Interleukin-2-secreting T helper cells promote extra-follicular B cell maturation via intrinsic regulation of a B cell mTOR-AKT-Blimp-1 axis

Immunity. 2024 Dec 10;57(12):2772-2789.e8. doi: 10.1016/j.immuni.2024.11.006. Epub 2024 Nov 28.

Abstract

During antigen-driven responses, B cells can differentiate at extra-follicular (EF) sites or initiate germinal centers (GCs) in processes that involve interactions with T cells. Here, we examined the roles of interleukin (IL)-2 secreted by T helper (Th) cells during cognate interactions with activated B cells. IL-2 boosted the expansion of EF plasma cells and the secretion of low-mutated immunoglobulin G (IgG). Conversely, genetically disrupting IL-2 expression by CD4+ T cells, or IL-2 receptor (CD25) expression by B cells, promoted B cell entry into the GC and high-affinity antibody secretion. Mechanistically, IL-2 induced early mTOR activity, expression of the transcriptional regulator IRF4, and metabolic changes in B cells required to form Blimp-1-expressing plasma cells. Thus, T cell help via IL-2 regulates an mTOR-AKT-Blimp-1 axis in activated B cells, providing insight into the mechanisms that determine EF versus GC fates and positioning IL-2 as an early switch controlling plasma cell versus GC B cell commitment.

Keywords: CD4 T cells; IL-2 cytokine; T follicular helper cells; Tfh cells; antibodies; mTOR; metabolism; plasma cells; vaccine.

MeSH terms

  • Animals
  • B-Lymphocytes* / immunology
  • B-Lymphocytes* / metabolism
  • Cell Differentiation* / immunology
  • Germinal Center* / immunology
  • Germinal Center* / metabolism
  • Immunoglobulin G / immunology
  • Immunoglobulin G / metabolism
  • Interferon Regulatory Factors / metabolism
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Interleukin-2* / immunology
  • Interleukin-2* / metabolism
  • Lymphocyte Activation* / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Plasma Cells / immunology
  • Plasma Cells / metabolism
  • Positive Regulatory Domain I-Binding Factor 1* / genetics
  • Positive Regulatory Domain I-Binding Factor 1* / metabolism
  • Proto-Oncogene Proteins c-akt* / metabolism
  • Signal Transduction*
  • T-Lymphocytes, Helper-Inducer* / immunology
  • T-Lymphocytes, Helper-Inducer* / metabolism
  • TOR Serine-Threonine Kinases* / metabolism

Substances

  • TOR Serine-Threonine Kinases
  • Positive Regulatory Domain I-Binding Factor 1
  • Interleukin-2
  • Proto-Oncogene Proteins c-akt
  • Prdm1 protein, mouse
  • mTOR protein, mouse
  • interferon regulatory factor-4
  • Interferon Regulatory Factors
  • Interleukin-2 Receptor alpha Subunit
  • Immunoglobulin G