Mutation-specific pathophysiological mechanisms define different neurodevelopmental disorders associated with SATB1 dysfunction.


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 02 2021
Historique:
received: 19 10 2020
accepted: 10 01 2021
pubmed: 30 1 2021
medline: 20 2 2021
entrez: 29 1 2021
Statut: ppublish

Résumé

Whereas large-scale statistical analyses can robustly identify disease-gene relationships, they do not accurately capture genotype-phenotype correlations or disease mechanisms. We use multiple lines of independent evidence to show that different variant types in a single gene, SATB1, cause clinically overlapping but distinct neurodevelopmental disorders. Clinical evaluation of 42 individuals carrying SATB1 variants identified overt genotype-phenotype relationships, associated with different pathophysiological mechanisms, established by functional assays. Missense variants in the CUT1 and CUT2 DNA-binding domains result in stronger chromatin binding, increased transcriptional repression, and a severe phenotype. In contrast, variants predicted to result in haploinsufficiency are associated with a milder clinical presentation. A similarly mild phenotype is observed for individuals with premature protein truncating variants that escape nonsense-mediated decay, which are transcriptionally active but mislocalized in the cell. Our results suggest that in-depth mutation-specific genotype-phenotype studies are essential to capture full disease complexity and to explain phenotypic variability.

Identifiants

pubmed: 33513338
pii: S0002-9297(21)00007-0
doi: 10.1016/j.ajhg.2021.01.007
pmc: PMC7895900
pii:
doi:

Substances chimiques

Chromatin 0
Matrix Attachment Region Binding Proteins 0
SATB1 protein, human 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

346-356

Subventions

Organisme : Medical Research Council
ID : MR/M014568/1
Pays : United Kingdom

Informations de copyright

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

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Auteurs

Joery den Hoed (J)

Language and Genetics Department, Max Planck Institute for Psycholinguistics, 6500 AH Nijmegen, the Netherlands; International Max Planck Research School for Language Sciences, Max Planck Institute for Psycholinguistics, 6500 AH Nijmegen, the Netherlands.

Elke de Boer (E)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands.

Norine Voisin (N)

Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland.

Alexander J M Dingemans (AJM)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands.

Nicolas Guex (N)

Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland; Bioinformatics Competence Center, University of Lausanne, 1015 Lausanne, Switzerland.

Laurens Wiel (L)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands; Center for Molecular and Biomolecular Informatics of the Radboudumc, 6500 HB Nijmegen, the Netherlands.

Christoffer Nellaker (C)

Nuffield Department of Women's and Reproductive Health, University of Oxford, Women's Centre, John Radcliffe Hospital, Oxford OX3 9DU, UK; Institute of Biomedical Engineering, Department of Engineering Science, University of Oxford, Oxford OX3 7DQ, UK; Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, University of Oxford, Oxford OX3 7LF, UK.

Shivarajan M Amudhavalli (SM)

University of Missouri-Kansas City School of Medicine, Kansas City, MO 64108, USA; Department of Pediatrics, Division of Clinical Genetics, Children's Mercy Hospital, Kansas City, MO 64108, USA.

Siddharth Banka (S)

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

Frederique S Bena (FS)

Service of Genetic Medicine, University Hospitals of Geneva, 1205 Geneva, Switzerland.

Bruria Ben-Zeev (B)

Edmomd and Lilly Safra Pediatric Hospital, Sheba Medical Center and Sackler School of Medicine, Tel Aviv University, Ramat Aviv 69978, Israel.

Vincent R Bonagura (VR)

Institute of Molecular Medicine, Feinstein Institutes for Medical Research, Manhasset, NY 11030, USA; Pediatrics and Molecular Medicine, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY 11549, USA.

Ange-Line Bruel (AL)

UMR1231-Inserm, Génétique des Anomalies du développement, Université de Bourgogne Franche-Comté, 21070 Dijon, France; Laboratoire de Génétique chromosomique et moléculaire, UF6254 Innovation en diagnostic génomique des maladies rares, Centre Hospitalier Universitaire de Dijon, 21070 Dijon, France.

Theresa Brunet (T)

Institute of Human Genetics, Technical University of Munich, 81675 Munich, Germany.

Han G Brunner (HG)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands; Maastricht University Medical Center, Department of Clinical Genetics, GROW School for Oncology and Developmental Biology, and MHeNS School for Mental health and Neuroscience, PO Box 5800, 6202AZ Maastricht, the Netherlands.

