CHD1 controls H3.3 incorporation in adult brain chromatin to maintain metabolic homeostasis and normal lifespan.
Animals
Animals, Genetically Modified
/ metabolism
Brain
/ metabolism
Cell Cycle Proteins
/ genetics
Chromatin
/ chemistry
Chromatin Assembly and Disassembly
DNA-Binding Proteins
/ deficiency
Drosophila Proteins
/ deficiency
Drosophila melanogaster
/ metabolism
Feeding Behavior
Female
Histone Chaperones
/ genetics
Histones
/ analysis
Longevity
Male
Metabolome
/ physiology
Signal Transduction
TOR Serine-Threonine Kinases
/ metabolism
Transcription Factors
/ deficiency
aging
calorie restriction
chronic inflammation
epigenetics
feeding behavior
heterochromatin
histone chaperone
longevity
metabolic disease
metabolome
quantitative proteomics
Journal
Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691
Informations de publication
Date de publication:
05 10 2021
05 10 2021
Historique:
received:
30
09
2020
revised:
26
07
2021
accepted:
08
09
2021
entrez:
5
10
2021
pubmed:
6
10
2021
medline:
17
2
2022
Statut:
ppublish
Résumé
The ATP-dependent chromatin remodeling factor CHD1 is essential for the assembly of variant histone H3.3 into paternal chromatin during sperm chromatin remodeling in fertilized eggs. It remains unclear, however, if CHD1 has a similar role in normal diploid cells. Using a specifically tailored quantitative mass spectrometry approach, we show that Chd1 disruption results in reduced H3.3 levels in heads of Chd1 mutant flies. Chd1 deletion perturbs brain chromatin structure in a similar way as H3.3 deletion and leads to global de-repression of transcription. The physiological consequences are reduced food intake, metabolic alterations, and shortened lifespan. Notably, brain-specific CHD1 expression rescues these phenotypes. We further demonstrate a strong genetic interaction between Chd1 and H3.3 chaperone Hira. Thus, our findings establish CHD1 as a factor required for the assembly of H3.3-containing chromatin in adult cells and suggest a crucial role for CHD1 in the brain as a regulator of organismal health and longevity.
Identifiants
pubmed: 34610319
pii: S2211-1247(21)01223-7
doi: 10.1016/j.celrep.2021.109769
pmc: PMC8607513
mid: NIHMS1746301
pii:
doi:
Substances chimiques
CHD1 protein, Drosophila
0
Cell Cycle Proteins
0
Chromatin
0
DNA-Binding Proteins
0
Drosophila Proteins
0
Hira protein, Drosophila
0
Histone Chaperones
0
Histones
0
Transcription Factors
0
target of rapamycin protein, Drosophila
EC 2.7.1.-
TOR Serine-Threonine Kinases
EC 2.7.11.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
109769Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM074233
Pays : United States
Informations de copyright
Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
PLoS Genet. 2013;9(2):e1003285
pubmed: 23408912
Elife. 2013 Aug 20;2:e00863
pubmed: 23986862
Mol Cell. 2011 Aug 19;43(4):638-48
pubmed: 21855802
Nat Methods. 2014 May;11(5):535-40
pubmed: 24681694
Curr Protoc Mol Biol. 2002 May;Chapter 21:Unit 21.7
pubmed: 18265309
Mol Cell. 2017 Oct 5;68(1):76-88.e6
pubmed: 28943314
Geriatr Gerontol Int. 2010 Jan;10(1):110-2
pubmed: 20102391
Nature. 2016 Feb 4;530(7588):113-6
pubmed: 26814966
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Nature. 2005 Oct 27;437(7063):1386-90
pubmed: 16251970
Genes Dev. 2010 Jun 15;24(12):1253-65
pubmed: 20504901
Genes Dev. 2011 Oct 15;25(20):2198-209
pubmed: 21979373
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Curr Biol. 2010 Jun 8;20(11):1000-5
pubmed: 20471268
Mol Cell. 2002 Dec;10(6):1441-52
pubmed: 12504018
J Biol Chem. 2004 Dec 3;279(49):50781-9
pubmed: 15385546
Sci Rep. 2019 May 24;9(1):7824
pubmed: 31127145
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
PLoS One. 2016 Apr 19;11(4):e0153476
pubmed: 27093431
Anal Chem. 2015 Oct 20;87(20):10222-9
pubmed: 26398777
Genome Biol. 2014;15(12):550
pubmed: 25516281
Epigenetics Chromatin. 2018 Jan 12;11(1):2
pubmed: 29329550
J Chromatogr. 1984 Dec 7;336(1):93-104
pubmed: 6396315
Development. 2015 Jan 1;142(1):118-27
pubmed: 25480920
Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15635-40
pubmed: 17893337
Bioinformatics. 2019 Jun 1;35(12):2084-2092
pubmed: 30395178
Cell. 2015 Mar 26;161(1):106-118
pubmed: 25815989
Nat Biotechnol. 2020 Mar;38(3):276-278
pubmed: 32055031
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7663-8
pubmed: 15136717
Annu Rev Biochem. 2009;78:273-304
pubmed: 19355820
Genetics. 2010 Feb;184(2):321-34
pubmed: 19948887
Elife. 2014 Apr 15;3:e02042
pubmed: 24737864
Mol Cell. 2017 Jan 19;65(2):272-284
pubmed: 28107649
Biol Reprod. 2016 Jun;94(6):140
pubmed: 27170440
Mol Cell Proteomics. 2012 Jun;11(6):O111.016717
pubmed: 22261725
PLoS Genet. 2008 Oct;4(10):e1000217
pubmed: 18846226
Cell. 2008 Jul 11;134(1):74-84
pubmed: 18614012
Cell Mol Life Sci. 2018 Jan;75(1):93-101
pubmed: 29026921
Science. 2001 Apr 6;292(5514):107-10
pubmed: 11292875
PLoS Genet. 2012;8(7):e1002811
pubmed: 22807688
EMBO Rep. 2012 Nov 6;13(11):997-1003
pubmed: 23032292
Genes Dev. 2012 May 1;26(9):914-9
pubmed: 22549955
Nature. 2009 Aug 13;460(7257):863-8
pubmed: 19587682
J Biol Chem. 2010 May 14;285(20):15027-15037
pubmed: 20154359
F1000Res. 2015 Dec 30;4:1521
pubmed: 26925227
Elife. 2016 Dec 29;5:
pubmed: 28032848
Genes Dev. 2015 Dec 15;29(24):2563-75
pubmed: 26680301
EMBO J. 2003 Apr 15;22(8):1846-56
pubmed: 12682017
Proc Natl Acad Sci U S A. 2019 Jun 4;116(23):11235-11240
pubmed: 31110016
Aging (Albany NY). 2020 Jan 6;12(1):690-706
pubmed: 31907335
Dev Biol. 2000 Jun 15;222(2):392-404
pubmed: 10837127
Proc Natl Acad Sci U S A. 2018 Apr 17;115(16):4158-4163
pubmed: 29618609
Nat Struct Mol Biol. 2012 Sep;19(9):884-92
pubmed: 22922743
Nat Rev Mol Cell Biol. 2020 Sep;21(9):522-541
pubmed: 32665685
Nat Rev Mol Cell Biol. 2010 Apr;11(4):264-75
pubmed: 20197778
Nat Methods. 2013 Dec;10(12):1213-8
pubmed: 24097267
J Biol Chem. 2006 Jun 16;281(24):16279-88
pubmed: 16606615
Open Biol. 2019 Mar 29;9(3):180259
pubmed: 30914005
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Mol Cell. 2010 May 28;38(4):576-89
pubmed: 20513432
Epigenetics Chromatin. 2015 Jan 15;8(1):4
pubmed: 25621013
Proc Natl Acad Sci U S A. 2012 Dec 26;109(52):21528-33
pubmed: 23236133
Nat Struct Mol Biol. 2005 Feb;12(2):160-6
pubmed: 15643425
Nucleic Acids Res. 2017 Jul 7;45(12):7180-7190
pubmed: 28460001
Dev Comp Immunol. 2019 May;94:22-34
pubmed: 30684503
Integr Biol (Camb). 2017 Nov 13;9(11):885-891
pubmed: 29043354
Cell Rep. 2017 Mar 21;18(12):2957-2968
pubmed: 28329687
Science. 2007 Aug 24;317(5841):1087-90
pubmed: 17717186
PLoS One. 2012;7(8):e43144
pubmed: 22912810
Cell. 2018 Aug 9;174(4):982-998.e20
pubmed: 29909982
Cell Rep. 2015 Oct 13;13(2):350-64
pubmed: 26440885
Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1525-30
pubmed: 14732680
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91
pubmed: 24799436
Curr Biol. 2009 Jul 28;19(14):1221-6
pubmed: 19523831
Nat Methods. 2004 Oct;1(1):19-26
pubmed: 15789029
Aging Cell. 2017 Dec;16(6):1219-1233
pubmed: 28971552
Annu Rev Genet. 2018 Nov 23;52:109-130
pubmed: 30183406
Mol Cell Proteomics. 2012 Nov;11(11):1475-88
pubmed: 22865924
Nat Methods. 2015 Feb;12(2):115-21
pubmed: 25633503
PLoS Genet. 2007 Oct;3(10):1991-2006
pubmed: 17967064
Nucleic Acids Res. 2011 Apr;39(8):3103-15
pubmed: 21177652
Nat Rev Endocrinol. 2018 Oct;14(10):576-590
pubmed: 30046148
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Cell Rep. 2013 Apr 25;3(4):1012-9
pubmed: 23602572
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Cell. 2010 Mar 5;140(5):678-91
pubmed: 20211137
Trends Biochem Sci. 2007 Apr;32(4):180-8
pubmed: 17412594
Aging (Albany NY). 2017 Mar 10;9(3):602-614
pubmed: 28284043
Mol Cell. 2007 Nov 30;28(4):665-76
pubmed: 18042460
Cancer Cell. 2019 Apr 15;35(4):603-617.e8
pubmed: 30930119
FEBS Lett. 2014 Nov 17;588(22):4250-7
pubmed: 24983497
Proc Natl Acad Sci U S A. 2005 Feb 22;102(8):3105-10
pubmed: 15708981
Prog Neurobiol. 2019 Aug;179:101607
pubmed: 30905728
Nat Protoc. 2007;2(6):1445-57
pubmed: 17545981
Dev Comp Immunol. 2014 Jan;42(1):102-10
pubmed: 23685204