Molecular insights into cell toxicity of a novel familial amyloidogenic variant of β2-microglobulin

J Cell Mol Med. 2016 Aug;20(8):1443-56. doi: 10.1111/jcmm.12833. Epub 2016 Mar 18.

Abstract

The first genetic variant of β2 -microglobulin (b2M) associated with a familial form of systemic amyloidosis has been recently described. The mutated protein, carrying a substitution of Asp at position 76 with an Asn (D76N b2M), exhibits a strongly enhanced amyloidogenic tendency to aggregate with respect to the wild-type protein. In this study, we characterized the D76N b2M aggregation path and performed an unprecedented analysis of the biochemical mechanisms underlying aggregate cytotoxicity. We showed that, contrarily to what expected from other amyloid studies, early aggregates of the mutant are not the most toxic species, despite their higher surface hydrophobicity. By modulating ganglioside GM1 content in cell membrane or synthetic lipid bilayers, we confirmed the pivotal role of this lipid as aggregate recruiter favouring their cytotoxicity. We finally observed that the aggregates bind to the cell membrane inducing an alteration of its elasticity (with possible functional unbalance and cytotoxicity) in GM1-enriched domains only, thus establishing a link between aggregate-membrane contact and cell damage.

Keywords: GM1 ganglioside; amyloid cytotoxicity; membrane bilayers; protein misfolding; systemic amyloidosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amyloid / toxicity*
  • Biophysical Phenomena / drug effects
  • Calcium / metabolism
  • Cell Death / drug effects
  • Cell Line, Tumor
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Diffusion
  • G(M1) Ganglioside
  • Humans
  • Lipid Bilayers / metabolism
  • Microscopy, Atomic Force
  • Mutant Proteins / toxicity*
  • Protein Aggregates / drug effects
  • Reactive Oxygen Species / metabolism
  • beta 2-Microglobulin / toxicity*

Substances

  • Amyloid
  • Lipid Bilayers
  • Mutant Proteins
  • Protein Aggregates
  • Reactive Oxygen Species
  • beta 2-Microglobulin
  • G(M1) Ganglioside
  • Calcium