Cited by 71Genetics and Neurodevelopmental DisordersGenomics and Rare DiseasesEpilepsy research and treatment

Spatially clustering de novo variants in CYFIP2, encoding the cytoplasmic FMRP interacting protein 2, cause intellectual disability and seizures

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Abstract

CYFIP2, encoding the evolutionary highly conserved cytoplasmic FMRP interacting protein 2, has previously been proposed as a candidate gene for intellectual disability and autism because of its important role linking FMRP-dependent transcription regulation and actin polymerization via the WAVE regulatory complex (WRC). Recently, de novo variants affecting the amino acid p.Arg87 of CYFIP2 were reported in four individuals with epileptic encephalopathy. We here report 12 independent patients harboring a variety of de novo variants in CYFIP2 broadening the molecular and clinical spectrum of a novel CYFIP2-related neurodevelopmental disorder. Using trio whole-exome or -genome sequencing, we identified 12 independent patients carrying a total of eight distinct de novo variants in CYFIP2 with a shared phenotype of intellectual disability, seizures, and muscular hypotonia. We detected seven different missense variants, of which two occurred recurrently (p.(Arg87Cys) and p.(Ile664Met)), and a splice donor variant in the last intron for which we showed exon skipping in the transcript. The latter is expected to escape nonsense-mediated mRNA decay resulting in a truncated protein. Despite the large spacing in the primary structure, the variants spatially cluster in the tertiary structure and are all predicted to weaken the interaction with WAVE1 or NCKAP1 of the actin polymerization regulating WRC-complex. Preliminary genotype-phenotype correlation indicates a profound phenotype in p.Arg87 substitutions and a more variable phenotype in other alterations. This study evidenced a variety of de novo variants in CYFIP2 as a novel cause of mostly severe intellectual disability with seizures and muscular hypotonia.

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  • These CYFIP2 variants spatially cluster in the tertiary structure and are all predicted to weaken the interaction with WAVE1 or NCKAP1 in the WAVE complex.

    “These variants spatially cluster in the tertiary structure and are all predicted to weaken the interaction with WAVE1 or NCKAP1 in the WAVE complex121.”

    From The WAVE complex in developmental and adulthood brain disorders (2025) · cites this paper as [121]

    The Variant modelling and Discussion passages (page unavailable) place five missense variants close together at the CYFIP2–WAVE1 interface and predict weakened WAVE1 interactions. They also predict disrupted NCKAP1 contacts for Ala455Pro and the splice variant, but do not place those variants in the same spatial cluster. Thus, the interaction prediction is supported, while the claim that all the variants spatially cluster is not. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • One of these eight CYFIP2 variants is a splice variant, while the remaining seven are missense variants.

    “One is a splice variant, while the remaining seven are missense variants (Table 2q).”
  • The phenotype in the heterozygous Cyfip2 knockout mouse model was milder than the severe phenotype observed in humans heterozygous for CYFIP2 variants.

    “However, the phenotype in the heterozygous Cyfip2 KO mouse model was milder than the severe phenotype observed in humans heterozygous for variants121.”
  • A total of eight distinct de novo variants in CYFIP2 were identified among 12 independent patients who shared a phenotype characterized by intellectual disability, seizures, and muscular hypotonia.

    “Using trio next-generation sequencing, a total of eight distinct de novo variants in CYFIP2 were identified among 12 independent patients who shared a phenotype characterized by ID, seizures, and muscular hypotonia.”

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Authors
Study, D. D. D. (., Zweier, M., Begemann, A., McWalter, K., Cho, M. T., Abela, L., Banka, S., Behring, B., Berger, A., Brown, C. W., Carneiro, M., Chen, J., Cooper, G. M., Finnila, C. R., Guillen Sacoto, M. J., Henderson, A., Hüffmeier, U., Joset, P., Kerr, B., Lesca, G., Leszinski, G. S., McDermott, J. H., Meltzer, M. R., Monaghan, K. G., Mostafavi, R., Õunap, K., Plecko, B., Powis, Z., Purcarin, G., Reimand, T., Riedhammer, K. M., Schreiber, J. M., Sirsi, D., Wierenga, K. J., Wojcik, M. H., Papuc, S. M., Steindl, K., Sticht, H., & Rauch, A.
Affiliations
  • University of Zurich (CH)
  • University of Manchester (GB)
  • Nuremberg Hospital (DE)
  • Klinikum Weiden (DE)
  • University of Tennessee Health Science Center (US)
  • Hospices Civils de Lyon (FR)
  • HudsonAlpha Institute for Biotechnology (US)
  • Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
  • Lyon 1 Université (FR)
  • TUM Klinikum (DE)
  • Children's National (US)
  • Le Bonheur Children's Hospital (US)
  • Tartu University Hospital (EE)
  • Medical University of Graz (AT)
  • Ambry Genetics (United States) (US)
  • University of Oklahoma Health Sciences Center (US)
  • Broad Institute (US)
Corresponding author
Rauch, Anita
Venue
European Journal of Human Genetics
Published
2019-01-21
Volume
27
Issue
5
Pages
747-759
ISSN
  • 1018-4813 (ISSN-L)
  • 1476-5438
OpenAlex
W2911076095
Cited by
71
References
9
Citations by year
2026: 7 · 2025: 12 · 2024: 8 · 2023: 10 · 2022: 12 · 2021: 10 · 2020: 8 · 2019: 3
FWCI
4.91
Type
journal article
Language
en
Open access
Locations
  • European Journal of Human Genetics (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Research Explorer (The University of Manchester) (publishedVersion, other-oa)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
  • mediaTUM – the media and publications repository of the Technical University Munich (Technical University Munich) (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • National Science Foundation (WT098051)
  • Wellcome Trust
  • National Institute for Health and Care Research (HICF-1009-003, ACF-2017-06-014)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (179547, 320030)
  • Universität Zürich
  • National Institutes of Health (NIH T32)
  • National Heart, Lung, and Blood Institute
  • National Human Genome Research Institute (HG008900, UM1HG008900)
  • National Eye Institute (HG008900)
  • National Institute of General Medical Sciences (T32GM007748)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomics and Rare Diseases
  • Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
Keywords
CYFIP2, de novo mutations, intellectual disability, seizures, hypotonia, WAVE regulatory complex, actin polymerization, FMRP, exon skipping, nonsense-mediated mRNA decay, genotype-phenotype correlation, neurodevelopmental disorders
MeSH terms
Child, Child, Preschool, Cytoplasm, Female, Humans, Infant, Male, Intellectual Disability, Models, Molecular, Mutation, Seizures, Facies, Adaptor Proteins, Signal Transducing

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