Hyperglycemia-triggered lipid peroxidation destabilizes STAT4 and impairs anti-viral Th1 responses in type 2 diabetes

Cell Metab. 2024 Dec 3;36(12):2511-2527.e7. doi: 10.1016/j.cmet.2024.10.004. Epub 2024 Nov 1.

Abstract

Patients with type 2 diabetes (T2D) are more susceptible to severe respiratory viral infections, but the underlying mechanisms remain elusive. Here, we show that patients with T2D and coronavirus disease 2019 (COVID-19) infections, and influenza-infected T2D mice, exhibit defective T helper 1 (Th1) responses, which are an essential component of anti-viral immunity. This defect stems from intrinsic metabolic perturbations in CD4+ T cells driven by hyperglycemia. Mechanistically, hyperglycemia triggers mitochondrial dysfunction and excessive fatty acid synthesis, leading to elevated oxidative stress and aberrant lipid accumulation within CD4+ T cells. These abnormalities promote lipid peroxidation (LPO), which drives carbonylation of signal transducer and activator of transcription 4 (STAT4), a crucial Th1-lineage-determining factor. Carbonylated STAT4 undergoes rapid degradation, causing reduced T-bet induction and diminished Th1 differentiation. LPO scavenger ameliorates Th1 defects in patients with T2D who have poor glycemic control and restores viral control in T2D mice. Thus, this hyperglycemia-LPO-STAT4 axis underpins reduced Th1 activity in T2D hosts, with important implications for managing T2D-related viral complications.

Keywords: T helper 1 responses; hyperglycemia; lipid peroxidation; protein carbonylation; type 2 diabetes.

MeSH terms

  • Aged
  • Animals
  • COVID-19* / immunology
  • COVID-19* / metabolism
  • Diabetes Mellitus, Type 2* / metabolism
  • Female
  • Humans
  • Hyperglycemia* / metabolism
  • Lipid Peroxidation*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Oxidative Stress
  • SARS-CoV-2 / metabolism
  • STAT4 Transcription Factor* / metabolism
  • Th1 Cells* / immunology
  • Th1 Cells* / metabolism

Substances

  • STAT4 Transcription Factor
  • Stat4 protein, mouse