Cellular interaction and cytotoxicity of the iowa mutation of apolipoprotein A-I (ApoA-IIowa) amyloid mediated by sulfate moieties of heparan sulfate

J Biol Chem. 2015 Oct 2;290(40):24210-21. doi: 10.1074/jbc.M115.652545. Epub 2015 Aug 19.

Abstract

The single amino acid mutation G26R in human apolipoprotein A-I (apoA-I) is associated with familial amyloid polyneuropathy III. ApoA-I carrying this mutation (apoA-IIowa) forms amyloid fibrils in vitro. Heparan sulfate (HS) is a glycosaminoglycan that is abundant at the cell surface and in the extracellular matrix. Although HS and its highly sulfated domains are involved in aggregation of amyloid-β and accumulate in cerebral amyloid plaques of patients with Alzheimer disease and mouse models of this disease, the role of HS in familial amyloid polyneuropathy III has never been addressed. Here, we used cell models to investigate the possible role of HS in the cytotoxicity of apoA-IIowa amyloid. Wild-type CHO cells, but not pgsD-677 cells, an HS-deficient CHO mutant, demonstrated uptake of apoA-IIowa amyloid after incubation with the amyloid. Addition of sulfated glycosaminoglycans to culture media prevented interaction with and cytotoxicity of apoA-IIowa amyloid to CHO cells. Elimination of cell surface HS or inhibition of HS sulfation with chemical reagents interfered with interaction of apoA-IIowa amyloid with CHO cells. We also found that cellular interaction and cytotoxicity of apoA-IIowa amyloid were significantly attenuated in CHO cells that stably expressed the human extracellular endoglucosamine 6-sulfatases HSulf-1 and HSulf-2. Our results thus suggest that cell surface HS mediates cytotoxicity of apoA-IIowa amyloid and that enzymatic remodeling of HS mitigates the cytotoxicity.

Keywords: HSulf; amyloid; amyloidosis; apolipoprotein; familial amyloid polyneuropathy; glycobiology; heparan sulfate; proteoglycan.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid / chemistry*
  • Amyloid Neuropathies, Familial / genetics*
  • Amyloid beta-Peptides / chemistry
  • Amyloidogenic Proteins / genetics
  • Animals
  • Apolipoprotein A-I / chemistry*
  • CHO Cells
  • Cell Membrane / chemistry
  • Cricetinae
  • Cricetulus
  • Female
  • Glycosides / chemistry
  • Heparin / chemistry
  • Heparitin Sulfate / chemistry*
  • Humans
  • Lysosomes / chemistry
  • Mice
  • Mice, Inbred BALB C
  • Microscopy, Fluorescence
  • Protein Binding
  • Protein Structure, Tertiary
  • Sulfates / chemistry*
  • Sulfur / chemistry
  • Swine

Substances

  • APOA1 protein, human
  • Amyloid
  • Amyloid beta-Peptides
  • Amyloidogenic Proteins
  • Apolipoprotein A-I
  • Glycosides
  • Sulfates
  • xylosides
  • Sulfur
  • Heparin
  • Heparitin Sulfate