Hui B Chew (HB)

Department of Genetics, Kuala Lumpur Hospital, Jalan Pahang, 50586 Kuala Lumpur, Malaysia.

Jacqueline Chrast (J)

Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland.

Loreta Cimbalistienė (L)

Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, 08661 Vilnius, Lithuania.

Hilary Coon (H)

Department of Psychiatry, University of Utah School of Medicine, Salt Lake City, UT 84112, USA.
Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, Cambridge CB10 1SA, UK.

Emmanuèlle C Délot (EC)

Center for Genetic Medicine Research, Children's National Hospital, Children's Research Institute and Department of Genomics and Precision Medicine, George Washington University, Washington, DC 20010, USA.

Florence Démurger (F)

Department of clinical genetics, Vannes hospital, 56017 Vannes, France.

Anne-Sophie Denommé-Pichon (AS)

UMR1231-Inserm, Génétique des Anomalies du développement, Université de Bourgogne Franche-Comté, 21070 Dijon, France; Laboratoire de Génétique chromosomique et moléculaire, UF6254 Innovation en diagnostic génomique des maladies rares, Centre Hospitalier Universitaire de Dijon, 21070 Dijon, France.

Christel Depienne (C)

Institute of Human Genetics, University Hospital Essen, University of Duisburg-Essen, 45147 Essen, Germany.

Dian Donnai (D)

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

David A Dyment (DA)

Children's Hospital of Eastern Ontario Research Institute, Ottawa, ON K1H 5B2, Canada.

Orly Elpeleg (O)

Department of Genetics, Hadassah Medical Center, Hebrew University Medical Center, 91120 Jerusalem, Israel.

Laurence Faivre (L)

UMR1231-Inserm, Génétique des Anomalies du développement, Université de Bourgogne Franche-Comté, 21070 Dijon, France; Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l'Interrégion Est, Centre Hospitalier Universitaire Dijon, 21079 Dijon, France; Fédération Hospitalo-Universitaire Médecine Translationnelle et Anomalies du Développement (TRANSLAD), Centre Hospitalier Universitaire Dijon, 21079 Dijon, France.

Christian Gilissen (C)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, 6500 HB Nijmegen, the Netherlands.

Leslie Granger (L)

Department of Rehabilitation and Development, Randall Children's Hospital at Legacy Emanuel Medical Center, Portland, OR 97227, USA.

Benjamin Haber (B)

Division of Child Neurology and Inherited Metabolic Diseases, Centre for Paediatrics and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany.

Yasuo Hachiya (Y)

Department of Neuropediatrics, Tokyo Metropolitan Neurological Hospital, Fuchu, Tokyo 183-0042, Japan.

Yasmin Hamzavi Abedi (YH)

Division of Allergy and Immunology, Northwell Health, Great Neck, NY 11021, USA; Departments of Medicine and Pediatrics, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY 11549, USA.

Jennifer Hanebeck (J)

Division of Child Neurology and Inherited Metabolic Diseases, Centre for Paediatrics and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany.

Jayne Y Hehir-Kwa (JY)

Princess Máxima Center for Pediatric Oncology, 3584 CS Utrecht, the Netherlands.

Brooke Horist (B)

Pediatrics & Genetics, Alpharetta, GA 30005, USA.

Toshiyuki Itai (T)

Department of Human Genetics, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa 236-0004, Japan.

Adam Jackson (A)

Manchester Centre for Genomic Medicine, Division of Evolution and Genomic Sciences, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PL, UK.

Rosalyn Jewell (R)

Yorkshire Regional Genetics Service, Chapel Allerton Hospital, Leeds LS7 4SA, UK.

Kelly L Jones (KL)

Division of Medical Genetics & Metabolism, Children's Hospital of The King's Daughters, Norfolk, VA 23507, USA; Department of Pediatrics, Eastern Virginia Medical School, Norfolk, VA 23507, USA.

Shelagh Joss (S)

West of Scotland Centre for Genomic Medicine, Queen Elizabeth University Hospital, Glasgow G51 4TF, UK.

Hirofumi Kashii (H)

Department of Neuropediatrics, Tokyo Metropolitan Neurological Hospital, Fuchu, Tokyo 183-0042, Japan.

Mitsuhiro Kato (M)

Department of Pediatrics, Showa University School of Medicine, Shinagawa-ku, Tokyo 142-8666, Japan.

Anja A Kattentidt-Mouravieva (AA)

Zuidwester, 3240AA Middelharnis, the Netherlands.

