p38δ MAPK: A Novel Regulator of NLRP3 Inflammasome Activation With Increased Expression in Coronary Atherogenesis

Arterioscler Thromb Vasc Biol. 2016 Sep;36(9):1937-46. doi: 10.1161/ATVBAHA.115.307312. Epub 2016 Jul 14.

Abstract

Objective: Activation of the inflammasome pathway in macrophages results in the secretion of 2 potent proinflammatory and proatherogenic cytokines, interleukin (IL)-1β, and IL-18. Atherosclerotic lesions are characterized by the presence of various endogenous activators of the NLR family pyrin domain containing 3 (NLRP3) inflammasome, including cholesterol crystals and extracellular ATP. The aim of this study was to comprehensively characterize the expression of inflammasome pathway components and regulators in human atherosclerotic lesions.

Approach and results: Twenty human coronary artery RNA samples from 10 explanted hearts were analyzed using an inflammasome pathway-focused quantitative polymerase chain reaction array. Advanced atherosclerotic plaques, when compared with early-to-intermediate lesions from the same coronary trees, displayed significant upregulation of 12 target genes, including the key inflammasome components apoptosis-associated speck-like protein containing a CARD domain, caspase-1, and IL-18. Immunohistochemical stainings of the advanced plaques revealed macrophage foam cells positive for NLRP3 inflammasome components around the necrotic lipid cores. The polymerase chain reaction array target p38δ mitogen-activated protein kinase was upregulated in advanced plaques and strongly expressed by lesional macrophage foam cells. In cultured human monocyte-derived macrophages, the p38δ mitogen-activated protein kinase was activated by intracellular stress signals triggered during ATP- and cholesterol crystal-induced NLRP3 inflammasome activation and was required for NLRP3-mediated IL-1β secretion.

Conclusions: Increased expression of the key inflammasome components in advanced coronary lesions implies enhanced activity of the inflammasome pathway in progression of coronary atherosclerosis. The p38δ mitogen-activated protein kinase was identified as a novel regulator of NLRP3 inflammasome activation in primary human macrophages, and thus, represents a potential target for modulation of atherosclerotic inflammation.

Keywords: coronary artery disease; inflammation; innate immunity; interleukin; macrophage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Cells, Cultured
  • Cholesterol / metabolism
  • Coronary Artery Disease / enzymology*
  • Coronary Artery Disease / genetics
  • Coronary Artery Disease / pathology
  • Coronary Vessels / enzymology*
  • Coronary Vessels / pathology
  • Crystallization
  • Enzyme Activation
  • Foam Cells / enzymology*
  • Foam Cells / pathology
  • Gene Expression Profiling / methods
  • Histocompatibility Antigens Class II / metabolism
  • Humans
  • Inflammasomes / genetics
  • Inflammasomes / metabolism*
  • Male
  • Middle Aged
  • Mitogen-Activated Protein Kinase 13 / genetics
  • Mitogen-Activated Protein Kinase 13 / metabolism*
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Necrosis
  • Nuclear Proteins / metabolism
  • Oligonucleotide Array Sequence Analysis
  • Plaque, Atherosclerotic*
  • Primary Cell Culture
  • Real-Time Polymerase Chain Reaction
  • Signal Transduction
  • Time Factors
  • Trans-Activators / metabolism
  • Up-Regulation

Substances

  • Histocompatibility Antigens Class II
  • Inflammasomes
  • MHC class II transactivator protein
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nuclear Proteins
  • Trans-Activators
  • Adenosine Triphosphate
  • Cholesterol
  • Mitogen-Activated Protein Kinase 13