Mechanical force regulates ligand binding and function of PD-1

Nat Commun. 2024 Sep 27;15(1):8339. doi: 10.1038/s41467-024-52565-2.

Abstract

Despite the success of PD-1 blockade in cancer therapy, how PD-1 initiates signaling remains unclear. Soluble PD-L1 is found in patient sera and can bind PD-1 but fails to suppress T cell function. Here, we show that PD-1 function is reduced when mechanical support on ligand is removed. Mechanistically, cells exert forces to PD-1 and prolong bond lifetime at forces <7 pN (catch bond) while accelerate dissociation at forces >8pN (slip bond). Molecular dynamics of PD-1-PD-L2 complex suggests force may cause relative rotation and translation between the two molecules yielding distinct atomic contacts not observed in the crystal structure. Compared to wild-type, PD-1 mutants targeting the force-induced distinct interactions maintain the same binding affinity but suppressed/eliminated catch bond, lowered rupture force, and reduced inhibitory function. Our results uncover a mechanism for cells to probe the mechanical support of PD-1-PD-Ligand bonds using endogenous forces to regulate PD-1 signaling.

MeSH terms

  • Animals
  • B7-H1 Antigen* / chemistry
  • B7-H1 Antigen* / metabolism
  • HEK293 Cells
  • Humans
  • Ligands
  • Molecular Dynamics Simulation*
  • Mutation
  • Programmed Cell Death 1 Ligand 2 Protein* / chemistry
  • Programmed Cell Death 1 Ligand 2 Protein* / genetics
  • Programmed Cell Death 1 Ligand 2 Protein* / metabolism
  • Programmed Cell Death 1 Receptor* / chemistry
  • Programmed Cell Death 1 Receptor* / genetics
  • Programmed Cell Death 1 Receptor* / metabolism
  • Protein Binding*
  • Signal Transduction
  • T-Lymphocytes / metabolism

Substances

  • Programmed Cell Death 1 Receptor
  • Ligands
  • B7-H1 Antigen
  • Programmed Cell Death 1 Ligand 2 Protein
  • PDCD1 protein, human
  • PDCD1LG2 protein, human
  • CD274 protein, human