Combinatorial effects on gene expression at the Lbx1/Fgf8 locus resolve split-hand/foot malformation type 3.


Journal

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

Informations de publication

Date de publication:
17 03 2023
Historique:
received: 21 03 2022
accepted: 01 03 2023
entrez: 17 3 2023
pubmed: 18 3 2023
medline: 22 3 2023
Statut: epublish

Résumé

Split-Hand/Foot Malformation type 3 (SHFM3) is a congenital limb malformation associated with tandem duplications at the LBX1/FGF8 locus. Yet, the disease patho-mechanism remains unsolved. Here we investigate the functional consequences of SHFM3-associated rearrangements on chromatin conformation and gene expression in vivo in transgenic mice. We show that the Lbx1/Fgf8 locus consists of two separate, but interacting, regulatory domains. Re-engineering of a SHFM3-associated duplication and a newly reported inversion in mice results in restructuring of the chromatin architecture. This leads to ectopic activation of the Lbx1 and Btrc genes in the apical ectodermal ridge (AER) in an Fgf8-like pattern induced by AER-specific enhancers of Fgf8. We provide evidence that the SHFM3 phenotype is the result of a combinatorial effect on gene misexpression in the developing limb. Our results reveal insights into the molecular mechanism underlying SHFM3 and provide conceptual framework for how genomic rearrangements can cause gene misexpression and disease.

Identifiants

pubmed: 36928426
doi: 10.1038/s41467-023-37057-z
pii: 10.1038/s41467-023-37057-z
pmc: PMC10020157
doi:

Substances chimiques

Fgf8 protein, mouse 0
Fibroblast Growth Factor 8 148997-75-5
Homeodomain Proteins 0
Lbx1h protein, mouse 0
Transcription Factors 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1475

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2023. The Author(s).

Références

Development. 2002 Aug;129(16):3957-64
pubmed: 12135932
Methods. 2020 Jan 1;170:17-32
pubmed: 31351925
BMC Bioinformatics. 2013 Apr 15;14:128
pubmed: 23586463
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nature. 2021 Apr;592(7852):93-98
pubmed: 33568816
Mamm Genome. 2008 Apr;19(4):272-8
pubmed: 18392654
Cell Rep. 2015 Feb 10;10(5):833-839
pubmed: 25660031
Int J Dev Biol. 2002;46(7):877-81
pubmed: 12455624
Clin Genet. 2019 Jan;95(1):132-139
pubmed: 30101460
Nat Genet. 2000 Dec;26(4):455-9
pubmed: 11101845
Eur J Hum Genet. 2019 Apr;27(4):525-534
pubmed: 30622331
Nature. 2003 Nov 6;426(6962):87-91
pubmed: 14603323
Orphanet J Rare Dis. 2014 Jul 29;9:108
pubmed: 25231166
Am J Med Genet A. 2006 Jul 1;140(13):1419-27
pubmed: 16688749
Clin Genet. 2022 Nov;102(5):451-456
pubmed: 35908152
Methods Mol Biol. 2011;693:37-56
pubmed: 21080273
J Med Genet. 2012 Feb;49(2):119-25
pubmed: 22147889
Cell. 2014 Dec 18;159(7):1665-80
pubmed: 25497547
Cold Spring Harb Perspect Biol. 2022 May 27;14(5):
pubmed: 34312246
Cell Syst. 2016 Jul;3(1):95-8
pubmed: 27467249
Curr Top Dev Biol. 2020;139:61-88
pubmed: 32450969
EMBO Rep. 2005 Jul;6 Spec No:S39-44
pubmed: 15995660
Nat Rev Genet. 2016 Oct 14;17(11):661-678
pubmed: 27739532
Nature. 2016 Oct 13;538(7624):265-269
pubmed: 27706140
Cell Rep. 2016 May 31;15(9):2038-49
pubmed: 27210764
Nat Genet. 2017 Jan;49(1):65-74
pubmed: 27869826
J Mol Biol. 2000 Aug 25;301(4):851-67
pubmed: 10966791
Cell. 2015 May 21;161(5):1012-1025
pubmed: 25959774
Genome Biol. 2019 Dec 23;20(1):296
pubmed: 31870423
Curr Opin Genet Dev. 2001 Aug;11(4):440-8
pubmed: 11448631
Dev Cell. 2013 Mar 11;24(5):530-42
pubmed: 23453598
Genesis. 2018 Jun;56(6-7):e23221
pubmed: 30134070
Nat Genet. 2019 Aug;51(8):1272-1282
pubmed: 31308546
Nucleic Acids Res. 2018 Jan 4;46(D1):D794-D801
pubmed: 29126249
Nat Genet. 2000 Dec;26(4):460-3
pubmed: 11101846
Nat Biotechnol. 2018 Jun;36(5):411-420
pubmed: 29608179
Nature. 2012 Sep 6;489(7414):57-74
pubmed: 22955616
Am J Med Genet A. 2006 Jul 1;140(13):1384-95
pubmed: 16691619
Development. 2000 Jan;127(2):413-24
pubmed: 10603357
PLoS One. 2013 May 02;8(5):e63610
pubmed: 23658844
Am J Respir Cell Mol Biol. 2004 Apr;30(4):428-34
pubmed: 14630615
BMC Bioinformatics. 2018 Sep 6;19(1):313
pubmed: 30189838
Cell Syst. 2019 Apr 24;8(4):281-291.e9
pubmed: 30954476
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
J Appl Genet. 2014 Feb;55(1):105-15
pubmed: 24163146
Cell. 1989 Jul 28;58(2):337-47
pubmed: 2568891
Hum Genet. 2005 Dec;118(3-4):477-83
pubmed: 16235095
Hum Mol Genet. 2003 Apr 1;12 Spec No 1:R51-60
pubmed: 12668597
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Nat Rev Genet. 2018 Jul;19(7):453-467
pubmed: 29692413
Nature. 2019 Feb;566(7745):496-502
pubmed: 30787437
Nat Commun. 2021 Jan 19;12(1):439
pubmed: 33469032
Nat Commun. 2022 Oct 29;13(1):6470
pubmed: 36309531
N Engl J Med. 2015 Jan 22;372(4):341-50
pubmed: 25564734
Mol Cell. 2003 Jun;11(6):1445-56
pubmed: 12820959
Hum Mol Genet. 2003 Aug 15;12(16):1959-71
pubmed: 12913067
Nat Genet. 2019 Aug;51(8):1263-1271
pubmed: 31358994
F1000Res. 2015 Nov 20;4:1310
pubmed: 26835000
Genome Biol. 2015 Dec 01;16:259
pubmed: 26619908
Am J Med Genet A. 2013 Nov;161A(11):2860-72
pubmed: 24115638
Genes Dev. 1999 Mar 1;13(5):505-10
pubmed: 10072378
Dev Biol. 2017 Sep 15;429(2):387-390
pubmed: 28131856

