Activation of AMP-activated protein kinase during sepsis/inflammation improves survival by preserving cellular metabolic fitness

FASEB J. 2020 May;34(5):7036-7057. doi: 10.1096/fj.201901900R. Epub 2020 Apr 4.

Abstract

The purpose was to determine the role of AMPK activation in the renal metabolic response to sepsis, the development of sepsis-induced acute kidney injury (AKI) and on survival. In a prospective experimental study, 167 10- to 12-week-old C57BL/6 mice underwent cecal ligation and puncture (CLP) and human proximal tubule epithelial cells (TEC; HK2) were exposed to inflammatory mix (IM), a combination of lipopolysaccharide (LPS) and high mobility group box 1 (HMGB1). Renal/TEC metabolic fitness was assessed by monitoring the expression of drivers of oxidative phosphorylation (OXPHOS), the rates of utilization of OXPHOS/glycolysis in response to metabolic stress, and mitochondrial function by measuring O2 consumption rates (OCR) and the membrane potential (Δψm ). Sepsis/IM resulted in AKI, increased mortality, and in renal AMPK activation 6-24 hours after CLP/IM. Pharmacologic activation of AMPK with 5-aminoimidazole-4-carboxamide ribonucleotide (AICAR) or metformin during sepsis improved the survival, while AMPK inhibition with Compound C increased mortality, impaired mitochondrial respiration, decreased OCR, and disrupted TEC metabolic fitness. AMPK-driven protection was associated with increased Sirt 3 expression and restoration of metabolic fitness. Renal AMPK activation in response to sepsis/IM is an adaptive mechanism that protects TEC, organs, and the host by preserving mitochondrial function and metabolic fitness likely through Sirt3 signaling.

Keywords: AMPK; Sirt3; metabolism; mitochondria; tubular epithelial cell.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • AMP-Activated Protein Kinases / antagonists & inhibitors
  • AMP-Activated Protein Kinases / metabolism*
  • Acute Kidney Injury / metabolism
  • Animals
  • Cells, Cultured
  • Disease Models, Animal
  • Enzyme Activation
  • Epithelial Cells / metabolism
  • Humans
  • Inflammation / metabolism*
  • Kidney / metabolism*
  • Kidney Tubules, Proximal / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Oxidative Phosphorylation
  • Oxygen Consumption
  • Sepsis / metabolism*

Substances

  • AMP-Activated Protein Kinases