Fernando Kok (F)

Mendelics Genomic Analysis, Sao Paulo, SP 04013-000, Brazil; University of Sao Paulo, School of Medicine, Sao Paulo, SP 01246-903, Brazil.

Urania Kotzaeridou (U)

Division of Child Neurology and Inherited Metabolic Diseases, Centre for Paediatrics and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany.

Vidya Krishnamurthy (V)

Pediatrics & Genetics, Alpharetta, GA 30005, USA.

Vaidutis Kučinskas (V)

Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, 08661 Vilnius, Lithuania.

Alma Kuechler (A)

Institute of Human Genetics, University Hospital Essen, University of Duisburg-Essen, 45147 Essen, Germany.

Alinoë Lavillaureix (A)

CHU Rennes, Univ Rennes, CNRS, IGDR, Service de Génétique Clinique, Centre de Référence Maladies Rares CLAD-Ouest, ERN ITHACA, Hôpital Sud, 35033 Rennes, France.

Pengfei Liu (P)

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

Linda Manwaring (L)

Department of Pediatrics, Division of Genetics and Genomic Medicine, Washington University School of Medicine, St. Louis, MO 63110-1093, USA.

Naomichi Matsumoto (N)

Department of Human Genetics, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa 236-0004, Japan.

Benoît Mazel (B)

Centre de Génétique et Centre de Référence Anomalies du Développement et Syndromes Malformatifs de l'Interrégion Est, Centre Hospitalier Universitaire Dijon, 21079 Dijon, France.

Kirsty McWalter (K)

GeneDx, 207 Perry Parkway, Gaithersburg, MD 20877, USA.

Vardiella Meiner (V)

Department of Genetics, Hadassah Medical Center, Hebrew University Medical Center, 91120 Jerusalem, Israel.

Mohamad A Mikati (MA)

Division of Pediatric Neurology, Duke University Medical Center, Durham, NC 27710, USA.

Satoko Miyatake (S)

Department of Human Genetics, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa 236-0004, Japan.

Takeshi Mizuguchi (T)

Department of Human Genetics, Yokohama City University Graduate School of Medicine, Yokohama, Kanagawa 236-0004, Japan.

Lip H Moey (LH)

Department of Genetics, Penang General Hospital, Jalan Residensi, 10990 Georgetown, Penang, Malaysia.

Shehla Mohammed (S)

Clinical Genetics, Guy's Hospital, Great Maze Pond, London SE1 9RT, UK.

Hagar Mor-Shaked (H)

Department of Genetics, Hadassah Medical Center, Hebrew University Medical Center, 91120 Jerusalem, Israel.

Hayley Mountford (H)

Department of Biological and Medical Sciences, Headington Campus, Oxford Brookes University, Oxford OX3 0BP, UK.

Ruth Newbury-Ecob (R)

Clinical Genetics, St Michael's Hospital Bristol, University Hospitals Bristol NHS Foundation Trust, Bristol BS2 8EG, UK.

Sylvie Odent (S)

CHU Rennes, Univ Rennes, CNRS, IGDR, Service de Génétique Clinique, Centre de Référence Maladies Rares CLAD-Ouest, ERN ITHACA, Hôpital Sud, 35033 Rennes, France.

Laura Orec (L)

Division of Child Neurology and Inherited Metabolic Diseases, Centre for Paediatrics and Adolescent Medicine, University Hospital Heidelberg, 69120 Heidelberg, Germany.

Matthew Osmond (M)

Children's Hospital of Eastern Ontario Research Institute, Ottawa, ON K1H 5B2, Canada.

Timothy B Palculict (TB)

GeneDx, 207 Perry Parkway, Gaithersburg, MD 20877, USA.

Michael Parker (M)

Sheffield Clinical Genetics Service, Sheffield Children's Hospital, Sheffield S5 7AU, UK.

Andrea K Petersen (AK)

Department of Rehabilitation and Development, Randall Children's Hospital at Legacy Emanuel Medical Center, Portland, OR 97227, USA.

Rolph Pfundt (R)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands.

Eglė Preikšaitienė (E)

Department of Human and Medical Genetics, Institute of Biomedical Sciences, Faculty of Medicine, Vilnius University, 08661 Vilnius, Lithuania.

Kelly Radtke (K)

Clinical Genomics Department, Ambry Genetics, Aliso Viejo, CA 92656, USA.

Emmanuelle Ranza (E)

Service of Genetic Medicine, University Hospitals of Geneva, 1205 Geneva, Switzerland; Medigenome, Swiss Institute of Genomic Medicine, 1207 Geneva, Switzerland.