Auteurs

Giulia Cova (G)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany. giulia.cova@nyulangone.org.
Institute of Medical and Human Genetics, Charité Universitätsmedizin Berlin, Berlin, 10117, Germany. giulia.cova@nyulangone.org.
Department of Pathology, New York University School of Medicine, Langone Health Medical Center, New York, NY, 10016, USA. giulia.cova@nyulangone.org.

Juliane Glaser (J)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.

Robert Schöpflin (R)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.
Institute of Medical and Human Genetics, Charité Universitätsmedizin Berlin, Berlin, 10117, Germany.
Department of Computational Molecular Biology, Max Planck Institute for Molecular Genetics, Berlin, 14195, Germany.

Cesar Augusto Prada-Medina (CA)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.
Kennedy Institute of Rheumatology, University of Oxford, Oxford, OX3 7FY, UK.

Salaheddine Ali (S)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.
Institute of Medical and Human Genetics, Charité Universitätsmedizin Berlin, Berlin, 10117, Germany.

Martin Franke (M)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.
Institute of Medical and Human Genetics, Charité Universitätsmedizin Berlin, Berlin, 10117, Germany.
Centro Andaluz de Biología del Desarrollo, Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide, Seville, 41013, Spain.

Rita Falcone (R)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.

Miriam Federer (M)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany.
Universität Innsbruck, Innsbruck, 6020, Austria.

Emanuela Ponzi (E)

Medical Genetics Unit, Department of Reproductive Medicine, ASL Bari, Bari, 70131, Italy.

Romina Ficarella (R)

Medical Genetics Unit, Department of Reproductive Medicine, ASL Bari, Bari, 70131, Italy.

Francesca Novara (F)

Microgenomics Laboratory, Pavia, 27100, Italy.

Lars Wittler (L)

Department of Developmental Genetics, Transgenic Unit, Max Planck Institute for Molecular Genetics, Berlin, 14195, Germany.

Bernd Timmermann (B)

Sequencing Core Facility, Max Planck Institute for Molecular Genetics, Berlin, 14195, Germany.

Mattia Gentile (M)

Medical Genetics Unit, Department of Reproductive Medicine, ASL Bari, Bari, 70131, Italy.

Orsetta Zuffardi (O)

Department of Molecular Medicine, University of Pavia, Pavia, 27100, Italy.

Malte Spielmann (M)

Institute of Human Genetics, Universitätsklinikum Schleswig Holstein Campus Kiel and Christian-Albrechts-Universität, Kiel, 24118, Germany.
Institute of Human Genetics, University of Lübeck, Lübeck, Germany.
Human Molecular Genomics Group, Max Planck Institute for Molecular Genetics, Berlin, 14195, Germany.

Stefan Mundlos (S)

Max Planck Institute for Molecular Genetics, RG Development & Disease, Berlin, 14195, Germany. mundlos@molgen.mpg.de.
Institute of Medical and Human Genetics, Charité Universitätsmedizin Berlin, Berlin, 10117, Germany. mundlos@molgen.mpg.de.
Berlin-Brandenburg Center for Regenerative Therapies (BCRT), Charité Universitätsmedizin Berlin, Berlin, 13353, Germany. mundlos@molgen.mpg.de.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH