Drosophila functional screening of de novo variants in autism uncovers damaging variants and facilitates discovery of rare neurodevelopmental diseases.

Drosophila melanogaster GLRA2 GluClalpha T2A-GAL4 TG4 autism spectrum disorder functional genomics humanization missense variants rare genetic diseases undiagnosed diseases

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
15 03 2022
Historique:
received: 02 02 2021
revised: 23 09 2021
accepted: 18 02 2022
entrez: 16 3 2022
pubmed: 17 3 2022
medline: 8 4 2022
Statut: ppublish

Résumé

Individuals with autism spectrum disorder (ASD) exhibit an increased burden of de novo mutations (DNMs) in a broadening range of genes. While these studies have implicated hundreds of genes in ASD pathogenesis, which DNMs cause functional consequences in vivo remains unclear. We functionally test the effects of ASD missense DNMs using Drosophila through "humanization" rescue and overexpression-based strategies. We examine 79 ASD variants in 74 genes identified in the Simons Simplex Collection and find 38% of them to cause functional alterations. Moreover, we identify GLRA2 as the cause of a spectrum of neurodevelopmental phenotypes beyond ASD in 13 previously undiagnosed subjects. Functional characterization of variants in ASD candidate genes points to conserved neurobiological mechanisms and facilitates gene discovery for rare neurodevelopmental diseases.

Identifiants

pubmed: 35294868
pii: S2211-1247(22)00253-4
doi: 10.1016/j.celrep.2022.110517
pmc: PMC8983390
mid: NIHMS1789669
pii:
doi:

Substances chimiques

Receptors, Glycine 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

110517

Subventions

Organisme : NHGRI NIH HHS
ID : UM1 HG008900
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007526
Pays : United States
Organisme : NIGMS NIH HHS
ID : R25 GM056929
Pays : United States
Organisme : NIMH NIH HHS
ID : F30 MH118804
Pays : United States
Organisme : NIH HHS
ID : R24 OD022005
Pays : United States
Organisme : NIGMS NIH HHS
ID : R25 GM069234
Pays : United States
Organisme : CIHR
ID : MFE-164712
Pays : Canada
Organisme : NHGRI NIH HHS
ID : R01 HG009141
Pays : United States
Organisme : NICHD NIH HHS
ID : U54 HD083092
Pays : United States
Organisme : NINDS NIH HHS
ID : F32 NS110174
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD103555
Pays : United States

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The Department of Molecular and Human Genetics at Baylor College of Medicine receives revenue from clinical genetic testing completed at Baylor Genetics Laboratories.

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Auteurs

Paul C Marcogliese (PC)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Samantha L Deal (SL)

Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Program in Developmental Biology, BCM, Houston, TX 77030, USA.

Jonathan Andrews (J)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

J Michael Harnish (JM)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

V Hemanjani Bhavana (VH)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Hillary K Graves (HK)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Sharayu Jangam (S)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Xi Luo (X)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Department of Pediatrics, Division of Hematology/Oncology, BCM, Houston, TX 77030, USA.

Ning Liu (N)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Baylor Genetics Laboratories, Houston, TX 77021, USA.

Danqing Bei (D)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Yu-Hsin Chao (YH)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Brooke Hull (B)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Pei-Tseng Lee (PT)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Hongling Pan (H)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Pradnya Bhadane (P)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Mei-Chu Huang (MC)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Colleen M Longley (CM)

Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Program in Developmental Biology, BCM, Houston, TX 77030, USA.

Hsiao-Tuan Chao (HT)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Department of Pediatrics, Division of Neurology and Developmental Neuroscience, BCM, Houston, TX 77030, USA; Department of Neuroscience, BCM, Houston, TX 77030, USA; McNair Medical Institute, The Robert and Janice McNair Foundation, Houston, TX 77030, USA; TCH, Houston, TX 77030, USA; Development, Disease Models & Therapeutics Graduate Program, BCM, Houston, TX 77030, USA.

Hyung-Lok Chung (HL)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Howard Hughes Medical Institute, Houston, TX 77030, USA.

Nele A Haelterman (NA)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Oguz Kanca (O)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Sathiya N Manivannan (SN)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Linda Z Rossetti (LZ)

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

Ryan J German (RJ)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA.

Amanda Gerard (A)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; TCH, Houston, TX 77030, USA.

Eva Maria Christina Schwaibold (EMC)

Institute of Human Genetics, Heidelberg University, Heidelberg, Germany.

Sarah Fehr (S)

Praxis für Humangenetik Tübingen, Tübingen, Germany.

Renzo Guerrini (R)

Neuroscience Department, Children's Hospital Meyer-University of Florence, Florence, Italy.

Annalisa Vetro (A)

Neuroscience Department, Children's Hospital Meyer-University of Florence, Florence, Italy.

Eleina England (E)

The Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.

Chaya N Murali (CN)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; TCH, Houston, TX 77030, USA.

