Expression of Amyloidogenic Transthyretin Drives Hepatic Proteostasis Remodeling in an Induced Pluripotent Stem Cell Model of Systemic Amyloid Disease

Stem Cell Reports. 2020 Aug 11;15(2):515-528. doi: 10.1016/j.stemcr.2020.07.003. Epub 2020 Jul 30.

Abstract

The systemic amyloidoses are diverse disorders in which misfolded proteins are secreted by effector organs and deposited as proteotoxic aggregates at downstream tissues. Although well described clinically, the contribution of synthesizing organs to amyloid disease pathogenesis is unknown. Here, we utilize hereditary transthyretin amyloidosis (ATTR amyloidosis) induced pluripotent stem cells (iPSCs) to define the contribution of hepatocyte-like cells (HLCs) to the proteotoxicity of secreted transthyretin (TTR). To this end, we generated isogenic, patient-specific iPSCs expressing either amyloidogenic or wild-type TTR. We combined this tool with single-cell RNA sequencing to identify hepatic proteostasis factors correlating with destabilized TTR production in iPSC-derived HLCs. By generating an ATF6 inducible patient-specific iPSC line, we demonstrated that enhancing hepatic ER proteostasis preferentially reduces the secretion of amyloidogenic TTR. These data highlight the liver's capacity to chaperone misfolded TTR prior to deposition, and moreover suggest the potential for unfolded protein response modulating therapeutics in the treatment of diverse systemic amyloidoses.

Keywords: amyloid; gene editing; hepatic disease; hereditary amyloidosis; pluripotent stem cells; protein folding disorders; proteostasis; single cell RNA sequencing; transthyretin; unfolded protein response.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 6 / metabolism
  • Amyloid / metabolism*
  • Amyloid Neuropathies, Familial / genetics
  • Amyloid Neuropathies, Familial / pathology*
  • Gene Editing
  • Gene Expression Regulation
  • Hepatocytes / metabolism
  • Hepatocytes / pathology
  • Humans
  • Induced Pluripotent Stem Cells / pathology*
  • Liver / pathology*
  • Models, Biological*
  • Mutation / genetics
  • Prealbumin / genetics
  • Prealbumin / metabolism*
  • Promoter Regions, Genetic / genetics
  • Protein Stability
  • Proteostasis*
  • Sequence Analysis, RNA
  • Signal Transduction
  • Single-Cell Analysis
  • Stress, Physiological
  • Transferrin / metabolism
  • Unfolded Protein Response

Substances

  • ATF6 protein, human
  • Activating Transcription Factor 6
  • Amyloid
  • Prealbumin
  • Transferrin

Supplementary concepts

  • Amyloidosis, Hereditary, Transthyretin-Related