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Cytomegalovirus antibodies are associated with mood disorders, suicide, markers of neuroinflammation, and microglia activation in postmortem brain samples

Molecular Psychiatry volume 28, pages 5282–5292 (2023)Cite this article

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Abstract

Cytomegalovirus (CMV) is a common, neurotrophic herpesvirus that can be reactivated by inflammation and cause central nervous system disease. We hypothesize that CMV may contribute to the neuroinflammation that underlies some psychiatric disorders by (1) exacerbating inflammation through the induction of anti-viral immune responses, and (2) translating peripheral inflammation into neuroinflammation. We investigated whether the presence of anti-CMV antibodies in blood were associated with mental illness, suicide, neuroinflammation, and microglial density in the dorsolateral prefrontal cortex (DLPFC) in postmortem samples. Data (n = 114 with schizophrenia; n = 78 with bipolar disorder; n = 87 with depression; n = 85 controls) were obtained from the Stanley Medical Research Institute. DLPFC gene expression data from a subset of 82 samples were categorized into “high” (n = 30), and “low” (n = 52) inflammation groups based on a recursive two-step cluster analysis using expression data for four inflammation-related genes. Measurements of the ratio of non-ramified to ramified microglia, a proxy of microglial activation, were available for a subset of 49 samples. All analyses controlled for age, sex, and ethnicity, as well as postmortem interval, and pH for gene expression and microglial outcomes. CMV seropositivity significantly increased the odds of a mood disorder diagnosis (bipolar disorder: OR = 2.45; major depression: OR = 3.70) and among the psychiatric samples, of suicide (OR = 2.09). Samples in the upper tercile of anti-CMV antibody titers were more likely to be members of the “high” inflammation group (OR = 4.41, an effect driven by schizophrenia and bipolar disorder samples). CMV positive samples also showed an increased ratio of non-ramified to ramified microglia in layer I of the DLPFC (Cohen’s d = 0.81) as well as a non-significant increase in this ratio for the DLPFC as a whole (d = 0.56). The results raise the possibility that the reactivation of CMV contributes to the neuroinflammation that underlies some cases of psychiatric disorders.

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Fig. 1: Sample inclusion and exclusion flowchart.
Fig. 2: Associations between CMV infection and psychiatric disorders.
Fig. 3: Associations between CMV infection and suicide status.
Fig. 4: Associations between CMV infection and microglia activation.

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Data availability

Data used in current study are available at https://stanleyresearch.org. The statistical analysis R scripts used for current study are available upon request to the corresponding author.

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Acknowledgements

This work was supported by The William K. Warren Foundation, the National Institute of Mental Health (R01MH123652), and the National Institute of General Medical Sciences (P20GM121312).

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Authors and Affiliations

  1. Laureate Institute for Brain Research, Tulsa, OK, USA

    Haixia Zheng, Martin P. Paulus & Jonathan Savitz

  2. Oxley College of Health Sciences, The University of Tulsa, Tulsa, OK, USA

    Haixia Zheng, Martin P. Paulus & Jonathan Savitz

  3. Laboratory of Brain Research, Stanley Medical Research Institute, 9800 Medical Center Drive, Rockville, MD, USA

    Maree J. Webster

  4. Department of Neuroscience & Physiology, Upstate Medical University, Syracuse, NY, 13210, USA

    Cynthia Shannon Weickert

  5. Schizophrenia Research Laboratory, Neuroscience Research Australia, Randwick, NSW, 2031, Australia

    Cynthia Shannon Weickert

  6. Department of Psychiatry, University of British Columbia, Vancouver, BC, Canada

    Clare L. Beasley

  7. Stanley Division of Developmental Neurovirology, Johns Hopkins School of Medicine, Baltimore, MD, USA

    Robert H. Yolken

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Conceptualization, HZ, MJW, MPP, RHY, and JS; data collection, MJW, CSW, CLB, and RHY; methodology and data analysis, HZ, MJW, CSW, CLB, and RHY; manuscript writing—original draft preparation, HZ, and JS; manuscript writing—review and editing, HZ, MJW, CSW, CLB, MPP, RHY, and JS; All authors have read and agreed to the published version of the manuscript.

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Zheng, H., Webster, M.J., Weickert, C.S. et al. Cytomegalovirus antibodies are associated with mood disorders, suicide, markers of neuroinflammation, and microglia activation in postmortem brain samples. Mol Psychiatry 28, 5282–5292 (2023). https://doi.org/10.1038/s41380-023-02162-4

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