The molecular basis of heterochromatin assembly and epigenetic inheritance.


Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
01 06 2023
Historique:
received: 26 10 2022
revised: 10 04 2023
accepted: 20 04 2023
pmc-release: 01 06 2024
medline: 5 6 2023
pubmed: 20 5 2023
entrez: 19 5 2023
Statut: ppublish

Résumé

Heterochromatin plays a fundamental role in gene regulation, genome integrity, and silencing of repetitive DNA elements. Histone modifications are essential for the establishment of heterochromatin domains, which is initiated by the recruitment of histone-modifying enzymes to nucleation sites. This leads to the deposition of histone H3 lysine-9 methylation (H3K9me), which provides the foundation for building high-concentration territories of heterochromatin proteins and the spread of heterochromatin across extended domains. Moreover, heterochromatin can be epigenetically inherited during cell division in a self-templating manner. This involves a "read-write" mechanism where pre-existing modified histones, such as tri-methylated H3K9 (H3K9me3), support chromatin association of the histone methyltransferase to promote further deposition of H3K9me. Recent studies suggest that a critical density of H3K9me3 and its associated factors is necessary for the propagation of heterochromatin domains across multiple generations. In this review, I discuss the key experiments that have highlighted the importance of modified histones for epigenetic inheritance.

Identifiants

pubmed: 37207657
pii: S1097-2765(23)00291-5
doi: 10.1016/j.molcel.2023.04.020
pmc: PMC10309086
mid: NIHMS1896593
pii:
doi:

Substances chimiques

Histones 0
Heterochromatin 0
Schizosaccharomyces pombe Proteins 0
Histone-Lysine N-Methyltransferase EC 2.1.1.43

Types de publication

Journal Article Review Research Support, N.I.H., Intramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1767-1785

Subventions

Organisme : Intramural NIH HHS
ID : Z01 BC010523
Pays : United States
Organisme : Intramural NIH HHS
ID : Z99 CA999999
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA BC010523
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA BC011208
Pays : United States

Informations de copyright

Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests The author is a member of the Molecular Cell advisory board.

