Change in the characteristics of ferritin induces iron imbalance in prion disease affected brains

Neurobiol Dis. 2012 Mar;45(3):930-8. doi: 10.1016/j.nbd.2011.12.012. Epub 2011 Dec 11.

Abstract

Prion disease associated neurotoxicity is mainly attributed to PrP-scrapie (PrP(Sc)), the disease associated isoform of a normal protein, the prion protein (PrP(C)). Participation of other proteins and processes is suspected, but their identity and contribution to the pathogenic process is unclear. Emerging evidence implicates imbalance of brain iron homeostasis as a significant cause of prion disease-associated neurotoxicity. The underlying cause of this change, however, remains unclear. We demonstrate that iron is sequestered in heat and SDS-stable protein complexes in sporadic-Creutzfeldt-Jakob-disease (sCJD) brains, creating a phenotype of iron deficiency. The underlying cause is change in the characteristics of ferritin, an iron storage protein that becomes aggregated, detergent-insoluble, and partitions with denatured ferritin using conventional methods of ferritin purification. A similar phenotype of iron deficiency is noted in the lumbar spinal cord (SC) tissue of scrapie infected hamsters, a site unlikely to be affected by massive neuronal death and non-specific iron deposition. As a result, the iron uptake protein transferrin (Tf) is upregulated in scrapie infected SC tissue, and increases with disease progression. A direct correlation between Tf and PrP(Sc) suggests sequestration of iron in dysfunctional ferritin that either co-aggregates with PrP(Sc) or is rendered dysfunctional by PrP(Sc) through an indirect process. Surprisingly, amplification of PrP(Sc)in vitro by the protein-misfolding-cyclic-amplification (PMCA) reaction using normal brain homogenate as substrate does not increase the heat and SDS-stable pool of iron even though both PrP(Sc) and ferritin aggregate by this procedure. These observations highlight important differences between PrP(Sc)-protein complexes generated in vivo during disease progression and in vitro by the PMCA reaction, and the significance of these complexes in PrP(Sc)-associated neurotoxicity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aged
  • Aged, 80 and over
  • Analysis of Variance
  • Animals
  • Brain / metabolism*
  • Creutzfeldt-Jakob Syndrome / pathology*
  • Cricetinae
  • Dementia / pathology
  • Disease Models, Animal
  • Female
  • Ferritins / metabolism*
  • Glial Fibrillary Acidic Protein / metabolism
  • Hot Temperature
  • Humans
  • Iron / metabolism*
  • Iron Isotopes / metabolism
  • Liver / drug effects
  • Liver / metabolism
  • Male
  • Mice
  • Middle Aged
  • Prions / metabolism*
  • Spinal Cord / metabolism
  • Time Factors
  • Transferrin

Substances

  • Glial Fibrillary Acidic Protein
  • Iron Isotopes
  • Prions
  • Transferrin
  • Ferritins
  • Iron