Serotonin transporter variant drives preventable gastrointestinal abnormalities in development and function
Open accessAbstract
Autism spectrum disorder (ASD) is an increasingly common behavioral condition that frequently presents with gastrointestinal (GI) disturbances. It is not clear, however, how gut dysfunction relates to core ASD features. Multiple, rare hyperfunctional coding variants of the serotonin (5-HT) transporter (SERT, encoded by SLC6A4) have been identified in ASD. Expression of the most common SERT variant (Ala56) in mice increases 5-HT clearance and causes ASD-like behaviors. Here, we demonstrated that Ala56-expressing mice display GI defects that resemble those seen in mice lacking neuronal 5-HT. These defects included enteric nervous system hypoplasia, slow GI transit, diminished peristaltic reflex activity, and proliferation of crypt epithelial cells. An opposite phenotype was seen in SERT-deficient mice and in progeny of WT dams given the SERT antagonist fluoxetine. The reciprocal phenotypes that resulted from increased or decreased SERT activity support the idea that 5-HT signaling regulates enteric neuronal development and can, when disturbed, cause long-lasting abnormalities of GI function. Administration of a 5-HT4 agonist to Ala56 mice during development prevented Ala56-associated GI perturbations, suggesting that excessive SERT activity leads to inadequate 5-HT4-mediated neurogenesis. We propose that deficient 5-HT signaling during development may contribute to GI and behavioral features of ASD. The consequences of therapies targeting SERT during pregnancy warrant further evaluation.
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Murine models with SERT abnormalities during development, such as SERT knockout mice and mice receiving SSRIs during pregnancy and breastfeeding, exhibit ENS hyperplasia and long-lasting deficits in ENS-mediated functions, including in vivo and in vitro GI motility.
“Murine models possessing abnormalities in SERT during development, such as SERT knockout mice, as well as mice that receive selective serotonin reuptake inhibitors during pregnancy and breastfeeding, exhibit ENS hyperplasia as well as long-lasting deficits in ENS-mediated functions, including in vivo and in vitro gastrointestinal motility [33].”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [33]
The increase in EC cells and Tph1 transcripts in SERT Ala56 mice may contribute to their increased whole blood 5-HT levels.
“both of which may be contributory to the demonstrated increase in whole blood 5-HT levels [33].”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [33]
SERT Ala56 mice have abnormally slowed in vivo and in vitro motility throughout the entire intestine, including a decrease in the frequency and speed of colonic peristaltic contractions.
“As a consequence of abnormal ENS development, SERT Ala56 mice have abnormally slowed in vivo and in vitro motility throughout the entire intestine, including a decrease in the frequency and speed of colonic peristaltic contractions”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [33]
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- Authors
- Margolis, K. G., Li, Z., Stevanovic, K., Saurman, V., Israelyan, N., Anderson, G. M., Snyder, I., Veenstra-VanderWeele, J., Blakely, R. D., & Gershon, M. D.
- Affiliations
- Columbia University (US)
- Yale University (US)
- Vanderbilt University (US)
- Corresponding author
- Margolis, Kara Gross
- ORCID
- Venue
- Journal of Clinical Investigation
- Published
- 2016-04-25
- Volume
- 126
- Issue
- 6
- Pages
- 2221-2235
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC4887174
- OpenAlex
- W2343547480
- Cited by
- 139
- References
- 77
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 12 · 2023: 23 · 2022: 17 · 2021: 15 · 2020: 16 · 2019: 17 · 2018: 10 · 2017: 11 · 2016: 4
- FWCI
- 8.91
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Autism Research Institute (NS15547, DK093786)
- National Institutes of Health (5r01ns015547-39, NS15547, MH096972)
- National Institute of Mental Health (P50MH096972, R01MH094604)
- National Institute of Diabetes and Digestive and Kidney Diseases (K08DK093786)
- National Institute of Neurological Disorders and Stroke (R01-NS015547)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- autism spectrum disorder, serotonin transporter, gastrointestinal dysfunction, fluoxetine, 5-HT4 receptor agonist, peristalsis, gut-brain axis, mouse model
- MeSH terms
- Autism Spectrum Disorder, Animals, Female, Gastrointestinal Motility, Humans, Male, Mice, Inbred C57BL, Mice, Mutant Strains, Pregnancy, Serotonin, Genetic Variation, Enteric Nervous System, Mice, Knockout, Models, Animal, Gastrointestinal Tract, Serotonin Plasma Membrane Transport Proteins, Mice, Neurogenesis, Mice, 129 Strain
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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