Références

Cell. 2004 Dec 17;119(6):789-802
pubmed: 15607976
Mol Cell Biol. 2005 Mar;25(6):2331-46
pubmed: 15743828
Mol Cell. 2005 Oct 28;20(2):173-85
pubmed: 16246721
Nat Cell Biol. 2021 Mar;23(3):243-256
pubmed: 33574613
Science. 2017 Apr 7;356(6333):
pubmed: 28302795
Cell. 2007 Feb 9;128(3):491-504
pubmed: 17289569
Cell. 2007 Feb 23;128(4):693-705
pubmed: 17320507
EMBO J. 2000 Apr 3;19(7):1587-97
pubmed: 10747027
Mol Cell. 2021 Oct 7;81(19):3979-3991.e4
pubmed: 34375584
Curr Biol. 2008 Apr 8;18(7):490-5
pubmed: 18394897
Nat Rev Genet. 2021 Jun;22(6):379-392
pubmed: 33500558
Science. 2015 Apr 3;348(6230):132-5
pubmed: 25838386
G3 (Bethesda). 2018 Feb 2;8(2):477-489
pubmed: 29187422
Genes Cells. 2013 Apr;18(4):327-39
pubmed: 23388053
Genetics. 1997 Mar;145(3):685-96
pubmed: 9055078
Nature. 2007 Dec 6;450(7171):908-12
pubmed: 17994007
Nature. 2020 Sep;585(7825):453-458
pubmed: 32908306
EMBO J. 2002 Mar 1;21(5):1121-31
pubmed: 11867540
Chromosome Res. 2012 Jul;20(5):521-34
pubmed: 22733402
EMBO J. 2004 Oct 1;23(19):3825-35
pubmed: 15372076
Nat Rev Mol Cell Biol. 2015 Sep;16(9):519-32
pubmed: 26296162
EMBO J. 2011 Mar 16;30(6):1027-39
pubmed: 21317872
Nature. 2018 Jun;558(7711):615-619
pubmed: 29925950
Trends Genet. 2023 Jun;39(6):505-519
pubmed: 36894374
Mol Cell. 2013 Jul 11;51(1):80-91
pubmed: 23849629
Elife. 2018 Jul 18;7:
pubmed: 30020075
Proc Natl Acad Sci U S A. 2009 Jun 2;106(22):8998-9003
pubmed: 19443688
Mol Cell. 2009 Apr 10;34(1):36-46
pubmed: 19362535
Trends Genet. 2021 Jun;37(6):547-565
pubmed: 33494958
Science. 2002 Sep 27;297(5590):2232-7
pubmed: 12215653
Cell. 2000 Apr 28;101(3):307-17
pubmed: 10847685
Nature. 1998 May 28;393(6683):386-9
pubmed: 9620804
Science. 2004 Jun 25;304(5679):1971-6
pubmed: 15218150
Cold Spring Harb Perspect Biol. 2013 Aug 01;5(8):a017780
pubmed: 23906716
Nature. 2017 Jul 13;547(7662):241-245
pubmed: 28636597
Cell. 2020 Jan 23;180(2):263-277.e20
pubmed: 31955845
Nat Rev Mol Cell Biol. 2022 Mar;23(3):185-203
pubmed: 34707241
Mol Cell Biol. 2002 Apr;22(7):2170-81
pubmed: 11884604
Nature. 2018 Aug;560(7719):504-508
pubmed: 30051891
Nature. 2001 Mar 1;410(6824):116-20
pubmed: 11242053
Cell Rep. 2021 Aug 17;36(7):109540
pubmed: 34407404
Nat Genet. 2004 Nov;36(11):1174-80
pubmed: 15475954
Science. 2001 Aug 10;293(5532):1074-80
pubmed: 11498575
Science. 2017 Apr 7;356(6333):88-91
pubmed: 28302794
Curr Opin Genet Dev. 2020 Apr;61:53-61
pubmed: 32403014
Mol Cell. 2020 Apr 16;78(2):236-249.e7
pubmed: 32101700
Science. 2001 Apr 6;292(5514):110-3
pubmed: 11283354
Nat Genet. 1999 Dec;23(4):457-61
pubmed: 10581035
Open Biol. 2012 Mar;2(3):120014
pubmed: 22645662
Genes Dev. 2005 Oct 1;19(19):2301-6
pubmed: 16204182
Nat Struct Mol Biol. 2011 Sep 04;18(10):1132-8
pubmed: 21892171
Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):11258-63
