Regulatory B1a Cells Suppress Melanoma Tumor Immunity via IL-10 Production and Inhibiting T Helper Type 1 Cytokine Production in Tumor-Infiltrating CD8+ T Cells

J Invest Dermatol. 2019 Jul;139(7):1535-1544.e1. doi: 10.1016/j.jid.2019.02.016. Epub 2019 Mar 2.

Abstract

In tumor immunity, the participation of IL-10-producing regulatory B cells (Bregs), which play an important role in suppressing immune responses, is unclear. In this study, we demonstrated an increase in B16F10 melanoma growth and a decrease in the proportion of IFN-γ- and TNF-α-secreting tumor-infiltrating CD8+ T cells in B cell-specific PTEN-deficient mice in which Bregs were expanded. The number of tumor-infiltrating Bregs significantly increased in B cell-specific PTEN-deficient mice. More than 50% of tumor-infiltrating B cells consisted of Bregs, predominantly CD19+CD5+CD43+ B1a Bregs, in both B cell-specific PTEN-deficient and control mice. Adoptive B1a B cell transfer, which includes >30% of Bregs, increased melanoma growth, whereas non-B1a B cell transfer, which includes <2% of Bregs, exhibited no effect. In addition, adoptive transfer of B1a B cells from wild-type mice, but not IL-10-/- mice, exacerbated B16F10 melanoma growth. The current study indicates that B1a Bregs negatively regulate anti-melanoma immunity by producing IL-10 and reducing T helper 1 type cytokine production in tumor-infiltrating CD8+ T cells. Therefore, B1a Bregs can be a potentially novel target for immunotherapy of melanomas.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / transplantation
  • B-Lymphocytes, Regulatory / immunology*
  • B-Lymphocytes, Regulatory / transplantation
  • CD8-Positive T-Lymphocytes / immunology*
  • Cytokines / metabolism
  • Humans
  • Immune Tolerance
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism*
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Melanoma / immunology*
  • Melanoma, Experimental
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms, Experimental
  • PTEN Phosphohydrolase / genetics
  • Th1 Cells / immunology*

Substances

  • Cytokines
  • Interleukin-10
  • PTEN Phosphohydrolase