Astrocyte pathology in Alexander disease causes a marked inflammatory environment

Acta Neuropathol. 2015 Oct;130(4):469-86. doi: 10.1007/s00401-015-1469-1. Epub 2015 Aug 22.

Abstract

Astrocytes and microglia are commonly involved in a wide variety of CNS pathologies. However, they are typically involved in a secondary response in which many cell types are affected simultaneously and therefore it is difficult to know their contributions to the pathology. Here, we show that pathological astrocytes in a mouse model of Alexander disease (AxD; GFAP (Tg);Gfap (+/R236H)) cause a pronounced immune response. We have studied the inflammatory response in the hippocampus and spinal cord of these mice and have found marked microglial activation, which follows that of astrocytes in a spatial pathological progression, as shown by increased levels of Iba1 and microglial cell (Iba1+) density. RNA sequencing and subsequent gene ontology (GO) analysis revealed that a majority of the most upregulated genes in GFAP (Tg);Gfap (+/R236H) mice are directly associated with immune function and that cytokine and chemokine GO attributes represent nearly a third of the total immune attributes. Cytokine and chemokine analysis showed CXCL10 and CCL2 to be the most and earliest increased molecules, showing concentrations as high as EAE or stroke models. CXCL10 was localized exclusively to astrocytes while CCL2 was also present in microglia. Despite the high levels of CXCL10 and CCL2, T cell infiltration was mild and no B cells were found. Thus, mutations in GFAP are sufficient to trigger a profound inflammatory response. The cellular stress caused by the accumulation of GFAP likely leads to the production of inflammatory molecules and microglial activation. Examination of human AxD CNS tissues also revealed microglial activation and T cell infiltrates. Therefore, the inflammatory environment may play an important role in producing the neuronal dysfunction and seizures of AxD.

Keywords: Alexander disease; Astrocytes; CCL2; CXCL10; Chemokines; Gliosis; Microglia; RNA-seq.

Publication types

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

MeSH terms

  • Alexander Disease / immunology*
  • Alexander Disease / pathology*
  • Animals
  • Astrocytes / immunology*
  • Astrocytes / pathology*
  • Child, Preschool
  • Cytokines / metabolism
  • Disease Models, Animal
  • Disease Progression
  • Female
  • Glial Fibrillary Acidic Protein / genetics
  • Glial Fibrillary Acidic Protein / metabolism
  • Hippocampus / immunology
  • Hippocampus / pathology
  • Humans
  • Infant
  • Male
  • Mice, Transgenic
  • Microglia / metabolism
  • Microglia / pathology
  • Neuroimmunomodulation / physiology
  • Spinal Cord / immunology
  • Spinal Cord / pathology

Substances

  • Cytokines
  • Glial Fibrillary Acidic Protein