Partial Loss of USP9X Function Leads to a Male Neurodevelopmental and Behavioral Disorder Converging on Transforming Growth Factor β Signaling

Brett V Johnson; Raman Kumar; Sabrina Oishi; Suzy Alexander; Maria Kasherman; Michelle Sanchez Vega; Atma Ivancevic; Alison Gardner; Deepti Domingo; Mark Corbett; Euan Parnell; Sehyoun Yoon; Tracey Oh; Matthew Lines; Henrietta Lefroy; Usha Kini; Margot Van Allen; Sabine Grønborg; Sandra Mercier; Sébastien Küry; Stéphane Bézieau; Laurent Pasquier; Martine Raynaud; Alexandra Afenjar; Thierry Billette de Villemeur; Boris Keren; Julie Désir; Lionel Van Maldergem; Martina Marangoni; Nicola Dikow; David A Koolen; Peter M VanHasselt; Marjan Weiss; Petra Zwijnenburg; Joaquim Sa; Claudia Falcao Reis; Carlos López-Otín; Olaya Santiago-Fernández; Alberto Fernández-Jaén; Anita Rauch; Katharina Steindl; Pascal Joset; Amy Goldstein; Suneeta Madan-Khetarpal; Elena Infante; Elaine Zackai; Carey Mcdougall; Vinodh Narayanan; Keri Ramsey; Saadet Mercimek-Andrews; Loren Pena; Vandana Shashi; Kelly Schoch; Jennifer A Sullivan; Maria T Acosta; Aaron Aday; Mercedes E Alejandro; Patrick Allard; Euan A Ashley; Mahshid S Azamian; Carlos A Bacino; Guney Bademci; Eva Baker; Ashok Balasubramanyam; Dustin Baldridge; Deborah Barbouth; Gabriel F Batzli; Alan H Beggs; Hugo J Bellen; Jonathan A Bernstein; Gerard T Berry; Anna Bican; David P Bick; Camille L Birch; Stephanie Bivona; Carsten Bonnenmann; Devon Bonner; Braden E Boone; Bret L Bostwick; Lauren C Briere; Elly Brokamp; Donna M Brown; Matthew Brush; Elizabeth A Burke; Lindsay C Burrage; Manish J Butte; Olveen Carrasquillo; Ta Chen Peter Chang; Hsiao-Tuan Chao; Gary D Clark; Terra R Coakley; Laurel A Cobban; Joy D Cogan; F. Sessions Cole; Heather A Colley; Cynthia M Cooper; Heidi Cope; William J Craigen; Precilla D'Souza; Surendra Dasari; Mariska Davids; Jean M Davidson; Jyoti G Dayal; Esteban C Dell'Angelica; Shweta U Dhar; Naghmeh Dorrani; Daniel C Dorset; Emilie D Douine; David D Draper; Annika M Dries; Laura Duncan; David J Eckstein; Lisa T Emrick; Christine M Eng; Gregory M Enns; Cecilia Esteves; Tyra Estwick; Liliana Fernandez; Carlos Ferreira; Elizabeth L Fieg; Paul G Fisher; Brent L Fogel; Irman Forghani; Noah D Friedman; William A Gahl; Rena A Godfrey; Alica M Goldman; David B Goldstein; Jean-Philippe F Gourdine; Alana Grajewski; Catherine A Groden; Andrea L Gropman; Melissa Haendel; Rizwan Hamid; Neil A Hanchard; Frances High; Ingrid A Holm; Jason Hom; Alden Huang; Yong Huang; Rosario Isasi; Fariha Jamal; Yong-hui Jiang; Jean M Johnston; Angela L Jones; Lefkothea Karaviti; Emily G Kelley; David M Koeller; Isaac S Kohane; Jennefer N Kohler; Deborah Krakow; Donna M Krasnewich; Susan Korrick; Mary Koziura; Joel B Krier; Jennifer E Kyle; Seema R Lalani; Byron Lam; Brendan C Lanpher; Ian R Lanza; C. Christopher Lau; Jozef Lazar; Kimberly LeBlanc; Brendan H Lee; Hane Lee; Roy Levitt; Shawn E Levy; Richard A Lewis; Sharyn A Lincoln; Pengfei Liu; Xue Zhong Liu; Sandra K Loo; Joseph Loscalzo; Richard L Maas; Ellen F Macnamara; Calum A MacRae; Valerie V Maduro; Marta M Majcherska; May Christine V Malicdan; Laura A Mamounas; Teri A Manolio; Thomas C Markello; Ronit Marom; Martin G Martin; Julian A Martínez-Agosto; Shruti Marwaha; Thomas May; Jacob McCauley; Allyn McConkie-Rosell; Colleen E McCormack; Alexa T McCray; Jason D Merker; Thomas O Metz; Matthew Might; Eva Morava-Kozicz; Paolo M Moretti; Marie Morimoto; John J Mulvihill; David R Murdock; Avi Nath; Stan F Nelson; J. Scott Newberry; Sarah K Nicholas; Donna Novacic; Devin Oglesbee; James P Orengo; Stephen Pak; J. Carl Pallais; Christina GS Palmer; Jeanette C Papp; Neil H Parker; John A Phillips; Jennifer E Posey; John H Postlethwait; Lorraine Potocki; Barbara N Pusey; Genecee Renteri; Chloe M Reuter; Lynette Rives; Amy K Robertson; Lance H Rodan; Jill A Rosenfeld; Robb K Rowley; Ralph Sacco; Jacinda B Sampson; Susan L Samson; Mario Saporta; Judy Schaechter; Timothy Schedl; Daryl A Scott; Lisa Shakachite; Prashant Sharma; Kathleen Shields; Jimann Shin; Rebecca Signer; Catherine H Sillari; Edwin K Silverman; Janet S Sinsheimer; Lilianna Solnica-Krezel; Rebecca C Spillmann; Joan M Stoler; Nicholas Stong; David A Sweetser; Cecelia P Tamburro; Queenie K.-G Tan; Mustafa Tekin; Fred Telischi; Willa Thorson; Cynthia J Tifft; Camilo Toro; Alyssa A Tran; Tiina K Urv; Tiphanie P Vogel; Daryl M Waggott; Colleen E Wahl; Nicole M Walley; Chris A Walsh; Melissa Walker; Jennifer Wambach; Jijun Wan; Lee-kai Wang; Michael F Wangler; Patricia A Ward; Katrina M Waters; Bobbie-Jo M Webb-Robertson; Daniel Wegner; Monte Westerfield; Matthew T Wheeler; Anastasia L Wise; Lynne A Wolfe; Jeremy D Woods; Elizabeth A Worthey; Shinya Yamamoto; John Yang; Amanda J Yoon; Guoyun Yu; Diane B Zastrow; Chunli Zhao; Stephan Zuchner; William Gahl; Filippo Pinto e Vairo; Pavel N Pichurin; Sarah A Ewing; Sarah S Barnett; Eric W Klee; M. Scott Perry; Mary Kay Koenig; Catherine E Keegan; Jane L Schuette; Stephanie Asher; Yezmin Perilla-Young; Laurie D Smith; Elizabeth Bhoj; Paige Kaplan; Dong Li; Renske Oegema; Ellen van Binsbergen; Bert van der Zwaag; Marie Falkenberg Smeland; Ioana Cutcutache; Matthew Page; Martin Armstrong; Angela E Lin; Marcie A Steeves; Nicolette den Hollander; Mariëtte J.V Hoffer; Margot R.F Reijnders; Serwet Demirdas; Daniel C Koboldt; Dennis Bartholomew; Theresa Mihalic Mosher; Scott E Hickey; Christine Shieh; Pedro A Sanchez-Lara; John M Graham; Kamer Tezcan; G.B Schaefer; Noelle R Danylchuk; Alexander Asamoah; Kelly E Jackson; Naomi Yachelevich; Margaret Au; Luis A Pérez-Jurado; Tjitske Kleefstra; Peter Penzes; Stephen A Wood; Thomas Burne; Tyler Mark Pierson; Michael Piper; Jozef Gécz; Lachlan A Jolly

doi:10.1016/j.biopsych.2019.05.028

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Partial Loss of USP9X Function Leads to a Male Neurodevelopmental and Behavioral Disorder Converging on Transforming Growth Factor β Signaling

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Peer reviewed

Partial Loss of USP9X Function Leads to a Male Neurodevelopmental and Behavioral Disorder Converging on Transforming Growth Factor β Signaling

Brett V Johnson, Raman Kumar, Sabrina Oishi, Suzy Alexander, Maria Kasherman, Michelle Sanchez Vega, Atma Ivancevic, Alison Gardner, Deepti Domingo, Mark Corbett, …

Biological psychiatry (1969), Vol.87(2), pp.100-112

2020-01-15

DOI: https://doi.org/10.1016/j.biopsych.2019.05.028

PMID: 31443933

Abstract

Brain malformation

TGFβ

Neurodevelopmental disorder

USP9X

Hippocampus

Deubiquitylating enzyme

The X-chromosome gene USP9X encodes a deubiquitylating enzyme that has been associated with neurodevelopmental disorders primarily in female subjects. USP9X escapes X inactivation, and in female subjects de novo heterozygous copy number loss or truncating mutations cause haploinsufficiency culminating in a recognizable syndrome with intellectual disability and signature brain and congenital abnormalities. In contrast, the involvement of USP9X in male neurodevelopmental disorders remains tentative. We used clinically recommended guidelines to collect and interrogate the pathogenicity of 44 USP9X variants associated with neurodevelopmental disorders in males. Functional studies in patient-derived cell lines and mice were used to determine mechanisms of pathology. Twelve missense variants showed strong evidence of pathogenicity. We define a characteristic phenotype of the central nervous system (white matter disturbances, thin corpus callosum, and widened ventricles); global delay with significant alteration of speech, language, and behavior; hypotonia; joint hypermobility; visual system defects; and other common congenital and dysmorphic features. Comparison of in silico and phenotypical features align additional variants of unknown significance with likely pathogenicity. In support of partial loss-of-function mechanisms, using patient-derived cell lines, we show loss of only specific USP9X substrates that regulate neurodevelopmental signaling pathways and a united defect in transforming growth factor β signaling. In addition, we find correlates of the male phenotype in Usp9x brain-specific knockout mice, and further resolve loss of hippocampal-dependent learning and memory. Our data demonstrate the involvement of USP9X variants in a distinctive neurodevelopmental and behavioral syndrome in male subjects and identify plausible mechanisms of pathogenesis centered on disrupted transforming growth factor β signaling and hippocampal function.

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Collaboration types: Industry collaboration; Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.25 Molecular & Cell Biology - Cancer, Autophagy & Apoptosis; 1.25.782 Proteasome
Web Of Science research areas: Neurosciences; Psychiatry
ESI research areas: Neuroscience & Behavior

