Tracking CNS and systemic sources of oxidative stress during the course of chronic neuroinflammation

Acta Neuropathol. 2015 Dec;130(6):799-814. doi: 10.1007/s00401-015-1497-x. Epub 2015 Oct 31.

Abstract

The functional dynamics and cellular sources of oxidative stress are central to understanding MS pathogenesis but remain elusive, due to the lack of appropriate detection methods. Here we employ NAD(P)H fluorescence lifetime imaging to detect functional NADPH oxidases (NOX enzymes) in vivo to identify inflammatory monocytes, activated microglia, and astrocytes expressing NOX1 as major cellular sources of oxidative stress in the central nervous system of mice affected by experimental autoimmune encephalomyelitis (EAE). This directly affects neuronal function in vivo, indicated by sustained elevated neuronal calcium. The systemic involvement of oxidative stress is mirrored by overactivation of NOX enzymes in peripheral CD11b(+) cells in later phases of both MS and EAE. This effect is antagonized by systemic intake of the NOX inhibitor and anti-oxidant epigallocatechin-3-gallate. Together, this persistent hyper-activation of oxidative enzymes suggests an "oxidative stress memory" both in the periphery and CNS compartments, in chronic neuroinflammation.

Keywords: Fluorescence lifetime microscopy; Intravital imaging; Multiple sclerosis; Neuronal dysfunction; Oxidative stress; Oxidative stress memory.

Publication types

  • Randomized Controlled Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants / therapeutic use
  • Astrocytes / drug effects
  • Astrocytes / enzymology
  • Astrocytes / pathology
  • CD11b Antigen / metabolism
  • Calcium / metabolism
  • Catechin / analogs & derivatives
  • Catechin / therapeutic use
  • Chronic Disease
  • Disease Progression
  • Encephalomyelitis, Autoimmune, Experimental / drug therapy
  • Encephalomyelitis, Autoimmune, Experimental / enzymology*
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Enzyme Inhibitors / therapeutic use
  • Glatiramer Acetate / therapeutic use
  • Humans
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microscopy, Fluorescence / methods
  • Multiple Sclerosis / drug therapy
  • Multiple Sclerosis / enzymology*
  • Multiple Sclerosis / pathology
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / metabolism*
  • Neurons / drug effects
  • Neurons / enzymology
  • Neurons / pathology
  • Oxidative Stress / drug effects
  • Oxidative Stress / physiology*

Substances

  • Antioxidants
  • CD11b Antigen
  • Enzyme Inhibitors
  • Glatiramer Acetate
  • Catechin
  • epigallocatechin gallate
  • NADPH Oxidases
  • Calcium