Follicular lymphoma triggers phenotypic and functional remodeling of the human lymphoid stromal cell landscape

Immunity. 2021 Aug 10;54(8):1788-1806.e7. doi: 10.1016/j.immuni.2021.05.019. Epub 2021 Jun 23.

Abstract

Lymphoid stromal cells (LSCs) are essential organizers of immune responses. We analyzed tonsillar tissue by combining flow cytometry, in situ imaging, RNA sequencing, and functional assays, defining three distinct human LSC subsets. The integrin CD49a designated perivascular stromal cells exhibiting features of local committed LSC precursors and segregated cytokine and chemokine-producing fibroblastic reticular cells (FRCs) supporting B and T cell survival. The follicular dendritic cell transcriptional profile reflected active responses to B cell and non-B cell stimuli. We therefore examined the effect of B cell stimuli on LSCs in follicular lymphoma (FL). FL B cells interacted primarily with CD49a+ FRCs. Transcriptional analyses revealed LSC reprogramming in situ downstream of the cytokines tumor necrosis factor (TNF) and transforming growth factor β (TGF-β), including increased expression of the chemokines CCL19 and CCL21. Our findings define human LSC populations in healthy tissue and reveal bidirectional crosstalk between LSCs and malignant B cells that may present a targetable axis in lymphoma.

Keywords: B cell lymphoma; cancer-associated fibroblasts; chemokines; fibroblastic reticular cells; follicular dendritic cells; tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • B-Lymphocytes / immunology*
  • Cells, Cultured
  • Chemokine CCL19 / metabolism
  • Chemokine CCL21 / metabolism
  • Dendritic Cells / immunology*
  • Humans
  • Integrin alpha1 / metabolism
  • Lymphoma, Follicular / immunology*
  • Lymphoma, Follicular / pathology*
  • Palatine Tonsil / cytology
  • Palatine Tonsil / immunology*
  • Signal Transduction / immunology
  • Stromal Cells / cytology
  • Stromal Cells / immunology*
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta1 / metabolism
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • CCL19 protein, human
  • CCL21 protein, human
  • Chemokine CCL19
  • Chemokine CCL21
  • Integrin alpha1
  • TGFB1 protein, human
  • TNF protein, human
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha