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Journal article

WNT signalling control by KDM5C during development affects cognition

Abstract:
Although KDM5C is one of the most frequently mutated genes in X-linked intellectual disability, the exact mechanisms that lead to cognitive impairment remain unknown. Here we use human patient-derived induced pluripotent stem cells and Kdm5c knockout mice to conduct cellular, transcriptomic, chromatin and behavioural studies. KDM5C is identified as a safeguard to ensure that neurodevelopment occurs at an appropriate timescale, the disruption of which leads to intellectual disability. Specifically, there is a developmental window during which KDM5C directly controls WNT output to regulate the timely transition of primary to intermediate progenitor cells and consequently neurogenesis. Treatment with WNT signalling modulators at specific times reveal that only a transient alteration of the canonical WNT signalling pathway is sufficient to rescue the transcriptomic and chromatin landscapes in patient-derived cells and to induce these changes in wild-type cells. Notably, WNT inhibition during this developmental period also rescues behavioural changes of Kdm5c knockout mice. Conversely, a single injection of WNT3A into the brains of wild-type embryonic mice cause anxiety and memory alterations. Our work identifies KDM5C as a crucial sentinel for neurodevelopment and sheds new light on KDM5C mutation-associated intellectual disability. The results also increase our general understanding of memory and anxiety formation, with the identification of WNT functioning in a transient nature to affect long-lasting cognitive function.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s41586-024-07067-y

Authors


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Role:
Author
ORCID:
0009-0006-6273-9814
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Role:
Author
ORCID:
0000-0001-7771-0850
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Institution:
University of Oxford
Division:
MSD
Department:
NDM
Sub department:
Oxford Ludwig Institute
Role:
Author


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Funder identifier:
https://ror.org/04pw6fb54
Grant:
UL1 TR002541


Publisher:
Springer Nature
Journal:
Nature More from this journal
Volume:
627
Issue:
8004
Pages:
594-603
Place of publication:
England
Publication date:
2024-02-21
Acceptance date:
2024-01-12
DOI:
EISSN:
1476-4687
ISSN:
0028-0836
Pmid:
38383780


Language:
English
Pubs id:
1632060
Local pid:
pubs:1632060
Deposit date:
2024-04-05

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