IL-21 and IL-4 Collaborate To Shape T-Dependent Antibody Responses

J Immunol. 2015 Dec 1;195(11):5123-35. doi: 10.4049/jimmunol.1501463. Epub 2015 Oct 21.

Abstract

The selection of affinity-matured Ab-producing B cells is supported by interactions with T follicular helper (Tfh) cells. In addition to cell surface-expressed molecules, cytokines produced by Tfh cells, such as IL-21 and IL-4, provide B cell helper signals. In this study, we analyze how the fitness of Th cells can influence Ab responses. To do this, we used a model in which IL-21R-sufficient (wild-type [WT]) and -deficient (Il21r(-/-)) Ag-specific Tfh cells were used to help immunodeficient Il21r(-/-) B cells following T-dependent immunization. Il21r(-/-) B cells that had received help from WT Tfh cells, but not from Il21r(-/-) Tfh cells, generated affinity-matured Ab upon recall immunization. This effect was dependent on IL-4 produced in the primary response and associated with an increased fraction of memory B cells. Il21r(-/-) Tfh cells were distinguished from WT Tfh cells by a decreased frequency, reduced conjugate formation with B cells, increased expression of programmed cell death 1, and reduced production of IL-4. IL-21 also influenced responsiveness to IL-4 because expression of both membrane IL-4R and the IL-4-neutralizing soluble (s)IL-4R were reduced in Il21r(-/-) mice. Furthermore, the concentration of sIL-4R was found to correlate inversely with the amount of IgE in sera, such that the highest IgE levels were observed in Il21r(-/-) mice with the least sIL-4R. Taken together, these findings underscore the important collaboration between IL-4 and IL-21 in shaping T-dependent Ab responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibody Formation / immunology
  • B-Lymphocytes / immunology*
  • Immunoglobulin E / blood
  • Interleukin-21 Receptor alpha Subunit / genetics*
  • Interleukin-21 Receptor alpha Subunit / immunology
  • Interleukin-4 / biosynthesis
  • Interleukin-4 / immunology*
  • Interleukins / biosynthesis
  • Interleukins / immunology*
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Sequence Data
  • Receptors, Cell Surface / biosynthesis
  • Signal Transduction / immunology
  • T-Lymphocytes, Helper-Inducer / immunology*

Substances

  • Il21r protein, mouse
  • Il4ra protein, mouse
  • Interleukin-21 Receptor alpha Subunit
  • Interleukins
  • Receptors, Cell Surface
  • Interleukin-4
  • Immunoglobulin E
  • interleukin-21

Associated data

  • GDB/BGT144240