Bi-allelic CAMSAP1 variants cause a clinically recognizable neuronal migration disorder.


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:
03 11 2022
Historique:
received: 04 08 2022
accepted: 27 09 2022
pubmed: 26 10 2022
medline: 9 11 2022
entrez: 25 10 2022
Statut: ppublish

Résumé

Non-centrosomal microtubules are essential cytoskeletal filaments that are important for neurite formation, axonal transport, and neuronal migration. They require stabilization by microtubule minus-end-targeting proteins including the CAMSAP family of molecules. Using exome sequencing on samples from five unrelated families, we show that bi-allelic CAMSAP1 loss-of-function variants cause a clinically recognizable, syndromic neuronal migration disorder. The cardinal clinical features of the syndrome include a characteristic craniofacial appearance, primary microcephaly, severe neurodevelopmental delay, cortical visual impairment, and seizures. The neuroradiological phenotype comprises a highly recognizable combination of classic lissencephaly with a posterior more severe than anterior gradient similar to PAFAH1B1(LIS1)-related lissencephaly and severe hypoplasia or absence of the corpus callosum; dysplasia of the basal ganglia, hippocampus, and midbrain; and cerebellar hypodysplasia, similar to the tubulinopathies, a group of monogenic tubulin-associated disorders of cortical dysgenesis. Neural cell rosette lineages derived from affected individuals displayed findings consistent with these phenotypes, including abnormal morphology, decreased cell proliferation, and neuronal differentiation. Camsap1-null mice displayed increased perinatal mortality, and RNAScope studies identified high expression levels in the brain throughout neurogenesis and in facial structures, consistent with the mouse and human neurodevelopmental and craniofacial phenotypes. Together our findings confirm a fundamental role of CAMSAP1 in neuronal migration and brain development and define bi-allelic variants as a cause of a clinically distinct neurodevelopmental disorder in humans and mice.

Identifiants

pubmed: 36283405
pii: S0002-9297(22)00415-3
doi: 10.1016/j.ajhg.2022.09.012
pmc: PMC9674946
pii:
doi:

Substances chimiques

Tubulin 0
CAMSAP1 protein, human 0
Microtubule-Associated Proteins 0
Camsap1 protein, mouse 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2068-2079

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : NIDCR NIH HHS
ID : R01 DE027091
Pays : United States
Organisme : Medical Research Council
ID : MC_PC_18047
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1001931
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1002279
Pays : United Kingdom
Organisme : NHGRI NIH HHS
ID : UM1 HG006542
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 authors declare no competing interests.

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Auteurs

Reham Khalaf-Nazzal (R)

Biomedical Sciences Department, Faculty of Medicine, Arab American University of Palestine, Jenin P227, Palestine.

James Fasham (J)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK; Peninsula Clinical Genetics Service, Royal Devon University Healthcare NHS Foundation Trust (Heavitree Hospital), Gladstone Road, Exeter EX1 2ED, UK.

Katherine A Inskeep (KA)

Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, USA; Institute for Genomic Medicine at Nationwide Children's Hospital, The Ohio State University College of Medicine, Columbus, OH 43205, USA.

Lauren E Blizzard (LE)

Division of Human Genetics, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, USA.

Joseph S Leslie (JS)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK.

Matthew N Wakeling (MN)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK.

Nishanka Ubeyratna (N)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK.

Tadahiro Mitani (T)

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

Jennifer L Griffith (JL)

Department of Neurology, Washington University School of Medicine, St. Louis, MO 63110, USA.

Wisam Baker (W)

Paediatrics Department, Dr. Khalil Suleiman Government Hospital, Jenin, Palestine.

Fida' Al-Hijawi (F)

Paediatrics Community Outpatient Clinics, Palestinian Ministry of Health, Jenin, Palestine.

Karen C Keough (KC)

Department of Pediatrics, Dell Medical School, 1400 Barbara Jordan Boulevard, Austin, TX 78723, USA; Child Neurology Consultants of Austin, 7940 Shoal Creek Boulevard, Suite 100, Austin, TX 78757, USA.

Alper Gezdirici (A)

Department of Medical Genetics, Başakşehir Çam and Sakura City Hospital, 34480 Istanbul, Turkey.

Loren Pena (L)

Division of Human Genetics, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229, USA.

Christine G Spaeth (CG)

Division of Human Genetics, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229, USA.

Peter D Turnpenny (PD)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK; Peninsula Clinical Genetics Service, Royal Devon University Healthcare NHS Foundation Trust (Heavitree Hospital), Gladstone Road, Exeter EX1 2ED, UK.

Joseph R Walsh (JR)

Department of Neurological Surgery, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, USA.

Randall Ray (R)

Departments of Pediatrics and Medical Genetics, Boston Children's Hospital and Harvard Medical School, Boston, MA 02115, USA.

Amber Neilson (A)

Genome Engineering & Stem Cell Center, Department of Genetics, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, USA.

Evguenia Kouranova (E)

Genome Engineering & Stem Cell Center, Department of Genetics, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, USA.

Xiaoxia Cui (X)

Genome Engineering & Stem Cell Center, Department of Genetics, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, USA.

David T Curiel (DT)

Department of Biomedical Engineering, McKelvey School of Engineering, Washington University in Saint Louis, St. Louis, MO 63130, USA; Division of Cancer Biology, Department of Radiation Oncology, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, USA; Biologic Therapeutics Center, Department of Radiation Oncology, School of Medicine, Washington University in Saint Louis, St. Louis, MO 63110, USA.

Davut Pehlivan (D)

Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA; Division of Neurology and Developmental Neuroscience, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030, USA; Texas Children's Hospital, Houston, TX 77030, USA.

Zeynep Coban Akdemir (ZC)

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.

James R Lupski (JR)

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, Baylor College of Medicine, Houston, TX 77030, USA; Texas Children's Hospital, Houston, TX 77030, USA.

William B Dobyns (WB)

Departments of Pediatrics and Genetics, University of Minnesota, Minneapolis, MN, USA.

Rolf W Stottmann (RW)

Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, USA; Institute for Genomic Medicine at Nationwide Children's Hospital, The Ohio State University College of Medicine, Columbus, OH 43205, USA; Division of Human Genetics, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 7016, Cincinnati, OH 45229, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229, USA.

Andrew H Crosby (AH)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK.

Emma L Baple (EL)

Department of Clinical and Biomedical Science, University of Exeter Faculty of Health and Life Science, RILD building, Barrack Road, Exeter EX2 5DW, UK; Peninsula Clinical Genetics Service, Royal Devon University Healthcare NHS Foundation Trust (Heavitree Hospital), Gladstone Road, Exeter EX1 2ED, UK. Electronic address: e.baple@exeter.ac.uk.

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