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Microbial modulation via cross-fostering prevents the effects of pervasive environmental stressors on microglia and social behavior, but not the dopamine system

Molecular Psychiatry volume 28, pages 2549–2562 (2023)Cite this article

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Abstract

Environmental toxicant exposure, including air pollution, is increasing worldwide. However, toxicant exposures are not equitably distributed. Rather, low-income and minority communities bear the greatest burden, along with higher levels of psychosocial stress. Both air pollution and maternal stress during pregnancy have been linked to neurodevelopmental disorders such as autism, but biological mechanisms and targets for therapeutic intervention remain poorly understood. We demonstrate that combined prenatal exposure to air pollution (diesel exhaust particles, DEP) and maternal stress (MS) in mice induces social behavior deficits only in male offspring, in line with the male bias in autism. These behavioral deficits are accompanied by changes in microglial morphology and gene expression as well as decreased dopamine receptor expression and dopaminergic fiber input in the nucleus accumbens (NAc). Importantly, the gut-brain axis has been implicated in ASD, and both microglia and the dopamine system are sensitive to the composition of the gut microbiome. In line with this, we find that the composition of the gut microbiome and the structure of the intestinal epithelium are significantly shifted in DEP/MS-exposed males. Excitingly, both the DEP/MS-induced social deficits and microglial alterations in males are prevented by shifting the gut microbiome at birth via a cross-fostering procedure. However, while social deficits in DEP/MS males can be reversed by chemogenetic activation of dopamine neurons in the ventral tegmental area, modulation of the gut microbiome does not impact dopamine endpoints. These findings demonstrate male-specific changes in the gut-brain axis following DEP/MS and suggest that the gut microbiome is an important modulator of both social behavior and microglia.

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Fig. 1: DEP/MS impairs social behavior in male but not female offspring.
Fig. 2: DEP/MS induces a hyper-ramified phenotype in male but not female microglia.
Fig. 3: Chemogenetic activation of VTA dopamine neurons rescues sociability in DEP/MS males.
Fig. 4: DEP/MS shifts the composition of the gut microbiome and epithelial gene expression and anatomy.
Fig. 5: Cross-fostering at birth prevents DEP/MS-induced social deficits in male offspring.
Fig. 6: Cross-fostering prevents changes in microglial hyper-ramification but does not alter dopaminergic endpoints.

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Acknowledgements

We would like to thank all the members of the Bilbo lab, past and present, for their helpful discussions and feedback. We would also like to thank the MGH Next-Generation Sequencing Core and the Duke Center for Genomic and Computational Biology for their assistance with RNA and 16S sequencing, and Lucas Li and Laura Dubois of the Duke Proteomics and Metabolomics Core Facility for conducting metabolite analyses. We thank the animal care staff at MGH and Duke University for their excellent animal care. This work was supported by R01 ES025549 to SDB, R01 ES033056 to SDB, F32 ES029912 to CJS, K99 ES033278 to CJS, and by the Robert and Donna Landreth Family Foundation.

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Authors and Affiliations

  1. Department of Psychology and Neuroscience, Duke University, Durham, NC, USA

    Caroline J. Smith, Danielle N. Rendina, Karen E. Malacon, Dang M. Nguyen, Benjamin A. Devlin, Madeline J. Clark, Lauren Burgett, Jason H. Zhang & Staci D. Bilbo

  2. Department of Pediatrics, Harvard Medical School, Massachusetts General Hospital, Lurie Center for Autism, Charlestown, MA, USA

    Marcy A. Kingsbury, Jessica J. Tran, Kevin Chen & Malvika S. Iyer

  3. Department of Pediatrics, Division of Newborn Medicine, Harvard Medical School, Boston Children’s Hospital, Boston, MA, USA

    Ravikiran M. Raju

  4. Massachusetts Institute of Technology, Picower Institute for Learning and Memory, Cambridge, MA, USA

    Ravikiran M. Raju

  5. Department of Neurobiology, Duke University Medical School, Durham, NC, USA

    Madeline J. Clark & Staci D. Bilbo

  6. Department of Molecular Biology, Massachusetts General Hospital, Boston, MA, USA

    Murat Cetinbas & Ruslan I. Sadreyev

  7. Department of Genetics, Massachusetts General Hospital, Boston, MA, USA

    Murat Cetinbas

  8. Department of Pathology, Harvard Medical School, Massachusetts General Hospital, Boston, MA, USA

    Ruslan I. Sadreyev

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  1. Caroline J. Smith
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Contributions

CJS and SDB designed the study. CJS, DNR, MAK, KEM, DMN, JJT, MJC, LB, JHZ, KC, and MSI conducted experiments and analyzed data. DNR, BAD, RMR, MC, and RIS assisted with sequencing data analysis. CJS and SDB wrote the manuscript. All authors approved the final version of the manuscript.

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Correspondence to Staci D. Bilbo.

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Smith, C.J., Rendina, D.N., Kingsbury, M.A. et al. Microbial modulation via cross-fostering prevents the effects of pervasive environmental stressors on microglia and social behavior, but not the dopamine system. Mol Psychiatry 28, 2549–2562 (2023). https://doi.org/10.1038/s41380-023-02108-w

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