Jill A Rosenfeld (JA)

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

Teresa Santiago-Sim (T)

GeneDx, 207 Perry Parkway, Gaithersburg, MD 20877, USA.

Caitlin Schwager (C)

University of Missouri-Kansas City School of Medicine, Kansas City, MO 64108, USA; Department of Pediatrics, Division of Clinical Genetics, Children's Mercy Hospital, Kansas City, MO 64108, USA.

Margje Sinnema (M)

Department of Clinical Genetics, Maastricht University Medical Center+, azM, 6202 AZ Maastricht, the Netherlands; Department of Genetics and Cell Biology, Faculty of Health Medicine Life Sciences, Maastricht University Medical Center+, Maastricht University, 6229 ER Maastricht, the Netherlands.

Lot Snijders Blok (L)

Language and Genetics Department, Max Planck Institute for Psycholinguistics, 6500 AH Nijmegen, the Netherlands; Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands.

Rebecca C Spillmann (RC)

Department of Pediatrics, Division of Medical Genetics, Duke University Medical Center, Durham, NC 27713, USA.

Alexander P A Stegmann (APA)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Department of Clinical Genetics, Maastricht University Medical Center+, azM, 6202 AZ Maastricht, the Netherlands.

Isabelle Thiffault (I)

University of Missouri-Kansas City School of Medicine, Kansas City, MO 64108, USA; Center for Pediatric Genomic Medicine, Children's Mercy Hospital, Kansas City, MO 64108, USA; Department of Pathology and Laboratory Medicine, Children's Mercy Hospital, Kansas City, MO 64108, USA.

Linh Tran (L)

Division of Pediatric Neurology, Duke University Medical Center, Durham, NC 27710, USA.

Adi Vaknin-Dembinsky (A)

Department of Neurology and Laboratory of Neuroimmunology, The Agnes Ginges Center for Neurogenetics, Hadassah Medical Center, Faculty of Medicine, Hebrew University of Jerusalem, 91120 Jerusalem, Israel.

Juliana H Vedovato-Dos-Santos (JH)

Mendelics Genomic Analysis, Sao Paulo, SP 04013-000, Brazil.

Samantha A Schrier Vergano (SA)

Division of Medical Genetics & Metabolism, Children's Hospital of The King's Daughters, Norfolk, VA 23507, USA.

Eric Vilain (E)

Center for Genetic Medicine Research, Children's National Hospital, Children's Research Institute and Department of Genomics and Precision Medicine, George Washington University, Washington, DC 20010, USA.

Antonio Vitobello (A)

UMR1231-Inserm, Génétique des Anomalies du développement, Université de Bourgogne Franche-Comté, 21070 Dijon, France; Laboratoire de Génétique chromosomique et moléculaire, UF6254 Innovation en diagnostic génomique des maladies rares, Centre Hospitalier Universitaire de Dijon, 21070 Dijon, France.

Matias Wagner (M)

Institute of Human Genetics, Technical University of Munich, 81675 Munich, Germany; Institute of Neurogenomics, Helmholtz Zentrum München, 85764 Munich, Germany.

Androu Waheeb (A)

Children's Hospital of Eastern Ontario Research Institute, Ottawa, ON K1H 5B2, Canada; Department of Genetics, Children's Hospital of Eastern Ontario, Ottawa, ON K1H 8L1, Canada.

Marcia Willing (M)

Department of Pediatrics, Division of Genetics and Genomic Medicine, Washington University School of Medicine, St. Louis, MO 63110-1093, USA.

Britton Zuccarelli (B)

The University of Kansas School of Medicine Salina Campus, Salina, KS 67401, USA.

Usha Kini (U)

Oxford Centre for Genomic Medicine, Oxford University Hospitals NHS Foundation Trust, Oxford OX3 7LE, UK.

Dianne F Newbury (DF)

Department of Biological and Medical Sciences, Headington Campus, Oxford Brookes University, Oxford OX3 0BP, UK.

Tjitske Kleefstra (T)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands.

Alexandre Reymond (A)

Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland.

Simon E Fisher (SE)

Language and Genetics Department, Max Planck Institute for Psycholinguistics, 6500 AH Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands. Electronic address: simon.fisher@mpi.nl.

Lisenka E L M Vissers (LELM)

Department of Human Genetics, Radboudumc, 6500 HB Nijmegen, the Netherlands; Donders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 GL Nijmegen, the Netherlands.

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