Dominant mutants of ceruloplasmin impair the copper loading machinery in aceruloplasminemia

J Biol Chem. 2009 Feb 13;284(7):4545-54. doi: 10.1074/jbc.M805688200. Epub 2008 Dec 18.

Abstract

The multicopper oxidase ceruloplasmin plays a key role in iron homeostasis, and its ferroxidase activity is required to stabilize cell surface ferroportin, the only known mammalian iron exporter. Missense mutations causing the rare autosomal neurodegenerative disease aceruloplasminemia were investigated by testing their ability to prevent ferroportin degradation in rat glioma C6 cells silenced for endogenous ceruloplasmin. Most of the mutants did not complement (i.e. did not stabilize ferroportin) because of the irreversible loss of copper binding ability. Mutant R701W, which was found in a heterozygous very young patient with severe neurological problems, was unable to complement per se but did so in the presence of copper-glutathione or when the yeast copper ATPase Ccc2p was co-expressed, indicating that the protein was structurally able to bind copper but that metal loading involving the mammalian copper ATPase ATP7B was impaired. Notably, R701W exerted a dominant negative effect on wild type, and it induced the subcellular relocalization of ATP7B. Our results constitute the first evidence of "functional silencing" of ATP7B as a novel molecular defect in aceruloplasminemia. The possibility to reverse the deleterious effects of some aceruloplasminemia mutations may disclose new possible therapeutic strategies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Amino Acid Substitution*
  • Animals
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism*
  • Cell Line, Tumor
  • Ceruloplasmin / genetics
  • Ceruloplasmin / metabolism*
  • Copper
  • Copper Transport Proteins
  • Copper-Transporting ATPases
  • Gene Expression
  • Gene Silencing
  • Heredodegenerative Disorders, Nervous System / enzymology*
  • Heredodegenerative Disorders, Nervous System / genetics
  • Homeostasis
  • Humans
  • Iron / metabolism
  • Metal Metabolism, Inborn Errors / enzymology*
  • Metal Metabolism, Inborn Errors / genetics
  • Mutation, Missense*
  • Protein Binding
  • Rats
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism

Substances

  • CCC2 protein, S cerevisiae
  • Cation Transport Proteins
  • Copper Transport Proteins
  • Saccharomyces cerevisiae Proteins
  • metal transporting protein 1
  • Copper
  • Iron
  • Ceruloplasmin
  • Adenosine Triphosphatases
  • ATP7B protein, human
  • Copper-Transporting ATPases