SPEN haploinsufficiency causes a neurodevelopmental disorder overlapping proximal 1p36 deletion syndrome with an episignature of X chromosomes in females.


Journal

American journal of human genetics
ISSN: 1537-6605
Titre abrégé: Am J Hum Genet
Pays: United States
ID NLM: 0370475

Informations de publication

Date de publication:
04 03 2021
Historique:
received: 07 12 2020
accepted: 26 01 2021
pubmed: 18 2 2021
medline: 25 3 2021
entrez: 17 2 2021
Statut: ppublish

Résumé

Deletion 1p36 (del1p36) syndrome is the most common human disorder resulting from a terminal autosomal deletion. This condition is molecularly and clinically heterogeneous. Deletions involving two non-overlapping regions, known as the distal (telomeric) and proximal (centromeric) critical regions, are sufficient to cause the majority of the recurrent clinical features, although with different facial features and dysmorphisms. SPEN encodes a transcriptional repressor commonly deleted in proximal del1p36 syndrome and is located centromeric to the proximal 1p36 critical region. Here, we used clinical data from 34 individuals with truncating variants in SPEN to define a neurodevelopmental disorder presenting with features that overlap considerably with those of proximal del1p36 syndrome. The clinical profile of this disease includes developmental delay/intellectual disability, autism spectrum disorder, anxiety, aggressive behavior, attention deficit disorder, hypotonia, brain and spine anomalies, congenital heart defects, high/narrow palate, facial dysmorphisms, and obesity/increased BMI, especially in females. SPEN also emerges as a relevant gene for del1p36 syndrome by co-expression analyses. Finally, we show that haploinsufficiency of SPEN is associated with a distinctive DNA methylation episignature of the X chromosome in affected females, providing further evidence of a specific contribution of the protein to the epigenetic control of this chromosome, and a paradigm of an X chromosome-specific episignature that classifies syndromic traits. We conclude that SPEN is required for multiple developmental processes and SPEN haploinsufficiency is a major contributor to a disorder associated with deletions centromeric to the previously established 1p36 critical regions.

Identifiants

pubmed: 33596411
pii: S0002-9297(21)00015-X
doi: 10.1016/j.ajhg.2021.01.015
pmc: PMC8008487
pii:
doi:

Substances chimiques

DNA-Binding Proteins 0
RNA-Binding Proteins 0
SPEN protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

502-516

Subventions

Organisme : NHGRI NIH HHS
ID : UM1 HG008900
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD098458
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG009141
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : R01 MH101221
Pays : United States

Informations de copyright

Copyright © 2021 American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.

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Auteurs

Francesca Clementina Radio (FC)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Kaifang Pang (K)

Division of Neurology and Developmental Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.

Andrea Ciolfi (A)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Michael A Levy (MA)

Molecular Genetics Laboratory, Molecular Diagnostics Division, London Health Sciences Centre, London, ON N6A5W9, Canada.

Andrés Hernández-García (A)

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

Lucia Pedace (L)

Oncohaematology Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Francesca Pantaleoni (F)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Zhandong Liu (Z)

Division of Neurology and Developmental Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.

Elke de Boer (E)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 GA Nijmegen, the Netherlands.

Adam Jackson (A)

Division of Evolution & Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, M13 9 WL Manchester, UK; Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University NHS Foundation Trust, M13 9WL Manchester, UK.

Alessandro Bruselles (A)

Department of Oncology and Molecular Medicine, Istituto Superiore di Sanità, 00161 Rome, Italy.

Haley McConkey (H)

Molecular Genetics Laboratory, Molecular Diagnostics Division, London Health Sciences Centre, London, ON N6A5W9, Canada.

Emilia Stellacci (E)

Department of Oncology and Molecular Medicine, Istituto Superiore di Sanità, 00161 Rome, Italy.

Stefania Lo Cicero (S)

Department of Oncology and Molecular Medicine, Istituto Superiore di Sanità, 00161 Rome, Italy.

Marialetizia Motta (M)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Rosalba Carrozzo (R)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Maria Lisa Dentici (ML)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Kirsty McWalter (K)

GeneDx, Gaithersburg, MD 20877, USA.

Megha Desai (M)

GeneDx, Gaithersburg, MD 20877, USA.

Kristin G Monaghan (KG)

GeneDx, Gaithersburg, MD 20877, USA.

Aida Telegrafi (A)

GeneDx, Gaithersburg, MD 20877, USA.

