Oxidative stress and programmed cell death in diabetic neuropathy

Ann N Y Acad Sci. 2002 Apr:959:368-83. doi: 10.1111/j.1749-6632.2002.tb02108.x.

Abstract

Recent evidence in both animal models and human sural nerve biopsies indicates an association with oxidative stress, mitochondrial (Mt) membrane depolarization (MMD), and induction of programmed cell death (PCD). In streptozotocin (STZ)-treated diabetic rats, hyperglycemia induces typical apoptotic changes as well as swelling and disruption of the Mt cristae in diabetic dorsal root ganglion neurons (DRG) and Schwann cells (SC), but these changes are only rarely observed in control neurons. In human sural nerve biopsies, from patients with diabetic sensory neuropathy, there is transmission electromicrograph evidence of swelling and disruption of the Mt and cristae compared to patients without peripheral neuropathy. In human SH-SY5Y neurons, rat sensory neurons, and SC, in vivo, there is an increase in reactive oxygen species (ROS) after exposure to 20 mM added glucose. In parallel, there is an initial Mt membrane hyperpolarization followed by depolarization (MMD). In turn, MMD is coupled with cleavage of caspases. Various strategies aimed at inhibiting the oxidative burst, or stabilizing the DeltaPsi(M), block induction of PCD. First, growth factors such as NGF can block induction of ROS and/or stabilize the DeltaPsi(M). This, in turn, is associated with inhibition of PCD. Second, reduction of ROS generation in neuronal Mt prevents neuronal PCD. Third, up-regulation of uncoupling proteins (UCPs), which stabilize the DeltaPsi(M), blocks induction of caspase cleavage. Collectively, these findings indicate that hyperglycemic conditions observed in diabetes mellitus are associated with oxidative stress-induced neuronal and SC death, and targeted therapies aimed at regulating ROS may prove effective in therapy of diabetic neuropathy.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Apoptosis*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Caspases / metabolism
  • Diabetic Neuropathies / physiopathology*
  • Ganglia, Spinal / cytology
  • Ganglia, Spinal / metabolism
  • Glucose / metabolism
  • Humans
  • Hyperglycemia / physiopathology
  • Ion Channels
  • Membrane Potentials
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mitochondria / metabolism*
  • Mitochondrial Proteins
  • Mitochondrial Swelling
  • Nerve Growth Factor / pharmacology
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism*
  • Oxidative Stress*
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • Schwann Cells / drug effects
  • Schwann Cells / metabolism
  • Schwann Cells / ultrastructure
  • Uncoupling Agents / metabolism
  • Uncoupling Protein 1

Substances

  • Carrier Proteins
  • Ion Channels
  • Membrane Proteins
  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • Uncoupling Agents
  • Uncoupling Protein 1
  • Nerve Growth Factor
  • Caspases
  • Glucose