IL-10-Dependent Crosstalk between Murine Marginal Zone B Cells, Macrophages, and CD8α+ Dendritic Cells Promotes Listeria monocytogenes Infection

Dong Liu, Xiangyun Yin, Sam J. Olyha, Manuela Sales L. Nascimento, Pei Chen, Theresa White, Uthaman Gowthaman, Tingting Zhang, Jake A. Gertie, Biyan Zhang, Lan Xu, Marina Yurieva, Lesley Devine, Adam Williams*, Stephanie C. Eisenbarth

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

22 Scopus citations

Abstract

Type 1 CD8α+ conventional dendritic cells (cDC1s) are required for CD8+ T cell priming but, paradoxically, promote splenic Listeria monocytogenes infection. Using mice with impaired cDC2 function, we ruled out a role for cDC2s in this process and instead discovered an interleukin-10 (IL-10)-dependent cellular crosstalk in the marginal zone (MZ) that promoted bacterial infection. Mice lacking the guanine nucleotide exchange factor DOCK8 or CD19 lost IL-10-producing MZ B cells and were resistant to Listeria. IL-10 increased intracellular Listeria in cDC1s indirectly by reducing inducible nitric oxide synthase expression early after infection and increasing intracellular Listeria in MZ metallophilic macrophages (MMMs). These MMMs trans-infected cDC1s, which, in turn, transported Listeria into the white pulp to prime CD8+ T cells. However, this also facilitated bacterial expansion. Therefore, IL-10-mediated crosstalk between B cells, macrophages, and cDC1s in the MZ promotes both Listeria infection and CD8+ T cell activation.

Original languageEnglish (US)
Pages (from-to)64-76.e7
JournalImmunity
Volume51
Issue number1
DOIs
StatePublished - Jul 16 2019

Keywords

  • DOCK8
  • IL-10
  • Listeria monocytogenes
  • T cell
  • dendritic cells
  • iNOS
  • macrophage
  • marginal zone B cells
  • spleen

ASJC Scopus subject areas

  • Infectious Diseases
  • Immunology and Allergy
  • Immunology

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