Christophe Philippe (C)

Inserm UMR 1231 GAD (Génétique des Anomalies du Développement), Université de Bourgogne, 21070 Dijon, France; UF Innovation en Diagnostic Génomique des Maladies Rares, CHU, Dijon Bourgogne, 21079 Dijon, France.

Antonio Vitobello (A)

Inserm UMR 1231 GAD (Génétique des Anomalies du Développement), Université de Bourgogne, 21070 Dijon, France; UF Innovation en Diagnostic Génomique des Maladies Rares, CHU, Dijon Bourgogne, 21079 Dijon, France.

Margaret Au (M)

Division of Medical Genetics, Department of Pediatrics, Cedars Sinai Medical Center, David Geffen School of Medicine at UCLA, Los Angeles, CA 90048, USA.

Katheryn Grand (K)

Division of Medical Genetics, Department of Pediatrics, Cedars Sinai Medical Center, David Geffen School of Medicine at UCLA, Los Angeles, CA 90048, USA.

Pedro A Sanchez-Lara (PA)

Division of Medical Genetics, Department of Pediatrics, Cedars Sinai Medical Center, David Geffen School of Medicine at UCLA, Los Angeles, CA 90048, USA.

Joanne Baez (J)

Division of Medical Genetics, Department of Pediatrics, Cedars Sinai Medical Center, David Geffen School of Medicine at UCLA, Los Angeles, CA 90048, USA.

Kristin Lindstrom (K)

Phoenix Children's Hospital, Phoenix, AZ 85016, USA.

Peggy Kulch (P)

Phoenix Children's Hospital, Phoenix, AZ 85016, USA.

Jessica Sebastian (J)

Division of Medical Genetics, Department of Pediatrics, UPMC Children's Hospital of Pittsburgh, Pittsburgh, PA 15224, USA.

Suneeta Madan-Khetarpal (S)

Division of Medical Genetics, Department of Pediatrics, UPMC Children's Hospital of Pittsburgh, Pittsburgh, PA 15224, USA.

Chelsea Roadhouse (C)

McMaster Children's Hospital, Hamilton, ON L8N 3Z5, Canada.

Jennifer J MacKenzie (JJ)

McMaster Children's Hospital, Hamilton, ON L8N 3Z5, Canada.

Berrin Monteleone (B)

Clinical genetics, NYU Langone Long Island School of Medicine, Mineola, NY 11501, USA.

Carol J Saunders (CJ)

Center for Pediatric Genomic Medicine, Children's Mercy Hospital, Kansas City, MO 64108, USA.

July K Jean Cuevas (JK)

Center for Pediatric Genomic Medicine, Children's Mercy Hospital, Kansas City, MO 64108, USA.

Laura Cross (L)

Center for Pediatric Genomic Medicine, Children's Mercy Hospital, Kansas City, MO 64108, USA.

Dihong Zhou (D)

Center for Pediatric Genomic Medicine, Children's Mercy Hospital, Kansas City, MO 64108, USA.

Taila Hartley (T)

Children's Hospital of Eastern Ontario, Ottawa, ON K1H 8L1, Canada.

Sarah L Sawyer (SL)

Children's Hospital of Eastern Ontario, Ottawa, ON K1H 8L1, Canada.

Fabíola Paoli Monteiro (FP)

Mendelics Genomic Analysis, Campo Belo - São Paulo 04013-000, Brazil.

Tania Vertemati Secches (TV)

Mendelics Genomic Analysis, Campo Belo - São Paulo 04013-000, Brazil.

Fernando Kok (F)

Mendelics Genomic Analysis, Campo Belo - São Paulo 04013-000, Brazil.

Laura E Schultz-Rogers (LE)

Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA.

Erica L Macke (EL)

Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA.

Eva Morava (E)

Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA; Department of Clinical Genomics, Mayo Clinic, Rochester, MN 55905, USA.

Eric W Klee (EW)

Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA.

Jennifer Kemppainen (J)

Center for Individualized Medicine, Mayo Clinic, Rochester, MN 55905, USA.

Maria Iascone (M)

Ospedale Papa Giovanni XXIII, 24127 Bergamo, Italy.

Angelo Selicorni (A)

Azienda Socio Sanitaria Territoriale Lariana, 22100 Como, Italy.

Romano Tenconi (R)

Dipartimento di Pediatria, Università di Padova, 35137 Padua, Italy.

