Targeting the NLRP3 Inflammasome With Inhibitor MCC950 Prevents Aortic Aneurysms and Dissections in Mice

J Am Heart Assoc. 2020 Apr 7;9(7):e014044. doi: 10.1161/JAHA.119.014044. Epub 2020 Mar 30.

Abstract

Background Aortic aneurysms and dissections are highly lethal diseases for which an effective treatment strategy is critically needed to prevent disease progression. The nucleotide-binding oligomerization domain-like receptor pyrin domain containing 3 (NLRP3)-caspase-1 inflammasome cascade was recently shown to play an important role in aortic destruction and disease development. In this study, we tested the effects of MCC950, a potent, selective NLRP3 inhibitor, on preventing aortic destruction and aortic aneurysm and dissection formation. Methods and Results In a model of sporadic aortic aneurysm and dissection induced by challenging wild-type mice with a high-fat, high-cholesterol diet and angiotensin II infusion, MCC950 treatment significantly inhibited challenge-induced aortic dilatation, dissection, and rupture in different thoracic and abdominal aortic segments in both male and female mice. Aortic disease reduction by MCC950 was associated with the prevention of NLRP3-caspase-1 upregulation, smooth muscle cell contractile protein degradation, aortic cell death, and extracellular matrix destruction. Further investigation revealed that preventing matrix metallopeptidase 9 (MMP-9) expression and activation in macrophages is an important mechanism underlying MCC950's protective effect. We found that caspase-1 directly activated MMP-9 by cleaving its N-terminal inhibitory domain. Moreover, the genetic knockdown of Nlrp3 or Casp-1 in mice or treatment of mice with MCC950 diminished the challenge-induced N-terminal cleavage of MMP-9, MMP-9 activation, and aortic destruction. Conclusions Our findings suggest that the NLRP3-caspase-1 inflammasome directly activates MMP-9. Targeting the inflammasome with MCC950 is a promising approach for preventing aortic destruction and aortic aneurysm and dissection development.

Keywords: MCC950; MMP‐9 activation; NLRP3 inflammasome inhibitor; aortic destruction.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Anti-Inflammatory Agents / pharmacology*
  • Aorta, Abdominal / drug effects*
  • Aorta, Abdominal / metabolism
  • Aorta, Abdominal / pathology
  • Aorta, Thoracic / drug effects*
  • Aorta, Thoracic / metabolism
  • Aorta, Thoracic / pathology
  • Aortic Aneurysm, Abdominal / metabolism
  • Aortic Aneurysm, Abdominal / pathology
  • Aortic Aneurysm, Abdominal / prevention & control*
  • Aortic Aneurysm, Thoracic / metabolism
  • Aortic Aneurysm, Thoracic / pathology
  • Aortic Aneurysm, Thoracic / prevention & control*
  • Aortic Dissection / metabolism
  • Aortic Dissection / pathology
  • Aortic Dissection / prevention & control*
  • Case-Control Studies
  • Caspase 1 / genetics
  • Caspase 1 / metabolism
  • Collagen / metabolism
  • Disease Models, Animal
  • Female
  • Furans
  • Heterocyclic Compounds, 4 or More Rings / pharmacology*
  • Humans
  • Indenes
  • Inflammasomes / antagonists & inhibitors*
  • Inflammasomes / metabolism
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Male
  • Matrix Metalloproteinase 9 / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • NLR Family, Pyrin Domain-Containing 3 Protein / antagonists & inhibitors*
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Prospective Studies
  • Signal Transduction
  • Sulfonamides
  • Sulfones / pharmacology*
  • THP-1 Cells
  • Vascular Remodeling / drug effects

Substances

  • Anti-Inflammatory Agents
  • Furans
  • Heterocyclic Compounds, 4 or More Rings
  • Indenes
  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nlrp3 protein, mouse
  • Sulfonamides
  • Sulfones
  • N-(1,2,3,5,6,7-hexahydro-S-indacen-4-ylcarbamoyl)-4-(2-hydroxy-2-propanyl)-2-furansulfonamide
  • Collagen
  • Casp1 protein, mouse
  • Caspase 1
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse