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Microbes & neurodevelopment – Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala

Stilling, Roman M., Ryan, Feargal J., Hoban, Alan E., Shanahan, Fergus, Clarke, Gerard, Claesson, Marcus J., Dinan, Timothy G., Cryan, John F.·2015·Brain Behavior and Immunity

DOI 10.1016/j.bbi.2015.07.009

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Abstract

The mammalian amygdala is a key emotional brain region for eliciting social behaviour, critically involved in anxiety and fear-related behaviours, and hence a focus of research on neurodevelopmental and stress-related disorders such as autism and anxiety. Recently, increasing evidence implicates host-microbe interactions in the aetiology of these conditions. Germ-free (GF) mice, devoid of any microbiota throughout organismal maturation, are a well-established tool to study the effects of absence of the microbiota on host physiology. A growing body of independently replicated findings confirm that GF animals demonstrate altered anxiety-related behaviour and impaired social behaviour. However, the underlying mechanisms of this interaction and the nature of the pathways involved are only insufficiently understood. To further elucidate the molecular underpinnings of microbe-brain interaction, we therefore exploited unbiased genome-wide transcriptional profiling to determine gene expression in the amygdala of GF and GF mice that have been colonised after weaning. Using RNA-sequencing and a comprehensive downstream analysis pipeline we studied the amygdala transcriptome and found significant differences at the levels of differential gene expression, exon usage and RNA-editing. Most surprisingly, we noticed upregulation of several immediate early response genes such as Fos, Fosb, Egr2 or Nr4a1 in association with increased CREB signalling in GF mice. In addition, we found differential expression and recoding of several genes implicated in brain physiology processes such as neurotransmission, neuronal plasticity, metabolism and morphology. In conclusion, our data suggest altered baseline neuronal activity in the amygdala of germ-free animals, which is established during early life and may have implications for understanding development and treatment of neurodevelopmental disorders.

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Preface
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Authors: Stilling, R. M., Ryan, F. J., Hoban, A. E., Shanahan, F., Clarke, G., Claesson, M. J., Dinan, T. G., & Cryan, J. F.
Affiliations: University College Cork (IE)
Corresponding author: Stilling, Roman M.
Cryan, John F.
ORCID: Stilling, Roman M.
Ryan, Feargal J.
Shanahan, Fergus
Clarke, Gerard
Claesson, Marcus J.
Dinan, Timothy G.
Cryan, John F.
Venue: Brain Behavior and Immunity
Publisher: Elsevier BV
Published: 2015-11
Volume: 50
Pages: 209-220
ISSN: 0889-1591 (ISSN-L)
DOI: 10.1016/j.bbi.2015.07.009
OpenAlex: W889536224
Cited by: 233
References: 106
Citations by year: 2026: 12 · 2025: 11 · 2024: 20 · 2023: 15 · 2022: 17 · 2021: 27 · 2020: 30 · 2019: 27 · 2018: 26 · 2017: 19 · 2016: 26 · 2015: 3
FWCI: 10.70
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Behavior and Immunity (publishedVersion)
PubMed (publishedVersion)
Funders: Science Foundation Ireland (07/CE/B1368, 12/RC/2273, 11/SIRG/B2162)
Irish Research Council (GOIPD/2014/355)
Dept. of Agriculture, Food & Fisheries and Forestry and Enterprise Ireland
Brain and Behavior Research Foundation (20771)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: gut microbiota, germ-free mice, amygdala, brain development, host-microbe interactions, anxiety-like behavior, social behavior, immediate early genes, gene expression, exon usage, RNA editing, neuronal activity, neurodevelopmental disorders
MeSH terms: Amygdala, Animals, Interpersonal Relations, Male, Neurons, Signal Transduction, Genes, Immediate-Early, Gene Expression Profiling, Mice, Microbiota

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Microbes & neurodevelopment – Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala

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