3-(2-Oxo-2-phenylethylidene)-2,3,6,7-tetrahydro-1H-pyrazino[2,1-a]isoquinolin-4(11bH)-one (compound 1), a novel potent Nrf2/ARE inducer, protects against DSS-induced colitis via inhibiting NLRP3 inflammasome

Biochem Pharmacol. 2016 Feb 1:101:71-86. doi: 10.1016/j.bcp.2015.11.015. Epub 2015 Nov 14.

Abstract

NLRP3 inflammasome is a key component of the inflammatory process and its dysregulation contributes to IBD for its ability to induce IL-1β release. Previously, we reported that a novel small molecular activator of Nrf2, 3-(2-oxo-2-phenylethylidene)-2,3,6,7-tetrahydro-1H-pyrazino-[2,1-a]isoquinolin-4(11bH)-one (compound 1) can prevent the development of colorectal adenomas in AOM-DSS models. Here we further investigated the anti-inflammatory effect of compound 1 in DSS-induced colitis in C57BL/6 and NLRP3(-/-) mice, and revealed the possible modulation by compound 1 of NLRP3 inflammasome-mediated IL-1β release from macrophages. In C57BL/6 mice, oral administration of compound 1 significantly attenuated DSS-induced colonic pathological damage, remarkably inhibited inflammatory cells infiltration and decreased myeloperoxidase (MPO) and IL-1β secretion in colons. In contrast, mice deficient for NLRP3 were less sensitive to DSS-induced acute colitis, and compound 1 treatment exerted no protective effect on DSS-induced intestinal inflammation in NLRP3(-/-) mice. The protective effect of compound 1 may be attributed to its inhibition of NLRP3 inflammasome and Nrf2 activation in colons. Furthermore, compound 1, as a small molecular activator of Nrf2, significantly inhibited NLRP3 inflammasome activation in both THP-1 derived macrophages and bone-marrow derived macrophages, as indicated by reduced expression of NLRP3 and cleaved caspase-1, and lowered IL-1β secretion. Finally, compound 1-induced NLRP3 inflammasome inhibition is through blocking NLRP3 priming step and dependent on Nrf2 activation. Taken together, our findings demonstrate that compound 1 might be a potential agent for the treatment of IBD by targeting Nrf2 and NLRP3 inflammasome.

Keywords: DSS; Inflammatory bowel disease; NLRP3 inflammasome; Nrf2; ROS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / administration & dosage
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use*
  • Antioxidant Response Elements / drug effects*
  • Carrier Proteins / antagonists & inhibitors*
  • Carrier Proteins / metabolism
  • Cell Line
  • Cells, Cultured
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / metabolism
  • Colitis, Ulcerative / pathology
  • Colitis, Ulcerative / prevention & control*
  • Colon / drug effects
  • Colon / immunology
  • Colon / metabolism
  • Colon / pathology
  • Dose-Response Relationship, Drug
  • Female
  • Gastrointestinal Agents / administration & dosage
  • Gastrointestinal Agents / pharmacology
  • Gastrointestinal Agents / therapeutic use
  • Genes, Reporter / drug effects
  • Humans
  • Inflammasomes / drug effects*
  • Inflammasomes / metabolism
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Isoquinolines / administration & dosage
  • Isoquinolines / pharmacology
  • Isoquinolines / therapeutic use*
  • Macrophages / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-E2-Related Factor 2 / agonists*
  • NF-E2-Related Factor 2 / antagonists & inhibitors
  • NF-E2-Related Factor 2 / genetics
  • NF-E2-Related Factor 2 / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Pyrazines / administration & dosage
  • Pyrazines / pharmacology
  • Pyrazines / therapeutic use*
  • RNA Interference

Substances

  • 3-(2-oxo-2-phenylethylidene)-2,3,6,7-tetrahydro-1H-pyrazino(2,1-a)isoquinolin-4(11bH)-one
  • Anti-Inflammatory Agents, Non-Steroidal
  • Carrier Proteins
  • Gastrointestinal Agents
  • Inflammasomes
  • Isoquinolines
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Pyrazines