David J Amor (DJ)

Victorian Clinical Genetics Services, Murdoch Children's Research Institute, Melbourne, VIC 3052, Australia; Department of Paediatrics, University of Melbourne, Royal Children's Hospital, Melbourne, VIC 3052, Australia.

Lynn Pais (L)

Medical and Populations Genetics Program, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

Lyndon Gallacher (L)

Victorian Clinical Genetics Services, Murdoch Children's Research Institute, Melbourne, VIC 3052, Australia; Department of Paediatrics, University of Melbourne, Royal Children's Hospital, Melbourne, VIC 3052, Australia.

Peter D Turnpenny (PD)

Royal Devon & Exeter NHS Foundation Trust, Exeter EX2 5DW, UK.

Karen Stals (K)

Royal Devon & Exeter NHS Foundation Trust, Exeter EX2 5DW, UK.

Sian Ellard (S)

Royal Devon & Exeter NHS Foundation Trust, Exeter EX2 5DW, UK.

Sara Cabet (S)

Department of Genetics, Hospices Civils de Lyon, Groupement Hospitalier Est, Claude Bernard Lyon 1 University, 69002 Lyon, France.

Gaetan Lesca (G)

Department of Genetics, Hospices Civils de Lyon, Groupement Hospitalier Est, Claude Bernard Lyon 1 University, 69002 Lyon, France.

Joset Pascal (J)

Institute of Medical Genetics, University of Zurich, 8952 Schlieren, Zurich, Switzerland.

Katharina Steindl (K)

Institute of Medical Genetics, University of Zurich, 8952 Schlieren, Zurich, Switzerland.

Sarit Ravid (S)

Pediatric Neurology Unit, Ruth Children's Hospital, Rambam Health Care Campus, Haifa 3109601, Israel.

Karin Weiss (K)

Genetics Institute, Rambam Health Care Campus, Rappaport Faculty of Medicine, Israel Institute of Technology, Haifa 3109601, Israel.

Alison M R Castle (AMR)

Department of Genetics, CHEO, University of Ottawa, Ottawa, ON K1N 6N5, Canada.

Melissa T Carter (MT)

Department of Genetics, CHEO, University of Ottawa, Ottawa, ON K1N 6N5, Canada.

Louisa Kalsner (L)

Connecticut Children's Medical Center, University of Connecticut School of Medicine, Farmington, CT 06032, USA.

Bert B A de Vries (BBA)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 GA Nijmegen, the Netherlands.

Bregje W van Bon (BW)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands.

Marijke R Wevers (MR)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands.

Rolph Pfundt (R)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands.

Alexander P A Stegmann (APA)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands; Department of Clinical Genetics, Maastricht University Medical Center+, 6229 HX Maastricht, the Netherlands.

Bronwyn Kerr (B)

Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University NHS Foundation Trust, M13 9WL Manchester, UK.

Helen M Kingston (HM)

Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University NHS Foundation Trust, M13 9WL Manchester, UK.

Kate E Chandler (KE)

Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University NHS Foundation Trust, M13 9WL Manchester, UK.

Willow Sheehan (W)

Department of Medical Genetics, Shodair Children's Hospital, Helena, MT 59601, USA.

Abdallah F Elias (AF)

Department of Medical Genetics, Shodair Children's Hospital, Helena, MT 59601, USA.

Deepali N Shinde (DN)

Ambry Genetics, Aliso Viejo, CA 92656, USA.

Meghan C Towne (MC)

Ambry Genetics, Aliso Viejo, CA 92656, USA.

Nathaniel H Robin (NH)

Department of Genetics, University of Alabama at Birmingham, Birmingham, AL 35294, USA.

Dana Goodloe (D)

Department of Genetics, University of Alabama at Birmingham, Birmingham, AL 35294, USA.

Adeline Vanderver (A)

Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, PA 19104, USA; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.

Omar Sherbini (O)

Department of Genetics, University of Alabama at Birmingham, Birmingham, AL 35294, USA.

Krista Bluske (K)

Illumina Clinical Services Laboratory, San Diego, CA 92122, USA.

R Tanner Hagelstrom (RT)

Illumina Clinical Services Laboratory, San Diego, CA 92122, USA.

Caterina Zanus (C)

Institute for Maternal and Child Health, IRCCS "Burlo Garofolo," 34137 Trieste, Italy.

Flavio Faletra (F)

Institute for Maternal and Child Health, IRCCS "Burlo Garofolo," 34137 Trieste, Italy.

