Lipopolysaccharide-induced innate immune responses are exacerbated by Prohibitin 1 deficiency and mitigated by S-adenosylmethionine in murine macrophages

PLoS One. 2020 Nov 11;15(11):e0241224. doi: 10.1371/journal.pone.0241224. eCollection 2020.

Abstract

Prohibitin 1 (Phb1) is a pleiotropic protein with multiple functions in mammalian cells including cell cycle regulation and mitochondrial protein stabilization. It has been proposed as a potential therapeutic target for a variety of diseases including inflammatory diseases. In this study, we investigated the potential immune-modulatory functions of Phb1 and anti-inflammatory properties of S-adenosylmethionine (SAMe) using macrophages, which play a major role in the innate immune system. The results showed that expressions of Phb1 mRNA and protein were reduced in lipopolysaccharide (LPS)-stimulated RAW 264.7 cells (p<0.05). Phb1 knockdown further ameliorated the mRNA expression of pro- and anti-inflammatory cytokines such as TNF-α, IL-1α, IL-1β, IL-6, and IL10 in LPS-stimulated RAW 264.7 cells. SAMe significantly attenuated LPS-induced inflammatory responses such as IL-1β, IL-10, Nos2, and NO production in the presence of siPhb1. Luciferase reporter assay was conducted to determine the mechanisms underlying the effects of Phb1 and SAMe on the immune system. The luciferase activity of nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) was significantly increased in LPS-treated RAW 264.7 cells. In addition, the luciferase reporter assay showed increased NF-κB activation in Phb1 knockdown RAW 264.7 cells (p<0.1) and SAMe treatment attenuated the NF-κB luciferase activity in Phb1 knockdown RAW 264.7 cells. Based on the results, we concluded that Phb1 possibly modulates the inflammatory response whereas SAMe has an anti-inflammatory effect on Phb1 knockdown macrophage cells. Furthermore, Phb1 expression level has potential properties of affecting on innate immune system by modulating the NF-κB signaling pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Survival / drug effects
  • Cytokines / genetics
  • Cytokines / metabolism
  • Immunity, Innate / drug effects*
  • Inflammation Mediators / metabolism
  • Lipopolysaccharides / pharmacology*
  • Macrophages / drug effects
  • Macrophages / immunology*
  • Mice
  • NF-kappa B / metabolism
  • Nitric Oxide / biosynthesis
  • Nitric Oxide Synthase Type II / metabolism
  • Prohibitins
  • RAW 264.7 Cells
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Repressor Proteins / deficiency*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • S-Adenosylmethionine / pharmacology*

Substances

  • Cytokines
  • Inflammation Mediators
  • Lipopolysaccharides
  • NF-kappa B
  • Prohibitins
  • RNA, Messenger
  • Repressor Proteins
  • Nitric Oxide
  • S-Adenosylmethionine
  • Nitric Oxide Synthase Type II

Grants and funding

The National Research Foundation of Korea provided support for this study in the form of grants awarded to KK (2016R1D1A1B04935653, 2020R1A2C1102451).