Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice
Social behaviour is regulated by activity of host-associated microbiota across multiple species. However, the molecular mechanisms mediating this relationship remain elusive. We therefore determined the dynamic, stimulus-dependent transcriptional regulation of germ-free (GF) and GF mice colonised po...
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eLife Sciences Publications Ltd
2018-05-01
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| Online Access: | https://elifesciences.org/articles/33070 |
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doaj-e259a28345df44e49b5200bc4b4769402021-05-05T15:53:13ZengeLife Sciences Publications LtdeLife2050-084X2018-05-01710.7554/eLife.33070Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient miceRoman M Stilling0https://orcid.org/0000-0001-7637-5851Gerard M Moloney1https://orcid.org/0000-0002-3672-1390Feargal J Ryan2https://orcid.org/0000-0002-1565-4598Alan E Hoban3Thomaz FS Bastiaanssen4https://orcid.org/0000-0001-6891-734XFergus Shanahan5Gerard Clarke6https://orcid.org/0000-0001-9771-3979Marcus J Claesson7https://orcid.org/0000-0002-5712-0623Timothy G Dinan8John F Cryan9https://orcid.org/0000-0001-5887-2723APC Microbiome Institute, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; School of Microbiology, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; School of Microbiology, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; Department of Psychiatry and Neurobehavioural Science, University College Cork, Cork, IrelandAPC Microbiome Institute, University College Cork, Cork, Ireland; Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandSocial behaviour is regulated by activity of host-associated microbiota across multiple species. However, the molecular mechanisms mediating this relationship remain elusive. We therefore determined the dynamic, stimulus-dependent transcriptional regulation of germ-free (GF) and GF mice colonised post weaning (exGF) in the amygdala, a brain region critically involved in regulating social interaction. In GF mice the dynamic response seen in controls was attenuated and replaced by a marked increase in expression of splicing factors and alternative exon usage in GF mice upon stimulation, which was even more pronounced in exGF mice. In conclusion, we demonstrate a molecular basis for how the host microbiome is crucial for a normal behavioural response during social interaction. Our data further suggest that social behaviour is correlated with the gene-expression response in the amygdala, established during neurodevelopment as a result of host-microbe interactions. Our findings may help toward understanding neurodevelopmental events leading to social behaviour dysregulation, such as those found in autism spectrum disorders (ASDs).https://elifesciences.org/articles/33070Social behaviourneurodevelopmentmicrobiomeamygdalaactivity-dependent transcriptionautism |
| collection |
DOAJ |
| language |
English |
| format |
Article |
| sources |
DOAJ |
| author |
Roman M Stilling Gerard M Moloney Feargal J Ryan Alan E Hoban Thomaz FS Bastiaanssen Fergus Shanahan Gerard Clarke Marcus J Claesson Timothy G Dinan John F Cryan |
| spellingShingle |
Roman M Stilling Gerard M Moloney Feargal J Ryan Alan E Hoban Thomaz FS Bastiaanssen Fergus Shanahan Gerard Clarke Marcus J Claesson Timothy G Dinan John F Cryan Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice eLife Social behaviour neurodevelopment microbiome amygdala activity-dependent transcription autism |
| author_facet |
Roman M Stilling Gerard M Moloney Feargal J Ryan Alan E Hoban Thomaz FS Bastiaanssen Fergus Shanahan Gerard Clarke Marcus J Claesson Timothy G Dinan John F Cryan |
| author_sort |
Roman M Stilling |
| title |
Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice |
| title_short |
Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice |
| title_full |
Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice |
| title_fullStr |
Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice |
| title_full_unstemmed |
Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice |
| title_sort |
social interaction-induced activation of rna splicing in the amygdala of microbiome-deficient mice |
| publisher |
eLife Sciences Publications Ltd |
| series |
eLife |
| issn |
2050-084X |
| publishDate |
2018-05-01 |
| description |
Social behaviour is regulated by activity of host-associated microbiota across multiple species. However, the molecular mechanisms mediating this relationship remain elusive. We therefore determined the dynamic, stimulus-dependent transcriptional regulation of germ-free (GF) and GF mice colonised post weaning (exGF) in the amygdala, a brain region critically involved in regulating social interaction. In GF mice the dynamic response seen in controls was attenuated and replaced by a marked increase in expression of splicing factors and alternative exon usage in GF mice upon stimulation, which was even more pronounced in exGF mice. In conclusion, we demonstrate a molecular basis for how the host microbiome is crucial for a normal behavioural response during social interaction. Our data further suggest that social behaviour is correlated with the gene-expression response in the amygdala, established during neurodevelopment as a result of host-microbe interactions. Our findings may help toward understanding neurodevelopmental events leading to social behaviour dysregulation, such as those found in autism spectrum disorders (ASDs). |
| topic |
Social behaviour neurodevelopment microbiome amygdala activity-dependent transcription autism |
| url |
https://elifesciences.org/articles/33070 |
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