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Title: Partial Loss of USP9X Function Leads to a Male Neurodevelopmental and Behavioral Disorder Converging on Transforming Growth Factor β Signaling
Creators: Brett V Johnson - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Raman Kumar - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Sabrina Oishi - School of Biomedical Sciences, The University of Queensland, Brisbane, Australia
Suzy Alexander - Queensland Brain Institute, The University of Queensland, Brisbane, Australia
Maria Kasherman - School of Biomedical Sciences, The University of Queensland, Brisbane, Australia
Michelle Sanchez Vega - Queensland Brain Institute, The University of Queensland, Brisbane, Australia
Atma Ivancevic - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Alison Gardner - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Deepti Domingo - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Mark Corbett - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Euan Parnell - Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois
Sehyoun Yoon - Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois
Tracey Oh - Department of Medical Genetics, British Columbia Women's Hospital and University of British Columbia, Vancouver, British Columbia, Canada
Matthew Lines - Children’s Hospital of Eastern Ontario, Ottawa, Ontario, Canada
Henrietta Lefroy - Oxford Centre for Genomic Medicine, Oxford University Hospitals National Health Services Foundation Trust, Oxford, United Kingdom
Usha Kini - Oxford Centre for Genomic Medicine, Oxford University Hospitals National Health Services Foundation Trust, Oxford, United Kingdom
Margot Van Allen - Department of Medical Genetics, University of British Columbia, Vancouver, British Columbia, Canada
Sabine Grønborg - Center for Rare Diseases, Department of Pediatrics and Department of Clinical Genetics, University Hospital Copenhagen, Copenhagen, Denmark
Sandra Mercier - Service de Génétique Médicale, Centre Hospitalier Universitaire Nantes and l’Institut du Thorax, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Université de Nantes, Nantes, France
Sébastien Küry - Service de Génétique Médicale, Centre Hospitalier Universitaire Nantes and l’Institut du Thorax, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Université de Nantes, Nantes, France
Stéphane Bézieau - Service de Génétique Médicale, Centre Hospitalier Universitaire Nantes and l’Institut du Thorax, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Université de Nantes, Nantes, France
Laurent Pasquier - Service de Génétique Clinique, Centre de Référence Déficiences Intellectuelles de Causes Rares, Centre Hospitalier Universitaire Hôpital Sud, Rennes, France
Martine Raynaud - Centre Hospitalier Régional Universitaire de Tours, Service de Génétique, Unité Nixte de Recherche 1253, iBrain, Université de Tours, Institut National de la Santé et de la Recherche Médicale, Tours, France
Alexandra Afenjar - Groupe de Recherche Clinique No. 19, ConCer-LD, Département de Génétique, Assistance Publique–Hôpitaux de Paris, Hôpital Armand Trousseau, Centres de Référence Maladies Rares des Déficits Intellectuels de Causes Rares, Paris, France
Thierry Billette de Villemeur - Sorbonne Université, Groupe de Recherche Clinique No. 19, ConCer-LD, Neuropédiatrie, Centres de Référence Maladies Rares Neurogénétique, Institut National de la Santé et de la Recherche Médicale, Assistance Publique–Hôpitaux de Paris, Hôpital Armand Trousseau, Paris, France
Boris Keren - Hôpital de la Pitié-Salpêtrière, Département de Génétique, Paris, France
Julie Désir - Erasme University Hospital, Université Libre de Bruxelles, Brussels, Belgium
Lionel Van Maldergem - Centre de Génétique Humaine, Université de Franche-Comté, Besançon, France
Martina Marangoni - Erasme University Hospital, Université Libre de Bruxelles, Brussels, Belgium
Nicola Dikow - Institute of Human Genetics, Heidelberg University, Heidelberg, Germany
David A Koolen - Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands
Peter M VanHasselt - Department of Metabolic Diseases, University Medical Center Utrecht, Utrecht, The Netherlands
Marjan Weiss - Department of Clinical Genetics, Vrije Universiteit University Medical Center, Amsterdam, The Netherlands
Petra Zwijnenburg - Medical Genetics Unit, Hospital Pediátrico, Centro Hospitalar e Universitário de Coimbra, Coimbra, Portugal
Joaquim Sa - Medical Genetics Unit, Hospital Pediátrico, Centro Hospitalar e Universitário de Coimbra, Coimbra, Portugal
Claudia Falcao Reis - Medical Genetics Unit, Hospital Pediátrico, Centro Hospitalar e Universitário de Coimbra, Coimbra, Portugal
Carlos López-Otín - Departamento de Bioquímica y Biología Molecular, Instituto Universitário de Oncología del Principado de Asturias, Universidad de Oviedo, Oviedo, Spain
Olaya Santiago-Fernández - Departamento de Bioquímica y Biología Molecular, Instituto Universitário de Oncología del Principado de Asturias, Universidad de Oviedo, Oviedo, Spain
Alberto Fernández-Jaén - Unidad de Neurología Infantil, Hospital Universitário Quirón Madrid, Madrid, Spain
Anita Rauch - Institute of Medical Genetics, University of Zurich, Schlieren, Switzerland
Katharina Steindl - Institute of Medical Genetics, University of Zurich, Schlieren, Switzerland
Pascal Joset - Institute of Medical Genetics, University of Zurich, Schlieren, Switzerland
Amy Goldstein - Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Suneeta Madan-Khetarpal - Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania
Elena Infante - Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania
Elaine Zackai - Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Carey Mcdougall - Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Vinodh Narayanan - Center for Rare Childhood Disorders, Translational Genomics Research Institute, Phoenix, Arizona
Keri Ramsey - Center for Rare Childhood Disorders, Translational Genomics Research Institute, Phoenix, Arizona
Saadet Mercimek-Andrews - Division of Clinical and Metabolic Genetics, Department of Pediatrics, University of Toronto, The Hospital for Sick Children, Toronto, Ontario, Canada
Loren Pena - Division of Human Genetics, Cincinnati Children’s Hospital; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio
Vandana Shashi - Department of Pediatrics, Division of Medical Genetics, Duke University Medical Center, Durham, North Carolina
Loren Pena
Vandana Shashi
Kelly Schoch
Jennifer A Sullivan
Maria T Acosta
Aaron Aday
Mercedes E Alejandro
Patrick Allard
Euan A Ashley
Mahshid S Azamian
Carlos A Bacino
Guney Bademci
Eva Baker
Ashok Balasubramanyam
Dustin Baldridge
Deborah Barbouth
Gabriel F Batzli
Alan H Beggs
Hugo J Bellen
Jonathan A Bernstein
Gerard T Berry
Anna Bican
David P Bick
Camille L Birch
Stephanie Bivona
Carsten Bonnenmann
Devon Bonner
Braden E Boone
Bret L Bostwick
Lauren C Briere
Elly Brokamp
Donna M Brown
Matthew Brush
Elizabeth A Burke
Lindsay C Burrage
Manish J Butte
Olveen Carrasquillo
Ta Chen Peter Chang
Hsiao-Tuan Chao
Gary D Clark
Terra R Coakley
Laurel A Cobban
Joy D Cogan
F. Sessions Cole
Heather A Colley
Cynthia M Cooper
Heidi Cope
William J Craigen
Precilla D'Souza
Surendra Dasari
Mariska Davids
Jean M Davidson
Jyoti G Dayal
Esteban C Dell'Angelica
Shweta U Dhar
Naghmeh Dorrani
Daniel C Dorset
Emilie D Douine
David D Draper
Annika M Dries
Laura Duncan
David J Eckstein
Lisa T Emrick
Christine M Eng
Gregory M Enns
Cecilia Esteves
Tyra Estwick
Liliana Fernandez
Carlos Ferreira
Elizabeth L Fieg
Paul G Fisher
Brent L Fogel
Irman Forghani
Noah D Friedman
William A Gahl
Rena A Godfrey
Alica M Goldman
David B Goldstein
Jean-Philippe F Gourdine
Alana Grajewski
Catherine A Groden
Andrea L Gropman
Melissa Haendel
Rizwan Hamid
Neil A Hanchard
Frances High
Ingrid A Holm
Jason Hom
Alden Huang
Yong Huang
Rosario Isasi
Fariha Jamal
Yong-hui Jiang
Jean M Johnston
Angela L Jones
Lefkothea Karaviti
Emily G Kelley
David M Koeller
Isaac S Kohane
Jennefer N Kohler
Deborah Krakow
Donna M Krasnewich
Susan Korrick
Mary Koziura
Joel B Krier
Jennifer E Kyle
