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Monoallelic de novo variants in DDX17 cause a neurodevelopmental disorder

Monoallelic de novo variants in DDX17 cause a neurodevelopmental disorder
Monoallelic de novo variants in DDX17 cause a neurodevelopmental disorder
DDX17 is an RNA helicase shown to be involved in critical processes during the early phases of neuronal differentiation. Globally, we compiled a case-series of 11 patients with neurodevelopmental phenotypes harbouring de novo monoallelic variants in DDX17. All 11 patients in our case series had a neurodevelopmental phenotype, whereby intellectual disability, delayed speech and language, and motor delay predominated.

We performed in utero cortical electroporation in the brain of developing mice, assessing axon complexity and outgrowth of electroporated neurons, comparing wild-type and Ddx17 knockdown. We then undertook ex vivo cortical electroporation on neuronal progenitors to quantitatively assess axonal development at a single cell resolution. Mosaic ddx17 crispants and heterozygous knockouts in Xenopus tropicalis were generated for assessment of morphology, behavioural assays, and neuronal outgrowth measurements. We further undertook transcriptomic analysis of neuroblastoma SH-SY5Y cells, to identify differentially expressed genes in DDX17-KD cells compared to controls.

Knockdown of Ddx17 in electroporated mouse neurons in vivo showed delayed neuronal migration as well as decreased cortical axon complexity. Mouse primary cortical neurons revealed reduced axon outgrowth upon knockdown of Ddx17 in vitro. The axon outgrowth phenotype was replicated in crispant ddx17 tadpoles and in heterozygotes. Heterozygous tadpoles had clear neurodevelopmental defects and showed an impaired neurobehavioral phenotype. Transcriptomic analysis identified a statistically significant number of differentially expressed genes involved in neurodevelopmental processes in DDX17-KD cells compared to control cells.
We have identified potential neurodevelopment disease-causing variants in a gene not previously associated with genetic disease, DDX17. We provide evidence for the role of the gene in neurodevelopment in both mammalian and non-mammalian species and in controlling the expression of key neurodevelopment genes.
Neurodevelopmental/motor delay, RNA helicase, Neuronal development, mouse model, xenopus model, novel gene disorder
0006-8950
Seaby, Eleanor G.
ec948f42-007c-4bd8-9dff-bb86278bf03f
Godwin, Annie
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Meyer-Dilhet, Géraldine
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Clerc, Valentine
66823af7-aa3d-42cc-9398-ddd5cce27728
Grand, Xavier
1c77fa75-1f91-43d8-aedf-5ba319fdc007
Fletcher, Tia
5df97201-5840-4c09-9941-cc844f1c6bc5
Monteiro, Laloe
66be56f7-eb13-499e-9b0b-46a28a98462a
Kerkhofs, Martijn
9f35a152-008b-4fa8-be8d-726279030dcb
Carelli, Valerio
8f8d92cc-2ba1-474d-bf34-fd7bc952bda7
Palombo, Flavia
19f011e6-d7a6-4d78-9f34-22251423e299
Lachlan, Katherine
175ce889-ede8-477e-93eb-afefc1af5dda
Baralle, Diana
faac16e5-7928-4801-9811-8b3a9ea4bb91
Bourgeois, Cyril F.
09b408d3-1ebf-4e28-9f29-8cb2ed41a609
Ennis, Sarah
7b57f188-9d91-4beb-b217-09856146f1e9
et al.
Seaby, Eleanor G.
ec948f42-007c-4bd8-9dff-bb86278bf03f
Godwin, Annie
90ba88ea-4a7c-44f4-bf70-9015c0d33194
Meyer-Dilhet, Géraldine
58b6462a-32cf-4236-a38e-35823d558cea
Clerc, Valentine
66823af7-aa3d-42cc-9398-ddd5cce27728
Grand, Xavier
1c77fa75-1f91-43d8-aedf-5ba319fdc007
Fletcher, Tia
5df97201-5840-4c09-9941-cc844f1c6bc5
Monteiro, Laloe
66be56f7-eb13-499e-9b0b-46a28a98462a
Kerkhofs, Martijn
9f35a152-008b-4fa8-be8d-726279030dcb
Carelli, Valerio
8f8d92cc-2ba1-474d-bf34-fd7bc952bda7
Palombo, Flavia
19f011e6-d7a6-4d78-9f34-22251423e299
Lachlan, Katherine
175ce889-ede8-477e-93eb-afefc1af5dda
Baralle, Diana
faac16e5-7928-4801-9811-8b3a9ea4bb91
Bourgeois, Cyril F.
09b408d3-1ebf-4e28-9f29-8cb2ed41a609
Ennis, Sarah
7b57f188-9d91-4beb-b217-09856146f1e9

