Identification of the functional PD-L1 interface region responsible for PD-1 binding and initiation of PD-1 signaling

J Biol Chem. 2023 Dec;299(12):105353. doi: 10.1016/j.jbc.2023.105353. Epub 2023 Oct 17.

Abstract

The PD-1/PD-L1 checkpoint pathway is important for regulating immune responses and can be targeted by immunomodulatory drugs to treat a variety of immune disorders. However, the precise protein-protein interactions required for the initiation of PD-1/PD-L1 signaling are currently unknown. Previously, we designed a series of first-generation PD-1 targeting peptides based on the native interface region of programmed death ligand 1 (PD-L1) that effectively reduced PD-1/PD-L1 binding. In this work, we further characterized the previously identified lead peptide, MN1.1, to identify key PD-1 binding residues and design an optimized peptide, MN1.4. We show MN1.4 is significantly more stable than MN1.1 in serum and retains the ability to block PD-1/PD-L1 complex formation. We further characterized the immunomodulatory effects of MN1.4 treatment by measuring markers of T cell activation in a co-culture model with ovarian cancer cells and peripheral blood mononuclear cells. We found MN1.4 treatment reduced cytokine secretion and suppressed T cell responses in a similar manner as recombinant PD-L1. Therefore, the PD-L1 interface region used to design MN1.4 appeared sufficient to initiate PD-1 signaling and likely represents the minimum necessary region of PD-L1 required for PD-1 recognition. We propose a peptide agonist for PD-1, such as MN1.4, could have several applications for treating autoimmune disorders caused by PD-1 deficiencies such as type 1 diabetes, inflammatory arthritis, or autoimmune side effects arising from monoclonal antibody-based cancer immunotherapies.

Keywords: PD-1 agonist; T cell activation; checkpoint; immunotherapy; inflammation; interfering peptide.

MeSH terms

  • B7-H1 Antigen* / chemistry
  • B7-H1 Antigen* / genetics
  • B7-H1 Antigen* / metabolism
  • Cell Line, Tumor
  • Humans
  • Immunity / drug effects
  • Immunotherapy
  • Leukocytes, Mononuclear / metabolism
  • Models, Molecular*
  • Mutation
  • Neoplasms* / drug therapy
  • Peptides / pharmacology
  • Programmed Cell Death 1 Receptor / agonists
  • Programmed Cell Death 1 Receptor / chemistry
  • Programmed Cell Death 1 Receptor / metabolism
  • Protein Binding
  • Protein Structure, Quaternary
  • Signal Transduction*

Substances

  • B7-H1 Antigen
  • Peptides
  • Programmed Cell Death 1 Receptor