Kabuki syndrome stem cell models reveal locus specificity of histone methyltransferase 2D (KMT2D/MLL4).


Journal

Human molecular genetics
ISSN: 1460-2083
Titre abrégé: Hum Mol Genet
Pays: England
ID NLM: 9208958

Informations de publication

Date de publication:
28 10 2022
Historique:
received: 14 02 2022
revised: 07 05 2022
accepted: 18 05 2022
pubmed: 1 6 2022
medline: 2 11 2022
entrez: 31 5 2022
Statut: ppublish

Résumé

Kabuki syndrome is frequently caused by loss-of-function mutations in one allele of histone 3 lysine 4 (H3K4) methyltransferase KMT2D and is associated with problems in neurological, immunological and skeletal system development. We generated heterozygous KMT2D knockout and Kabuki patient-derived cell models to investigate the role of reduced dosage of KMT2D in stem cells. We discovered chromosomal locus-specific alterations in gene expression, specifically a 110 Kb region containing Synaptotagmin 3 (SYT3), C-Type Lectin Domain Containing 11A (CLEC11A), Chromosome 19 Open Reading Frame 81 (C19ORF81) and SH3 And Multiple Ankyrin Repeat Domains 1 (SHANK1), suggesting locus-specific targeting of KMT2D. Using whole genome histone methylation mapping, we confirmed locus-specific changes in H3K4 methylation patterning coincident with regional decreases in gene expression in Kabuki cell models. Significantly reduced H3K4 peaks aligned with regions of stem cell maps of H3K27 and H3K4 methylation suggesting KMT2D haploinsufficiency impact bivalent enhancers in stem cells. Preparing the genome for subsequent differentiation cues may be of significant importance for Kabuki-related genes. This work provides a new insight into the mechanism of action of an important gene in bone and brain development and may increase our understanding of a specific function of a human disease-relevant H3K4 methyltransferase family member.

Identifiants

pubmed: 35640156
pii: 6594512
doi: 10.1093/hmg/ddac121
pmc: PMC9616574
doi:

Substances chimiques

Histone-Lysine N-Methyltransferase EC 2.1.1.43
Histones 0
MLL4 protein, human EC 2.1.1.43
KMT2D protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3715-3728

Subventions

Organisme : NCI NIH HHS
ID : P01 CA196539
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS111997
Pays : United States

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.

Références

Mol Cell Biol. 2013 Dec;33(23):4745-54
pubmed: 24081332
Nat Protoc. 2012 Sep;7(9):1728-40
pubmed: 22936215
Nature. 2021 Sep;597(7878):726-731
pubmed: 34526716
Mol Cell. 2017 Jul 20;67(2):308-321.e6
pubmed: 28732206
Annu Rev Biochem. 2012;81:65-95
pubmed: 22663077
Hum Mutat. 2014 Jul;35(7):841-50
pubmed: 24633898
Wiley Interdiscip Rev RNA. 2020 Jan;11(1):e1560
pubmed: 31359616
Genome Biol. 2009;10(3):R25
pubmed: 19261174
Am J Med Genet A. 2020 May;182(5):1053-1065
pubmed: 32083401
Methods Enzymol. 2016;574:3-29
pubmed: 27423855
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Genome Res. 2012 Sep;22(9):1813-31
pubmed: 22955991
Proc Natl Acad Sci U S A. 2016 Oct 18;113(42):11871-11876
pubmed: 27698142
Biochem Soc Trans. 2021 Jun 30;49(3):1041-1054
pubmed: 34156443
Trends Mol Med. 2021 Dec;27(12):1106-1114
pubmed: 34690045
Nat Protoc. 2012 Mar 01;7(3):562-78
pubmed: 22383036
Proc Natl Acad Sci U S A. 2009 May 26;106(21):8513-8
pubmed: 19433796
Nat Biotechnol. 2020 Mar;38(3):276-278
pubmed: 32055031
JCI Insight. 2019 Oct 17;4(20):
pubmed: 31465303
Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):12902-7
pubmed: 11687631
Nature. 2016 Feb 25;530(7591):447-52
pubmed: 26886794
Gene. 2017 Sep 5;627:337-342
pubmed: 28669924
Nat Rev Cancer. 2015 Jun;15(6):334-46
pubmed: 25998713
Cell. 2006 Apr 21;125(2):315-26
pubmed: 16630819
Nat Rev Genet. 2012 Mar 06;13(4):246-59
pubmed: 22392217
Am J Med Genet. 1988 Nov;31(3):565-89
pubmed: 3067577
Stem Cells Transl Med. 2017 Mar;6(3):886-896
pubmed: 28170165
Nat Rev Mol Cell Biol. 2011 Nov 23;12(12):799-814
pubmed: 22108599
Am J Med Genet A. 2020 Mar;182(3):441-445
pubmed: 31846209
Elife. 2013 Dec 24;2:e01503
pubmed: 24368734
Genet Med. 2020 May;22(5):867-877
pubmed: 31949313
Nat Genet. 2010 Sep;42(9):790-3
pubmed: 20711175
Mol Cell. 2007 Aug 17;27(4):573-84
pubmed: 17707229
Genetics. 2019 Mar;211(3):831-845
pubmed: 30593494
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Cell. 2015 Mar 12;160(6):1049-59
pubmed: 25768903
J Vis Exp. 2016 May 17;(111):
pubmed: 27286567
Nature. 2010 Sep 16;467(7313):285-90
pubmed: 20644535
Elife. 2016 Dec 13;5:
pubmed: 27976999
Mol Cell. 2011 Sep 16;43(6):950-61
pubmed: 21925383
Am J Hum Genet. 2012 May 4;90(5):879-87
pubmed: 22503632
Cold Spring Harb Perspect Med. 2016 Nov 1;6(11):
pubmed: 27638352
J Hum Genet. 2019 Feb;64(2):161-170
pubmed: 30459467
Nat Genet. 2004 Aug;36(8):801-8
pubmed: 15284851
Science. 2001 Feb 16;291(5507):1289-92
pubmed: 11181992
Am J Med Genet A. 2013 Sep;161A(9):2234-43
pubmed: 23913813

Auteurs

Malvin Jefri (M)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Xin Zhang (X)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Patrick S Stumpf (PS)

Institute for Computational Biomedicine, RWTH Aachen University, Aachen 52056, Germany.

Li Zhang (L)

McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.

Huashan Peng (H)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Nuwan Hettige (N)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Jean-Francois Theroux (JF)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Zahia Aouabed (Z)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Khadija Wilson (K)

Department of Biochemistry and Molecular, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA.

Shriya Deshmukh (S)

Division of Experimental Medicine, Department of Medicine, McGill University, Montreal, QC H4A 3J1, Canada.

Lilit Antonyan (L)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Anjie Ni (A)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Shaima Alsuwaidi (S)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Ying Zhang (Y)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.

Nada Jabado (N)

Division of Experimental Medicine, Department of Medicine, McGill University, Montreal, QC H4A 3J1, Canada.
Department of Human Genetics, McGill University, Montreal, QC H3A 0C7, Canada.
Department of Pediatrics, McGill University and The Research Institute of the McGill University Health Centre, Montreal, QC H4A 3J1, Canada.

Benjamin A Garcia (BA)

Department of Biochemistry and Molecular, Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA.

Andreas Schuppert (A)

Institute for Computational Biomedicine, RWTH Aachen University, Aachen 52056, Germany.

Hans T Bjornsson (HT)

McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
Department of Genetics and Molecular Medicine, Landspitali University Hospital, 101 Reykjavik, Iceland.

Carl Ernst (C)

Psychiatric Genetics Group, McGill University, 6875 LaSalle Boulevard, Frank Common Building, Room 2101.2, Verdun, Montreal, QC H4H 1R3, Canada.
Department of Psychiatry, McGill University and Douglas Hospital Research Institute, Montreal, QC H4H 1R3, Canada.
Department of Human Genetics, McGill University, Montreal, QC H3A 0C7, Canada.

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