De novo and inherited TCF20 pathogenic variants are associated with intellectual disability, dysmorphic features, hypotonia, and neurological impairments with similarities to Smith-Magenis syndrome.


Journal

Genome medicine
ISSN: 1756-994X
Titre abrégé: Genome Med
Pays: England
ID NLM: 101475844

Informations de publication

Date de publication:
28 02 2019
Historique:
received: 27 10 2018
accepted: 15 02 2019
entrez: 2 3 2019
pubmed: 2 3 2019
medline: 14 6 2019
Statut: epublish

Résumé

Neurodevelopmental disorders are genetically and phenotypically heterogeneous encompassing developmental delay (DD), intellectual disability (ID), autism spectrum disorders (ASDs), structural brain abnormalities, and neurological manifestations with variants in a large number of genes (hundreds) associated. To date, a few de novo mutations potentially disrupting TCF20 function in patients with ID, ASD, and hypotonia have been reported. TCF20 encodes a transcriptional co-regulator structurally related to RAI1, the dosage-sensitive gene responsible for Smith-Magenis syndrome (deletion/haploinsufficiency) and Potocki-Lupski syndrome (duplication/triplosensitivity). Genome-wide analyses by exome sequencing (ES) and chromosomal microarray analysis (CMA) identified individuals with heterozygous, likely damaging, loss-of-function alleles in TCF20. We implemented further molecular and clinical analyses to determine the inheritance of the pathogenic variant alleles and studied the spectrum of phenotypes. We report 25 unique inactivating single nucleotide variants/indels (1 missense, 1 canonical splice-site variant, 18 frameshift, and 5 nonsense) and 4 deletions of TCF20. The pathogenic variants were detected in 32 patients and 4 affected parents from 31 unrelated families. Among cases with available parental samples, the variants were de novo in 20 instances and inherited from 4 symptomatic parents in 5, including in one set of monozygotic twins. Two pathogenic loss-of-function variants were recurrent in unrelated families. Patients presented with a phenotype characterized by developmental delay, intellectual disability, hypotonia, variable dysmorphic features, movement disorders, and sleep disturbances. TCF20 pathogenic variants are associated with a novel syndrome manifesting clinical characteristics similar to those observed in Smith-Magenis syndrome. Together with previously described cases, the clinical entity of TCF20-associated neurodevelopmental disorders (TAND) emerges from a genotype-driven perspective.

Sections du résumé

BACKGROUND
Neurodevelopmental disorders are genetically and phenotypically heterogeneous encompassing developmental delay (DD), intellectual disability (ID), autism spectrum disorders (ASDs), structural brain abnormalities, and neurological manifestations with variants in a large number of genes (hundreds) associated. To date, a few de novo mutations potentially disrupting TCF20 function in patients with ID, ASD, and hypotonia have been reported. TCF20 encodes a transcriptional co-regulator structurally related to RAI1, the dosage-sensitive gene responsible for Smith-Magenis syndrome (deletion/haploinsufficiency) and Potocki-Lupski syndrome (duplication/triplosensitivity).
METHODS
Genome-wide analyses by exome sequencing (ES) and chromosomal microarray analysis (CMA) identified individuals with heterozygous, likely damaging, loss-of-function alleles in TCF20. We implemented further molecular and clinical analyses to determine the inheritance of the pathogenic variant alleles and studied the spectrum of phenotypes.
RESULTS
We report 25 unique inactivating single nucleotide variants/indels (1 missense, 1 canonical splice-site variant, 18 frameshift, and 5 nonsense) and 4 deletions of TCF20. The pathogenic variants were detected in 32 patients and 4 affected parents from 31 unrelated families. Among cases with available parental samples, the variants were de novo in 20 instances and inherited from 4 symptomatic parents in 5, including in one set of monozygotic twins. Two pathogenic loss-of-function variants were recurrent in unrelated families. Patients presented with a phenotype characterized by developmental delay, intellectual disability, hypotonia, variable dysmorphic features, movement disorders, and sleep disturbances.
CONCLUSIONS
TCF20 pathogenic variants are associated with a novel syndrome manifesting clinical characteristics similar to those observed in Smith-Magenis syndrome. Together with previously described cases, the clinical entity of TCF20-associated neurodevelopmental disorders (TAND) emerges from a genotype-driven perspective.

Identifiants

pubmed: 30819258
doi: 10.1186/s13073-019-0623-0
pii: 10.1186/s13073-019-0623-0
pmc: PMC6393995
doi:

Substances chimiques

TCF20 protein, human 0
Transcription Factors 0

Types de publication

Case Reports Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

12

Subventions

Organisme : NHGRI NIH HHS
ID : UM1HG006542
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS105078-01
Pays : United States
Organisme : Department of Health
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R35 NS105078
Pays : United States
Organisme : NHGRI NIH HHS
ID : K08 HG008986
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT098051
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_16018
Pays : United Kingdom
Organisme : NHGRI NIH HHS
ID : UM1 HG006542
Pays : United States

Commentaires et corrections

Type : ErratumIn
Type : CommentIn

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Auteurs

Francesco Vetrini (F)

Baylor Genetics, Houston, TX, 77021, USA.
Present address: Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN, 46202, USA.

Shane McKee (S)

Northern Ireland Regional Genetics Service, Belfast City Hospital, Belfast, UK.

Jill A Rosenfeld (JA)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Mohnish Suri (M)

Nottingham Genetics Service, Nottingham City Hospital, Nottingham, UK.

Andrea M Lewis (AM)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Kimberly Margaret Nugent (KM)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Department of Pediatrics, Baylor College of Medicine, San Antonio, TX, 78207, USA.

Elizabeth Roeder (E)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Department of Pediatrics, Baylor College of Medicine, San Antonio, TX, 78207, USA.

