016/j.molcel.2017.04.017
– ident: 2021111620145409000_33.19-20.1346.74
  doi: 10.1038/s41467-018-07364-x
– ident: 2021111620145409000_33.19-20.1346.58
  doi: 10.1371/journal.pgen.1000858
– ident: 2021111620145409000_33.19-20.1346.53
  doi: 10.1007/s00412-017-0658-1
– ident: 2021111620145409000_33.19-20.1346.37
  doi: 10.1038/emboj.2013.24
– ident: 2021111620145409000_33.19-20.1346.51
  doi: 10.1371/journal.pgen.1007942
– ident: 2021111620145409000_33.19-20.1346.59
  doi: 10.1016/j.tibs.2015.02.006
– ident: 2021111620145409000_33.19-20.1346.21
  doi: 10.1016/j.molcel.2014.11.014
– ident: 2021111620145409000_33.19-20.1346.19
  doi: 10.15252/embr.201440017
– ident: 2021111620145409000_33.19-20.1346.6
  doi: 10.1016/j.celrep.2016.06.015
– ident: 2021111620145409000_33.19-20.1346.15
  doi: 10.1016/j.molcel.2015.01.022
– ident: 2021111620145409000_33.19-20.1346.82
  doi: 10.1101/gad.238535.114
– ident: 2021111620145409000_33.19-20.1346.84
  doi: 10.1074/mcp.O114.044792
– ident: 2021111620145409000_33.19-20.1346.69
  doi: 10.1038/s41467-017-00183-6
– ident: 2021111620145409000_33.19-20.1346.73
  doi: 10.1534/genetics.114.166140
– ident: 2021111620145409000_33.19-20.1346.17
  doi: 10.1038/nature08657
– ident: 2021111620145409000_33.19-20.1346.35
  doi: 10.1083/jcb.201010117
– ident: 2021111620145409000_33.19-20.1346.23
  doi: 10.1074/jbc.M512757200
– ident: 2021111620145409000_33.19-20.1346.12
  doi: 10.1074/jbc.RA118.006006
– ident: 2021111620145409000_33.19-20.1346.47
  doi: 10.1016/j.molcel.2005.06.001
– ident: 2021111620145409000_33.19-20.1346.20
  doi: 10.1080/10409238.2018.1488803
– ident: 2021111620145409000_33.19-20.1346.7
  doi: 10.1016/j.cell.2006.08.050
– ident: 2021111620145409000_33.19-20.1346.34
  doi: 10.1093/nar/gks270
– ident: 2021111620145409000_33.19-20.1346.79
  doi: 10.1016/j.molcel.2012.02.017
– ident: 2021111620145409000_33.19-20.1346.80
  doi: 10.1101/sqb.2015.80.027649
– ident: 2021111620145409000_33.19-20.1346.33
  doi: 10.1534/genetics.116.196568
– ident: 2021111620145409000_33.19-20.1346.9
  doi: 10.1093/nar/gkv1523
– ident: 2021111620145409000_33.19-20.1346.85
  doi: 10.1371/journal.pone.0051540
– ident: 2021111620145409000_33.19-20.1346.65
  doi: 10.1242/jcs.133744
– ident: 2021111620145409000_33.19-20.1346.1
  doi: 10.1093/nar/gkq195
– ident: 2021111620145409000_33.19-20.1346.70
  doi: 10.1038/nature01965
– ident: 2021111620145409000_33.19-20.1346.62
  doi: 10.1038/nrm.2016.58
– ident: 2021111620145409000_33.19-20.1346.48
  doi: 10.1038/nature03665
– ident: 2021111620145409000_33.19-20.1346.3
  doi: 10.1038/ncb2729
– ident: 2021111620145409000_33.19-20.1346.10
  doi: 10.1101/gad.265058.115
– ident: 2021111620145409000_33.19-20.1346.71
  doi: 10.1038/nature19071
– ident: 2021111620145409000_33.19-20.1346.44
  doi: 10.3390/biom6010014
– ident: 2021111620145409000_33.19-20.1346.83
  doi: 10.1038/sj.emboj.7600394
– ident: 2021111620145409000_33.19-20.1346.2
  doi: 10.1371/journal.pone.0214102
– ident: 2021111620145409000_33.19-20.1346.42
