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Missense variants in ATP1A3 and FXYD gene family are associated with childhood-onset schizophrenia

Molecular Psychiatry volume 25, pages 821–830 (2020)Cite this article

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Abstract

Childhood-onset schizophrenia (COS) is a rare and severe form of schizophrenia defined as onset before age of 13. Here we report on two unrelated cases diagnosed with both COS and alternating hemiplegia of childhood (AHC), and for whom two distinct pathogenic de novo variants were identified in the ATP1A3 gene. ATP1A3 encodes the α-subunit of a neuron-specific ATP-dependent transmembrane sodium–potassium pump. Using whole exome sequencing data derived from a cohort of 17 unrelated COS cases, we also examined ATP1A3 and all of its interactors known to be expressed in the brain to establish if variants could be identified. This led to the identification of a third case with a possibly damaging missense mutation in ATP1A3 and three others cases with predicted pathogenic missense variants in the FXYD gene family (FXYD1, FXYD6, and FXYD6-FXYD2 readthrough). FXYD genes encode proteins that modulate the ATP-dependant pump function. This report is the first to identify variants in the same pathway for COS. Our COS study illustrates the interest of stratifying a complex condition according to the age of onset for the identification of deleterious variants. Whereas ATP1A3 is a replicated gene in rare neuropediatric diseases, this gene has previously been linked with COS in only one case report. The association with rare variants in FXYD gene family is novel and highlights the interest of exploring these genes in COS as well as in pediatric neurodevelopmental disorders.

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Acknowledgements

We thank the patients and the family members who participate in the study as well as the involved medical teams. We thank Daniel Rochefort and Sylvia Dobrezenicka for the technical support; also Edouard Henrion and Ousmane Diallo for their bioinformatics support. We also thank Dr Maryam Soleimani and Dr Laure Bera for their comments, as well as Dr Elodie Hainque for her advice.

Funding

The American cohort was supported by the National institute of Mental health (NIMH). Its genetic assessment was supported by the Genome Canada and Genome Quebec (Grant No. RMF_92086). Bioinformatics analysis was supported by the Canadian Institutes of Health Research (CIHR). Boris Chaumette receives a postdoctoral fellowship from the Healthy Brains for Healthy Lives project (Talent program).

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  1. These authors contributed equally: Boris Chaumette, Vladimir Ferrafiat.

Authors and Affiliations

  1. Montreal Neurological Institute and Hospital, Department of Neurology and Neurosurgery, McGill University, Montreal, QC, Canada

    Boris Chaumette, Alexandre Dionne-Laporte, Dan Spiegelman, Patrick A. Dion & Guy A. Rouleau

  2. Department of Child and Adolescent Psychiatry, CHU Rouen, Rouen, France

    Vladimir Ferrafiat & Priscille Gerardin

  3. Centre Référent Maladies Rares à Expression Psychiatrique, CHU Rouen, Rouen, France

    Vladimir Ferrafiat, Alice Goldenberg & Priscille Gerardin

  4. Department of Child and Adolescent Psychiatry, Arthur Rimbaud, CH Sotteville les Rouen, Rouen, France

    Vladimir Ferrafiat & Priscille Gerardin

  5. Department of Human Genetics, McGill University, Montreal, QC, Canada

    Amirthagowri Ambalavanan & Guy A. Rouleau

  6. Service de génétique, CHU de Rouen, Centre Normand de Génomique Médicale et Médecine Personnalisée, Rouen, France

    Alice Goldenberg

  7. Department of Child and Adolescent Psychiatry, Université Pierre et Marie Curie, Hôpital Pitié-Salpêtrière, AP-HP, Paris, France

    Claudine Laurent & David Cohen

  8. Department of Psychiatry, Stanford University, Stanford, CA, USA

    Claudine Laurent

  9. Institut des Systèmes Intelligents et Robotique, ISIR, Université ́Pierre et Marie Curie, CNRS UMR 7222, Paris, France

    David Cohen

  10. Child Psychiatry Branch Research Group at the National Institute of Mental Health (NIMH), National Institutes of Health (NIH), Bethesda, MD, USA

    Judith Rapoport

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Chaumette, B., Ferrafiat, V., Ambalavanan, A. et al. Missense variants in ATP1A3 and FXYD gene family are associated with childhood-onset schizophrenia. Mol Psychiatry 25, 821–830 (2020). https://doi.org/10.1038/s41380-018-0103-8

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