Coupling cellular drug-target engagement to downstream pharmacology with CeTEAM

Nat Commun. 2024 Dec 6;15(1):10347. doi: 10.1038/s41467-024-54415-7.

Abstract

Cellular target engagement technologies enable quantification of intracellular drug binding; however, simultaneous assessment of drug-associated phenotypes has proven challenging. Here, we present cellular target engagement by accumulation of mutant as a platform that can concomitantly evaluate drug-target interactions and phenotypic responses using conditionally stabilized drug biosensors. We observe that drug-responsive proteotypes are prevalent among reported mutants of known drug targets. Compatible mutants appear to follow structural and biophysical logic that permits intra-protein and paralogous expansion of the biosensor pool. We then apply our method to uncouple target engagement from divergent cellular activities of MutT homolog 1 (MTH1) inhibitors, dissect Nudix hydrolase 15 (NUDT15)-associated thiopurine metabolism with the R139C pharmacogenetic variant, and profile the dynamics of poly(ADP-ribose) polymerase 1/2 (PARP1/2) binding and DNA trapping by PARP inhibitors (PARPi). Further, PARP1-derived biosensors facilitated high-throughput screening for PARP1 binders, as well as multimodal ex vivo analysis and non-invasive tracking of PARPi binding in live animals. This approach can facilitate holistic assessment of drug-target engagement by bridging drug binding events and their biological consequences.

MeSH terms

  • Animals
  • Biosensing Techniques / methods
  • DNA Repair Enzymes / genetics
  • DNA Repair Enzymes / metabolism
  • HEK293 Cells
  • High-Throughput Screening Assays / methods
  • Humans
  • Mice
  • Mutation
  • Poly (ADP-Ribose) Polymerase-1* / antagonists & inhibitors
  • Poly (ADP-Ribose) Polymerase-1* / genetics
  • Poly (ADP-Ribose) Polymerase-1* / metabolism
  • Poly(ADP-ribose) Polymerase Inhibitors* / pharmacology
  • Protein Binding
  • Pyrophosphatases / genetics
  • Pyrophosphatases / metabolism

Substances

  • Poly(ADP-ribose) Polymerase Inhibitors
  • Poly (ADP-Ribose) Polymerase-1
  • Pyrophosphatases
  • DNA Repair Enzymes
  • PARP1 protein, human