Neutrophils promote VLA-4-dependent B cell antigen presentation and accumulation within the meninges during neuroinflammation

Proc Natl Acad Sci U S A. 2019 Nov 26;116(48):24221-24230. doi: 10.1073/pnas.1909098116. Epub 2019 Nov 7.

Abstract

The success of B cell depletion therapies and identification of leptomeningeal ectopic lymphoid tissue (ELT) in patients with multiple sclerosis (MS) has renewed interest in the antibody-independent pathogenic functions of B cells during neuroinflammation. The timing and location of B cell antigen presentation during MS and its animal model experimental autoimmune encephalomyelitis (EAE) remain undefined. Using a new EAE system that incorporates temporal regulation of MHCII expression by myelin-specific B cells, we observed the rapid formation of large B cell clusters in the spinal cord subarachnoid space. Neutrophils preceded the accumulation of meningeal B cell clusters, and inhibition of CXCR2-mediated granulocyte trafficking to the central nervous system reduced pathogenic B cell clusters and disease severity. Further, B cell-restricted very late antigen-4 (VLA-4) deficiency abrogated EAE dependent on B cell antigen presentation. Together, our findings demonstrate that neutrophils coordinate VLA-4-dependent B cell accumulation within the meninges during neuroinflammation, a key early step in the formation of ELT observed in MS.

Keywords: B cell; EAE; multiple sclerosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Animals
  • Antigen Presentation
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / pathology
  • Chemokines / metabolism
  • Disease Models, Animal
  • Encephalomyelitis, Autoimmune, Experimental / immunology*
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Female
  • Integrin alpha4beta1 / immunology
  • Integrin alpha4beta1 / metabolism*
  • Lymphoid Tissue / immunology
  • Lymphoid Tissue / pathology
  • Male
  • Meninges / immunology*
  • Meninges / pathology
  • Meningitis / immunology
  • Meningitis / pathology
  • Mice, Inbred C57BL
  • Multiple Sclerosis / immunology
  • Multiple Sclerosis / pathology*
  • Myeloid Cells / pathology
  • Neutrophils / immunology
  • Neutrophils / pathology
  • Rabbits
  • Receptors, Interleukin-8B / metabolism
  • Subarachnoid Space / pathology

Substances

  • Chemokines
  • Cxcr2 protein, mouse
  • Integrin alpha4beta1
  • Receptors, Interleukin-8B

Associated data

  • figshare/10.6084/m9.figshare.10052051.v1