Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
02 06 2023
02 06 2023
Historique:
received:
14
09
2022
accepted:
16
05
2023
medline:
5
6
2023
pubmed:
3
6
2023
entrez:
2
6
2023
Statut:
epublish
Résumé
In the mammalian DNA damage response, ADP-ribosylation signalling is of crucial importance to mark sites of DNA damage as well as recruit and regulate repairs factors. Specifically, the PARP1:HPF1 complex recognises damaged DNA and catalyses the formation of serine-linked ADP-ribosylation marks (mono-Ser-ADPr), which are extended into ADP-ribose polymers (poly-Ser-ADPr) by PARP1 alone. Poly-Ser-ADPr is reversed by PARG, while the terminal mono-Ser-ADPr is removed by ARH3. Despite its significance and apparent evolutionary conservation, little is known about ADP-ribosylation signalling in non-mammalian Animalia. The presence of HPF1, but absence of ARH3, in some insect genomes, including Drosophila species, raises questions regarding the existence and reversal of serine-ADP-ribosylation in these species. Here we show by quantitative proteomics that Ser-ADPr is the major form of ADP-ribosylation in the DNA damage response of Drosophila melanogaster and is dependent on the dParp1:dHpf1 complex. Moreover, our structural and biochemical investigations uncover the mechanism of mono-Ser-ADPr removal by Drosophila Parg. Collectively, our data reveal PARP:HPF1-mediated Ser-ADPr as a defining feature of the DDR in Animalia. The striking conservation within this kingdom suggests that organisms that carry only a core set of ADP-ribosyl metabolising enzymes, such as Drosophila, are valuable model organisms to study the physiological role of Ser-ADPr signalling.
Identifiants
pubmed: 37268618
doi: 10.1038/s41467-023-38793-y
pii: 10.1038/s41467-023-38793-y
pmc: PMC10238386
doi:
Substances chimiques
Serine
452VLY9402
Poly Adenosine Diphosphate Ribose
26656-46-2
Adenosine Diphosphate Ribose
20762-30-5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3200Subventions
Organisme : Medical Research Council
ID : MR/V033417/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 210634/Z/18/Z
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/R007195/1
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C35050/A22284
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 210634
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 101794
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s).
Références
Science. 2003 Jan 24;299(5606):560-2
pubmed: 12543974
Methods Mol Biol. 2011;780:209-26
pubmed: 21870263
Cell Rep. 2018 Aug 14;24(7):1916-1929.e5
pubmed: 30110646
Acta Crystallogr D Biol Crystallogr. 2006 Sep;62(Pt 9):1002-11
pubmed: 16929101
Nat Methods. 2009 Nov;6(11):786-7
pubmed: 19876014
Cell Rep. 2018 Aug 28;24(9):2493-2505.e4
pubmed: 30157440
Biochem J. 1999 Sep 1;342 ( Pt 2):249-68
pubmed: 10455009
DNA Repair (Amst). 2015 Jun;30:68-79
pubmed: 25800440
Elife. 2018 Feb 26;7:
pubmed: 29480802
DNA Repair (Amst). 2014 Nov;23:4-16
pubmed: 24865146
Biochem J. 2015 Jun 1;468(2):293-301
pubmed: 25789582
Nat Commun. 2021 Oct 8;12(1):5893
pubmed: 34625544
Cell Death Dis. 2021 Jun 25;12(7):651
pubmed: 34172715
Nat Commun. 2012 Jun 06;3:878
pubmed: 22673905
Nucleic Acids Res. 2022 Jul 5;50(W1):W216-W221
pubmed: 35325185
Mol Cell. 2011 Jan 7;41(1):46-55
pubmed: 21211722
Cell Mol Life Sci. 2020 Jan;77(1):19-33
pubmed: 31754726
J Proteome Res. 2014 Aug 1;13(8):3510-22
pubmed: 24920161
J Biol Chem. 1997 May 2;272(18):11895-901
pubmed: 9115250
Mol Cell Proteomics. 2019 May;18(5):1010-1026
pubmed: 30798302
PLoS One. 2012;7(12):e50889
pubmed: 23251397
Nat Commun. 2021 Jul 1;12(1):4055
pubmed: 34210965
J Biol Chem. 1995 Feb 17;270(7):3247-54
pubmed: 7852410
Elife. 2021 Jan 21;10:
pubmed: 33475084
Biochem Soc Trans. 1980 Apr;8(2):215-27
pubmed: 6768625
Cell Rep. 2020 Sep 22;32(12):108176
pubmed: 32966781
Mol Cell. 2021 Jun 17;81(12):2640-2655.e8
pubmed: 34019811
Nat Chem Biol. 2016 Dec;12(12):998-1000
pubmed: 27723750
Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55
pubmed: 15299926
Mol Cell. 2021 Nov 18;81(22):4591-4604.e8
pubmed: 34592134
Nat Commun. 2021 Jul 28;12(1):4581
pubmed: 34321462
Comput Struct Biotechnol J. 2021 Apr 17;19:2366-2383
pubmed: 34025930
Mol Biol Evol. 2008 Jul;25(7):1307-20
pubmed: 18367465
Methods Mol Biol. 2023;2609:111-132
pubmed: 36515833
Front Cell Dev Biol. 2021 Nov 15;9:745922
pubmed: 34869334
J Am Chem Soc. 2015 Mar 18;137(10):3558-64
pubmed: 25706250
Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):82-6
pubmed: 14676324
Nature. 2020 Sep;585(7826):609-613
pubmed: 32939087
Nat Commun. 2016 Sep 30;7:12917
pubmed: 27686526
Ann Oncol. 2019 Sep 1;30(9):1437-1447
pubmed: 31218365
PLoS One. 2014 Jan 21;9(1):e86010
pubmed: 24465839
Front Biosci (Landmark Ed). 2020 Jan 1;25(1):118-133
pubmed: 31585880
Semin Cell Dev Biol. 2017 Mar;63:92-101
pubmed: 27670719
Nat Biotechnol. 2008 Dec;26(12):1367-72
pubmed: 19029910
Org Lett. 2018 Jul 6;20(13):4140-4143
pubmed: 29947522
Genetics. 2006 Jan;172(1):363-71
pubmed: 16219773
Nat Commun. 2020 Jul 7;11(1):3391
pubmed: 32636369
EMBO J. 2013 May 2;32(9):1225-37
pubmed: 23481255
Nucleic Acids Res. 2017 Aug 21;45(14):8129-8141
pubmed: 28854736
Am J Hum Genet. 2018 Sep 6;103(3):431-439
pubmed: 30100084
Genes Dev. 2002 Aug 15;16(16):2108-19
pubmed: 12183365
Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6406-11
pubmed: 20371698
Nat Commun. 2021 Feb 15;12(1):1028
pubmed: 33589610
Genes Dev. 2020 Mar 1;34(5-6):302-320
pubmed: 32029452
Genes Dev. 2020 Mar 1;34(5-6):263-284
pubmed: 32029451
EMBO Rep. 2018 Aug;19(8):
pubmed: 29954836
Sci Rep. 2020 Dec 3;10(1):21151
pubmed: 33273587
PLoS Genet. 2015 Jan 08;11(1):e1004936
pubmed: 25569773
J Biol Chem. 2007 Nov 2;282(44):32511-9
pubmed: 17827147
Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32
pubmed: 15572765
Bioinformatics. 2009 May 1;25(9):1189-91
pubmed: 19151095
Nature. 2020 Mar;579(7800):598-602
pubmed: 32028527
Cell Death Dis. 2016 Mar 31;7:e2166
pubmed: 27031963
Cells. 2021 Oct 28;10(11):
pubmed: 34831150
Cell Res. 2019 Mar;29(3):233-247
pubmed: 30728452
Biol Open. 2017 Feb 15;6(2):141-147
pubmed: 28011627
Nat Methods. 2013 Oct;10(10):981-4
pubmed: 23955771
Cell. 2004 Dec 17;119(6):803-14
pubmed: 15607977
Mol Cell. 2017 Mar 2;65(5):932-940.e6
pubmed: 28190768
DNA Repair (Amst). 2007 Mar 1;6(3):329-43
pubmed: 17188026
Mol Biol Evol. 2021 Jun 25;38(7):3022-3027
pubmed: 33892491
Acta Crystallogr D Biol Crystallogr. 2004 Mar;60(Pt 3):432-8
pubmed: 14993666
Nat Commun. 2014 Jul 21;5:4426
pubmed: 25043379
Proc Natl Acad Sci U S A. 2019 May 14;116(20):9941-9946
pubmed: 31028139
DNA Repair (Amst). 2016 Dec;48:8-16
pubmed: 27793508
Gene. 2013 Sep 10;526(2):187-94
pubmed: 23711619
Elife. 2017 Jun 26;6:
pubmed: 28650317
Life Sci Alliance. 2021 Sep 3;4(11):
pubmed: 34479984
Nature. 2011 Sep 04;477(7366):616-20
pubmed: 21892188
Chem Rev. 2018 Feb 14;118(3):1092-1136
pubmed: 29172462
Nat Struct Mol Biol. 2023 May;30(5):678-691
pubmed: 37106138
Nucleic Acids Res. 2022 Jan 7;50(D1):D543-D552
pubmed: 34723319
Nat Methods. 2006 Oct;3(10):833-8
pubmed: 16964256
Nat Methods. 2016 Sep;13(9):731-40
pubmed: 27348712
Am J Hum Genet. 2018 Nov 1;103(5):817-825
pubmed: 30401461
Acta Crystallogr Sect F Struct Biol Cryst Commun. 2006 Mar 1;62(Pt 3):224-7
pubmed: 16511307
Nucleic Acids Res. 2009 Jun;37(11):3501-13
pubmed: 19346337
Mol Cell. 2016 May 5;62(3):432-442
pubmed: 27067600
Cell Rep. 2018 Sep 25;24(13):3488-3502.e5
pubmed: 30257210
Curr Opin Genet Dev. 2021 Dec;71:106-113
pubmed: 34340015
Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):470-8
pubmed: 20383000
Chemistry. 2021 Jul 21;27(41):10621-10627
pubmed: 33769608
ACS Chem Biol. 2016 Nov 18;11(11):3179-3190
pubmed: 27689388
Exp Cell Res. 2009 May 1;315(8):1403-14
pubmed: 19150446
Bioinformatics. 2010 Aug 1;26(15):1899-900
pubmed: 20427515
Acta Crystallogr D Biol Crystallogr. 2013 Jul;69(Pt 7):1260-73
pubmed: 23793152