Social interaction-induced activation of RNA splicing in the amygdala of microbiome-deficient mice
Open accessAbstract
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).
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In response to social interaction, there are profound alterations in the transcriptome and spliceosome in the amygdala of GF mice, which may contribute to the social deficits observed.
“In response to social interaction, there are profound alterations in the transcriptome and spliceosome in the amygdala of GF mice, which may contribute to the social deficits observed (Stilling et al., 2018).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Stilling et al., 2018
The Results sections on gene expression and alternative splicing report a distinct transcriptomic response and markedly increased splicing in the amygdala of GF mice after social interaction; the Results also report reduced social interaction in GF mice. The Discussion, however, interprets increased splicing as a possible compensatory response that supports behavioural performance, rather than as a contributor to the social deficits. (LLM, conf=0.86)
Experimental — accuracy not yet measuredGerm-free animals show enhanced expression of gene splicing factors and alternative exon usage.
“as well as enhanced expression of gene splicing factors and alternative exon usage (Stilling et al., 2018).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Stilling et al., 2018
GF mice are unable to distinguish between a novel and a familiar conspecific, representing a cognitive deficit in the identification of social novelty.
“Moreover, while a conventionally colonized mouse will prefer to spend more time interacting with a novel conspecific over a familiar one, GF mice are unable to distinguish between either animal, which represents a cognitive deficit in the identification of social novelty (Desbonnet et al., 2014;Stilling et al., 2018).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Stilling et al., 2018
The Methods (3-chamber social interaction test; page unavailable) describe a choice between one conspecific and a non-social object, not between a novel and a familiar conspecific. The Results report reduced social interaction in germ-free mice, but do not test whether they can identify social novelty (searched: familiar conspecific, social novelty preference). (LLM, conf=0.78)
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Activity-induced histone modifications govern Neurexin-1 mRNA splicing and memory preservation
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Gut microbiota regulates key modulators of social behavior
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The Amygdala, Autism and Anxiety
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Social odours covary with bacterial community in the anal secretions of wild meerkats
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Microbes can help explain the evolution of host altruism
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Neuronal activity-regulated alternative mRNA splicing
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Social Neuroeconomics: The Influence of Microbiota in Partner-Choice and Sociality
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Self-citationThe gut microbiome in neurological disorders
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Self-citationHuman Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice
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Self-citationGutted! Unraveling the Role of the Microbiome in Major Depressive Disorder
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Self-citationSocioeconomic Status and the Gut Microbiome: A TwinsUK Cohort Study
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Microbiota‐gut‐brain axis as a regulator of reward processes
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Self-citationThe role of the microbiome in the neurobiology of social behaviour
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The role of the gut microbiome in the development of schizophrenia
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Self-citationGastrointestinal involvement of autism spectrum disorder: focus on gut microbiota
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Volatility as a Concept to Understand the Impact of Stress on the Microbiome
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Self-citationThe Brain-Gut-Microbiome System: Pathways and Implications for Autism Spectrum Disorder
Chernikova, M. A., Flores, G. D., Kilroy, E., Labus, J. S., Mayer, E. A., & Aziz‐Zadeh, L. (2021) · Nutrients · doi:10.3390/nu13124497 · Cited by 86 · see citing works
The gut virome is associated with stress-induced changes in behaviour and immune responses in mice
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Self-citationGut-brain axis: A matter of concern in neuropsychiatric disorders…!
Naveed, M., Zhou, Q.-G., Chu, X., Taleb, A., Meng, F. J., Ahmed, B., Zhang, Y., Fukunaga, K., & Han, F. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110051 · Cited by 81 · see citing works
A biological framework for emotional dysregulation in alcohol misuse: from gut to brain
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Self-citationGut-brain axis serotonergic responses to acute stress exposure are microbiome-dependent
Lyte, J. M., Gheorghe, C. E., Goodson, M. S., Kelley‐Loughnane, N., Dinan, T. G., Cryan, J. F., & Clarke, G. (2020) · Neurogastroenterology & Motility · doi:10.1111/nmo.13881 · Cited by 77 · see citing works
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Modeling human embryo development with embryonic and extra-embryonic stem cells
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Prediction and perception: Insights for (and from) tinnitus
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Slow update of internal representations impedes synchronization in autism
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Self-citationGururajan, A., van de Wouw, M., Boehme, M., Becker, T., O’Connor, R., Bastiaanssen, T. F. S., Moloney, G. M., Lyte, J. M., Silva, A. P. V., Merckx, B., et al. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.05.004 · Cited by 63 · see citing works
Self-citationAlteration of Gut Microbiota: New Strategy for Treating Autism Spectrum Disorder
Liu, J., Gao, Z., Chuanqi, L., Liu, T., Gao, J., Cai, Y., & Fan, X. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.792490 · Cited by 62 · see citing works
Gut Microbiota and Neuroplasticity
