Discovery of selective Orai channel blockers bearing an indazole or a pyrazole scaffold

Eur J Med Chem. 2024 Nov 15:278:116805. doi: 10.1016/j.ejmech.2024.116805. Epub 2024 Aug 28.

Abstract

The calcium release activated calcium (CRAC) channel is highly expressed in T lymphocytes and plays a critical role in regulating T cell proliferation and functions including activation of the transcription factor nuclear factor of activated T cells (NFAT), cytokine production and cytotoxicity. The CRAC channel consists of the Orai pore subunit and STIM (stromal interacting molecule) endoplasmic reticulum calcium sensor. Loss of CRAC channel mediated calcium signaling has been identified as an underlying cause of severe combined immunodeficiency (SCID), leading to drastically weakened immunity against infections. Gain-of-function mutations in Orai and STIM have been associated with tubular aggregated myopathy (TAM), a skeletal muscle disease. While a number of small molecules have shown activity in inhibiting the CRAC signaling pathway, the usefulness of those tool compounds is limited by their off-target activity against TRPM4 and TRPM7 ion channels, high lipophilicity, and a lack of understanding of their mechanism of action. We report structure-activity relationship (SAR) studies that resulted in the characterization of compound 4k [1-(cyclopropylmethyl)-N-(3-fluoropyridin-4-yl)-1H-indazole-3-carboxamie] as a fast onset, reversible, and selective CRAC channel blocker. 4k fully blocked the CRAC current (IC50: 4.9 μM) and the nuclear translocation of NFAT at 30 and 10 μM, respectively, without affecting the electrophysiological function of TRPM4 and TRPM7 channels. Computational modeling appears to support its direction binding to Orai proteins that form the transmembrane CRACchannel.

Keywords: Autoimmune diseases; Calcium release activated calcium (CRAC) channel; Nuclear factor of activated T cells (NFAT); Orai blockers; Store-operated calcium entry (SOCE); Transient receptor potential melastatin 4 and 7 (TRPM4 and TRPM7) channels.

MeSH terms

  • Calcium Channel Blockers* / chemical synthesis
  • Calcium Channel Blockers* / chemistry
  • Calcium Channel Blockers* / pharmacology
  • Calcium Release Activated Calcium Channels / antagonists & inhibitors
  • Calcium Release Activated Calcium Channels / metabolism
  • Dose-Response Relationship, Drug
  • Drug Discovery
  • Humans
  • Indazoles* / chemical synthesis
  • Indazoles* / chemistry
  • Indazoles* / pharmacology
  • Molecular Structure
  • ORAI1 Protein / antagonists & inhibitors
  • ORAI1 Protein / metabolism
  • Pyrazoles* / chemical synthesis
  • Pyrazoles* / chemistry
  • Pyrazoles* / pharmacology
  • Structure-Activity Relationship

Substances

  • Calcium Channel Blockers
  • Indazoles
  • Pyrazoles
  • Calcium Release Activated Calcium Channels
  • ORAI1 Protein