Impact of 3-Amino-1,2,4-Triazole (3-AT)-Derived Increase in Hydrogen Peroxide Levels on Inflammation and Metabolism in Human Differentiated Adipocytes

PLoS One. 2016 Mar 29;11(3):e0152550. doi: 10.1371/journal.pone.0152550. eCollection 2016.

Abstract

Obesity is characterized by an excessive accumulation of fat in adipose tissue, which is associated with oxidative stress and chronic inflammation. Excessive H2O2 levels are degraded by catalase (CAT), the activity of which is decreased in obesity. We investigated the effects of inhibition of catalase activity on metabolism and inflammation by incubating human differentiated adipocytes with 10 mM 3-amino-1,2,4-triazole (3-AT) for 24 h. As expected, the treatment decreased CAT activity and increased intracellular H2O2 levels significantly. Glutathione peroxidase (GPX) activity was also reduced, and the gene expression levels of the antioxidant enzymes GPX4 and peroxiredoxins (1, 3 and 5) were inhibited. Interestingly, this occurred along with lower mRNA levels of the transcription factors nuclear factor (erythroid 2-like 2) and forkhead box O, which are involved in redox homeostasis. However, superoxide dismutase activity and expression were increased. Moreover, 3-AT led to nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) activation and increased tumor necrosis alpha and interleukin 6 protein and gene expression levels, while lowering peroxisome proliferator-activated receptor gamma (PPARγ) mRNA and protein levels. These alterations were accompanied by an altered glucose and lipid metabolism. Indeed, adipocytes treated with 3-AT showed reduced basal glucose uptake, reduced glucose transporter type 4 gene and protein expression, reduced lipolysis, reduced AMP-activated protein kinase activation and reduced gene expression of lipases. Our results indicate that increased H2O2 levels caused by 3-AT treatment impair the antioxidant defense system, lower PPARγ expression and initiate inflammation, thus affecting glucose and lipid metabolism in human differentiated adipocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipocytes / drug effects
  • Adipocytes / metabolism*
  • Adipocytes / pathology*
  • Adult
  • Amitrole / pharmacology*
  • Antioxidants / metabolism
  • Catalase / antagonists & inhibitors
  • Catalase / metabolism
  • Cell Differentiation / drug effects*
  • Glucose / metabolism
  • Humans
  • Hydrogen Peroxide / metabolism*
  • Inflammation / metabolism*
  • Intracellular Space / metabolism
  • Lipid Metabolism / drug effects
  • PPAR gamma / metabolism

Substances

  • Antioxidants
  • PPAR gamma
  • Hydrogen Peroxide
  • Catalase
  • Glucose
  • Amitrole

Grants and funding

This work was supported by Junta de Andalucía (Project number CTS-6770; Secretaría General de Universidades, Investigación y Tecnología. Consejería de Economía, Innovación y Ciencia), and Instituto de Salud Carlos III, Fondo de Investigaciones Sanitarias, Redes temáticas de investigación cooperativa RETIC (Red SAMID RD08/0072/0028). FJRO was funded by a Formación de Profesorado Universitario stipend from the Ministry of Education and Science of the Spanish Government (AP2012-02068). CGL and AIR are recipients of fellowships from the University of Granada Plan Propio. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.