A BET Protein Inhibitor Targeting Mononuclear Myeloid Cells Affects Specific Inflammatory Mediators and Pathways in Crohn's Disease

Cells. 2022 Sep 12;11(18):2846. doi: 10.3390/cells11182846.

Abstract

Background: Myeloid cells are critical determinants of the sustained inflammation in Crohn's Disease (CD). Targeting such cells may be an effective therapeutic approach for refractory CD patients. Bromodomain and extra-terminal domain protein inhibitors (iBET) are potent anti-inflammatory agents; however, they also possess wide-ranging toxicities. In the current study, we make use of a BET inhibitor containing an esterase sensitive motif (ESM-iBET), which is cleaved by carboxylesterase-1 (CES1), a highly expressed esterase in mononuclear myeloid cells.

Methods: We profiled CES1 protein expression in the intestinal biopsies, peripheral blood, and CD fistula tract (fCD) cells of CD patients using mass cytometry. The anti-inflammatory effect of ESM-iBET or its control (iBET) were evaluated in healthy donor CD14+ monocytes and fCD cells, using cytometric beads assay or RNA-sequencing.

Results: CES1 was specifically expressed in monocyte, macrophage, and dendritic cell populations in the intestinal tissue, peripheral blood, and fCD cells of CD patients. ESM-iBET inhibited IL1β, IL6, and TNFα secretion from healthy donor CD14+ monocytes and fCD immune cells, with 10- to 26-fold more potency over iBET in isolated CD14+ monocytes. Transcriptomic analysis revealed that ESM-iBET inhibited multiple inflammatory pathways, including TNF, JAK-STAT, NF-kB, NOD2, and AKT signaling, with superior potency over iBET.

Conclusions: We demonstrate specific CES1 expression in mononuclear myeloid cell subsets in peripheral blood and inflamed tissues of CD patients. We report that low dose ESM-iBET accumulates in CES1-expressing cells and exerts robust anti-inflammatory effects, which could be beneficial in refractory CD patients.

Keywords: BET inhibitor; CES1; IBD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Inflammatory Agents* / pharmacology
  • Anti-Inflammatory Agents* / therapeutic use
  • Carboxylic Ester Hydrolases
  • Crohn Disease* / drug therapy
  • Crohn Disease* / metabolism
  • Humans
  • Inflammation Mediators
  • Interleukin-6
  • Myeloid Cells / metabolism
  • NF-kappa B
  • Proto-Oncogene Proteins c-akt
  • RNA
  • Tumor Necrosis Factor-alpha

Substances

  • Anti-Inflammatory Agents
  • Inflammation Mediators
  • Interleukin-6
  • NF-kappa B
  • Tumor Necrosis Factor-alpha
  • RNA
  • Proto-Oncogene Proteins c-akt
  • Carboxylic Ester Hydrolases

Grants and funding

This work was supported by the European Union’s Horizon 2020 research and innovation program under grant agreement no. ITN-2014-EID-641665. WJ was funded by a grant from the Dutch Economic Affairs Top Sector Life Sciences and Health (LSH)—Top Consortia for Knowledge and Innovation’s (TKI), grant no. TKI-LSH T2017, and the European Crohn’s and Colitis Organization (ECCO) Pioneer Grant, 2018. Furthermore, this project was in collaboration with GlaxoSmithKline Research Collaboration Agreement No. COL300035595.