UCP2-induced fatty acid synthase promotes NLRP3 inflammasome activation during sepsis

J Clin Invest. 2015 Feb;125(2):665-80. doi: 10.1172/JCI78253. Epub 2015 Jan 9.

Abstract

Cellular lipid metabolism has been linked to immune responses; however, the precise mechanisms by which de novo fatty acid synthesis can regulate inflammatory responses remain unclear. The NLRP3 inflammasome serves as a platform for caspase-1-dependent maturation and secretion of proinflammatory cytokines. Here, we demonstrated that the mitochondrial uncoupling protein-2 (UCP2) regulates NLRP3-mediated caspase-1 activation through the stimulation of lipid synthesis in macrophages. UCP2-deficient mice displayed improved survival in a mouse model of polymicrobial sepsis. Moreover, UCP2 expression was increased in human sepsis. Consistently, UCP2-deficient mice displayed impaired lipid synthesis and decreased production of IL-1β and IL-18 in response to LPS challenge. In macrophages, UCP2 deficiency suppressed NLRP3-mediated caspase-1 activation and NLRP3 expression associated with inhibition of lipid synthesis. In UCP2-deficient macrophages, inhibition of lipid synthesis resulted from the downregulation of fatty acid synthase (FASN), a key regulator of fatty acid synthesis. FASN inhibition by shRNA and treatment with the chemical inhibitors C75 and cerulenin suppressed NLRP3-mediated caspase-1 activation and inhibited NLRP3 and pro-IL-1β gene expression in macrophages. In conclusion, our results suggest that UCP2 regulates the NLRP3 inflammasome by inducing the lipid synthesis pathway in macrophages. These results identify UCP2 as a potential therapeutic target in inflammatory diseases such as sepsis.

Publication types

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

MeSH terms

  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Caspase 1 / genetics
  • Caspase 1 / metabolism
  • Down-Regulation / genetics
  • Enzyme Induction / genetics
  • Fatty Acid Synthase, Type I / biosynthesis*
  • Fatty Acid Synthase, Type I / genetics
  • Humans
  • Inflammasomes / genetics
  • Inflammasomes / metabolism*
  • Interleukin-18 / genetics
  • Interleukin-18 / metabolism
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Ion Channels / genetics
  • Ion Channels / metabolism*
  • Lipids / biosynthesis
  • Lipids / genetics
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Mice
  • Mice, Knockout
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Sepsis / chemically induced
  • Sepsis / genetics
  • Sepsis / metabolism*
  • Sepsis / pathology
  • Sepsis / therapy
  • Uncoupling Protein 2

Substances

  • Carrier Proteins
  • IL1B protein, rat
  • Inflammasomes
  • Interleukin-18
  • Interleukin-1beta
  • Ion Channels
  • Lipids
  • Mitochondrial Proteins
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • UCP2 protein, human
  • Ucp2 protein, mouse
  • Ucp2 protein, rat
  • Uncoupling Protein 2
  • Fatty Acid Synthase, Type I
  • Caspase 1