Release of Histone H3K4-reading transcription factors from chromosomes in mitosis is independent of adjacent H3 phosphorylation.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
09 11 2023
Historique:
received: 05 04 2023
accepted: 31 10 2023
medline: 13 11 2023
pubmed: 10 11 2023
entrez: 9 11 2023
Statut: epublish

Résumé

Histone modifications influence the recruitment of reader proteins to chromosomes to regulate events including transcription and cell division. The idea of a histone code, where combinations of modifications specify unique downstream functions, is widely accepted and can be demonstrated in vitro. For example, on synthetic peptides, phosphorylation of Histone H3 at threonine-3 (H3T3ph) prevents the binding of reader proteins that recognize trimethylation of the adjacent lysine-4 (H3K4me3), including the TAF3 component of TFIID. To study these combinatorial effects in cells, we analyzed the genome-wide distribution of H3T3ph and H3K4me2/3 during mitosis. We find that H3T3ph anti-correlates with adjacent H3K4me2/3 in cells, and that the PHD domain of TAF3 can bind H3K4me2/3 in isolated mitotic chromatin despite the presence of H3T3ph. Unlike in vitro, H3K4 readers are still displaced from chromosomes in mitosis in Haspin-depleted cells lacking H3T3ph. H3T3ph is therefore unlikely to be responsible for transcriptional downregulation during cell division.

Identifiants

pubmed: 37945563
doi: 10.1038/s41467-023-43115-3
pii: 10.1038/s41467-023-43115-3
pmc: PMC10636195
doi:

Substances chimiques

Histones 0
Transcription Factors 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

7243

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom

Informations de copyright

© 2023. The Author(s).

