Myeloid-derived miR-223 regulates intestinal inflammation via repression of the NLRP3 inflammasome

J Exp Med. 2017 Jun 5;214(6):1737-1752. doi: 10.1084/jem.20160462. Epub 2017 May 9.

Abstract

MicroRNA (miRNA)-mediated RNA interference regulates many immune processes, but how miRNA circuits orchestrate aberrant intestinal inflammation during inflammatory bowel disease (IBD) is poorly defined. Here, we report that miR-223 limits intestinal inflammation by constraining the nlrp3 inflammasome. miR-223 was increased in intestinal biopsies from patients with active IBD and in preclinical models of intestinal inflammation. miR-223-/y mice presented with exacerbated myeloid-driven experimental colitis with heightened clinical, histopathological, and cytokine readouts. Mechanistically, enhanced NLRP3 inflammasome expression with elevated IL-1β was a predominant feature during the initiation of colitis with miR-223 deficiency. Depletion of CCR2+ inflammatory monocytes and pharmacologic blockade of IL-1β or NLRP3 abrogated this phenotype. Generation of a novel mouse line, with deletion of the miR-223 binding site in the NLRP3 3' untranslated region, phenocopied the characteristics of miR-223-/y mice. Finally, nanoparticle-mediated overexpression of miR-223 attenuated experimental colitis, NLRP3 levels, and IL-1β release. Collectively, our data reveal a previously unappreciated role for miR-223 in regulating the innate immune response during intestinal inflammation.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Antibodies / metabolism
  • Base Sequence
  • Colitis / chemically induced
  • Colitis / genetics
  • Colitis / pathology
  • Dextran Sulfate
  • Disease Susceptibility
  • Hematopoiesis
  • Humans
  • Inflammasomes / metabolism*
  • Inflammation / genetics*
  • Inflammation / pathology
  • Inflammatory Bowel Diseases / genetics
  • Inflammatory Bowel Diseases / pathology
  • Interleukin-1beta / metabolism
  • Intestines / pathology*
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • Monocytes / metabolism
  • Myeloid Cells / metabolism*
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Nanoparticles / chemistry
  • Neutrophils / metabolism
  • Receptors, CCR2 / metabolism

Substances

  • Antibodies
  • Ccr2 protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • MIRN223 microRNA, human
  • MIRN223 microRNA, mouse
  • MicroRNAs
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nlrp3 protein, mouse
  • Receptors, CCR2
  • Dextran Sulfate