Mammalian Target of Rapamycin (mTOR) and the Proteasome Attenuates IL-1β Expression in Primary Mouse Cardiac Fibroblasts

Front Immunol. 2019 Jun 6:10:1285. doi: 10.3389/fimmu.2019.01285. eCollection 2019.

Abstract

Background: IL-1β is a highly potent pro-inflammatory cytokine and its secretion is tightly regulated. Inactive pro-IL-1β is transcribed in response to innate immune receptors activating NFκB. If tissue damage occurs, danger signals released from necrotic cells, such as ATP, can activate NLRP3-inflammasomes (multiprotein complexes consisting of NLRP3, ASC, and active caspase-1) which cleaves and activates pro-IL-1β. NLRP3 activation also depends on NEK7 and mitochondrial ROS-production. Thus, IL-1β secretion may be regulated at the level of each involved component. We have previously shown that NLRP3-dependent IL-1β release can be induced in cardiac fibroblasts by pro-inflammatory stimuli. However, anti-inflammatory mechanisms targeting IL-1β release in cardiac cells have not been investigated. mTOR is a key regulator of protein metabolism, including autophagy and proteasome activity. In this study we explored whether autophagy or proteasomal degradation are regulators of NLRP3 inflammasome activation and IL-1β release from cardiac fibroblasts. Methods and Results: Serum starvation selectively reduced LPS/ATP-induced IL-1β secretion from cardiac fibroblasts. However, no other inflammasome components, nor mitochondrial mass, were affected. The mTOR inhibitor rapamycin restored pro-IL-1β protein levels as well as LPS/ATP-induced IL-1β release from serum starved cells. However, neither serum starvation nor rapamycin induced autophagy in cardiac fibroblasts. Conversely, chloroquine and bafilomycin A (inhibitors of autophagy) and betulinic acid (a proteasome activator) effectively reduced LPS-induced pro-IL-1β protein levels. Key findings were reinvestigated in human monocyte-derived macrophages. Conclusion: In cardiac fibroblasts, mTOR inhibition selectively favors pro-IL-1β synthesis while proteasomal degradation and not autophagy is the major catabolic anti-inflammatory mechanism for degradation of this cytokine.

Keywords: IL-1; NLRP3; cardiac; chloroquine; fibroblasts; inflammasome; mTOR; proteasome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers
  • Cell Line
  • Cells, Cultured
  • Chloroquine
  • Cytokines
  • Fibroblasts / metabolism*
  • Gene Expression*
  • Inflammasomes / metabolism*
  • Interleukin-1beta / genetics*
  • Interleukin-1beta / metabolism
  • Macrophages / immunology
  • Macrophages / metabolism
  • Mice
  • Mitochondria / metabolism
  • Proteolysis
  • Reactive Oxygen Species / metabolism
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Biomarkers
  • Cytokines
  • Inflammasomes
  • Interleukin-1beta
  • Reactive Oxygen Species
  • Chloroquine
  • TOR Serine-Threonine Kinases