Aberrant Humoral Immune Responses in Neurosyphilis: CXCL13/CXCR5 Play a Pivotal Role for B-Cell Recruitment to the Cerebrospinal Fluid

J Infect Dis. 2017 Sep 1;216(5):534-544. doi: 10.1093/infdis/jix233.

Abstract

Background: Previous studies documented that humoral immune responses participated in neurological damage in neurosyphilis patients. However, the mechanisms that trigger and maintain humoral immunity involved in neurosyphilis remain unknown.

Methods: Using flow cytometry, expression of B cells was measured in neurosyphilis and non-neurosyphilis. Expression of immunoglobulin indices and chemokine ligand CXCL13 was detected by enzyme-linked immunosorbent assay. The migration and inhibition assays were evaluated by modified chamber assays. The presence of CXCL13+ cells, cluster of differentiation (CD)20+ B cells, CD3+ T cells, CD138+ plasma cells and CD35+ follicular dendritic cells was studied by immunohistochemistry.

Results: Enrichment of B cells was observed and activated in the cerebrospinal fluid (CSF) of neurosyphilis patients. Immunoglobulin indices were increased and associated with the progress to neurosyphilis. High expression of CSF CXCL13 mediated B cell migration both in vitro and in vivo. There was a positive correlation among the CSF B cells, immunoglobulin indices, and CSF CXCL13 levels. Ectopic germinal centers (EGCs), important structures for humoral immunity, were observed in the intracranial syphilitic gumma.

Conclusions: CXCL13/CXCR5 mediated the aggregation of B cells, that directed the aberrant humoral immune responses via the formation of EGCs, which suggests a molecular mechanism of neurological damage in neurosyphilis.

Keywords: CXCL13; Treponema pallidum; ectopic germinal centers; follicular dendritic cells; neurosyphilis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Aged, 80 and over
  • Antibody Formation
  • B-Lymphocytes / metabolism*
  • Biomarkers / cerebrospinal fluid
  • Case-Control Studies
  • Cell Differentiation
  • Chemokine CXCL13 / cerebrospinal fluid*
  • Female
  • Flow Cytometry
  • Follow-Up Studies
  • Humans
  • Immunity, Humoral*
  • Immunoglobulin A / blood
  • Immunoglobulin G / blood
  • Immunoglobulin M / blood
  • Male
  • Middle Aged
  • Neurosyphilis / cerebrospinal fluid*
  • Neurosyphilis / diagnosis
  • Plasma Cells / metabolism
  • Receptors, CXCR5 / metabolism*
  • T-Lymphocytes / metabolism
  • Treponema pallidum
  • Young Adult

Substances

  • Biomarkers
  • CXCL13 protein, human
  • CXCR5 protein, human
  • Chemokine CXCL13
  • Immunoglobulin A
  • Immunoglobulin G
  • Immunoglobulin M
  • Receptors, CXCR5