Tumor-Associated Neutrophils Drive B-cell Recruitment and Their Differentiation to Plasma Cells

Cancer Immunol Res. 2021 Jul;9(7):811-824. doi: 10.1158/2326-6066.CIR-20-0839. Epub 2021 Apr 27.

Abstract

A major mechanism through which neutrophils have been suggested to modulate tumor progression involves the interaction and subsequent modulation of other infiltrating immune cells. B cells have been found to infiltrate various cancer types and play a role in tumor immunity, offering new immunotherapy opportunities. Nevertheless, the specific impact of tumor-associated neutrophils (TAN) on B cells has largely been overlooked. In the current study, we aimed to characterize the role of TANs in the recruitment and modulation of B cells in the tumor microenvironment (TME). We showed that TANs actively participate in the recruitment of B cells to the TME and identified TNFα as the major cytokine mediating B-cell chemotaxis by TANs. The recruitment of CD45+B220+CD138- splenic B cells by TANs in vitro resulted in B-cell phenotypic modulation, with 68.6% ± 2.1% of the total migrated B cells displaying a CD45-B220+CD138+ phenotype, which is typical for plasma cells. This phenotype mirrored the large proportion (54.0% ± 6.1%) of CD45-B220+CD138+ intratumoral B cells (i.e., plasma cells) in Lewis lung carcinoma tumors. We next confirmed that the differentiation of CD45+B220+CD138- B cells to functionally active CD45-B220+CD138+ plasma cells required contact with TANs, was independent of T cells, and resulted in IgG production. We further identified membranal B-cell activating factor (BAFF) on TANs as a potential contact mechanism mediating B-cell differentiation, as blocking BAFF-receptor (BAFF-R) significantly reduced IgG production by 20%. Our study, therefore, demonstrates that TANs drive the recruitment and modulation of B cells into plasma cells in the TME, hence opening new avenues in the targeting of the immune system in cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Cell Activating Factor / metabolism
  • B-Cell Activation Factor Receptor / antagonists & inhibitors
  • B-Cell Activation Factor Receptor / metabolism
  • Breast Neoplasms / immunology*
  • Breast Neoplasms / pathology
  • Carcinoma, Lewis Lung / immunology*
  • Carcinoma, Lewis Lung / pathology
  • Cell Differentiation / immunology
  • Cell Line, Tumor
  • Chemotaxis, Leukocyte / immunology
  • Disease Models, Animal
  • Female
  • Humans
  • Lymphocyte Activation
  • Mice
  • Neutrophils / immunology*
  • Neutrophils / metabolism
  • Plasma Cells / immunology*
  • Plasma Cells / metabolism
  • Tumor Microenvironment / immunology*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • B-Cell Activating Factor
  • B-Cell Activation Factor Receptor
  • Tnf protein, mouse
  • Tnfrsf13c protein, mouse
  • Tnfsf13b protein, mouse
  • Tumor Necrosis Factor-alpha