Expression of iron homeostasis proteins in the spinal cord in experimental autoimmune encephalomyelitis and their implications for iron accumulation

Neurobiol Dis. 2015 Sep:81:93-107. doi: 10.1016/j.nbd.2015.02.001. Epub 2015 Feb 25.

Abstract

Iron accumulation occurs in the CNS in multiple sclerosis (MS) and in experimental autoimmune encephalomyelitis (EAE). However, the mechanisms underlying such iron accumulation are not fully understood. We studied the expression and cellular localization of molecules involved in cellular iron influx, storage, and efflux. This was assessed in two mouse models of EAE: relapsing-remitting (RR-EAE) and chronic (CH-EAE). The expression of molecules involved in iron homeostasis was assessed at the onset, peak, remission/progressive and late stages of the disease. We provide several lines of evidence for iron accumulation in the EAE spinal cord which increases with disease progression and duration, is worse in CH-EAE, and is localized in macrophages and microglia. We also provide evidence that there is a disruption of the iron efflux mechanism in macrophages/microglia that underlie the iron accumulation seen in these cells. Macrophages/microglia also lack expression of the ferroxidases (ceruloplasmin and hephaestin) which have antioxidant effects. In contrast, astrocytes which do not accumulate iron, show robust expression of several iron influx and efflux proteins and the ferroxidase ceruloplasmin which detoxifies ferrous iron. Astrocytes therefore are capable of efficiently recycling iron from sites of EAE lesions likely into the circulation. We also provide evidence of marked dysregulation of mitochondrial function and energy metabolism genes, as well as of NADPH oxidase genes in the EAE spinal cord. This data provides the basis for the selective iron accumulation in macrophage/microglia and further evidence of severe mitochondrial dysfunction in EAE. It may provide insights into processes underling iron accumulation in MS and other neurodegenerative diseases in which iron accumulation occurs.

Keywords: Ceruloplasmin; Experimental autoimmune encephalomyelitis; Ferroportin; Hepcidin; Iron; Iron efflux; Iron influx; MS; Macrophage; Microglia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD11b Antigen / genetics
  • CD11b Antigen / metabolism
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism
  • Ceruloplasmin / genetics
  • Ceruloplasmin / metabolism
  • Disease Models, Animal
  • Encephalomyelitis, Autoimmune, Experimental / chemically induced
  • Encephalomyelitis, Autoimmune, Experimental / complications*
  • Encephalomyelitis, Autoimmune, Experimental / pathology*
  • Female
  • Ferritins / genetics
  • Ferritins / metabolism*
  • Ferroportin
  • Freund's Adjuvant / toxicity
  • Glial Fibrillary Acidic Protein / metabolism
  • Hepcidins / genetics
  • Hepcidins / metabolism
  • Iron / metabolism*
  • Iron Metabolism Disorders / etiology*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Myelin-Oligodendrocyte Glycoprotein / toxicity
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Peptide Fragments / toxicity
  • Receptors, Transferrin / genetics
  • Receptors, Transferrin / metabolism
  • Spinal Cord / metabolism*
  • Spinal Cord / pathology
  • Spinal Cord / ultrastructure
  • Time Factors

Substances

  • CD11b Antigen
  • Cation Transport Proteins
  • Glial Fibrillary Acidic Protein
  • Hepcidins
  • Heph protein, mouse
  • Membrane Proteins
  • Myelin-Oligodendrocyte Glycoprotein
  • Nerve Tissue Proteins
  • Peptide Fragments
  • Receptors, Transferrin
  • TPPP protein, mouse
  • Tfrc protein, mouse
  • Ferroportin
  • myelin oligodendrocyte glycoprotein (35-55)
  • solute carrier family 11- (proton-coupled divalent metal ion transporters), member 2
  • Ferritins
  • Freund's Adjuvant
  • Iron
  • Ceruloplasmin