Down-regulation of insulin signaling is involved in painful diabetic neuropathy in type 2 diabetes

Pain Physician. 2013 Mar-Apr;16(2):E71-83.

Abstract

Background: Previous theories considered that the main cause of painful diabetic neuropathy (PDN) was due to hyperglycemia. However, recent evidence indicated that hyperinsulinemia plays a greater role in type 2 diabetic metabolisms (T2DM).

Objectives: Our aim was to explore insulin signaling to determine the molecular mechanism involved in the pathogenesis of PDN in T2DM.

Study design: A randomized, double blind, controlled animal trial.

Methods: We observed the localization of insulin receptor (IR) and phosphorylated insulin receptor substrate 1 (IRS-1) in the spinal cord using in situ hybridization and immunohistochemistry. Then we investigated the alternations of IR and pIRS-1 and the activity of the JAK2/STAT3 pathway by immunohistochemistry, Western Blotting, and cell culture. Finally, we detected the influence of intrathecal JAK2/STAT3 inhibitor (AG490) on nociceptive behavior and insulin signaling in ob/ob mice using Western Blotting.

Results: We found that IR and pIRS-1 are mainly located in neurons in the superficial layer of the spinal dorsal horn. The expressions of IR and pIRS-1 decreased and the JAK2/STAT3 pathway activated in the spinal dorsal horn in ob/ob mice with mechanical hyperalgesia. Next, our in vitro RESULTS indicated that hyperinsulinemia and hyperglycemia impaired insulin signaling along with the activated JAK2/STAT3 pathway in differentiated human neuronal cells (SH-SY5Y). Treatment through intrathecal injection of AG490, an inhibitor of the JAK2/STAT3 pathway, alleviated mechanical hyperalgesia in ob/ob mice and prevented impaired insulin signaling in the spinal cord.

Limitations: The activation of the JAK2/STAT3 pathway could not explain the mechanism of PDN in T1DM.

Conclusions: We demonstrate that insulin signaling impairment in the spinal dorsal horn is associated with the activated JAK2/STAT3 pathway, which contributes to the progressive PDN in T2DM.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Line
  • Diabetes Mellitus, Type 2 / complications
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diabetic Neuropathies / metabolism*
  • Down-Regulation
  • Humans
  • Immunohistochemistry
  • In Situ Hybridization
  • Insulin / metabolism*
  • Insulin Receptor Substrate Proteins / metabolism
  • Janus Kinase 2 / metabolism
  • Mice
  • Mice, Obese
  • Pain / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Insulin / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / physiology*
  • Spinal Cord / metabolism

Substances

  • Insulin
  • Insulin Receptor Substrate Proteins
  • STAT3 Transcription Factor
  • Receptor, Insulin
  • Janus Kinase 2