Luciana Musante (L)

Institute for Maternal and Child Health, IRCCS "Burlo Garofolo," 34137 Trieste, Italy.

Evangeline C Kurtz-Nelson (EC)

Department of Psychiatry & Behavioral Sciences, University of Washington, Seattle, WA 98195, USA.

Rachel K Earl (RK)

Department of Psychiatry & Behavioral Sciences, University of Washington, Seattle, WA 98195, USA.

Britt-Marie Anderlid (BM)

Department of Molecular Medicine and Surgery, Karolinska Institutet and Department of Clinical Genetics, Karolinska University Hospital, 17176 Stockholm, Sweden.

Gilles Morin (G)

CA de Génétique Clinique & Oncogénétique, CHU Amiens-Picardie, 80054 Amiens, France.

Marjon van Slegtenhorst (M)

Department of Clinical Genetics, Erasmus MC University Medical Center, 3015 GD Rotterdam, the Netherlands.

Karin E M Diderich (KEM)

Department of Clinical Genetics, Erasmus MC University Medical Center, 3015 GD Rotterdam, the Netherlands.

Alice S Brooks (AS)

Department of Clinical Genetics, Erasmus MC University Medical Center, 3015 GD Rotterdam, the Netherlands.

Joost Gribnau (J)

Department of Developmental Biology, Oncode Institute, Erasmus MC, University Medical Center, 3015 GD Rotterdam, the Netherlands.

Ruben G Boers (RG)

Department of Developmental Biology, Oncode Institute, Erasmus MC, University Medical Center, 3015 GD Rotterdam, the Netherlands.

Teresa Robert Finestra (TR)

Department of Developmental Biology, Oncode Institute, Erasmus MC, University Medical Center, 3015 GD Rotterdam, the Netherlands.

Lauren B Carter (LB)

Department of Pediatrics, Division of Medical Genetics, Levine Children's Hospital Atrium Health, Charlotte, NC 28203, USA.

Anita Rauch (A)

Institute of Medical Genetics, University of Zurich, 8952 Schlieren, Zurich, Switzerland.

Paolo Gasparini (P)

Institute for Maternal and Child Health, IRCCS "Burlo Garofolo," 34137 Trieste, Italy; Department of Medicine, Surgery & Health Science, University of Trieste, 34143 Trieste, Italy.

Kym M Boycott (KM)

Children's Hospital of Eastern Ontario, Ottawa, ON K1H 8L1, Canada.

Tahsin Stefan Barakat (TS)

Department of Clinical Genetics, Erasmus MC University Medical Center, 3015 GD Rotterdam, the Netherlands.

John M Graham (JM)

Division of Medical Genetics, Department of Pediatrics, Cedars Sinai Medical Center, David Geffen School of Medicine at UCLA, Los Angeles, CA 90048, USA.

Laurence Faivre (L)

Centre de Référence Maladies Rares « Anomalies du Développement et Syndromes Malformatifs », Centre de Génétique, FHU-TRANSLAD et Institut GIMI, 77908 Dijon, France; UMR 1231 GAD, Inserm - Université Bourgogne-Franche Comté, 77908 Dijon, France.

Siddharth Banka (S)

Division of Evolution & Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, M13 9 WL Manchester, UK; Manchester Centre for Genomic Medicine, St Mary's Hospital, Manchester University NHS Foundation Trust, M13 9WL Manchester, UK.

Tianyun Wang (T)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA 98195, USA.

Evan E Eichler (EE)

Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA 98195, USA; Howard Hughes Medical Institute, University of Washington, Seattle, WA 98195, USA.

Manuela Priolo (M)

UOSD Genetica Medica del Grande Ospedale Metropolitano "Bianchi Melacrino Morelli" di Reggio Calabria, 89124 Reggio Calabria, Italy.

Bruno Dallapiccola (B)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy.

Lisenka E L M Vissers (LELM)

Department of Human Genetics, Radboudumc, 6525 GA Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6525 GA Nijmegen, the Netherlands.

Bekim Sadikovic (B)

Molecular Genetics Laboratory, Molecular Diagnostics Division, London Health Sciences Centre, London, ON N6A5W9, Canada.

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.

Jimmy Lloyd Holder (JL)

Division of Neurology and Developmental Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.

Marco Tartaglia (M)

Genetics and Rare Disease Research Division, Ospedale Pediatrico Bambino Gesù, IRCCS, 00146 Rome, Italy. Electronic address: marco.tartaglia@opbg.net.

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