During Aspergillus Infection, Monocyte-Derived DCs, Neutrophils, and Plasmacytoid DCs Enhance Innate Immune Defense through CXCR3-Dependent Crosstalk

Cell Host Microbe. 2020 Jul 8;28(1):104-116.e4. doi: 10.1016/j.chom.2020.05.002. Epub 2020 Jun 1.

Abstract

Aspergillus fumigatus, a ubiquitous mold, is a common cause of invasive aspergillosis (IA) in immunocompromised patients. Host defense against IA relies on lung-infiltrating neutrophils and monocyte-derived dendritic cells (Mo-DCs). Here, we demonstrate that plasmacytoid dendritic cells (pDCs), which are prototypically antiviral cells, participate in innate immune crosstalk underlying mucosal antifungal immunity. Aspergillus-infected murine Mo-DCs and neutrophils recruited pDCs to the lung by releasing the CXCR3 ligands, CXCL9 and CXCL10, in a Dectin-1 and Card9- and type I and III interferon signaling-dependent manner, respectively. During aspergillosis, circulating pDCs entered the lung in response to CXCR3-dependent signals. Via targeted pDC ablation, we found that pDCs were essential for host defense in the presence of normal neutrophil and Mo-DC numbers. Although interactions between pDC and fungal cells were not detected, pDCs regulated neutrophil NADPH oxidase activity and conidial killing. Thus, pDCs act as positive feedback amplifiers of neutrophil effector activity against inhaled mold conidia.

Keywords: Aspergillus fumigatus; CXCL10; CXCL9; CXCR3; fungus; innate immunity; lung; monocyte-derived dendritic cell; neutrophil; plasmacytoid DC.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aspergillosis / immunology*
  • Aspergillus fumigatus / immunology
  • CARD Signaling Adaptor Proteins / immunology
  • Chemokine CXCL10 / immunology
  • Chemokine CXCL9 / immunology
  • Dendritic Cells / immunology*
  • Immunity, Innate
  • Immunocompromised Host
  • Interferons / immunology
  • Lectins, C-Type / immunology
  • Lung / immunology
  • Lung / microbiology
  • Lymphocytes / immunology
  • Mice
  • Mice, Inbred C57BL
  • Neutrophils / immunology*
  • Reactive Oxygen Species / immunology
  • Receptors, CCR2 / immunology
  • Receptors, CXCR3 / genetics
  • Receptors, CXCR3 / immunology*
  • Signal Transduction / immunology
  • Spores, Fungal / immunology*

Substances

  • CARD Signaling Adaptor Proteins
  • Card9 protein, mouse
  • Ccr2 protein, mouse
  • Chemokine CXCL10
  • Chemokine CXCL9
  • Cxcl10 protein, mouse
  • Cxcl9 protein, mouse
  • Cxcr3 protein, mouse
  • Lectins, C-Type
  • Reactive Oxygen Species
  • Receptors, CCR2
  • Receptors, CXCR3
  • dectin 1
  • Interferons