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Deficiency of the ywhaz gene, involved in neurodevelopmental disorders, alters brain activity and behaviour in zebrafish

Molecular Psychiatry volume 27, pages 3739–3748 (2022)Cite this article

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Abstract

Genetic variants in YWHAZ contribute to psychiatric disorders such as autism spectrum disorder and schizophrenia, and have been related to an impaired neurodevelopment in humans and mice. Here, we have used zebrafish to investigate the mechanisms by which YWHAZ contributes to neurodevelopmental disorders. We observed that ywhaz expression was pan-neuronal during developmental stages and restricted to Purkinje cells in the adult cerebellum, cells that are described to be reduced in number and size in autistic patients. We then performed whole-brain imaging in wild-type and ywhaz CRISPR/Cas9 knockout (KO) larvae and found altered neuronal activity and connectivity in the hindbrain. Adult ywhaz KO fish display decreased levels of monoamines in the hindbrain and freeze when exposed to novel stimuli, a phenotype that can be reversed with drugs that target monoamine neurotransmission. These findings suggest an important role for ywhaz in establishing neuronal connectivity during development and modulating both neurotransmission and behaviour in adults.

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Fig. 1: Whole-brain imaging methods.
Fig. 2: ywhaz mRNA is widely expressed during zebrafish development but restricted to the Purkinje cells in the cerebellum in adults.
Fig. 3: Decreased coherence in neuronal activity and decreased connectivity in the hindbrain of zebrafish ywhaz−/− larvae.
Fig. 4: Alterations in the monoamine neurotransmission in the hindbrain of adult KO.
Fig. 5: Treatment with fluoxetine and quinpirole reverses the freezing behaviour observed in ywhaz−/− mutants.

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Acknowledgements

GCaMP6s albino zebrafish embryos were generated by the National Institute of Genetics (Japan) and obtained from Dr. Matt Parker from the University of Portsmouth, UK. The Tg(aldoca:gap43-Venus) line was obtained from Masahiko Hibi from the Bioscience and Biotechnology Center of Nagoya University, Japan. Tg(olig2:egfp)vu12 brains were obtained from the Center for Developmental Biology, UMR 5547 CNRS, Toulouse, France. Major financial support for this research was received by BC from the Spanish ‘Ministerio de Ciencia, Innovación y Universidades’ (RTI2018-100968-B-100, PID2021-1277760B-I100), the ‘Ministerio de Sanidad, Servicios Sociales e Igualdad/Plan Nacional Sobre Drogas’ (PNSD-2017I050 and PNSD-2020I042), ‘Generalitat de Catalunya/AGAUR’ (2017-SGR-738), ICREA Academia 2021, and the European Union H2020 Program [H2020/2014-2020] under grant agreements n° 667302 (CoCA) and Eat2beNICE (728018). EA-G was supported by the Ministerio de Economía y Competitividad (Spanish Government) and the EU H2020 programme (Eat2beNICE-728018). GC, EG and PL-A acknowledge financial support from the Spanish Ministerio de Economía y Competitividad (MINECO) through the “Severo Ochoa” programme for Centres of Excellence in R&D CEX2019-000910-S), MINECO/FEDER Ramon y Cajal programme (RYC-2015-17935); Laserlab-Europe EU-H2020 GA no. 871124, Fundació Privada Cellex, Fundación Mig-Puig and from the Generalitat de Catalunya through the CERCA programme. FA acknowledges financial support from the Spanish ‘Ministerio de Ciencia, Innovación y Universidades’ (PID2019-107738RB-I00, MICINN/FEDER) and SGR (2017SGR1255).

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Author notes

  1. These authors contributed equally: Ester Antón-Galindo, Elisa Dalla Vecchia.

  2. These authors jointly supervised this work: Bru Cormand, William H. J. Norton, Noèlia Fernàndez-Castillo.

Authors and Affiliations

  1. Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain

    Ester Antón-Galindo, Marc Guasch-Piqueras, Concepció Arenas, Carlos Herrera-Úbeda, Jordi Garcia-Fernàndez, Bru Cormand & Noèlia Fernàndez-Castillo

  2. Centro de Investigación Biomédica en Red de Enfermedades raras (CIBERER), Madrid, 28029, Spain

    Ester Antón-Galindo, Bru Cormand & Noèlia Fernàndez-Castillo

  3. Institut de Biomedicina de la Universitat de Barcelona (IBUB), Barcelona, Catalunya, 08028, Spain

    Ester Antón-Galindo, Marc Guasch-Piqueras, Carlos Herrera-Úbeda, Jordi Garcia-Fernàndez, Bru Cormand & Noèlia Fernàndez-Castillo

  4. Institut de Recerca Sant Joan de Déu (IRSJD), Esplugues de Llobregat, Catalunya, 08950, Spain

    Ester Antón-Galindo, Bru Cormand & Noèlia Fernàndez-Castillo

  5. Department of Genetics and Genome Biology, College of Life Sciences, University of Leicester, Leicester, LE1 7RH, UK

    Elisa Dalla Vecchia & William H. J. Norton

  6. RIKEN Center for Brain Science, Wako-shi, Saitama, 351-0198, Japan

    Javier G. Orlandi

  7. ICFO - Institut de Ciències Fotòniques, The Barcelona Institute of Science and Technology, Castelldefels, Catalunya, 08860, Spain

    Gustavo Castro, Emilio J. Gualda & Pablo Loza-Alvarez

  8. Department of Neuroscience, Psychology and Behaviour, College of Life Sciences, University of Leicester, Leicester, LE1 7RH, UK

    Andrew M. J. Young

  9. Departament de Biologia cel·lular, Fisiologia i Immunologia, Facultat de Biologia, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain

    Fernando Aguado

  10. Institute of Neurosciences, Universitat de Barcelona, Barcelona, Catalunya, 08028, Spain

    Fernando Aguado

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  1. Ester Antón-Galindo
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  2. Elisa Dalla Vecchia
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  15. Noèlia Fernàndez-Castillo
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Contributions

NF-C, WHJN and BC conceived and coordinated the study, NF-C designed the experimental approaches for whole-brain imaging, WHJN designed the behavioural and pharmacological approaches and BC designed the genetic approaches. EA-G designed and conducted the whole-brain imaging and behavioural experiments and wrote the paper, EDV designed and conducted the CRISPR/Cas9, ISH, IHC, HPLC and behavioural experiments. AMJY contributed to the HPLC experiments. CH-U and JG-F carried out the phylogenetic analysis. MG-P contributed to the behavioural experiments. CA contributed to the statistical analysis of the behavioural tests. JGO designed the pipeline and methodology for the whole-brain imaging analyses, GC and EG conducted the whole-brain imaging recordings, EA-G analysed the imaging data, FA contributed to the whole-brain imaging analysis and PL-A supervised the whole-brain imaging recordings. All authors discussed and commented on the manuscript.

Corresponding authors

Correspondence to Bru Cormand, William H. J. Norton or Noèlia Fernàndez-Castillo.

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Antón-Galindo, E., Dalla Vecchia, E., Orlandi, J.G. et al. Deficiency of the ywhaz gene, involved in neurodevelopmental disorders, alters brain activity and behaviour in zebrafish. Mol Psychiatry 27, 3739–3748 (2022). https://doi.org/10.1038/s41380-022-01577-9

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