Vimentin Regulates Chemokine Expression and NOD2 Activation in Brain Endothelium during Group B Streptococcal Infection

Infect Immun. 2021 Nov 16;89(12):e0034021. doi: 10.1128/IAI.00340-21. Epub 2021 Sep 7.

Abstract

Streptococcus agalactiae (group B Streptococcus, or GBS) is an opportunistic pathogen capable of causing invasive disease in susceptible individuals, including the newborn. Currently, GBS is the leading cause of meningitis in the neonatal period. We have recently shown that GBS interacts directly with host type III intermediate filament vimentin to gain access to the central nervous system. This results in characteristic meningeal inflammation and disease progression; however, the specific role of vimentin in the inflammatory process is unknown. Here, we investigate the contribution of vimentin to the pathogenesis of GBS meningitis. We show that a CRISPR-targeted deletion of vimentin in human cerebral microvascular endothelial cells (hCMEC) reduced GBS induction of neutrophil attractants interleukin-8 (IL-8) and CXCL-1 as well as NF-κB activation. We further show that inhibition of vimentin localization also prevented similar chemokine activation by GBS. One known chemokine regulator is the nucleotide-binding oligomerization domain containing protein 2 (NOD2), which is known to interact directly with vimentin. Thus, we hypothesized that NOD2 would also promote GBS chemokine induction. We show that GBS infection induced NOD2 transcription in hCMEC comparably to the muramyl dipeptide (MDP) NOD2 agonist, and the chemokine induction was reduced in the presence of a NOD2 inhibitor. Using a mouse model of GBS meningitis, we also observed increased NOD2 transcript and NOD2 activation in brain tissue of infected mice. Lastly, we show that NOD2-mediated IL-8 and CXCL1 induction required vimentin, further indicating the importance of vimentin in mediating inflammatory responses in brain endothelium.

Keywords: NOD2; chemokine; group B Streptococcus; meningitis; vimentin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Biomarkers
  • Brain / metabolism*
  • Chemokines / genetics*
  • Chemokines / metabolism
  • Disease Susceptibility
  • Endothelium / metabolism*
  • Gene Expression Regulation*
  • Host-Pathogen Interactions
  • Humans
  • Nod2 Signaling Adaptor Protein / metabolism*
  • Streptococcal Infections / etiology*
  • Streptococcal Infections / metabolism*
  • Vimentin / metabolism*

Substances

  • Biomarkers
  • Chemokines
  • NOD2 protein, human
  • Nod2 Signaling Adaptor Protein
  • Vimentin