Mitochondrial NLRP3 protein induces reactive oxygen species to promote Smad protein signaling and fibrosis independent from the inflammasome

J Biol Chem. 2014 Jul 11;289(28):19571-84. doi: 10.1074/jbc.M114.550624. Epub 2014 May 19.

Abstract

Nucleotide-binding domain and leucine-rich repeat containing PYD-3 (NLRP3) is a pattern recognition receptor that is implicated in the pathogenesis of inflammation and chronic diseases. Although much is known regarding the NLRP3 inflammasome that regulates proinflammatory cytokine production in innate immune cells, the role of NLRP3 in non-professional immune cells is unclear. Here we report that NLRP3 is expressed in cardiac fibroblasts and increased during TGFβ stimulation. NLRP3-deficient cardiac fibroblasts displayed impaired differentiation and R-Smad activation in response to TGFβ. Only the central nucleotide binding domain of NLRP3 was required to augment R-Smad signaling because the N-terminal Pyrin or C-terminal leucine-rich repeat domains were dispensable. Interestingly, NLRP3 regulation of myofibroblast differentiation proceeded independently from the inflammasome, IL-1β/IL-18, or caspase 1. Instead, mitochondrially localized NLRP3 potentiated reactive oxygen species to augment R-Smad activation. In vivo, NLRP3-deficient mice were protected against angiotensin II-induced cardiac fibrosis with preserved cardiac architecture and reduced collagen 1. Together, these results support a distinct role for NLRP3 in non-professional immune cells independent from the inflammasome to regulate differential aspects of wound healing and chronic disease.

Keywords: Fibrosis; Heart Failure; Inflammation; Myofibroblast; Transforming Growth Factor β (TGFβ).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / adverse effects
  • Angiotensin II / pharmacology
  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Collagen Type I / biosynthesis
  • Collagen Type I / genetics
  • Fibrosis
  • Heart Diseases / chemically induced
  • Heart Diseases / genetics
  • Heart Diseases / metabolism
  • Heart Diseases / pathology
  • Inflammasomes*
  • Interleukin-18 / genetics
  • Interleukin-18 / metabolism
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Mice
  • Mice, Knockout
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism*
  • Myocardium / metabolism*
  • Myocardium / pathology
  • Myofibroblasts / metabolism*
  • Myofibroblasts / pathology
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Reactive Oxygen Species / metabolism*
  • Signal Transduction*
  • Smad Proteins, Receptor-Regulated / genetics
  • Smad Proteins, Receptor-Regulated / metabolism*
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism
  • Vasoconstrictor Agents / adverse effects
  • Vasoconstrictor Agents / pharmacology

Substances

  • Carrier Proteins
  • Collagen Type I
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-18
  • Interleukin-1beta
  • Mitochondrial Proteins
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Reactive Oxygen Species
  • Smad Proteins, Receptor-Regulated
  • Transforming Growth Factor beta
  • Vasoconstrictor Agents
  • Angiotensin II