Fentanyl induces autism-like behaviours in mice by hypermethylation of the glutamate receptor gene Grin2b
Open accessAbstract
Background Environmental factors contribute to autism spectrum disorder. Fentanyl, one of the most widely used opioid analgesics in anaesthesia, can induce neurotoxicity, but its role in autism remains unknown. We determined whether fentanyl induced autism-like behaviours in young mice and the underlying mechanisms. Methods Young male and female mice received fentanyl at postnatal days 6, 8, and 10, and performed behavioural tests, including three-chamber social preference, elevated plus maze, grooming behaviour, and open-field test, from postnatal days 30-32. Expression of Grin2b, the gene encoding the GluN2B subunit of the N-methyl-d-aspartate receptor, was assessed in the anterior cingulate cortex of male mice using fluorescence in situ hybridisation histochemistry. We used bisulfite target sequencing to determine Grin2b hypermethylation sites after fentanyl treatment. In the specific activation and rescue experiments, we injected the mu opioid receptor agonist [D-Ala,2 N-MePhe,4 Gly-ol]-enkephalin (DAMGO) or Grin2b overexpression lentivirus into the anterior cingulate cortex of male mice. Results Fentanyl induced autism-like behaviours in both young male and female mice, and downregulated Grin2b expression (0.49-fold [0.08] vs 1.00-fold [0.09]; P<0.01) and GluN2B protein amounts (0.38-fold [0.07] vs 1.00-fold [0.12]; P<0.01) in the anterior cingulate cortex through hypermethylation of Grin2b. The mu-opioid receptor antagonist naloxone and overexpression of Grin2b in anterior cingulate cortex attenuated the fentanyl-induced effects, whereas DAMGO injection into the anterior cingulate cortex induced autism-like behaviours. Conclusions These data suggest that fentanyl induces autism-like behaviours in young mice via an epigenetic mechanism. Further research is required to determine possible clinical relevance to autism risk.
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Rare, often de novo, missense or truncating variants in GRIN1, GRIN2A, GRIN2B, and GRIA2 alter receptor kinetics, calcium signaling, and synaptic strength, and have been implicated in ASD.
“Rare, often de novo, missense or truncating variants in these genes alter receptor kinetics, calcium signaling, and synaptic strength, and have been implicated in ASD (Deutsch et al., 2022; Sheng et al., 2022; Gjerulfsen et al., 2024).”
From Biological hierarchy from genotype to phenotype in syndromic and non-syndromic autism spectrum disorder (2026) · cites this paper as Sheng et al., 2022
The introductory passage (listed under Editor’s key points; page unavailable) says that variations in GRIN2A and GRIN2B are associated with ASD. It does not establish the claim for GRIN1 or GRIA2, describe the variants as rare, often de novo, missense or truncating, or say that they alter receptor kinetics, calcium signaling, and synaptic strength. The paper’s Discussion (page unavailable) instead focuses on fentanyl-induced changes in Grin2b expression and autism-like behaviours in mice. (LLM, conf=0.88)
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- Authors
- Sheng, Z., Liu, Q., Cheng, C., Li, M., Barash, J., Kofke, W. A., Shen, Y., & Xie, Z.
- Affiliations
- Tongji University (CN)
- University of Pennsylvania (US)
- Harvard University (US)
- Corresponding author
- Shen, Yuan
- Xie, Zhongcong
- ORCID
- Venue
- British Journal of Anaesthesia
- Publisher
- Elsevier BV
- Published
- 2022-10
- Volume
- 129
- Issue
- 4
- Pages
- 544-554
- ISSN
- 0007-0912 (ISSN-L)
- OpenAlex
- W4282936428
- Cited by
- 28
- References
- 45
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 8 · 2023: 7
- FWCI
- 2.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- British Journal of Anaesthesia (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Harvard University
- National Natural Science Foundation of China (81720108012)
- Ministry of Science and Technology of the People's Republic of China (2021ZD0202003)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Anesthesia and Neurotoxicity Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- fentanyl, autism spectrum disorder, autism-like behavior, NR2B subunit, GluN2B, NMDA receptor, DNA methylation, epigenetic regulation, mu-opioid receptor, DAMGO, naloxone, anterior cingulate cortex, opioid neurotoxicity, social behavior, environmental risk factors
- MeSH terms
- Autism Spectrum Disorder, Analgesics, Opioid, Animals, Autistic Disorder, Female, Fentanyl, Male, Naloxone, Narcotic Antagonists, Receptors, N-Methyl-D-Aspartate, Receptors, Opioid, mu, Glutamic Acid, Enkephalin, Ala(2)-MePhe(4)-Gly(5)-, Mice
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