Suleiman-El-Hattab syndrome: a histone modification disorder caused by TASP1 deficiency.


Journal

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

Informations de publication

Date de publication:
10 09 2022
Historique:
received: 04 01 2022
revised: 04 04 2022
accepted: 23 04 2022
pubmed: 6 5 2022
medline: 20 9 2022
entrez: 5 5 2022
Statut: ppublish

Résumé

TASP1 encodes an endopeptidase activating histone methyltransferases of the KMT2 family. Homozygous loss-of-function variants in TASP1 have recently been associated with Suleiman-El-Hattab syndrome. We report six individuals with Suleiman-El-Hattab syndrome and provide functional characterization of this novel histone modification disorder in a multi-omics approach. Chromosomal microarray/exome sequencing in all individuals. Western blotting from fibroblasts in two individuals. RNA sequencing and proteomics from fibroblasts in one individual. Methylome analysis from blood in two individuals. Knock-out of tasp1 orthologue in zebrafish and phenotyping. All individuals had biallelic TASP1 loss-of-function variants and a phenotype including developmental delay, multiple congenital anomalies (including cardiovascular and posterior fossa malformations), a distinct facial appearance and happy demeanor. Western blot revealed absence of TASP1. RNA sequencing/proteomics showed HOX gene downregulation (HOXA4, HOXA7, HOXA1 and HOXB2) and dysregulation of transcription factor TFIIA. A distinct methylation profile intermediate between control and Kabuki syndrome (KMT2D) profiles could be produced. Zebrafish tasp1 knock-out revealed smaller head size and abnormal cranial cartilage formation in tasp1 crispants. This work further delineates Suleiman-El-Hattab syndrome, a recognizable neurodevelopmental syndrome. Possible downstream mechanisms of TASP1 deficiency include perturbed HOX gene expression and dysregulated TFIIA complex. Methylation pattern suggests that Suleiman-El-Hattab syndrome can be categorized into the group of histone modification disorders including Wiedemann-Steiner and Kabuki syndrome.

Sections du résumé

BACKGROUND
TASP1 encodes an endopeptidase activating histone methyltransferases of the KMT2 family. Homozygous loss-of-function variants in TASP1 have recently been associated with Suleiman-El-Hattab syndrome. We report six individuals with Suleiman-El-Hattab syndrome and provide functional characterization of this novel histone modification disorder in a multi-omics approach.
METHODS
Chromosomal microarray/exome sequencing in all individuals. Western blotting from fibroblasts in two individuals. RNA sequencing and proteomics from fibroblasts in one individual. Methylome analysis from blood in two individuals. Knock-out of tasp1 orthologue in zebrafish and phenotyping.
RESULTS
All individuals had biallelic TASP1 loss-of-function variants and a phenotype including developmental delay, multiple congenital anomalies (including cardiovascular and posterior fossa malformations), a distinct facial appearance and happy demeanor. Western blot revealed absence of TASP1. RNA sequencing/proteomics showed HOX gene downregulation (HOXA4, HOXA7, HOXA1 and HOXB2) and dysregulation of transcription factor TFIIA. A distinct methylation profile intermediate between control and Kabuki syndrome (KMT2D) profiles could be produced. Zebrafish tasp1 knock-out revealed smaller head size and abnormal cranial cartilage formation in tasp1 crispants.
CONCLUSION
This work further delineates Suleiman-El-Hattab syndrome, a recognizable neurodevelopmental syndrome. Possible downstream mechanisms of TASP1 deficiency include perturbed HOX gene expression and dysregulated TFIIA complex. Methylation pattern suggests that Suleiman-El-Hattab syndrome can be categorized into the group of histone modification disorders including Wiedemann-Steiner and Kabuki syndrome.

Identifiants

pubmed: 35512351
pii: 6577269
doi: 10.1093/hmg/ddac098
pmc: PMC9476618
doi:

Substances chimiques

Transcription Factor TFIIA 0
Histone Methyltransferases EC 2.1.1.-
Endopeptidases EC 3.4.-

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

3083-3094

Subventions

Organisme : NEI NIH HHS
ID : R01 EY032976
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.