Seaby, Eleanor G., Godwin, Annie and Meyer-Dilhet, Géraldine , et al. (2024) Monoallelic de novo variants in DDX17 cause a neurodevelopmental disorder. Brain, [awae320]. (doi:10.1093/brain/awae320).

Record type: Article

Abstract

DDX17 is an RNA helicase shown to be involved in critical processes during the early phases of neuronal differentiation. Globally, we compiled a case-series of 11 patients with neurodevelopmental phenotypes harbouring de novo monoallelic variants in DDX17. All 11 patients in our case series had a neurodevelopmental phenotype, whereby intellectual disability, delayed speech and language, and motor delay predominated.

We performed in utero cortical electroporation in the brain of developing mice, assessing axon complexity and outgrowth of electroporated neurons, comparing wild-type and Ddx17 knockdown. We then undertook ex vivo cortical electroporation on neuronal progenitors to quantitatively assess axonal development at a single cell resolution. Mosaic ddx17 crispants and heterozygous knockouts in Xenopus tropicalis were generated for assessment of morphology, behavioural assays, and neuronal outgrowth measurements. We further undertook transcriptomic analysis of neuroblastoma SH-SY5Y cells, to identify differentially expressed genes in DDX17-KD cells compared to controls.

Knockdown of Ddx17 in electroporated mouse neurons in vivo showed delayed neuronal migration as well as decreased cortical axon complexity. Mouse primary cortical neurons revealed reduced axon outgrowth upon knockdown of Ddx17 in vitro. The axon outgrowth phenotype was replicated in crispant ddx17 tadpoles and in heterozygotes. Heterozygous tadpoles had clear neurodevelopmental defects and showed an impaired neurobehavioral phenotype. Transcriptomic analysis identified a statistically significant number of differentially expressed genes involved in neurodevelopmental processes in DDX17-KD cells compared to control cells.
We have identified potential neurodevelopment disease-causing variants in a gene not previously associated with genetic disease, DDX17. We provide evidence for the role of the gene in neurodevelopment in both mammalian and non-mammalian species and in controlling the expression of key neurodevelopment genes.

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Accepted/In Press date: 11 October 2024
e-pub ahead of print date: 15 October 2024
Keywords: Neurodevelopmental/motor delay, RNA helicase, Neuronal development, mouse model, xenopus model, novel gene disorder

Identifiers

Local EPrints ID: 495348
URI: http://eprints.soton.ac.uk/id/eprint/495348
ISSN: 0006-8950
PURE UUID: a3ed5ecf-8cdb-497f-9f99-f7188ecbe8a7
ORCID for Eleanor G. Seaby: ORCID iD orcid.org/0000-0002-6814-8648
ORCID for Diana Baralle: ORCID iD orcid.org/0000-0003-3217-4833
ORCID for Sarah Ennis: ORCID iD orcid.org/0000-0003-2648-0869

Catalogue record

Date deposited: 11 Nov 2024 17:57
Last modified: 12 Nov 2024 03:06

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Contributors

Author: Eleanor G. Seaby ORCID iD
Author: Annie Godwin
Author: Géraldine Meyer-Dilhet
Author: Valentine Clerc
Author: Xavier Grand
Author: Tia Fletcher
Author: Laloe Monteiro
Author: Martijn Kerkhofs
Author: Valerio Carelli
Author: Flavia Palombo
Author: Katherine Lachlan
Author: Diana Baralle ORCID iD
Author: Cyril F. Bourgeois
Author: Sarah Ennis ORCID iD
Corporate Author: et al.

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