β-cell dysfunctional ERAD/ubiquitin/proteasome system in type 2 diabetes mediated by islet amyloid polypeptide-induced UCH-L1 deficiency

Diabetes. 2011 Jan;60(1):227-38. doi: 10.2337/db10-0522. Epub 2010 Oct 27.

Abstract

Objective: The islet in type 2 diabetes is characterized by β-cell apoptosis, β-cell endoplasmic reticulum stress, and islet amyloid deposits derived from islet amyloid polypeptide (IAPP). Toxic oligomers of IAPP form intracellularly in β-cells in humans with type 2 diabetes, suggesting impaired clearance of misfolded proteins. In this study, we investigated whether human-IAPP (h-IAPP) disrupts the endoplasmic reticulum-associated degradation/ubiquitin/proteasome system.

Research design and methods: We used pancreatic tissue from humans with and without type 2 diabetes, isolated islets from h-IAPP transgenic rats, isolated human islets, and INS 832/13 cells transduced with adenoviruses expressing either h-IAPP or a comparable expression of rodent-IAPP. Immunofluorescence and Western blotting were used to detect polyubiquitinated proteins and ubiquitin carboxyl-terminal hydrolase L1 (UCH-L1) protein levels. Proteasome activity was measured in isolated rat and human islets. UCH-L1 was knocked down by small-interfering RNA in INS 832/13 cells and apoptosis was evaluated.

Results: We report accumulation of polyubiquinated proteins and UCH-L1 deficiency in β-cells of humans with type 2 diabetes. These findings were reproduced by expression of oligomeric h-IAPP but not soluble rat-IAPP. Downregulation of UCH-L1 expression and activity to reproduce that caused by h-IAPP in β-cells induced endoplasmic reticulum stress leading to apoptosis.

Conclusions: Our results indicate that defective protein degradation in β-cells in type 2 diabetes can, at least in part, be attributed to misfolded h-IAPP leading to UCH-L1 deficiency, which in turn further compromises β-cell viability.

Publication types

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

MeSH terms

  • Animals
  • Autopsy
  • Diabetes Mellitus, Type 2 / drug therapy
  • Diabetes Mellitus, Type 2 / genetics*
  • Diabetes Mellitus, Type 2 / metabolism
  • Humans
  • Hypoglycemic Agents / therapeutic use
  • Insulin / therapeutic use
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / pathology
  • Insulin-Secreting Cells / physiology*
  • Islet Amyloid Polypeptide / genetics
  • Islet Amyloid Polypeptide / pharmacology*
  • Nuclear Proteins / drug effects
  • Nuclear Proteins / metabolism
  • Obesity / complications
  • Obesity / pathology
  • Proteasome Endopeptidase Complex / metabolism*
  • Rats
  • Rats, Transgenic
  • Ubiquitin / drug effects
  • Ubiquitin / metabolism*
  • Ubiquitin Thiolesterase / deficiency*
  • Ubiquitin Thiolesterase / drug effects

Substances

  • Hypoglycemic Agents
  • Insulin
  • Islet Amyloid Polypeptide
  • Nuclear Proteins
  • UCHL1 protein, human
  • Ubiquitin
  • Ubiquitin Thiolesterase
  • Proteasome Endopeptidase Complex