Cited by 209Neurobiology and Insect Physiology ResearchGut microbiota and healthGenetics and Neurodevelopmental Disorders

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Drosophila Histone Demethylase KDM5 Regulates Social Behavior through Immune Control and Gut Microbiota Maintenance

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Chen, Kun, Luan, Xiaoting, Liu, Qisha, Wang, Jianwei, Chang, Xinxia, Snijders, Antoine M., Mao, Jian-Hua, Secombe, Julie, Dan, Zhou, Chen, Jian-Huan, Wang, Zibin, Dong, Xiao, Qiu, Chen, Chang, Xiaoai, Zhang, Dong, Celniker, Susan E., Liu, Xingyin·2019·Cell Host & Microbe

DOI 10.1016/j.chom.2019.02.003PMC PMC6749836

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Abstract

Loss-of-function mutations in the histone demethylases KDM5A, KDM5B, or KDM5C are found in intellectual disability (ID) and autism spectrum disorders (ASD) patients. Here, we use the model organism Drosophila melanogaster to delineate how KDM5 contributes to ID and ASD. We show that reducing KDM5 causes intestinal barrier dysfunction and changes in social behavior that correlates with compositional changes in the gut microbiota. Therapeutic alteration of the dysbiotic microbiota through antibiotic administration or feeding with a probiotic Lactobacillus strain partially rescues the behavioral, lifespan, and cellular phenotypes observed in kdm5-deficient flies. Mechanistically, KDM5 was found to transcriptionally regulate component genes of the immune deficiency (IMD) signaling pathway and subsequent maintenance of host-commensal bacteria homeostasis in a demethylase-dependent manner. Together, our study uses a genetic approach to dissect the role of KDM5 in the gut-microbiome-brain axis and suggests that modifying the gut microbiome may provide therapeutic benefits for ID and ASD patients.

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Authors: Chen, K., Luan, X., Liu, Q., Wang, J., Chang, X., Snijders, A. M., Mao, J.-H., Secombe, J., Dan, Z., Chen, J.-H., Wang, Z., Dong, X., Qiu, C., Chang, X., Zhang, D., Celniker, S. E., & Liu, X.
Affiliations: Second Affiliated Hospital of Nanjing Medical University (CN)
State Key Laboratory of Reproductive Medicine (CN)
Lawrence Berkeley National Laboratory (US)
Albert Einstein College of Medicine (US)
Jiangnan University (CN)
Nanjing Medical University (CN)
Corresponding author: Liu, Xingyin
ORCID: Chen, Kun
Liu, Qisha
Chang, Xinxia
Snijders, Antoine M.
Mao, Jian-Hua
Secombe, Julie
Chen, Jian-Huan
Wang, Zibin
Dong, Xiao
Qiu, Chen
Zhang, Dong
Celniker, Susan E.
Liu, Xingyin
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2019-04
Volume: 25
Issue: 4
Pages: 537-552.e8
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2019.02.003
PMC: PMC6749836
OpenAlex: W2924425749
Cited by: 208
References: 65
Citations by year: 2026: 18 · 2025: 27 · 2024: 34 · 2023: 37 · 2022: 37 · 2021: 35 · 2020: 14 · 2019: 6
FWCI: 10.99
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 376 d)
Locations: Cell Host & Microbe (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders: Lawrence Berkeley National Laboratory
Laboratory Directed Research and Development (DE AC02-05CH11231, M2B)
National Natural Science Foundation of China (81671983, 81871628)
National Institutes of Health (31671311, R01GM112783)
Qinglan Project of Jiangsu Province of China
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
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
Keywords: KDM5, histone demethylase, social behavior, intellectual disability, autism spectrum disorder, gut microbiota, intestinal barrier dysfunction, probiotics, Lactobacillus, lifespan, Drosophila melanogaster
MeSH terms: Autism Spectrum Disorder, Gastrointestinal Microbiome, Animals, Behavior, Animal, Disease Models, Animal, Drosophila, Drosophila melanogaster, Female, Humans, Intestinal Mucosa, Male, Social Behavior, Drosophila Proteins, Histone Demethylases

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Drosophila Histone Demethylase KDM5 Regulates Social Behavior through Immune Control and Gut Microbiota Maintenance

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