Palmitic Acid Induces Oxidative Stress and Senescence in Human Brainstem Astrocytes, Downregulating Glutamate Reuptake Transporters-Implications for Obesity-Related Sympathoexcitation

Nutrients. 2024 Aug 26;16(17):2852. doi: 10.3390/nu16172852.

Abstract

Obesity has been associated with a chronic increase in sympathetic nerve activity, which can lead to hypertension and other cardiovascular diseases. Preliminary studies from our lab found that oxidative stress and neuroinflammation in the brainstem contribute to sympathetic overactivity in high-fat-diet-induced obese mice. However, with glial cells emerging as significant contributors to various physiological processes, their role in causing these changes in obesity remains unknown. In this study, we wanted to determine the role of palmitic acid, a major form of saturated fatty acid in the high-fat diet, in regulating sympathetic outflow. Human brainstem astrocytes (HBAs) were used as a cell culture model since astrocytes are the most abundant glial cells and are more closely associated with the regulation of neurons and, hence, sympathetic nerve activity. In the current study, we hypothesized that palmitic acid-mediated oxidative stress induces senescence and downregulates glutamate reuptake transporters in HBAs. HBAs were treated with palmitic acid (25 μM for 24 h) in three separate experiments. After the treatment period, the cells were collected for gene expression and protein analysis. Our results showed that palmitic acid treatment led to a significant increase in the mRNA expression of oxidative stress markers (NQO1, SOD2, and CAT), cellular senescence markers (p21 and p53), SASP factors (TNFα, IL-6, MCP-1, and CXCL10), and a downregulation in the expression of glutamate reuptake transporters (EAAT1 and EAAT2) in the HBAs. Protein levels of Gamma H2AX, p16, and p21 were also significantly upregulated in the treatment group compared to the control. Our results showed that palmitic acid increased oxidative stress, DNA damage, cellular senescence, and SASP factors, and downregulated the expression of glutamate reuptake transporters in HBAs. These findings suggest the possibility of excitotoxicity in the neurons of the brainstem, sympathoexcitation, and increased risk for cardiovascular diseases in obesity.

Keywords: EAAT2; glial cells; obesity; oxidative stress; p21/p53; senescence.

MeSH terms

  • Amino Acid Transport System X-AG / metabolism
  • Astrocytes* / drug effects
  • Astrocytes* / metabolism
  • Brain Stem* / drug effects
  • Brain Stem* / metabolism
  • Cells, Cultured
  • Cellular Senescence* / drug effects
  • Down-Regulation*
  • Humans
  • Obesity* / metabolism
  • Oxidative Stress* / drug effects
  • Palmitic Acid* / pharmacology
  • Sympathetic Nervous System / drug effects
  • Sympathetic Nervous System / metabolism

Substances

  • Palmitic Acid
  • Amino Acid Transport System X-AG

Grants and funding

This research was supported by grants from NIH-NHLBI R01HL163775 (M.S.); NIH-NHLBI R15 HL14884401 (M.S.), AHA-AIREA Grant #959725 (M.S.), OCASCR Research Grant (M.S.), and K01AG073613 (P.B.).