Extracellular vesicles shed by follicular lymphoma B cells promote polarization of the bone marrow stromal cell niche

Blood. 2021 Jul 8;138(1):57-70. doi: 10.1182/blood.2020008791.

Abstract

Follicular lymphoma (FL) originates in the lymph nodes (LNs) and infiltrates bone marrow (BM) early in the course of the disease. BM FL B cells are characterized by a lower cytological grade, decreased proliferation, and a specific phenotypic and subclonal profile. Mesenchymal stromal cells (MSCs) obtained from FL BM display a specific gene expression profile (GEP), including enrichment for a lymphoid stromal cell signature, and an increased capacity to sustain FL B-cell growth. However, the mechanisms triggering the formation of the medullar FL permissive stromal niche have not been identified. In the current work, we demonstrate that FL B cells produce extracellular vesicles (EVs) that can be internalized by BM-MSCs, making them more efficient to support FL B-cell survival and quiescence. Accordingly, EVs purified from FL BM plasma activate transforming growth factor β-dependent and independent pathways in BM-MSCs and modify their GEP, triggering an upregulation of factors classically associated with hematopoietic stem cell niche, including CXCL12 and angiopoietin-1. Moreover, we provide the first characterization of BM FL B-cell GEP, allowing the definition of the landscape of molecular interactions they could engage with EV-primed BM-MSCs. This work identifies FL-derived EVs as putative mediators of BM stroma polarization and supports further investigation of their clinical interest for targeting the crosstalk between BM-MSCs and malignant B cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • B-Lymphocytes / pathology*
  • Base Sequence
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / pathology*
  • Cell Communication
  • Cell Differentiation
  • Cell Polarity*
  • Endocytosis
  • Extracellular Vesicles / metabolism
  • Extracellular Vesicles / pathology*
  • Extracellular Vesicles / ultrastructure
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Hematopoietic Stem Cells / metabolism
  • Humans
  • Lymphoma, Follicular / genetics
  • Lymphoma, Follicular / pathology*
  • Lymphotoxin alpha1, beta2 Heterotrimer / metabolism
  • Mesenchymal Stem Cells / metabolism
  • Phenotype
  • Signal Transduction
  • Stromal Cells / metabolism
  • Stromal Cells / pathology
  • Tumor Necrosis Factor-alpha / metabolism
  • Up-Regulation / genetics

Substances

  • Lymphotoxin alpha1, beta2 Heterotrimer
  • Tumor Necrosis Factor-alpha