Abnormal microglial activation in the Cstb(-/-) mouse, a model for progressive myoclonus epilepsy, EPM1

Glia. 2015 Mar;63(3):400-11. doi: 10.1002/glia.22760. Epub 2014 Oct 18.

Abstract

Progressive myoclonus epilepsy of Unverricht-Lundborg type (EPM1) is an autosomal-recessively inherited neurodegenerative disorder characterized by severely incapacitating myoclonus, seizures, and ataxia, and caused by loss-of-function mutations in the cystatin B gene (CSTB). A central neuropathological finding in the Cstb(-/-) mouse, an animal model for EPM1, is early microglial activation, which precedes astroglial activation, neuronal loss, and onset of myoclonus, thus implying a critical role for microglia in EPM1 pathogenesis. Here, we characterized phenotypic and functional properties of microglia from Cstb(-/-) mice utilizing brain tissue, microglia directly isolated from the brain, and primary microglial cultures. Our results show significantly higher Cstb mRNA expression in microglia than in neurons and astrocytes. In Cstb(-/-) mouse brain, expression of the inflammatory marker p-p38 MAPK and the proportion of both pro-inflammatory M1 and anti-inflammatory M2 microglia is higher than in control mice. Moreover, M1/M2 polarization of microglia in presymptomatic Cstb(-/-) mice is, compared to control mice, skewed towards M2 type at postnatal day 14 (P14), but towards M1 type at P30, a time point associated with onset of myoclonus. At this age, the high expression of both pro-inflammatory inducible nitric oxide synthase (iNOS) and anti-inflammatory arginase 1 (ARG1) in Cstb(-/-) mouse cortex is accompanied by the presence of peripheral immune cells. Consistently, activated Cstb(-/-) microglia show elevated chemokine release and chemotaxis. However, their MHCII surface expression is suppressed. Taken together, our results link CSTB deficiency to neuroinflammation with early activation and dysfunction of microglia and will open new avenues for therapeutic interventions for EPM1.

Keywords: M1/M2; chemokine; cystatin B; neuroinflammation; p38 MAPK; pro-inflammatory microglia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / metabolism
  • Astrocytes / metabolism
  • Brain / immunology*
  • Cells, Cultured
  • Cystatin B / deficiency*
  • Cystatin B / genetics
  • Disease Models, Animal
  • Genes, MHC Class II / physiology
  • Granulocytes / physiology
  • Macrophages / physiology
  • Mice, 129 Strain
  • Microglia / physiology*
  • Neuroimmunomodulation / physiology
  • Neurons / metabolism
  • Nitric Oxide Synthase Type II / metabolism
  • RNA, Messenger / metabolism
  • T-Lymphocytes / physiology
  • Unverricht-Lundborg Syndrome / immunology*
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Cstb protein, mouse
  • RNA, Messenger
  • Cystatin B
  • Nitric Oxide Synthase Type II
  • Nos2 protein, mouse
  • p38 Mitogen-Activated Protein Kinases
  • Arg1 protein, mouse
  • Arginase