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Shank3 Deficiency is Associated With Altered Profile of Neurotransmission Markers in Pups and Adult Mice

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Abstract

Alterations in the balance between excitation and inhibition, especially in the brain’s critical developmental periods, are considered an integral part of the pathophysiology of autism. However, the precise mechanisms have not yet been established. SH3 and multiple Ankyrin repeat domains 3 (Shank3) deficient mice represent a well-established transgenic model of a neurodevelopmental disorder with autistic symptomatology. In this study, we characterize the consequences of Shank3 deficiency according to (1) expression of specific markers of different neuronal populations in pups and adult mice and (2) social behaviour and anxiety in adult mice. Our research found enhanced expression of serotonin transporter and choline acetyltransferase in the hippocampus and hypothalamus in Shank3-deficient pups. We demonstrated marked brain region differences in expression of excitatory glutamatergic markers in pups and adult Shank3 deficient mice. We also observed reduced expression of inhibitory GABAergic markers and GABA receptor subunits in several brain areas in both pups and adult Shank3 deficient mice. Further analysis of dopaminergic brain areas (nucleus accumbens, ventral tegmental area) revealed lower expression levels of GABAergic markers in adult Shank3 deficient mice. Adult Shank3− deficient mice exhibited excessive repetitive behaviour, a higher level of anxiety, and lower locomotor activity. Our data support the theory of an imbalance between excitatory and inhibitory neurotransmission in conditions of abnormal SHANK3 protein. We therefore suggest that autism-like conditions are accompanied by reduced expression of GABAergic markers in the brain during early development as well as in the adult age, which could be associated with long-lasting behavioural abnormalities.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

This study was funded by the Grant Agency of the Ministry of Education and the Slovak Academy of Sciences (VEGA 2/0155/20, VEGA 2/0148/21), as well as by the Slovak Research and Development Agency project (APVV-15-205 and APVV-15-0045). We would like to thank Michael Sabo for proofreading of the manuscript.

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Authors and Affiliations

  1. Biomedical Research Center, Institute of Experimental Endocrinology, The Slovak Academy of Sciences, Dubravska cesta 9, 845 05, Bratislava, Slovakia

    Stanislava Bukatova, Alexandra Reichova, Anna Sadlonova, Boris Mravec, Jan Bakos & Zuzana Bacova

  2. Faculty of Medicine, Institute of Molecular Biomedicine, Comenius University in Bratislava, Bratislava, Slovakia

    Emese Renczes & Johan Filo

  3. Faculty of Medicine, Institute of Physiology, Comenius University in Bratislava, Bratislava, Slovakia

    Boris Mravec, Daniela Ostatnikova & Jan Bakos

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  1. Stanislava Bukatova
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  2. Emese Renczes
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  9. Zuzana Bacova
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Contributions

All authors had full access to all the data in the study and take responsibility for the integrity of the data and accuracy of the data analysis. Conceptualization: JB; ZB; Investigation: SB; ER; AR; JF; AS; BM.; Resources: ER, DO; ZB, JB; Writing - Original Draft: SB; ER; JB; ZB; Writing - Review & Editing: SB, DO, JB; ZB; Funding Acquisition: DO; JB; ZB.

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Correspondence to Jan Bakos.

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Bukatova, S., Renczes, E., Reichova, A. et al. Shank3 Deficiency is Associated With Altered Profile of Neurotransmission Markers in Pups and Adult Mice. Neurochem Res 46, 3342–3355 (2021). https://doi.org/10.1007/s11064-021-03435-6

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