Références

Genome Res. 2015 Feb;25(2):213-25
pubmed: 25373146
Cell. 1991 Oct 18;67(2):303-10
pubmed: 1680567
PLoS One. 2013 Sep 11;8(9):e73495
pubmed: 24039962
Elife. 2016 Nov 19;5:
pubmed: 27855781
Elife. 2016 Feb 15;5:e10877
pubmed: 26880562
Cell. 2011 Sep 2;146(5):720-31
pubmed: 21884934
Proc Natl Acad Sci U S A. 2015 Jul 7;112(27):8487-92
pubmed: 26100864
Mol Cell. 2021 Apr 15;81(8):1732-1748.e8
pubmed: 33730542
Nat Commun. 2013;4:2537
pubmed: 24088984
Nature. 2019 Dec;576(7785):158-162
pubmed: 31776509
J Cell Biol. 2012 Oct 15;199(2):269-84
pubmed: 23071153
Science. 2018 Feb 9;359(6376):
pubmed: 29348367
EMBO J. 2005 Jan 26;24(2):347-57
pubmed: 15616580
Mol Cell. 2015 Aug 6;59(3):502-11
pubmed: 26212453
EMBO J. 2016 Jul 15;35(14):1565-81
pubmed: 27266525
Genes Dev. 2020 Jul 1;34(13-14):913-930
pubmed: 32499403
Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5
pubmed: 27079975
Nucleic Acids Res. 2019 Nov 4;47(19):10086-10103
pubmed: 31529049
Structure. 2017 Oct 3;25(10):1530-1539.e3
pubmed: 28919441
Nat Cell Biol. 2002 Jan;4(1):79-82
pubmed: 11744923
Sci Adv. 2017 Jun 21;3(6):e1700191
pubmed: 28691095
Bioinformatics. 2012 Jul 15;28(14):1919-20
pubmed: 22576172
Bioinformatics. 2017 Oct 01;33(19):3088-3090
pubmed: 28575171
Biochemistry. 2005 Oct 4;44(39):13202-13
pubmed: 16185088
Proc Natl Acad Sci U S A. 2007 Feb 20;104(8):2691-6
pubmed: 17299043
Ann N Y Acad Sci. 1960 Oct 7;90:409-21
pubmed: 13775619
Mol Cell Proteomics. 2015 Apr;14(4):1148-58
pubmed: 25680960
Genome Res. 2018 Oct;28(10):1455-1466
pubmed: 30166406
J Cell Sci. 2014 Dec 1;127(Pt 23):5066-78
pubmed: 25315835
Sci Rep. 2021 Oct 6;11(1):19901
pubmed: 34615946
Nucleic Acids Res. 2019 Jul 2;47(W1):W199-W205
pubmed: 31114916
Mol Reprod Dev. 2015 Jul-Aug;82(7-8):518-29
pubmed: 26153368
Mol Cell Proteomics. 2007 Nov;6(11):1917-32
pubmed: 17644761
Genes Dev. 2012 Apr 15;26(8):857-71
pubmed: 22508729
Stem Cell Reports. 2013 Oct 24;1(5):371-8
pubmed: 24286025
Nature. 2003 Oct 2;425(6957):475-9
pubmed: 14523437
Nature. 2005 Dec 22;438(7071):1116-22
pubmed: 16222246
Science. 2010 Oct 8;330(6001):235-9
pubmed: 20705815
Mol Plant. 2013 Mar;6(2):574-6
pubmed: 23220945
Bioorg Med Chem. 2011 Apr 1;19(7):2373-7
pubmed: 21397507
Cell Rep. 2017 May 16;19(7):1283-1293
pubmed: 28514649
Mol Cell Proteomics. 2014 Jul;13(7):1724-40
pubmed: 24732914
Int J Mol Sci. 2021 Jul 20;22(14):
pubmed: 34299370
Mol Cell. 2022 Feb 3;82(3):696-708.e4
pubmed: 35090599
Trends Biochem Sci. 2020 Apr;45(4):321-331
pubmed: 32001093
Science. 1982 Aug 13;217(4560):648-50
pubmed: 6283640
Mol Cell. 2018 Oct 4;72(1):162-177.e7
pubmed: 30244833
Genes Dev. 2016 Jun 15;30(12):1423-39
pubmed: 27340175
Nature. 2017 Jul 5;547(7661):61-67
pubmed: 28682332
J Cell Biol. 2012 Oct 15;199(2):251-68
pubmed: 23071152
Nat Commun. 2015 Jul 23;6:7815
pubmed: 26204128
Epigenetics Chromatin. 2020 Jan 24;13(1):3
pubmed: 31980037
Cell Rep. 2019 Apr 9;27(2):400-415.e5
pubmed: 30970245
Cell. 2013 Feb 28;152(5):1021-36
pubmed: 23452851
Nat Commun. 2018 Oct 2;9(1):4048
pubmed: 30279501
Genes Dev. 2008 Dec 15;22(24):3375-82
pubmed: 19141469
J Cell Biol. 1963 Nov;19:267-77
pubmed: 14086755
Cell Rep. 2013 Jul 11;4(1):148-58
pubmed: 23831028
Epigenetics Chromatin. 2016 Mar 22;9:11
pubmed: 27006701
Science. 2010 Oct 8;330(6001):239-43
pubmed: 20929775
Science. 2017 Oct 6;358(6359):119-122
pubmed: 28912132
Trends Cell Biol. 2013 Apr;23(4):175-84
pubmed: 23246430
Curr Biol. 2007 Apr 3;17(7):R233-6
pubmed: 17407749
Mol Cell. 2010 Sep 24;39(6):901-11
pubmed: 20864037
Nat Commun. 2019 Jan 30;10(1):487
pubmed: 30700703
Proteomics. 2004 May;4(5):1382-96
pubmed: 15188406
J Biol Chem. 2011 Jan 21;286(3):2236-44
pubmed: 20959462
Mol Cell. 2015 Jul 2;59(1):89-103
pubmed: 26073541
Science. 2010 Oct 8;330(6001):231-5
pubmed: 20705812
Trends Biochem Sci. 1997 Jun;22(6):197-202
pubmed: 9204705
Mol Cell. 2015 Nov 5;60(3):435-45
pubmed: 26527278
Nature. 2023 Mar;615(7951):339-348
pubmed: 36859550
