Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-gamma

J Cell Biol. 2005 May 23;169(4):603-12. doi: 10.1083/jcb.200502086.

Abstract

Interferon-gamma (IFN-gamma) is believed to contribute to immune-mediated demyelinating disorders by targeting the myelin-producing oligodendrocyte, a cell known to be highly sensitive to the disruption of protein synthesis and to the perturbation of the secretory pathway. We found that apoptosis induced by IFN-gamma in cultured rat oligodendrocytes was associated with endoplasmic reticulum (ER) stress. ER stress also accompanied oligodendrocyte apoptosis and hypomyelination in transgenic mice that inappropriately expressed IFN-gamma in the central nervous system (CNS). Compared with a wild-type genetic background, the enforced expression of IFN-gamma in mice that were heterozygous for a loss of function mutation in pancreatic ER kinase (PERK) dramatically reduced animal survival, promoted CNS hypomyelination, and enhanced oligodendrocyte loss. PERK encodes an ER stress-inducible kinase that phosphorylates eukaryotic translation initiation factor 2alpha and specifically maintains client protein homeostasis in the stressed ER. Therefore, the hypersensitivity of PERK+/- mice to IFN-gamma implicates ER stress in demyelinating disorders that are induced by CNS inflammation.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Apoptosis / genetics
  • Apoptosis / immunology
  • Demyelinating Diseases / genetics
  • Demyelinating Diseases / immunology
  • Demyelinating Diseases / metabolism*
  • Encephalitis / genetics
  • Encephalitis / immunology
  • Encephalitis / metabolism*
  • Endoplasmic Reticulum / immunology
  • Endoplasmic Reticulum / metabolism*
  • Eukaryotic Initiation Factor-2 / genetics
  • Eukaryotic Initiation Factor-2 / immunology
  • Eukaryotic Initiation Factor-2 / metabolism
  • Female
  • Homeostasis
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Microscopy, Electron, Transmission
  • Mutation / genetics
  • Myelin Sheath / metabolism
  • Myelin Sheath / pathology
  • Myelin Sheath / ultrastructure
  • Oligodendroglia / immunology
  • Oligodendroglia / metabolism*
  • Phosphorylation
  • Rats
  • Stress, Physiological / genetics
  • Stress, Physiological / immunology
  • Stress, Physiological / metabolism*
  • eIF-2 Kinase / genetics
  • eIF-2 Kinase / metabolism

Substances

  • Eukaryotic Initiation Factor-2
  • Interferon-gamma
  • PERK kinase
  • eIF-2 Kinase