  doi: 10.1016/j.molcel.2011.11.010
– ident: 2021111620145409000_33.19-20.1346.76
  doi: 10.1038/ncb1619
– ident: 2021111620145409000_33.19-20.1346.32
  doi: 10.1074/jbc.M115.685891
– ident: 2021111620145409000_33.19-20.1346.26
  doi: 10.1038/nature00991
– ident: 2021111620145409000_33.19-20.1346.60
  doi: 10.1016/j.celrep.2014.08.054
– ident: 2021111620145409000_33.19-20.1346.39
  doi: 10.7554/eLife.22195
– ident: 2021111620145409000_33.19-20.1346.55
  doi: 10.1074/jbc.M009476200
– ident: 2021111620145409000_33.19-20.1346.8
  doi: 10.1038/emboj.2013.9
– ident: 2021111620145409000_33.19-20.1346.66
  doi: 10.1016/j.dnarep.2016.04.001
– ident: 2021111620145409000_33.19-20.1346.27
  doi: 10.1080/15384101.2017.1302628
– ident: 2021111620145409000_33.19-20.1346.29
  doi: 10.1146/annurev.biochem.73.011303.074118
– ident: 2021111620145409000_33.19-20.1346.38
  doi: 10.1016/j.celrep.2016.05.007
– ident: 2021111620145409000_33.19-20.1346.57
  doi: 10.1074/jbc.M100006200
– ident: 2021111620145409000_33.19-20.1346.63
  doi: 10.1016/j.gde.2016.10.005
– ident: 2021111620145409000_33.19-20.1346.16
  doi: 10.1146/annurev-biochem-061909-093311
– ident: 2021111620145409000_33.19-20.1346.77
  doi: 10.1101/gad.265629.115
– ident: 2021111620145409000_33.19-20.1346.72
  doi: 10.3109/10409238.2016.1172552
– ident: 2021111620145409000_33.19-20.1346.11
  doi: 10.1016/j.molcel.2011.11.028
– ident: 2021111620145409000_33.19-20.1346.13
  doi: 10.1016/j.molcel.2010.07.021
– ident: 2021111620145409000_33.19-20.1346.14
  doi: 10.1371/journal.pgen.1003833
– ident: 2021111620145409000_33.19-20.1346.56
  doi: 10.1038/ncb1488
– ident: 2021111620145409000_33.19-20.1346.86
  doi: 10.1073/pnas.0500537102
– ident: 2021111620145409000_33.19-20.1346.28
  doi: 10.1093/hmg/ddp478
– ident: 2021111620145409000_33.19-20.1346.46
  doi: 10.1016/j.molcel.2014.11.015
– ident: 2021111620145409000_33.19-20.1346.81
  doi: 10.1016/j.ceb.2016.02.018
– ident: 2021111620145409000_33.19-20.1346.50
  doi: 10.1515/bmc-2016-0030
– ident: 2021111620145409000_33.19-20.1346.18
  doi: 10.1098/rstb.2016.0281
– ident: 2021111620145409000_33.19-20.1346.5
  doi: 10.1080/15384101.2015.1060381
– ident: 2021111620145409000_33.19-20.1346.45
  doi: 10.3389/fgene.2013.00167
– ident: 2021111620145409000_33.19-20.1346.30
  doi: 10.1371/journal.pone.0080442
– ident: 2021111620145409000_33.19-20.1346.22
  doi: 10.1146/annurev-genet-120215-035043
– ident: 2021111620145409000_33.19-20.1346.36
  doi: 10.1093/nar/gkn441
– ident: 2021111620145409000_33.19-20.1346.61
  doi: 10.1371/journal.pgen.1004899
– ident: 2021111620145409000_33.19-20.1346.52
  doi: 10.1016/j.cell.2012.10.021
– ident: 2021111620145409000_33.19-20.1346.68
  doi: 10.1073/pnas.0403498101
– ident: 2021111620145409000_33.19-20.1346.24
  doi: 10.1101/cshperspect.a016501
SSID ssj0006066
Score 2.3902998
SecondaryResourceType review_article
Snippet The homologous recombination (HR) machinery plays multiple roles in genome maintenance. Best studied in the context of DNA double-stranded break (DSB) repair,...
