Glucagon-Like Peptide-1 Receptor Agonist Protects Dorsal Root Ganglion Neurons against Oxidative Insult

J Diabetes Res. 2019 Feb 21:2019:9426014. doi: 10.1155/2019/9426014. eCollection 2019.

Abstract

Objective: Diabetic polyneuropathy (DPN) is one of the most prevalent diabetic complications. We previously demonstrated that exendin-4 (Ex4), a glucagon-like peptide-1 receptor agonist (GLP-1RA), has beneficial effects in animal models of DPN. We hypothesized that GLP-1 signaling would protect neurons of the peripheral nervous system from oxidative insult in DPN. Here, the therapeutic potential of GLP-1RAs on DPN was investigated in depth using the cellular oxidative insult model applied to the dorsal root ganglion (DRG) neuronal cell line.

Research design and methods: Immortalized DRG neuronal 50B11 cells were cultured with and without hydrogen peroxide in the presence or absence of Ex4 or GLP-1(7-37). Cytotoxicity and viability were determined using a lactate dehydrogenase assay and MTS (3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium inner salt), respectively. Antioxidant enzyme activity was evaluated using a superoxide dismutase assay. Alteration of neuronal characteristics of 50B11 cells induced by GLP-1RAs was evaluated with immunocytochemistry utilizing antibodies for transient receptor potential vanilloid subfamily member 1, substance P, and calcitonin gene-related peptide. Cell proliferation and apoptosis were also examined by ethynyl deoxyuridine incorporation assay and APOPercentage dye, respectively. The neurite projection ratio induced by treatment with GLP-1RAs was counted. Intracellular activation of adenylate cyclase/cyclic adenosine monophosphate (cAMP) signaling was also quantified after treatment with GLP-1RAs.

Results: Neither Ex4 nor GLP-1(7-37) demonstrated cytotoxicity in the cells. An MTS assay revealed that GLP-1RAs amended impaired cell viability induced by oxidative insult in 50B11 cells. GLP-1RAs activated superoxide dismutase. GLP-1RAs induced no alteration of the distribution pattern in neuronal markers. Ex4 rescued the cells from oxidative insult-induced apoptosis. GLP-1RAs suppressed proliferation and promoted neurite projections. No GLP-1RAs induced an accumulation of cAMP.

Conclusions: Our findings indicate that GLP-1RAs have neuroprotective potential which is achieved by their direct actions on DRG neurons. Beneficial effects of GLP-1RAs on DPN could be related to these direct actions on DRG neurons.

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Apoptosis*
  • Calcitonin / metabolism
  • Cell Line
  • Cell Proliferation
  • Cell Survival
  • Cyclic AMP / metabolism
  • Diabetic Neuropathies / drug therapy
  • Ganglia, Spinal / cytology*
  • Ganglia, Spinal / drug effects*
  • Glucagon-Like Peptide-1 Receptor / agonists*
  • Hypoglycemic Agents / therapeutic use
  • Neurons / drug effects
  • Neuroprotective Agents / therapeutic use
  • Oxidative Stress*
  • Rats
  • Substance P / metabolism
  • Superoxide Dismutase / metabolism

Substances

  • Antioxidants
  • Glucagon-Like Peptide-1 Receptor
  • Hypoglycemic Agents
  • Neuroprotective Agents
  • Substance P
  • Calcitonin
  • Cyclic AMP
  • Superoxide Dismutase