NLRP3 (Nucleotide Oligomerization Domain-Like Receptor Family, Pyrin Domain Containing 3)-Caspase-1 Inflammasome Degrades Contractile Proteins: Implications for Aortic Biomechanical Dysfunction and Aneurysm and Dissection Formation

Arterioscler Thromb Vasc Biol. 2017 Apr;37(4):694-706. doi: 10.1161/ATVBAHA.116.307648. Epub 2017 Feb 2.

Abstract

Objective: Increasing evidence suggests that contractile dysfunction in smooth muscle cells (SMCs) plays a critical role in aortic biomechanical dysfunction and aortic aneurysm and dissection (AAD) development. However, the mechanisms underlying SMC contractile dysfunction in sporadic AAD are poorly understood. In this study, we examined the role of the NLRP3 (nucleotide oligomerization domain-like receptor family, pyrin domain containing 3)-caspase-1 inflammasome, a key inflammatory cascade, in SMC contractile dysfunction in AAD.

Approach and results: We observed significant SMC contractile protein degradation in aortas from patients with sporadic thoracic AAD. The contractile protein degradation was associated with activation of the NLRP3-caspase-1 inflammasome cascade. In SMCs, caspase-1 bound and directly cleaved and degraded contractile proteins, leading to contractile dysfunction. Furthermore, Nlrp3 or caspase-1 deficiency in mice significantly reduced angiotensin II-induced contractile protein degradation, biomechanical dysfunction, and AAD formation in both thoracic and abdominal aortas. Finally, blocking this cascade with the inflammasome inhibitor, glyburide (an antidiabetic medication), reduced angiotensin II-induced AAD formation.

Conclusions: Inflammasome-caspase-1-mediated degradation of SMC contractile proteins may contribute to aortic biomechanical dysfunction and AAD development. This cascade may be a therapeutic target in AAD formation. In addition, glyburide may have protective effects against AAD development.

Keywords: aortic aneurysm; caspase 1; contractile proteins; glyburide; inflammasomes; proteolysis.

Publication types

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

MeSH terms

  • Aged
  • Angiotensin II
  • Animals
  • Aorta, Abdominal / drug effects
  • Aorta, Abdominal / enzymology
  • Aorta, Abdominal / pathology
  • Aorta, Abdominal / physiopathology
  • Aorta, Thoracic / drug effects
  • Aorta, Thoracic / enzymology
  • Aorta, Thoracic / pathology
  • Aorta, Thoracic / physiopathology
  • Aortic Aneurysm, Abdominal / enzymology*
  • Aortic Aneurysm, Abdominal / genetics
  • Aortic Aneurysm, Abdominal / physiopathology
  • Aortic Aneurysm, Abdominal / prevention & control
  • Aortic Aneurysm, Thoracic / enzymology*
  • Aortic Aneurysm, Thoracic / genetics
  • Aortic Aneurysm, Thoracic / physiopathology
  • Aortic Aneurysm, Thoracic / prevention & control
  • Aortic Dissection / enzymology*
  • Aortic Dissection / genetics
  • Aortic Dissection / physiopathology
  • Aortic Dissection / prevention & control
  • Biomechanical Phenomena
  • Caspase 1 / deficiency
  • Caspase 1 / genetics
  • Caspase 1 / metabolism*
  • Cells, Cultured
  • Disease Models, Animal
  • Female
  • Genetic Predisposition to Disease
  • Glyburide / pharmacology
  • Humans
  • Inflammasomes / antagonists & inhibitors
  • Inflammasomes / genetics
  • Inflammasomes / metabolism*
  • Male
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged
  • Muscle Proteins / metabolism*
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / enzymology*
  • Muscle, Smooth, Vascular / pathology
  • Muscle, Smooth, Vascular / physiopathology
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / enzymology*
  • Myocytes, Smooth Muscle / pathology
  • NLR Family, Pyrin Domain-Containing 3 Protein / deficiency
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Phenotype
  • Proteolysis
  • Vasoconstriction* / drug effects

Substances

  • Inflammasomes
  • Muscle Proteins
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Angiotensin II
  • Caspase 1
  • Glyburide