Rebecca O Littlejohn (RO)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Department of Pediatrics, Baylor College of Medicine, San Antonio, TX, 78207, USA.

Sue Holder (S)

North West Thames Regional Genetics Service, 759 Northwick Park Hospital, London, UK.

Wenmiao Zhu (W)

Baylor Genetics, Houston, TX, 77021, USA.

Joseph T Alaimo (JT)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Brett Graham (B)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Present address: Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN, 46202, USA.

Jill M Harris (JM)

Dell Children's Medical Group, Austin, TX, 78723, USA.

James B Gibson (JB)

Dell Children's Medical Group, Austin, TX, 78723, USA.

Matthew Pastore (M)

Division of Genetic and Genomic Medicine, Nationwide Children's Hospital; and Department of Pediatrics, College of Medicine, Ohio State University, Columbus, OH, 43205, USA.

Kim L McBride (KL)

Division of Genetic and Genomic Medicine, Nationwide Children's Hospital; and Department of Pediatrics, College of Medicine, Ohio State University, Columbus, OH, 43205, USA.

Makanko Komara (M)

Department of Pediatrics, College of Medicine & Health Sciences, United Arab University, Al Ain, UAE.

Lihadh Al-Gazali (L)

Department of Pediatrics, College of Medicine & Health Sciences, United Arab University, Al Ain, UAE.

Aisha Al Shamsi (A)

Department of Pediatrics, Tawam Hospital, Al-Ain, UAE.

Elizabeth A Fanning (EA)

Department of Pediatrics, Section of Genetics, University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73104, USA.

Klaas J Wierenga (KJ)

Department of Pediatrics, Section of Genetics, University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73104, USA.
Present address: Mayo Clinic Florida, Department of Clinical Genomics, Jacksonville, FL, 32224, USA.

Daryl A Scott (DA)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Department of Molecular Physiology and Biophysics, Baylor College of Medicine, Houston, TX, 77030, USA.

Ziva Ben-Neriah (Z)

Department of Human Genetics and Metabolic Diseases, Hadassah-Hebrew University Medical Center, Jerusalem, Israel.

Vardiella Meiner (V)

Department of Human Genetics and Metabolic Diseases, Hadassah-Hebrew University Medical Center, Jerusalem, Israel.

Hanoch Cassuto (H)

The Hebrew University of Jerusalem, Jerusalem, Israel.

Orly Elpeleg (O)

Monique and Jacques Roboh Department of Genetic Research, Hadassah-Hebrew University Medical Center, 91120, Jerusalem, Israel.

J Lloyd Holder (JL)

Department of Pediatrics, Texas Children's Hospital, Houston, TX, 77030, USA.

Lindsay C Burrage (LC)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Laurie H Seaver (LH)

Department of Pediatrics, University of Hawaii, Honolulu, HI, 96826, USA.

Lionel Van Maldergem (L)

Centre de Génétique Humaine, Université de Franche-Comté, Besançon, France.

Sonal Mahida (S)

Department of Neurology, Boston Children's Hospital, Boston, MA, 0211, USA.

Janet S Soul (JS)

Department of Neurology, Boston Children's Hospital, Boston, MA, 0211, USA.

Margaret Marlatt (M)

Department of Neurology, Boston Children's Hospital, Boston, MA, 0211, USA.

Ludmila Matyakhina (L)

Gene DX, Gaithersburg, MD, 20877, USA.

Julie Vogt (J)

West Midlands Regional Clinical Genetics Service and Birmingham Health Partners; and Women's and Children's Hospitals NHS Foundation Trust, Birmingham, UK.

June-Anne Gold (JA)

East Anglia Regional Genetics Service, Addenbrooke's Hospital, Cambridge, UK.

Soo-Mi Park (SM)

East Anglia Regional Genetics Service, Addenbrooke's Hospital, Cambridge, UK.

Vinod Varghese (V)

All-Wales Medical Genetics Service, University Hospital of Wales, Cardiff, UK.

Anne K Lampe (AK)

South East of Scotland Clinical Genetic Service, Western General Hospital, Edinburgh, UK.

Ajith Kumar (A)

North East Thames Regional Genetics Service, Great Ormond Street Hospital, London, UK.

Melissa Lees (M)

North East Thames Regional Genetics Service, Great Ormond Street Hospital, London, UK.

Muriel Holder-Espinasse (M)

South East Thames Regional Genetics Service, Guy's Hospital, London, UK.

Vivienne McConnell (V)

Northern Ireland Regional Genetics Service, Belfast City Hospital, Belfast, UK.

Birgitta Bernhard (B)

North West Thames Regional Genetics Service, 759 Northwick Park Hospital, London, UK.

Ed Blair (E)

Oxford Regional Genetics Service, Oxford University Hospitals, Oxford, UK.

Victoria Harrison (V)

Wessex Clinical Genetics Service, Princess Anne Hospital, Southampton, UK.

Donna M Muzny (DM)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA.

Richard A Gibbs (RA)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA.

Sarah H Elsea (SH)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Jennifer E Posey (JE)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Weimin Bi (W)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Seema Lalani (S)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Department of Pediatrics, Texas Children's Hospital, Houston, TX, 77030, USA.

Fan Xia (F)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Yaping Yang (Y)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

Christine M Eng (CM)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.

James R Lupski (JR)

Baylor Genetics, Houston, TX, 77021, USA.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, 77030, USA.
Department of Pediatrics, Texas Children's Hospital, Houston, TX, 77030, USA.

Pengfei Liu (P)

Baylor Genetics, Houston, TX, 77021, USA. pengfeil@bcm.edu.
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA. pengfeil@bcm.edu.

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