pubmed: 22733737
Nature. 2015 May 14;521(7551):232-6
pubmed: 25915022
RNA Biol. 2005 Jul-Sep;2(3):106-11
pubmed: 17114925
Nat Commun. 2021 Jun 8;12(1):3456
pubmed: 34103492
Science. 2010 Jan 1;327(5961):94-7
pubmed: 19965720
Nature. 2001 Nov 15;414(6861):277-83
pubmed: 11713521
Biochim Biophys Acta. 2014 Aug;1839(8):728-36
pubmed: 24583555
Science. 2002 Sep 13;297(5588):1833-7
pubmed: 12193640
Nature. 2017 Jul 13;547(7662):236-240
pubmed: 28636604
Nat Rev Genet. 2005 Jan;6(1):24-35
pubmed: 15630419
Science. 2003 Jan 31;299(5607):719-21
pubmed: 12560554
Curr Biol. 2003 Jul 15;13(14):1192-200
pubmed: 12867029
Science. 2008 Oct 24;322(5901):602-6
pubmed: 18948543
Nat Struct Mol Biol. 2013 May;20(5):547-54
pubmed: 23604080
EMBO J. 2022 Apr 4;41(7):e108677
pubmed: 35199868
Mol Cell. 2019 Jan 3;73(1):61-72.e3
pubmed: 30472189
Cell. 2014 Nov 6;159(4):884-95
pubmed: 25417163
Nat Genet. 2021 Dec;53(12):1686-1697
pubmed: 34782763
Annu Rev Cell Dev Biol. 2018 Oct 6;34:265-288
pubmed: 30044650
Cold Spring Harb Perspect Biol. 2013 Sep 01;5(9):
pubmed: 24003213
Nat Rev Mol Cell Biol. 2021 Oct;22(10):653-670
pubmed: 34341548
Nature. 2002 Apr 4;416(6880):556-60
pubmed: 11898023
Nat Genet. 2003 Jun;34(2):187-92
pubmed: 12740577
Nat Cell Biol. 2021 Aug;23(8):905-914
pubmed: 34354237
Nature. 2011 Mar 24;471(7339):527-31
pubmed: 21430782
Nature. 2015 Apr 9;520(7546):248-252
pubmed: 25807481
Genome Res. 2015 Jun;25(6):872-83
pubmed: 25778913
Cell. 2012 Sep 14;150(6):1147-57
pubmed: 22980978
Science. 2017 Apr 7;356(6333):85-88
pubmed: 28302792
Nat Commun. 2021 Jul 16;12(1):4359
pubmed: 34272378
Nat Commun. 2016 Apr 19;7:11310
pubmed: 27090491
Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6159-64
pubmed: 22474355
J Biol Chem. 2019 Feb 1;294(5):1451-1463
pubmed: 30514760
Nat Genet. 2013 Jan;45(1):34-42
pubmed: 23202127
Cell. 1996 Jul 12;86(1):95-101
pubmed: 8689692
Mol Cell. 2017 Apr 6;66(1):50-62.e6
pubmed: 28318821
Genes Dev. 2016 Jan 15;30(2):133-48
pubmed: 26744419
Nat Struct Mol Biol. 2022 Sep;29(9):898-909
pubmed: 36064597
Proc Natl Acad Sci U S A. 2015 Dec 22;112(51):15548-55
pubmed: 26631744
Genetics. 2020 Jul;215(3):569-578
pubmed: 32357961
Elife. 2015 Mar 16;4:
pubmed: 25774602
Nat Cell Biol. 2020 Apr;22(4):361-371
pubmed: 32231312
Cell Rep. 2020 Dec 29;33(13):108561
pubmed: 33378674
EMBO Rep. 2015 Dec;16(12):1673-87
pubmed: 26518661
Trends Cell Biol. 2018 Feb;28(2):113-127
pubmed: 29103884
Cell. 2015 Jun 4;161(6):1453-67
pubmed: 26046444
Nature. 2008 Feb 7;451(7179):734-7
pubmed: 18216783
Cell. 2013 Mar 14;152(6):1308-23
pubmed: 23498939
Mol Cell. 2016 Mar 3;61(5):747-759
pubmed: 26942678
Genes Dev. 2001 Feb 15;15(4):428-43
pubmed: 11230151
Cell Rep. 2021 Nov 2;37(5):109944
pubmed: 34731638
Science. 2001 Aug 10;293(5532):1150-5
pubmed: 11498594