Genome Biol. 2008;9(9):R137
pubmed: 18798982
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Nature. 2005 Dec 22;438(7071):1176-80
pubmed: 16222244
Nat Chem Biol. 2010 Apr;6(4):283-90
pubmed: 20190764
Nat Methods. 2012 Feb 28;9(3):215-6
pubmed: 22373907
Nat Struct Mol Biol. 2018 Dec;25(12):1119-1127
pubmed: 30510221
Nucleic Acids Res. 2016 Jul 27;44(13):6102-12
pubmed: 27016734
Oncogene. 2012 Mar 15;31(11):1408-18
pubmed: 21804608
Mol Biol Cell. 2009 Dec;20(23):4899-909
pubmed: 19812244
Science. 1991 Dec 20;254(5039):1814-6
pubmed: 1684878
Genome Res. 2019 Feb;29(2):236-249
pubmed: 30655336
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
J Biol Chem. 2005 Dec 30;280(52):42592-600
pubmed: 16199528
Cell. 2007 Oct 5;131(1):58-69
pubmed: 17884155
Sci Rep. 2022 Jul 1;12(1):11210
pubmed: 35778595
Mol Cell. 2013 Mar 7;49(5):773-82
pubmed: 23473598
Annu Rev Genomics Hum Genet. 2022 Aug 31;23:53-71
pubmed: 35440147
PLoS One. 2012;7(11):e50645
pubmed: 23226345
Epigenetics Chromatin. 2017 Mar 14;10:12
pubmed: 28293301
Science. 2010 Jan 8;327(5962):172-7
pubmed: 19965387
Proc Natl Acad Sci U S A. 2013 Jul 9;110(28):11296-301
pubmed: 23798402
PLoS Genet. 2020 Aug 4;16(8):e1008962
pubmed: 32750047
Curr Biol. 2017 Apr 3;27(7):992-1004
pubmed: 28343965
Genes Dev. 2005 Feb 15;19(4):472-88
pubmed: 15681610
Nature. 1997 Aug 28;388(6645):895-9
pubmed: 9278053
EMBO J. 2010 Dec 1;29(23):3967-78
pubmed: 20953165
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Genes Dev. 1996 Oct 1;10(19):2389-400
pubmed: 8843192
Nat Cell Biol. 2011 Oct 09;13(11):1295-304
pubmed: 21983563
Mol Cell Biol. 2007 Dec;27(24):8533-46
pubmed: 17938195
Cell. 1995 Oct 6;83(1):29-38
pubmed: 7553870
Anal Chem. 2013 Sep 3;85(17):8232-9
pubmed: 23889513
Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6486-91
pubmed: 18420823
Bioinformatics. 2010 Mar 15;26(6):841-2
pubmed: 20110278
Elife. 2022 Mar 16;11:
pubmed: 35293859
Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20198-203
pubmed: 19918057
Science. 2013 Nov 22;342(6161):948-53
pubmed: 24200812
Nat Commun. 2020 Aug 17;11(1):4118
pubmed: 32807789
Genome Res. 2019 Feb;29(2):250-260
pubmed: 30655337
J Cell Sci. 2009 Aug 15;122(Pt 16):2809-19
pubmed: 19622635
Mol Cell. 2013 Sep 12;51(5):647-61
pubmed: 24034696
Bioinformatics. 2015 Jun 15;31(12):2032-4
pubmed: 25697820

Auteurs

Rebecca J Harris (RJ)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Maninder Heer (M)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Mark D Levasseur (MD)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Tyrell N Cartwright (TN)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Bethany Weston (B)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Jennifer L Mitchell (JL)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Jonathan M Coxhead (JM)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Luke Gaughan (L)

Translational and Clinical Research Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.
Newcastle University Centre for Cancer, Faculty of Medical Sciences, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Lisa Prendergast (L)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK.

Daniel Rico (D)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK. daniel.rico@cabimer.es.
Newcastle University Centre for Cancer, Faculty of Medical Sciences, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK. daniel.rico@cabimer.es.
Centro Andaluz de Biología Molecular y Medicina Regenerativa (CABIMER), CSIC-Universidad Sevilla-Universidad Pablo de Olavide-Junta de Andalucía, 41092, Seville, Spain. daniel.rico@cabimer.es.

Jonathan M G Higgins (JMG)

Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK. jonathan.higgins@ncl.ac.uk.
Newcastle University Centre for Cancer, Faculty of Medical Sciences, Framlington Place, Newcastle Upon Tyne, NE2 1HH, UK. jonathan.higgins@ncl.ac.uk.

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Classifications MeSH