Angiotensin II Alters Mitochondrial Membrane Potential and Lipid Metabolism in Rat Colonic Epithelial Cells

Biomolecules. 2024 Aug 9;14(8):974. doi: 10.3390/biom14080974.

Abstract

An over-active renin-angiotensin system (RAS) is characterized by elevated angiotensin II (Ang II). While Ang II can promote metabolic and mitochondrial dysfunction in tissues, little is known about its role in the gastrointestinal system (GI). Here, we treated rat primary colonic epithelial cells with Ang II (1-5000 nM) to better define their role in the GI. We hypothesized that Ang II would negatively affect mitochondrial bioenergetics as these organelles express Ang II receptors. Ang II increased cellular ATP production but reduced the mitochondrial membrane potential (MMP) of colonocytes. However, cells maintained mitochondrial oxidative phosphorylation and glycolysis with treatment, reflecting metabolic compensation with impaired MMP. To determine whether lipid dysregulation was evident, untargeted lipidomics were conducted. A total of 1949 lipids were detected in colonocytes spanning 55 distinct (sub)classes. Ang II (1 nM) altered the abundance of some sphingosines [So(d16:1)], ceramides [Cer-AP(t18:0/24:0)], and phosphatidylcholines [OxPC(16:0_20:5(2O)], while 100 nM Ang II altered some triglycerides and phosphatidylserines [PS(19:0_22:1). Ang II did not alter the relative expression of several enzymes in lipid metabolism; however, the expression of pyruvate dehydrogenase kinase 2 (PDK2) was increased, and PDK2 can be protective against dyslipidemia. This study is the first to investigate the role of Ang II in colonic epithelial cell metabolism.

Keywords: angiotensin II; bioenergetics; colonocytes; lipidomics; lipids; mitochondria.

MeSH terms

  • Angiotensin II* / metabolism
  • Angiotensin II* / pharmacology
  • Animals
  • Colon* / cytology
  • Colon* / drug effects
  • Colon* / metabolism
  • Epithelial Cells* / drug effects
  • Epithelial Cells* / metabolism
  • Lipid Metabolism* / drug effects
  • Lipidomics
  • Membrane Potential, Mitochondrial* / drug effects
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Angiotensin II

Grants and funding

This research was funded by 1R56HL136692-01 to J.Z. and C.J.M., R21AT010192 Award AWD05242 P0104932 to J.Z. and C.J.M., the University of Florida College of Veterinary Medicine (UFCVM) Start Up Funds to J.Z. and C.J.M., and R01HL152162 to J.Z. K.S. was supported by a University of Florida Graduate student scholarship. D.D.T. was supported by the University of Florida College of Veterinary Medicine Florida Veterinary Scholars Program (funded by Boehringer Ingelheim).