Microglial control of astrocytes in response to microbial metabolites

Nature. 2018 May;557(7707):724-728. doi: 10.1038/s41586-018-0119-x. Epub 2018 May 16.

Abstract

Microglia and astrocytes modulate inflammation and neurodegeneration in the central nervous system (CNS)1-3. Microglia modulate pro-inflammatory and neurotoxic activities in astrocytes, but the mechanisms involved are not completely understood4,5. Here we report that TGFα and VEGF-B produced by microglia regulate the pathogenic activities of astrocytes in the experimental autoimmune encephalomyelitis (EAE) mouse model of multiple sclerosis. Microglia-derived TGFα acts via the ErbB1 receptor in astrocytes to limit their pathogenic activities and EAE development. Conversely, microglial VEGF-B triggers FLT-1 signalling in astrocytes and worsens EAE. VEGF-B and TGFα also participate in the microglial control of human astrocytes. Furthermore, expression of TGFα and VEGF-B in CD14+ cells correlates with the multiple sclerosis lesion stage. Finally, metabolites of dietary tryptophan produced by the commensal flora control microglial activation and TGFα and VEGF-B production, modulating the transcriptional program of astrocytes and CNS inflammation through a mechanism mediated by the aryl hydrocarbon receptor. In summary, we identified positive and negative regulators that mediate the microglial control of astrocytes. Moreover, these findings define a pathway through which microbial metabolites limit pathogenic activities of microglia and astrocytes, and suppress CNS inflammation. This pathway may guide new therapies for multiple sclerosis and other neurological disorders.

Publication types

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

MeSH terms

  • Animals
  • Astrocytes / metabolism*
  • Astrocytes / pathology
  • Cells, Cultured
  • Central Nervous System / metabolism
  • Central Nervous System / microbiology
  • Central Nervous System / pathology
  • Disease Models, Animal
  • Encephalomyelitis, Autoimmune, Experimental / metabolism*
  • Encephalomyelitis, Autoimmune, Experimental / microbiology*
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Encephalomyelitis, Autoimmune, Experimental / prevention & control
  • ErbB Receptors / metabolism
  • Female
  • Humans
  • Inflammation / metabolism
  • Inflammation / microbiology
  • Inflammation / pathology
  • Inflammation / prevention & control
  • Lipopolysaccharide Receptors / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microglia / metabolism*
  • Microglia / pathology
  • Multiple Sclerosis / metabolism
  • Multiple Sclerosis / pathology
  • Receptors, Aryl Hydrocarbon / metabolism
  • Symbiosis
  • Transforming Growth Factor alpha / biosynthesis
  • Transforming Growth Factor alpha / metabolism
  • Tryptophan / deficiency
  • Tryptophan / metabolism
  • Vascular Endothelial Growth Factor B / biosynthesis
  • Vascular Endothelial Growth Factor B / metabolism
  • Vascular Endothelial Growth Factor Receptor-1 / metabolism

Substances

  • Lipopolysaccharide Receptors
  • Receptors, Aryl Hydrocarbon
  • Transforming Growth Factor alpha
  • Vascular Endothelial Growth Factor B
  • Tryptophan
  • ErbB Receptors
  • Flt1 protein, mouse
  • Vascular Endothelial Growth Factor Receptor-1