Human Borna disease virus 1 encephalitis shows marked pro-inflammatory biomarker and tissue immunoactivation during the course of disease

Emerg Microbes Infect. 2022 Dec;11(1):1843-1856. doi: 10.1080/22221751.2022.2098831.

Abstract

Human Borna disease virus 1 (BoDV-1) encephalitis is a severe emerging disease with a very high case-fatality rate. While the clinical disease, case definitions, diagnostic algorithms and neuropathology have been described, very little is known about the immunological processes of human BoDV-1 encephalitis. Here, we analyzed serum and cerebrospinal fluid (CSF) samples from 10 patients with fatal BoDV-1 encephalitis for changes of different cytokines, chemokines, growth factors and other biomarkers over time. From one of these individuals, also autoptic formalin-fixed brain tissue was analyzed for the expression of inflammatory biomarkers by mRNA levels and immunostaining; in a further patient, only formalin-fixed brain tissue was available and examined in addition. A marked and increasing immune activation from the initial phase to the last phase of acute BoDV-1 encephalitis is shown in serum and CSF, characterized by cytokine concentration changes (IFNγ, IL-5, IL-6, IL-9, IL-10, IL-12p40, IL-13, IL-18, TGF-β1) with a predominantly pro-inflammatory pattern over time. IFNγ production was demonstrated in endothelial cells, astrocytes and microglia, IL-6 in activated microglia, and TGF-β1 in endothelial cells, activated astrocytes and microglia. This was paralleled by an increase of chemokines (CCL-2, CCL-5, CXCL-10, IL-8) to attract immune cells to the site of infection, contributing to inflammation and tissue damage. Pathologically low growth factor levels (BDNF, β-NGF, PDGF) were seen. Changed levels of arginase and sTREM further fostered the pro-inflammatory state. This dysbalanced, pro-inflammatory state likely contributes importantly to the fatal outcome of human BoDV-1 encephalitis, and might be a key target for possible treatment attempts.

Keywords: BoDV-1; astrocyte; bornavirus; chemokine; cytokine; microglia.

MeSH terms

  • Biomarkers
  • Borna disease virus*
  • Chemokines
  • Cytokines / metabolism
  • Encephalitis* / virology
  • Endothelial Cells / metabolism
  • Formaldehyde
  • Humans
  • Interleukin-6
  • Transforming Growth Factor beta1

Substances

  • Biomarkers
  • Chemokines
  • Cytokines
  • Interleukin-6
  • Transforming Growth Factor beta1
  • Formaldehyde

Grants and funding

This work was supported by Bundesministerium für Bildung und Forschung [grant number 01KI2005C]; Joachim Herz Stiftung [grant number 34901609]; Bornavirus Focal Point Bavaria [grant number 01KI2002].