In this review, Dhingra et al. discuss the roles of SUMO in light of its newly identified effects on recombinational repair, and present further thoughts on...
SourceID pubmedcentral
proquest
pubmed
crossref
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage 1346
SubjectTerms Animals
Gene Expression Regulation - genetics
Homologous Recombination - genetics
Humans
Rad51 Recombinase - metabolism
Review
SUMO-1 Protein - metabolism
Sumoylation
Title Intricate SUMO-based control of the homologous recombination machinery
URI https://www.ncbi.nlm.nih.gov/pubmed/31575678
https://www.proquest.com/docview/2300178851
https://pubmed.ncbi.nlm.nih.gov/PMC6771382
Volume 33
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwELagCNQL4s3yUpCQOFQuSWzH8REVqhYocGilvUV-pa3UzVawPZRfz_gRJ9mCBL1EG6831vr7Mp4Zj2cQetMWqrSUK0xBnca0lgbXmhVYM9MaK2ojfLWGg6_V3hH9NGfzYSvGny5ZqW3964_nSq6DKrQBru6U7H8gmx4KDfAZ8IUrIAzXf8J4v1v5Kj92C4TjN-xWJJOCz-Pm_8ly4eSbi3R1xu8CLOGA-cKHUa4diXZZqH96Opghmigpu85b5esSgVB2JypHXmfvcZ2fSrCUu7EnoRApJi0G9CzPQMX17kR3gggouPUlENHt9o8jQrxwEjl2xQDDOhKFJxWY0ViWJUrXkOaiZ5HAZT4SlwWJ_kcbb0NC6ati3ZcTOJZmm5SgX1BoEeOOAMv5woNMCtA_q1AVaC2R9veDnYpzl3PxJrpVglXhCl582P-cFm5ny3mjI_61mOMTBn83HXoT3enHmaozV2yU9VDbke5yeA_djUZH9j4w6D66YbsH6HYoQ3r5EO0mHmUDj7LIo2zZZsCjbOBRNuFRlnj0CB3tfjzc2cOxvgbWhAMUSkjJa6KJqllVC1kxw6iiLJdEEdvCa6xrXpqWGUUKRVuuqdbGGFYX0tnh5DHa6JadfYoyKRmtcqtLLjW1tVbSSp6bvFXWSqrFDOF-mhodk8-7GihnjTdC86KBGW7CDMM99H-b-p-HtCt_7fm6n_UGJKPb7pKdhclowLiG5aYGk2KGngQU0rN6-GaIT_BJHVzW9ek33emJz74eOfTs2r98jjaHt-8F2lj9uLAvQbNdqVeej78BvzKmrw
linkProvider Flying Publisher
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=Intricate+SUMO-based+control+of+the+homologous+recombination+machinery&rft.jtitle=Genes+%26+development&rft.au=Dhingra%2C+Nalini&rft.au=Zhao%2C+Xiaolan&rft.date=2019-10-01&rft.pub=Cold+Spring+Harbor+Laboratory+Press&rft.issn=0890-9369&rft.eissn=1549-5477&rft.volume=33&rft.issue=19-20&rft.spage=1346&rft.epage=1354&rft_id=info:doi/10.1101%2Fgad.328534.119&rft_id=info%3Apmid%2F31575678&rft.externalDocID=PMC6771382
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0890-9369&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0890-9369&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0890-9369&client=summon