Identification of a Covalent Molecular Inhibitor of Anti-apoptotic BFL-1 by Disulfide Tethering

Cell Chem Biol. 2020 Jun 18;27(6):647-656.e6. doi: 10.1016/j.chembiol.2020.04.004. Epub 2020 May 14.

Abstract

The BCL-2 family is composed of anti- and pro-apoptotic members that respectively protect or disrupt mitochondrial integrity. Anti-apoptotic overexpression can promote oncogenesis by trapping the BCL-2 homology 3 (BH3) "killer domains" of pro-apoptotic proteins in a surface groove, blocking apoptosis. Groove inhibitors, such as the relatively large BCL-2 drug venetoclax (868 Da), have emerged as cancer therapies. BFL-1 remains an undrugged oncogenic protein and can cause venetoclax resistance. Having identified a unique C55 residue in the BFL-1 groove, we performed a disulfide tethering screen to determine if C55 reactivity could enable smaller molecules to block BFL-1's BH3-binding functionality. We found that a disulfide-bearing N-acetyltryptophan analog (304 Da adduct) effectively targeted BFL-1 C55 and reversed BFL-1-mediated suppression of mitochondrial apoptosis. Structural analyses implicated the conserved leucine-binding pocket of BFL-1 as the interaction site, resulting in conformational remodeling. Thus, therapeutic targeting of BFL-1 may be achievable through the design of small, cysteine-reactive drugs.

Keywords: BCL-2 family; BFL-1/A1; BH3; anti-apoptotic; apoptosis; cancer; covalent inhibitor; disulfide tethering; mitochondria; small molecule.

Publication types

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

MeSH terms

  • Apoptosis / drug effects*
  • Disulfides / chemistry
  • Disulfides / pharmacology*
  • Dose-Response Relationship, Drug
  • Humans
  • Minor Histocompatibility Antigens / metabolism
  • Models, Molecular
  • Molecular Structure
  • Peptides / chemical synthesis
  • Peptides / chemistry
  • Peptides / pharmacology*
  • Proto-Oncogene Proteins c-bcl-2 / antagonists & inhibitors*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Structure-Activity Relationship
  • Tryptophan / analogs & derivatives
  • Tryptophan / chemistry
  • Tryptophan / pharmacology

Substances

  • BCL2-related protein A1
  • Disulfides
  • Minor Histocompatibility Antigens
  • Peptides
  • Proto-Oncogene Proteins c-bcl-2
  • N-acetyltryptophan
  • Tryptophan