Seema R Lalani
Byron Lam
Brendan C Lanpher
Ian R Lanza
C. Christopher Lau
Jozef Lazar
Kimberly LeBlanc
Brendan H Lee
Hane Lee
Roy Levitt
Shawn E Levy
Richard A Lewis
Sharyn A Lincoln
Pengfei Liu
Xue Zhong Liu
Sandra K Loo
Joseph Loscalzo
Richard L Maas
Ellen F Macnamara
Calum A MacRae
Valerie V Maduro
Marta M Majcherska
May Christine V Malicdan
Laura A Mamounas
Teri A Manolio
Thomas C Markello
Ronit Marom
Martin G Martin
Julian A Martínez-Agosto
Shruti Marwaha
Thomas May
Jacob McCauley
Allyn McConkie-Rosell
Colleen E McCormack
Alexa T McCray
Jason D Merker
Thomas O Metz
Matthew Might
Eva Morava-Kozicz
Paolo M Moretti
Marie Morimoto
John J Mulvihill
David R Murdock
Avi Nath
Stan F Nelson
J. Scott Newberry
Sarah K Nicholas
Donna Novacic
Devin Oglesbee
James P Orengo
Stephen Pak
J. Carl Pallais
Christina GS Palmer
Jeanette C Papp
Neil H Parker
John A Phillips
Jennifer E Posey
John H Postlethwait
Lorraine Potocki
Barbara N Pusey
Genecee Renteri
Chloe M Reuter
Lynette Rives
Amy K Robertson
Lance H Rodan
Jill A Rosenfeld
Robb K Rowley
Ralph Sacco
Jacinda B Sampson
Susan L Samson
Mario Saporta
Judy Schaechter
Timothy Schedl
Daryl A Scott
Lisa Shakachite
Prashant Sharma
Kathleen Shields
Jimann Shin
Rebecca Signer
Catherine H Sillari
Edwin K Silverman
Janet S Sinsheimer
Lilianna Solnica-Krezel
Rebecca C Spillmann
Joan M Stoler
Nicholas Stong
David A Sweetser
Cecelia P Tamburro
Queenie K.-G Tan
Mustafa Tekin
Fred Telischi
Willa Thorson
Cynthia J Tifft
Camilo Toro
Alyssa A Tran
Tiina K Urv
Tiphanie P Vogel
Daryl M Waggott
Colleen E Wahl
Nicole M Walley
Chris A Walsh
Melissa Walker
Jennifer Wambach
Jijun Wan
Lee-kai Wang
Michael F Wangler
Patricia A Ward
Katrina M Waters
Bobbie-Jo M Webb-Robertson
Daniel Wegner
Monte Westerfield
Matthew T Wheeler
Anastasia L Wise
Lynne A Wolfe
Jeremy D Woods
Elizabeth A Worthey
Shinya Yamamoto
John Yang
Amanda J Yoon
Guoyun Yu
Diane B Zastrow
Chunli Zhao
Stephan Zuchner
William Gahl
Kelly Schoch - Department of Pediatrics, Division of Medical Genetics, Duke University Medical Center, Durham, North Carolina
Jennifer A Sullivan - Department of Pediatrics, Division of Medical Genetics, Duke University Medical Center, Durham, North Carolina
Filippo Pinto e Vairo - Department of Clinical Genomics, Mayo Clinic, Rochester, Minnesota
Pavel N Pichurin - Department of Clinical Genomics, Mayo Clinic, Rochester, Minnesota
Sarah A Ewing - Department of Clinical Genomics, Mayo Clinic, Rochester, Minnesota
Sarah S Barnett - Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minnesota
Eric W Klee - Department of Clinical Genomics, Mayo Clinic, Rochester, Minnesota
M. Scott Perry - Jane and John Justin Neuroscience Center, Cook Children's Medical Center, Fort Worth, Texas
Mary Kay Koenig - Department of Pediatrics, University of Texas Medical School at Houston, Houston, Texas
Catherine E Keegan - Division of Genetics, Department of Pediatrics, University of Michigan, Ann Arbor, Michigan
Jane L Schuette - Division of Genetics, Department of Pediatrics, University of Michigan, Ann Arbor, Michigan
Stephanie Asher - Translational Medicine & Human Genetics, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania
Yezmin Perilla-Young - Division of Pediatric Genetics and Metabolism, University of North Carolina, Chapel Hill, North Carolina
Laurie D Smith - Division of Pediatric Genetics and Metabolism, University of North Carolina, Chapel Hill, North Carolina
Jill A Rosenfeld - Baylor College of Medicine, Houston, Texas
Elizabeth Bhoj - Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Paige Kaplan - Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Dong Li - Children's Hospital of Philadelphia, Philadelphia, Pennsylvania
Renske Oegema - Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands
Ellen van Binsbergen - Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands
Bert van der Zwaag - Department of Genetics, University Medical Center Utrecht, Utrecht, The Netherlands
Marie Falkenberg Smeland - Department of Medical Genetics, University Hospital of North Norway, Tromsø, Norway