Mol Cell. 2013 Oct 24;52(2):173-83
pubmed: 24095277
Mol Cell. 2006 Jun 9;22(5):681-92
pubmed: 16762840
Science. 2001 Sep 28;293(5539):2453-5
pubmed: 11498546
Science. 2005 Jul 15;309(5733):467-9
pubmed: 15947136
Nat Rev Genet. 2020 May;21(5):311-331
pubmed: 32051563
Nat Commun. 2015 May 20;6:7050
pubmed: 25989903
Genes Dev. 2018 Jul 1;32(13-14):953-964
pubmed: 29967291
Cell. 2012 Nov 21;151(5):994-1004
pubmed: 23159369
Nature. 2001 Mar 1;410(6824):120-4
pubmed: 11242054
Nat Commun. 2020 May 15;11(1):2412
pubmed: 32415063
Epigenetics Chromatin. 2015 Jan 15;8:3
pubmed: 25788984
Science. 2010 May 28;328(5982):1161-4
pubmed: 20508129
Curr Biol. 2000 May 4;10(9):517-25
pubmed: 10801440
Mol Cell. 2018 Feb 1;69(3):385-397.e8
pubmed: 29336876
Cell. 2013 Feb 28;152(5):957-68
pubmed: 23415457
Nat Cell Biol. 2002 Jan;4(1):89-93
pubmed: 11780129
PLoS Genet. 2016 Feb 18;12(2):e1005873
pubmed: 26889830
Cell. 2020 Jan 9;180(1):150-164.e15
pubmed: 31883795
J Biol Chem. 2011 Mar 18;286(11):9308-20
pubmed: 21224386
EMBO J. 2009 Dec 16;28(24):3832-44
pubmed: 19942857
Nat Commun. 2016 May 11;7:11518
pubmed: 27167753
Nature. 2009 Oct 8;461(7265):762-7
pubmed: 19767730
Genetics. 2002 Jun;161(2):611-22
pubmed: 12072458
Proc Natl Acad Sci U S A. 2021 Jun 1;118(22):
pubmed: 34035174
Cell Rep. 2022 May 17;39(7):110828
pubmed: 35584672
Genes Dev. 2005 Jul 15;19(14):1705-14
pubmed: 16024659
Nat Rev Mol Cell Biol. 2004 Apr;5(4):296-304
pubmed: 15071554
Nat Struct Mol Biol. 2012 Oct;19(10):1023-30
pubmed: 22983563
Nature. 1998 Feb 19;391(6669):806-11
pubmed: 9486653
Genes Dev. 2011 Feb 1;25(3):214-9
pubmed: 21289066
Mol Cell. 2008 Dec 26;32(6):778-90
pubmed: 19111658
Genes Dev. 2016 Apr 1;30(7):827-39
pubmed: 26988418
Nature. 2021 May;593(7858):289-293
pubmed: 33854237
Science. 2002 Sep 13;297(5588):1831
pubmed: 12193644
Nature. 2000 Aug 10;406(6796):593-9
pubmed: 10949293
Nat Commun. 2022 Apr 6;13(1):1861
pubmed: 35387992
Nat Rev Genet. 2007 Jan;8(1):35-46
pubmed: 17173056
Trends Biochem Sci. 2018 Feb;43(2):136-148
pubmed: 29292063
Science. 2004 Jan 30;303(5658):672-6
pubmed: 14704433
Cell. 2015 Apr 9;161(2):404-16
pubmed: 25843628
Science. 2002 Mar 15;295(5562):2080-3
pubmed: 11859155
Elife. 2021 Sep 15;10:
pubmed: 34524082
Nat Struct Mol Biol. 2008 Apr;15(4):381-8
pubmed: 18345014
Mol Cell. 2016 Nov 3;64(3):520-533
pubmed: 27871484
Genes Dev. 2019 Jan 1;33(1-2):116-126
pubmed: 30573453
Cell. 2004 Nov 12;119(4):469-80
pubmed: 15537537
Proc Natl Acad Sci U S A. 2005 Jan 4;102(1):152-7
pubmed: 15615848
Science. 2015 Apr 3;348(6230):1258699
pubmed: 25831549
Cell. 2019 Oct 31;179(4):953-963.e11
pubmed: 31675501
Proc Natl Acad Sci U S A. 2019 Oct 8;116(41):20605-20611
pubmed: 31511420
J Biol Chem. 2014 Mar 7;289(10):6850-6861
pubmed: 24415761
Elife. 2020 Mar 20;9:
pubmed: 32195666
Science. 2012 Jan 6;335(6064):96-100
pubmed: 22144463
Science. 2001 Dec 21;294(5551):2539-42
pubmed: 11598266
Nat Commun. 2015 Jun 18;6:7313
pubmed: 26084584
Nat Cell Biol. 2005 Oct;7(10):1007-13
pubmed: 16127433
Trends Genet. 2017 Nov;33(11):871-881
pubmed: 28935117
Science. 2003 Aug 22;301(5636):1090-3
pubmed: 12934006
Curr Biol. 2005 Oct 25;15(20):1808-19
pubmed: 16243027
Trends Genet. 2016 Jan;32(1):29-41
pubmed: 26675384
Nat Cell Biol. 2018 May;20(5):620-631
pubmed: 29686265
EMBO Rep. 2019 Oct 4;20(10):e48111
pubmed: 31468675
Nature. 2010 Jan 14;463(7278):237-40
pubmed: 20075919
Elife. 2015 May 08;4:
pubmed: 25955967
Mol Cell Biol. 2004 Apr;24(8):3157-67
pubmed: 15060140
Cell. 2013 Nov 21;155(5):1061-74
pubmed: 24210919
Mol Cell. 2019 May 2;74(3):534-541.e4
pubmed: 30898439
Nat Struct Mol Biol. 2018 May;25(5):372-383
pubmed: 29686279
Mol Cell. 2016 Apr 21;62(2):207-221
pubmed: 27105116
Cell. 2021 Dec 9;184(25):6174-6192.e32
pubmed: 34813726
Nat Commun. 2020 Nov 5;11(1):5609
pubmed: 33154383
Cell. 2010 Mar 5;140(5):666-77
pubmed: 20211136
Nat Cell Biol. 2008 Nov;10(11):1291-300
pubmed: 18931660
Genes Dev. 2019 Jul 1;33(13-14):799-813
pubmed: 31171700
Cell. 2011 Jun 24;145(7):1049-61
pubmed: 21703449
Nat Genet. 2005 Aug;37(8):809-19
pubmed: 15976807
Cell Rep. 2019 Jul 2;28(1):267-281.e5
pubmed: 31269446
Genes Dev. 2016 Dec 1;30(23):2571-2580
pubmed: 27941123
Nature. 2014 Dec 18;516(7531):432-435
pubmed: 25307058
Nat Commun. 2022 Aug 24;13(1):4969
pubmed: 36002457
EMBO J. 1999 Apr 1;18(7):1923-38
pubmed: 10202156
Nature. 2006 Jul 6;442(7098):45-50
pubmed: 16823445
EMBO J. 2017 Sep 1;36(17):2626-2641
pubmed: 28765164
Nature. 2021 Mar;591(7849):317-321
pubmed: 33505026
Nat Struct Mol Biol. 2022 Aug;29(8):745-758
pubmed: 35879419
Science. 2007 Sep 21;317(5845):1760-4
pubmed: 17673620
Mol Cell Biol. 2003 Jun;23(12):4356-70
pubmed: 12773576
Cell Rep. 2020 Feb 25;30(8):2686-2698.e8
pubmed: 32101745
Cell. 2012 Jun 22;149(7):1447-60
pubmed: 22704655
Nat Chem Biol. 2016 Mar;12(3):188-93
pubmed: 26807716
Science. 2003 Jan 31;299(5607):721-5
pubmed: 12560555
Annu Rev Biochem. 2003;72:481-516
pubmed: 12676793
Genes Dev. 2012 Aug 15;26(16):1811-24
pubmed: 22895252
Oncogene. 2007 Aug 13;26(37):5433-8
pubmed: 17694084
Nat Commun. 2019 Jan 16;10(1):251
pubmed: 30651569
Mol Cell. 2022 Oct 6;82(19):3566-3579.e5
pubmed: 36041432
Nature. 2016 Sep 15;537(7620):369-373
pubmed: 27602518
Mol Cell. 2011 Jan 7;41(1):67-81
pubmed: 21211724
Open Biol. 2015 May;5(5):
pubmed: 25972440
EMBO J. 2001 Jun 1;20(11):2857-66
pubmed: 11387218
Curr Opin Genet Dev. 2019 Apr;55:1-10
pubmed: 31103921

Auteurs

Shiv I S Grewal (SIS)

Laboratory of Biochemistry and Molecular Biology, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA. Electronic address: grewals@mail.nih.gov.

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