Neuropilin-1 expression characterizes T follicular helper (Tfh) cells activated during B cell differentiation in human secondary lymphoid organs

PLoS One. 2013 Dec 30;8(12):e85589. doi: 10.1371/journal.pone.0085589. eCollection 2013.

Abstract

T follicular helper (Tfh) cells play an essential role in the development of antigen-specific B cell immunity. Tfh cells regulate the differentiation and survival of activated B cells outside and inside germinal centers (GC) of secondary lymphoid organs. They act through cognate contacts with antigen-presenting B cells, but there is no current marker to specifically identify those Tfh cells which productively interact with B cells. Here we show that neuropilin 1 (Nrp1), a cell surface receptor, is selectively expressed by a subset of Tfh cells in human secondary lymphoid organs. Nrp1 expression on Tfh cells correlates with B cell differentiation in vivo and in vitro, is transient, and can be induced upon co-culture with autologous memory B cells in a cell contact-dependent manner. Comparative analysis of ex vivo Nrp1(+) and Nrp1(-) Tfh cells reveals gene expression modulation during activation. Finally, Nrp1 is expressed by malignant Tfh-like cells in a severe case of angioimmunoblastic T-cell lymphoma (AITL) associated with elevated terminal B cell differentiation. Thus, Nrp1 is a specific marker of Tfh cells cognate activation in humans, which may prove useful as a prognostic factor and a therapeutic target in neoplastic diseases associated with Tfh cells activity.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • Cell Differentiation / immunology*
  • Child
  • Child, Preschool
  • Female
  • Gene Expression Regulation, Neoplastic / immunology
  • Germinal Center / immunology*
  • Germinal Center / metabolism
  • Germinal Center / pathology
  • Humans
  • Immunologic Memory
  • Lymphocyte Activation
  • Lymphoma, T-Cell / immunology
  • Lymphoma, T-Cell / metabolism
  • Lymphoma, T-Cell / pathology
  • Male
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / immunology
  • Neuropilin-1 / biosynthesis
  • Neuropilin-1 / immunology*
  • T-Lymphocytes, Helper-Inducer / immunology*
  • T-Lymphocytes, Helper-Inducer / metabolism
  • T-Lymphocytes, Helper-Inducer / pathology

Substances

  • Neoplasm Proteins
  • Neuropilin-1

Grants and funding

This work was supported by grants from Ligue Nationale contre le Cancer (LNCC, France), Fondation pour la Recherche Médicale (FRM, France), Ministère de la Recherche, Association pour la Recherche contre le Cancer (ARC, France), INCa (France), ANR (France), Cancéropole (France) and the Fondation de France (France). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.