Insulin-mediated oxidative stress and DNA damage in LLC-PK1 pig kidney cell line, female rat primary kidney cells, and male ZDF rat kidneys in vivo

Endocrinology. 2013 Apr;154(4):1434-43. doi: 10.1210/en.2012-1768. Epub 2013 Mar 1.

Abstract

Hyperinsulinemia, a condition with excessively high insulin blood levels, is related to an increased cancer incidence. Diabetes mellitus is the most common of several diseases accompanied by hyperinsulinemia. Because an elevated kidney cancer risk was reported for diabetic patients, we investigated the induction of genomic damage by insulin in LLC-PK1 pig kidney cells, rat primary kidney cells, and ZDF rat kidneys. Insulin at a concentration of 5nM caused a significant increase in DNA damage in vitro. This was associated with the formation of reactive oxygen species (ROS). In the presence of antioxidants, blockers of the insulin, and IGF-I receptors, and a phosphatidylinositol 3-kinase inhibitor, the insulin-mediated DNA damage was reduced. Phosphorylation of protein kinase B (PKB or AKT) was increased and p53 accumulated. Inhibition of the mitochondrial and nicotinamide adenine dinucleotide phosphatase oxidase-related ROS production reduced the insulin-mediated damage. In primary rat cells, insulin also induced genomic damage. In kidneys from healthy, lean ZDF rats, which were infused with insulin to yield normal or high blood insulin levels, while keeping blood glucose levels constant, the amounts of ROS and the tumor protein (p53) were elevated in the high-insulin group compared with the control level group. ROS and p53 were also elevated in diabetic obese ZDF rats. Overall, insulin-induced oxidative stress resulted in genomic damage. If the same mechanisms are active in patients, hyperinsulinemia might cause genomic damage through the induction of ROS contributing to the increased cancer risk, against which the use of antioxidants and/or ROS production inhibitors might exert protective effects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants / pharmacology
  • Cells, Cultured
  • Comet Assay
  • DNA Damage*
  • Female
  • HL-60 Cells / drug effects
  • Humans
  • Hyperinsulinism / complications
  • Hypoglycemic Agents / adverse effects*
  • Insulin / adverse effects*
  • Kidney / cytology
  • Kidney / drug effects*
  • LLC-PK1 Cells / drug effects
  • Male
  • Neoplasms / complications
  • Oncogene Protein v-akt / drug effects
  • Oxidative Stress*
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Rats
  • Reactive Oxygen Species / metabolism
  • Receptor, IGF Type 1 / antagonists & inhibitors
  • Receptor, Insulin / antagonists & inhibitors
  • Swine
  • Tumor Suppressor Protein p53 / drug effects

Substances

  • Antioxidants
  • Hypoglycemic Agents
  • Insulin
  • Phosphoinositide-3 Kinase Inhibitors
  • Reactive Oxygen Species
  • Tumor Suppressor Protein p53
  • Receptor, IGF Type 1
  • Receptor, Insulin
  • Oncogene Protein v-akt