Polo-like kinase 1 (Plk1) regulates DNA replication origin firing and interacts with Rif1 in Xenopus.
Animals
Ataxia Telangiectasia Mutated Proteins
/ metabolism
Cell Cycle Proteins
/ metabolism
Checkpoint Kinase 1
/ metabolism
Chromatin
/ metabolism
DNA Replication
Protein Serine-Threonine Kinases
/ metabolism
Proteome
/ metabolism
Replication Origin
S Phase
/ genetics
Xenopus Proteins
/ metabolism
Xenopus laevis
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
27 09 2021
27 09 2021
Historique:
accepted:
20
08
2021
revised:
16
08
2021
received:
17
12
2020
pubmed:
2
9
2021
medline:
17
12
2021
entrez:
1
9
2021
Statut:
ppublish
Résumé
The activation of eukaryotic DNA replication origins needs to be strictly controlled at multiple steps in order to faithfully duplicate the genome and to maintain its stability. How the checkpoint recovery and adaptation protein Polo-like kinase 1 (Plk1) regulates the firing of replication origins during non-challenged S phase remained an open question. Using DNA fiber analysis, we show that immunodepletion of Plk1 in the Xenopus in vitro system decreases replication fork density and initiation frequency. Numerical analyses suggest that Plk1 reduces the overall probability and synchrony of origin firing. We used quantitative chromatin proteomics and co-immunoprecipitations to demonstrate that Plk1 interacts with firing factors MTBP/Treslin/TopBP1 as well as with Rif1, a known regulator of replication timing. Phosphopeptide analysis by LC/MS/MS shows that the C-terminal domain of Rif1, which is necessary for its repressive action on origins through protein phosphatase 1 (PP1), can be phosphorylated in vitro by Plk1 on S2058 in its PP1 binding site. The phosphomimetic S2058D mutant interrupts the Rif1-PP1 interaction and modulates DNA replication. Collectively, our study provides molecular insights into how Plk1 regulates the spatio-temporal replication program and suggests that Plk1 controls origin activation at the level of large chromatin domains in vertebrates.
Identifiants
pubmed: 34469577
pii: 6362107
doi: 10.1093/nar/gkab756
pmc: PMC8464078
doi:
Substances chimiques
Cell Cycle Proteins
0
Chromatin
0
Proteome
0
Rif1 protein, Xenopus
0
Xenopus Proteins
0
Atr protein, Xenopus
EC 2.7.1.-
Ataxia Telangiectasia Mutated Proteins
EC 2.7.11.1
Checkpoint Kinase 1
EC 2.7.11.1
Chek1 protein, Xenopus
EC 2.7.11.1
Plk1 protein, Xenopus
EC 2.7.11.1
Protein Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9851-9869Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Informations de copyright
© The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Sci Signal. 2011 Jun 28;4(179):rs5
pubmed: 21712546
EMBO J. 2001 Apr 17;20(8):2097-107
pubmed: 11296242
Genes (Basel). 2019 Jan 29;10(2):
pubmed: 30700024
Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):1919-24
pubmed: 18250300
J Cell Biol. 2011 Jun 13;193(6):995-1007
pubmed: 21646402
J Biol Chem. 2001 May 18;276(20):17092-100
pubmed: 11279043
Genes (Basel). 2021 Aug 09;12(8):
pubmed: 34440398
Science. 2003 Feb 21;299(5610):1228-31
pubmed: 12595692
Curr Opin Cell Biol. 2019 Jun;58:134-141
pubmed: 31200185
Cell Cycle. 2019 Jul;18(13):1458-1472
pubmed: 31130065
EMBO J. 2011 Nov 11;30(23):4805-14
pubmed: 22081107
PLoS Biol. 2018 May 10;16(5):e2005687
pubmed: 29746464
Cell Cycle. 2007 Nov 15;6(22):2760-7
pubmed: 17986860
J Cell Biol. 2016 Feb 1;212(3):281-8
pubmed: 26811421
Cold Spring Harb Perspect Biol. 2013 Aug 01;5(8):a010132
pubmed: 23838440
