Fungal sensing enhances neutrophil metabolic fitness by regulating antifungal Glut1 activity

Cell Host Microbe. 2022 Apr 13;30(4):530-544.e6. doi: 10.1016/j.chom.2022.02.017. Epub 2022 Mar 21.

Abstract

Combating fungal pathogens poses metabolic challenges for neutrophils, key innate cells in anti-Candida albicans immunity, yet how host-pathogen interactions cause remodeling of the neutrophil metabolism is unclear. We show that neutrophils mediate renal immunity to disseminated candidiasis by upregulating glucose uptake via selective expression of glucose transporter 1 (Glut1). Mechanistically, dectin-1-mediated recognition of β-glucan leads to activation of PKCδ, which triggers phosphorylation, localization, and early glucose transport by a pool of pre-formed Glut1 in neutrophils. These events are followed by increased Glut1 gene transcription, leading to more sustained Glut1 accumulation, which is also dependent on the β-glucan/dectin-1/CARD9 axis. Card9-deficient neutrophils show diminished glucose incorporation in candidiasis. Neutrophil-specific Glut1-ablated mice exhibit increased mortality in candidiasis caused by compromised neutrophil phagocytosis, reactive oxygen species (ROS), and neutrophil extracellular trap (NET) formation. In human neutrophils, β-glucan triggers metabolic remodeling and enhances candidacidal function. Our data show that the host-pathogen interface increases glycolytic activity in neutrophils by regulating Glut1 expression, localization, and function.

Keywords: Candida albicans; fungus; glucose; glucose transporter 1; immunometabolism; kidney; neutrophils.

MeSH terms

  • Animals
  • CARD Signaling Adaptor Proteins / metabolism
  • Candida albicans
  • Candidiasis* / immunology
  • Glucose / metabolism
  • Glucose Transporter Type 1* / metabolism
  • Mice
  • Neutrophils* / immunology
  • beta-Glucans* / metabolism

Substances

  • CARD Signaling Adaptor Proteins
  • Card9 protein, mouse
  • Glucose Transporter Type 1
  • Slc2a1 protein, mouse
  • beta-Glucans
  • Glucose