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Auteurs

Korbinian M Riedhammer (KM)

Institute of Human Genetics, Klinikum rechts der Isar, School of Medicine, Technical University of Munich, 81675 Munich, Germany.
Department of Nephrology, Klinikum rechts der Isar, School of Medicine, Technical University of Munich, 81675 Munich, Germany.

Anna L Burgemeister (AL)

Genetikum, Genetic Counseling and Diagnostics, 70173 Stuttgart, Germany.

Vincent Cantagrel (V)

Developmental Brain Disorders Laboratory, Université Paris Cité, Imagine Institute, INSERM UMR, 75015 Paris, France.

Jeanne Amiel (J)

Department of Genetics, AP-HP, Necker Enfants Malades Hospital, Université Paris Cité, Imagine Institute, 75015 Paris, France.

Karine Siquier-Pernet (K)

Developmental Brain Disorders Laboratory, Université Paris Cité, Imagine Institute, INSERM UMR, 75015 Paris, France.

Nathalie Boddaert (N)

Département de radiologie pédiatrique, INSERM UMR 1163 and INSERM U1000, AP-HP, Necker Enfants Malades Hospital, 75015 Paris, France.

Jozef Hertecant (J)

Division of Genetics and Metabolics, Department of Pediatrics, Tawam Hospital, Al Ain, United Arab Emirates.

Patricia L Kannouche (PL)

CNRS UMR 9019, Université Paris-Saclay, Equipe labellisée Ligue contre le Cancer, Gustave Roussy, 94805 Villejuif, France.

Caroline Pouvelle (C)

CNRS UMR 9019, Université Paris-Saclay, Equipe labellisée Ligue contre le Cancer, Gustave Roussy, 94805 Villejuif, France.

Stephanie Htun (S)

Department of Pediatrics, Division of Genetics, University of California, San Francisco, San Francisco, CA 94143, USA.

Anne M Slavotinek (AM)

Department of Pediatrics, Division of Genetics, University of California, San Francisco, San Francisco, CA 94143, USA.

Christian Beetz (C)

Centogene GmbH, 18055 Rostock, Germany.

Dan Diego-Alvarez (D)

Centogene GmbH, 18055 Rostock, Germany.

Kapil Kampe (K)

Centogene GmbH, 18055 Rostock, Germany.

Nicole Fleischer (N)

FDNA Inc., Boston, MA 02111, USA.

Zain Awamleh (Z)

Genetics and Genome Biology, Research Institute, The Hospital for Sick Children, Toronto, Ontario M5G 0A4, Canada.

Rosanna Weksberg (R)

Genetics and Genome Biology, Research Institute, The Hospital for Sick Children, Toronto, Ontario M5G 0A4, Canada.
Division of Clinical and Metabolic Genetics, The Hospital for Sick Children, Toronto, Ontario M5G 1X8, Canada.
Department of Molecular Genetics, Institute of Medical Sciences, University of Toronto, Toronto, Ontario M5S 1A1, Canada.

Robert Kopajtich (R)

Institute of Human Genetics, Klinikum rechts der Isar, School of Medicine, Technical University of Munich, 81675 Munich, Germany.
Institute of Neurogenomics, Helmholtz Zentrum München, 85764 Neuherberg, Germany.

Thomas Meitinger (T)

Institute of Human Genetics, Klinikum rechts der Isar, School of Medicine, Technical University of Munich, 81675 Munich, Germany.

Jehan Suleiman (J)

Division of Neurology, Department of Pediatrics, Tawam Hospital, Al Ain, United Arab Emirates.
Department of Pediatrics, College of Medicine and Health Sciences, United Arab Emirates University, Al Ain, United Arab Emirates.

Ayman W El-Hattab (AW)

Department of Clinical Sciences, College of Medicine, University of Sharjah, Sharjah, United Arab Emirates.
Pediatrics Department, University Hospital Sharjah, Sharjah, United Arab Emirates.
Genetics and Metabolic Department, KidsHeart Medical Center, Abu Dhabi, United Arab Emirates.

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