Nat Commun. 2016 Apr 07;7:11207
pubmed: 27052359
PLoS Comput Biol. 2011 Dec;7(12):e1002322
pubmed: 22219720
Sci Rep. 2017 May 18;7(1):2119
pubmed: 28522851
J Biol Chem. 2011 May 27;286(21):18602-13
pubmed: 21460226
J Cell Biol. 2001 Jan 8;152(1):15-25
pubmed: 11149917
Genome Biol. 2011 Aug 18;12(8):R78
pubmed: 21851590
Mol Cell Biol. 2006 Sep;26(18):6993-7004
pubmed: 16943439
J Biol Chem. 2004 Jul 2;279(27):28071-81
pubmed: 15123715
J Cell Sci. 2013 Mar 15;126(Pt 6):1297-306
pubmed: 23645160
Nat Rev Drug Discov. 2010 Aug;9(8):643-60
pubmed: 20671765
Proc Natl Acad Sci U S A. 2019 Jul 2;116(27):13374-13383
pubmed: 31209037
Curr Biol. 2011 Jul 12;21(13):1152-7
pubmed: 21700459
EMBO J. 2006 Apr 19;25(8):1753-63
pubmed: 16601689
Nat Cell Biol. 2004 Jul;6(7):648-55
pubmed: 15220931
Cell. 2004 May 28;117(5):575-88
pubmed: 15163406
Nat Commun. 2020 Mar 12;11(1):1345
pubmed: 32165637
EMBO J. 2008 Mar 19;27(6):876-85
pubmed: 18309293
EMBO J. 2009 Oct 7;28(19):2992-3004
pubmed: 19661920
EMBO J. 2010 Sep 15;29(18):3140-55
pubmed: 20711169
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Genes Dev. 2014 Feb 15;28(4):372-83
pubmed: 24532715
EMBO J. 2012 Sep 12;31(18):3667-77
pubmed: 22850674
EMBO J. 2011 May 18;30(10):2019-30
pubmed: 21487389
Eur J Cell Biol. 2007 Jan;86(1):37-50
pubmed: 17157410
Dev Cell. 2015 Nov 9;35(3):383-94
pubmed: 26555057
Nucleic Acids Res. 2019 Jan 8;47(D1):D506-D515
pubmed: 30395287
J Biol Chem. 2002 Sep 6;277(36):33049-57
pubmed: 12087101
Science. 2013 Aug 23;341(6148):893-6
pubmed: 23907533
PLoS One. 2015 Jun 05;10(6):e0129090
pubmed: 26046346
Cell Cycle. 2020 Jul;19(14):1817-1832
pubmed: 32573322
Cell. 1986 Nov 21;47(4):577-87
pubmed: 3779837
J Biol Chem. 2014 May 16;289(20):13903-11
pubmed: 24634216
Nucleic Acids Res. 2019 Jan 8;47(D1):D442-D450
pubmed: 30395289
Chromosome Res. 2010 Jan;18(1):35-43
pubmed: 20205352
Genes Dev. 2010 Jan 15;24(2):183-94
pubmed: 20080954
PLoS One. 2014 May 30;9(5):e98501
pubmed: 24879017
Mol Cell. 2016 Jan 21;61(2):260-73
pubmed: 26725008
Mol Biol Cell. 2017 Nov 1;28(22):2998-3012
pubmed: 28877985
Sci Signal. 2018 May 15;11(530):
pubmed: 29764992
Cell Rep. 2014 Apr 10;7(1):53-61
pubmed: 24656819
Open Biol. 2014 Jan 08;4:130138
pubmed: 24403013
Cell. 2010 Feb 5;140(3):349-59
pubmed: 20116089
Cell Rep. 2014 Apr 10;7(1):62-9
pubmed: 24685139
EMBO J. 2007 May 2;26(9):2262-73
pubmed: 17446864
Cell Rep. 2020 Sep 22;32(12):108178
pubmed: 32966791
EMBO J. 2012 Sep 12;31(18):3678-90
pubmed: 22850673
Cell Cycle. 2012 Mar 15;11(6):1183-94
pubmed: 22391207
Sci Rep. 2021 Feb 19;11(1):4242
pubmed: 33608586
Cell Rep. 2020 Sep 1;32(9):108096
pubmed: 32877678
Mol Cell. 2015 Feb 5;57(3):492-505
pubmed: 25557548
J Biol Chem. 2005 Mar 25;280(12):11943-7
pubmed: 15654075
EMBO J. 2010 Feb 17;29(4):806-18
pubmed: 20057355
Genes Dev. 2012 Jan 15;26(2):137-50
pubmed: 22279046
Nat Methods. 2016 Sep;13(9):731-40
pubmed: 27348712
EMBO J. 2007 Jun 6;26(11):2719-31
pubmed: 17491592
Nat Commun. 2021 May 18;12(1):2910
pubmed: 34006872
J Cell Biol. 2019 Sep 2;218(9):2865-2875
pubmed: 31366665
Science. 2015 May 1;348(6234):1253671
pubmed: 25931565
Cell. 2008 Sep 19;134(6):969-80
pubmed: 18805090
Methods Mol Biol. 2009;521:575-603
pubmed: 19563130
Cell Rep. 2017 Mar 7;18(10):2508-2520
pubmed: 28273463
Nucleic Acids Res. 2018 Jan 4;46(D1):D861-D868
pubmed: 29059324
Science. 2013 May 24;340(6135):981-4
pubmed: 23704573
EMBO Rep. 2017 Mar;18(3):403-419
pubmed: 28077461
Mol Cell Biol. 2011 Dec;31(23):4844-56
pubmed: 21947279