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Metabolic Programming Drives Protective and Inflammatory Monocyte Fates in Viral Encephalitis.

Claire L Wishart1,2, Alanna G Spiteri1,2, Jian Tan1,3

  • 1Infection, Immunity, Inflammation Research Theme, School of Medical Sciences, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW, NSW 2006, Australia.

Advanced Science (Weinheim, Baden-Wurttemberg, Germany)
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Summary

Targeting monocyte metabolism in the central nervous system (CNS) can reduce neuroinflammation during viral encephalitis. Inhibiting glycolysis selectively decreases pathogenic inflammatory monocytes, offering a promising therapeutic strategy for CNS diseases.

Keywords:
ImmunometabolismWest Nile virusglycolysismonocytesmonocyte‐derived cellsviral encephalitis

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Area of Science:

  • Immunology
  • Neuroscience
  • Metabolic Biology

Background:

  • Monocytes infiltrating the central nervous system (CNS) have dual roles in inflammation, but their metabolic regulation is unclear.
  • Understanding these metabolic mechanisms is crucial for developing targeted therapies for CNS inflammatory diseases.

Purpose of the Study:

  • To map the metabolic signatures of monocyte-derived cells (MCs) during lethal West Nile virus encephalitis.
  • To identify metabolic pathways that dictate the divergent functions of MCs in CNS inflammation.

Main Methods:

  • Single-cell RNA-sequencing and metabolic flow analysis of brain and bone marrow (BM) monocytes.
  • Trajectory analysis to track metabolic profiles of MCs during viral encephalitis.
  • In vivo glycolysis inhibition to assess therapeutic effects.

Main Results:

  • BM monocytes transition through distinct metabolic states before brain infiltration and differentiation.
  • Pro-inflammatory MCs exhibit high glycolysis and amino acid metabolism, while protective MCs are glycolytically quiescent.
  • Inhibiting glycolysis selectively reduced inflammatory iNOS+ MC migration, mitigating neuroinflammation without increasing viral load.
  • HIF1-α activity was independent of glycolysis, allowing differentiation of protective antigen-presenting MCs.

Conclusions:

  • Key metabolic drivers of MC function in viral CNS disease were identified.
  • Selective metabolic reprogramming, specifically targeting glycolysis, can reduce severe neuroinflammation.
  • This approach demonstrates a promising therapeutic strategy for viral encephalitis and other CNS inflammatory conditions.