Endoplasmic reticulum stress contributes to prediabetic peripheral neuropathy

Exp Neurol. 2013 Sep:247:342-8. doi: 10.1016/j.expneurol.2012.11.001. Epub 2012 Nov 8.

Abstract

Growing evidence suggests that prediabetes and metabolic syndrome are associated with increased risk for the development of microvascular complications including retinopathy, nephropathy, and, most commonly, peripheral painful neuropathy and/or autonomic neuropathy. The etiology of these disabling neuropathies is unclear, and several clinical and experimental studies implicated obesity, impaired fasting glycemia/impaired glucose tolerance, elevated triglyceride and non-esterified fatty acids, as well as oxidative-nitrative stress. Endoplasmic reticulum stress resulting from abnormal folding of newly synthesized proteins and leading to the impairment of metabolism, transcriptional regulation, and gene expression, is emerging as a key mechanism of metabolic diseases including obesity and diabetes. We evaluated the role for this phenomenon in prediabetic neuropathy using two animal models i.e., Zucker (fa/fa) rats and high-fat diet fed mice which displayed obesity and impaired glucose tolerance in the absence of overt hyperglycemia. Endoplasmic reticulum stress manifest in upregulation of the glucose-regulated proteins BiP/GRP78 and GRP94 of unfolded protein response was identified in the sciatic nerve of Zucker rats. A chemical chaperone, trimethylamine oxide, blunted endoplasmic reticulum stress and alleviated sensory nerve conduction velocity deficit, thermal and mechanical hypoalgesia, and tactile allodynia. A selective inhibitor of eukaryotic initiation factor-2α dephosphorylation, salubrinal, improved glucose intolerance and alleviated peripheral nerve dysfunction in high-fat diet fed mice. Our findings suggest an important role of endoplasmic reticulum stress in the neurobiology of prediabetic peripheral neuropathy, and identify a new therapeutic target.

Keywords: Diabetic peripheral neuropathy; Endoplasmic reticulum stress; Eukaryotic initiation factor-2α; High-fat diet fed mouse; Motor nerve conduction velocity; Prediabetic peripheral neuropathy; Salubrinal; Sensory nerve conduction velocity; Streptozotocin; Trimethylamine oxide; Unfolded protein response; Zucker (fa/fa) rat.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials
  • Analysis of Variance
  • Animals
  • Diet, High-Fat / adverse effects
  • Disease Models, Animal
  • Electric Stimulation
  • Endoplasmic Reticulum Chaperone BiP
  • Endoplasmic Reticulum Stress / physiology*
  • Fatty Acids / blood
  • Glucose Tolerance Test
  • Insulin / blood
  • Lipids / blood
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neural Conduction
  • Peripheral Nervous System Diseases / blood
  • Peripheral Nervous System Diseases / etiology*
  • Prediabetic State / blood
  • Prediabetic State / complications*
  • Prediabetic State / etiology
  • Rats
  • Rats, Zucker
  • Sciatic Nerve / metabolism
  • Sciatic Nerve / pathology
  • Spinal Cord / metabolism
  • Spinal Cord / pathology

Substances

  • Endoplasmic Reticulum Chaperone BiP
  • Fatty Acids
  • Hspa5 protein, mouse
  • Insulin
  • Lipids