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The Hypothalamic–Pituitary–Adrenal Axis and Serotonin Metabolism in Individual Brain Nuclei of Mice with Genetic Disruption of the NK1 Receptor Exposed to Acute Stress

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Abstract

Mice lacking the substance P (SP) neurokinin-1 (NK1) receptor (NK1R−/−mice) were used to investigate whether SP affects serotonin (5-HT) function in the brain and to assess the effects of acute immobilisation stress on the hypothalamic–pituitary–adrenocortical (HPA) axis and 5-HT turnover in individual brain nuclei. Basal HPA activity and the expression of hypothalamic corticotropin-releasing hormone (CRH) in wild-type (WT)- and NK1R−/− mice were identical. Stress-induced increases in plasma ACTH concentration were considerably higher in NK1R−/− mice than in WT mice while corticosterone concentrations were equally elevated in both mouse lines. Acute stress did not alter the expression of CRH. In the dorsal raphe nucleus (DRN), basal 5-HT turnover was increased in NK1R−/− mice and a 15 min stress further magnified 5-HT utilisation in this region. In the frontoparietal cortex, medial prefrontal cortex, central nucleus of amygdala, and the hippocampal CA1 region, stress increased 5-HT and/or 5-hydroxyindoleacetic acid (5-HIAA) concentrations to a similar extent in WT and NK1R−/− mice. 5-HT turnover in the hypothalamic paraventricular nucleus was not affected by stress, but stress induced similar increases in 5-HT and 5-HIAA in the ventromedial and dorsomedial hypothalamic nuclei in WT and NK1R−/− mice. Our findings indicate that NK1 receptor activation suppresses ACTH release during acute stress but does not exert sustained inhibition of the HPA axis. Genetic deletion of the NK1 receptor accelerates 5-HT turnover in DRN under basal and stress conditions. No differences between the responses of serotonergic system to acute stress in WT and NK1R−/− mice occur in forebrain nuclei linked to the regulation of anxiety and neuroendocrine stress responses.

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Acknowledgements

The authors would like to thank Ms. Britta Schwarten for her excellent technical assistance.

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  1. Juraj Culman and Stephan Mühlenhoff have been equally contributed to this work.

Authors and Affiliations

  1. Institute of Experimental and Clinical Pharmacology, University Hospital of Schleswig-Holstein, Campus Kiel, Arnold-Heller-Strasse 3, 24105, Kiel, Germany

    Juraj Culman, Stephan Mühlenhoff & Annegret Blume

  2. Institute of Medical Informatics and Statistics, University Hospital of Schleswig-Holstein, Campus Kiel, Brunswiker Strasse 10, 24105, Kiel, Germany

    Jürgen Hedderich

  3. Department of Nuclear Medicine, Molecular Imaging, Diagnostics and Therapy, University Hospital of Schleswig-Holstein, Campus Kiel, Arnold-Heller-Strasse 3, 24105, Kiel, Germany

    Juraj Culman, Ulf Lützen & Yi Zhao

  4. Department of Cell and Developmental Biology, University College London, Gower Street, London, WC1E 6BT, UK

    Stephen P. Hunt

  5. CNS Pharma Consulting LLC, Spring, TX, USA

    Nadia M. J. Rupniak

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  1. Juraj Culman
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Contributions

Juraj Culman conceived and designed the study, isolated brain nuclei, supervised the study and drafted and approved the article. Stephan Mühlenhoff performed experimental work (5-HT determination and CRH expression). Annegret Blume performed experimental work (ACTH determination, CRH expression). Jürgen Hedderich performed statistical analyses. Ulf Lützen contributed to the design of experiments and approved the manuscript. Stephen P Hunt provided mice for the study and made critical revision of the manuscript. Nadia M.J. Rupniak revised the manuscript for intellectual content and contributed to creating its final version. Yi Zhao conceived the work, performed the experimental work (ACTH and indole determination) and collected most of the data.

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Correspondence to Juraj Culman.

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Culman, J., Mühlenhoff, S., Blume, A. et al. The Hypothalamic–Pituitary–Adrenal Axis and Serotonin Metabolism in Individual Brain Nuclei of Mice with Genetic Disruption of the NK1 Receptor Exposed to Acute Stress. Cell Mol Neurobiol 38, 1271–1281 (2018). https://doi.org/10.1007/s10571-018-0594-5

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