Tahsin Stefan Barakat (TS)

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

Marieke F van Dooren (MF)

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

Martina Wilke (M)

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

Marjon van Slegtenhorst (M)

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

Gaetan Lesca (G)

Department of Medical Genetics, Lyon University Hospital, Université Claude Bernard Lyon 1, Lyon, France; Institut NeuroMyoGène, CNRS UMR 5310 - INSERM U1217, Université Claude Bernard Lyon 1, Lyon, France.

Isabelle Sabatier (I)

Department of Pediatric Neurology, Lyon University Hospitals, Lyon, France.

Nicolas Chatron (N)

Department of Medical Genetics, Lyon University Hospital, Université Claude Bernard Lyon 1, Lyon, France; Institut NeuroMyoGène, CNRS UMR 5310 - INSERM U1217, Université Claude Bernard Lyon 1, Lyon, France.

Catherine A Brownstein (CA)

Division of Genetics and Genomics, Boston Children's Hospital, Boston, MA 02115, USA; The Manton Center for Orphan Disease Research, Boston Children's Hospital, Boston, MA 02115, USA; Department of Pediatrics, Harvard Medical School, Boston, MA 02115, USA.

Jill A Madden (JA)

Division of Genetics and Genomics, Boston Children's Hospital, Boston, MA 02115, USA; The Manton Center for Orphan Disease Research, Boston Children's Hospital, Boston, MA 02115, USA.

Pankaj B Agrawal (PB)

Division of Genetics and Genomics, Boston Children's Hospital, Boston, MA 02115, USA; The Manton Center for Orphan Disease Research, Boston Children's Hospital, Boston, MA 02115, USA; Department of Pediatrics, Harvard Medical School, Boston, MA 02115, USA; Division of Newborn Medicine, Boston Children's Hospital, Boston, MA 02115, USA.

Boris Keren (B)

Genetic Department, Pitié-Salpêtrière Hospital, APHP.Sorbonne Université, Paris 75013, France.

Thomas Courtin (T)

Genetic Department, Pitié-Salpêtrière Hospital, APHP.Sorbonne Université, Paris 75013, France.

Laurence Perrin (L)

Genetic Department, Robert Debré Hospital, APHP.Nord-Université de Paris, Paris 75019, France.

Melanie Brugger (M)

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

Timo Roser (T)

Division of Pediatric Neurology, Developmental Medicine and Social Pediatrics, Department of Pediatrics, Dr. von Hauner Children's Hospital, Ludwig-Maximilians-University, Lindwurmstraße 4, 80337 Munich, Germany.

Steffen Leiz (S)

Department of Pediatrics and Adolescent Medicine, Hospital Dritter Orden, Munich, Germany.

Frederic Tran Mau-Them (FT)

INSERM U1231, LNC UMR1231 GAD, Burgundy University, 21000 Dijon, France; Laboratoire de Génétique, Innovation en Diagnostic Génomique des Maladies Rares UF6254, Plateau Technique de Biologie, CHU Dijon, 14 Rue Paul Gaffarel, BP 77908, 21079 Dijon, France.

Julian Delanne (J)

INSERM U1231, LNC UMR1231 GAD, Burgundy University, 21000 Dijon, France.

Elena Sukarova-Angelovska (E)

Department of Endocrinology and Genetics, University Clinic for Children's Diseases, Medical Faculty, University Sv. Kiril i Metodij, Skopje, Republic of Macedonia.

Slavica Trajkova (S)

Department of Medical Sciences, University of Torino, Turin, Italy.

Erik Rosenhahn (E)

Institute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.

Vincent Strehlow (V)

Institute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.

Konrad Platzer (K)

Institute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.

Roberto Keller (R)

Adult Autism Center, Mental Health Department, Health Unit ASL Città di Torino, Turin, Italy.

Lisa Pavinato (L)

Department of Medical Sciences, University of Torino, Turin, Italy; Institute of Human Genetics and Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany.

Alfredo Brusco (A)

Department of Medical Sciences, University of Torino, Turin, Italy; Medical Genetics Unit, Città della Salute e della Scienza, University Hospital, Turin, Italy.

Jill A Rosenfeld (JA)

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

Ronit Marom (R)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; TCH, Houston, TX 77030, USA.

Michael F Wangler (MF)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; TCH, Houston, TX 77030, USA; Development, Disease Models & Therapeutics Graduate Program, BCM, Houston, TX 77030, USA. Electronic address: mw147467@bcm.edu.

Shinya Yamamoto (S)

Department of Molecular and Human Genetics, Baylor College of Medicine (BCM), Houston, TX 77030, USA; Jan and Dan Duncan Neurological Research Institute, Texas Children's Hospital (TCH), Houston, TX 77030, USA; Program in Developmental Biology, BCM, Houston, TX 77030, USA; Department of Neuroscience, BCM, Houston, TX 77030, USA; Development, Disease Models & Therapeutics Graduate Program, BCM, Houston, TX 77030, USA. Electronic address: yamamoto@bcm.edu.

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