Ioana Cutcutache - Translational Medicine, UCB Pharma, Slough, United Kingdom
Matthew Page - Translational Medicine, UCB Pharma, Braine-l'Alleud, Belgium
Martin Armstrong - Translational Medicine, UCB Pharma, Braine-l'Alleud, Belgium
Angela E Lin - Medical Genetics Unit, Mass General Hospital for Children, Boston, Massachusetts
Marcie A Steeves - Medical Genetics Unit, Mass General Hospital for Children, Boston, Massachusetts
Nicolette den Hollander - Department of Clinical Genetics, Leiden University Medical Center, Leiden, The Netherlands
Mariëtte J.V Hoffer - Department of Clinical Genetics, Leiden University Medical Center, Leiden, The Netherlands
Margot R.F Reijnders - Department of Clinical Genetics, Maastricht University Medical Center, Maastricht, The Netherlands
Serwet Demirdas - Department of Clinical Genetics, Erasmus University Medical Center, Rotterdam, The Netherlands
Daniel C Koboldt - Nationwide Children’s Hospital, Columbus, Ohio
Dennis Bartholomew - Nationwide Children’s Hospital, Columbus, Ohio
Theresa Mihalic Mosher - Nationwide Children’s Hospital, Columbus, Ohio
Scott E Hickey - Department of Pediatrics, The Ohio State University College of Medicine, Columbus, Ohio
Christine Shieh - David Geffen School of Medicine, University of California–Los Angeles, California
Pedro A Sanchez-Lara - Department of Pediatrics, Cedars-Sinai Medical Center, Los Angeles, California
John M Graham - Department of Pediatrics, Cedars-Sinai Medical Center, Los Angeles, California
Kamer Tezcan - Department of Genetics, Kaiser Permanente, Sacramento, California
G.B Schaefer - Section of Genetics and Metabolism, University of Arkansas for Medical Sciences, Little Rock, Arkansas
Noelle R Danylchuk - Department of Genetic Counseling, University of Arkansas for Medical Sciences, Little Rock, Arkansas
Alexander Asamoah - Department of Pediatrics, University of Louisville School of Medicine, Louisville, Kentucky
Kelly E Jackson - Department of Pediatrics, University of Louisville School of Medicine, Louisville, Kentucky
Naomi Yachelevich - Clinical Genetics Services, Department of Pediatrics, New York University School of Medicine, New York, New York
Margaret Au - Department of Pediatrics, Cedars-Sinai Medical Center, Los Angeles, California
Luis A Pérez-Jurado - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Tjitske Kleefstra - Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands
Peter Penzes - Department of Physiology, Northwestern University Feinberg School of Medicine, Chicago, Illinois
Stephen A Wood - Griffith Institute for Drug Discovery, Griffith University, Brisbane, Australia
Thomas Burne - Queensland Brain Institute, The University of Queensland, Brisbane, Australia
Tyler Mark Pierson - Department of Pediatrics, Cedars-Sinai Medical Center, Los Angeles, California
Michael Piper - School of Biomedical Sciences, The University of Queensland, Brisbane, Australia
Jozef Gécz - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Lachlan A Jolly - University of Adelaide and Robinson Research Institute, Adelaide, Australia
Publication Details: Biological psychiatry (1969), Vol.87(2), pp.100-112
Publisher: Elsevier Inc
Academic Unit: UMMG Dept of Human Genetics (Dr. John T. Macdonald Foundation); UMMG Dept of Medicine - General Internal Medicine; UMMG Dept of Neurology - Neuromuscular Disorders Div; UMMG Dept of Pediatrics - Administration; Miller School of Medicine; UMMG Dept of Human Genetics - Clinical and Translational Genetics; UMMG Dept of Human Genetics (Dr. John T. Macdonald Foundation); Leadership Department; Miller School of Medicine; John P. Hussman Institute for Human Genomics; UMMG Department of Anesthesiology; UMMG Department of Neurology; UMMG Department of Ophthalmology; UMMG Department of Otolaryngology; UMMG Dept of Human Genetics - Clinical and Translational Genetics; John P. Hussman Institute for Human Genomics
Language: English
Resource Type: Journal article
PMID: 31443933
Record Identifier: 991031575990502976