Murciano-Brea, J., García-Montes, M. E., Geuna, S., & Herrera‐Rincon, C. (2021) · Cells · doi:10.3390/cells10082084 · Cited by 59 · see citing works
Enduring neurobehavioral effects induced by microbiota depletion during the adolescent period
Lach, G., Fülling, C., Bastiaanssen, T. F. S., Fouhy, F., Donovan, A. N. O., Ventura‐Silva, A. P., Stanton, C., Dinan, T. G., & Cryan, J. F. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-01073-0 · Cited by 55 · see citing works
Self-citationManipulation of gut microbiota blunts the ventilatory response to hypercapnia in adult rats
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Neural Circuits for Social Interactions: From Microcircuits to Input-Output Circuits
Xu, S., Jiang, M., Liu, X., Sun, Y., Yang, L., Yang, Q., & Bai, Z. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.768294 · Cited by 47 · see citing works
Human Gut Microbiota for Diagnosis and Treatment of Depression
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Microbial memories: Sex‐dependent impact of the gut microbiome on hippocampal plasticity
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Self-citationAlteration of Gut Microbiota in Autism Spectrum Disorder: An Overview
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Rewiring the Brain Through the Gut: Insights into Microbiota–Nervous System Interactions
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The Many Faces of Microbiota-Gut-Brain Axis in Autism Spectrum Disorder
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The Role of MicroRNA and Microbiota in Depression and Anxiety
Rosa, J. M., Formolo, D. A., Yu, J., Lee, T. H.-Y., & Yau, S. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.828258 · Cited by 37 · see citing works
Gut Microbiota and Aging: Traditional Chinese Medicine and Modern Medicine
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Self-citationSeeking the Psilocybiome: Psychedelics meet the microbiota-gut-brain axis
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Sociability in a non-captive macaque population is associated with beneficial gut bacteria
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Microbial regulation of microRNA expression in the brain–gut axis
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Exploring Interactions between the Gut Microbiota and Social Behavior through Nutrition
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Without a bug’s life: Germ-free rodents to interrogate microbiota-gut-neuroimmune interactions
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Bioinformatic and cell-based tools for pooled CRISPR knockout screening in mosquitos
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Infant fecal microbiota composition and attention to emotional faces.
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Self-citationThe gut microbiome and pharmacology: a prescription for therapeutic targeting of the gut–brain axis
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Self-citationIdentifying essential genes across eukaryotes by machine learning
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The matrix revolutions: towards the decoding of the plant chromatin three-dimensional reality
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Parkinson’s Disease and the Metal–Microbiome–Gut–Brain Axis: A Systems Toxicology Approach
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The host genetics affects gut microbiome diversity in Chinese depressed patients
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Modulating host gene expression via gut microbiome–microRNA interplay to treat human diseases
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A review on gut microbiota and miRNA crosstalk: implications for Alzheimer’s disease
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The milk-based diet of infancy and the gut microbiome
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Mental Disorders Linked to Crosstalk between The Gut Microbiome and The Brain
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A Sympoietic View of Life: Gaia as a Holobiont CommunityPreprint
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Host Microbiota Regulates Central Nervous System Serotonin Receptor 2C Editing in Rodents
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Self-citationGut–brain axis in health and brain disease
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Self-citationHolobiont Development: Embryology and Ecological Succession
Gilbert, S. F. (2023) · Human Development · doi:10.1159/000534203 · Cited by 10 · see citing works
Inter-kingdom communication and the sympoietic way of life
Gilbert, S. F. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1427798 · Cited by 8 · see citing works
Sex‐dependent impact of microbiota status on cerebral μ‐opioid receptor density in fischer rats
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Tryptophan Metabolism and the Microbiome-Gut-Brain Axis
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- Authors
- Stilling, R. M., Moloney, G. M., Ryan, F. J., Hoban, A. E., Bastiaanssen, T. F., 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
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2018-05-29
- Volume
- 7
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5995540
- OpenAlex
- W2805802451
- Cited by
- 106
- References
- 90
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 8 · 2023: 10 · 2022: 13 · 2021: 21 · 2020: 26 · 2019: 15 · 2018: 3 · 2017: 1
- FWCI
- 5.78
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Arrow@dit (Dublin Institute of Technology) (acceptedVersion)
- Cork Open Research Archive (University College Cork, Ireland) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- Funders
- Science Foundation Ireland (12/RC/2273)
- Irish Research Council (GOIPD/2014/355)
- Irish Health Board
- National Alliance for Research on Schizophrenia and Depression (20771)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- host microbiome, germ-free mice, amygdala, RNA splicing, social interaction, social behavior, splicing factors, alternative exon usage, host-microbe interactions, brain development, autism spectrum disorder, gene expression regulation
- MeSH terms
- Autism Spectrum Disorder, Gastrointestinal Microbiome, RNA Splicing Factors, Amygdala, Animals, Animal Communication, Disease Models, Animal, Germ-Free Life, Male, Nerve Tissue Proteins, RNA Splicing, Weaning, Mice, Neurogenesis
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