Neuropilin-1 mediates neutrophil elastase uptake and cross-presentation in breast cancer cells

J Biol Chem. 2017 Jun 16;292(24):10295-10305. doi: 10.1074/jbc.M116.773051. Epub 2017 May 3.

Abstract

Neutrophil elastase (NE) can be rapidly taken up by tumor cells that lack endogenous NE expression, including breast cancer, which results in cross-presentation of PR1, an NE-derived HLA-A2-restricted peptide that is an immunotherapy target in hematological and solid tumor malignancies. The mechanism of NE uptake, however, remains unknown. Using the mass spectrometry-based approach, we identify neuropilin-1 (NRP1) as a NE receptor that mediates uptake and PR1 cross-presentation in breast cancer cells. We demonstrated that soluble NE is a specific, high-affinity ligand for NRP1 with a calculated Kd of 38.7 nm Furthermore, we showed that NRP1 binds to the RRXR motif in NE. Notably, NRP1 knockdown with interfering RNA or CRISPR-cas9 system and blocking using anti-NRP1 antibody decreased NE uptake and, subsequently, susceptibility to lysis by PR1-specific cytotoxic T cells. Expression of NRP1 in NRP1-deficient cells was sufficient to induce NE uptake. Altogether, because NRP1 is broadly expressed in tumors, our findings suggest a role for this receptor in immunotherapy strategies that target cross-presented antigens.

Keywords: antigen presentation; breast cancer; cross-presentation; immunotherapy; neuropilin-1; neutrophil elastase; receptor internalization; serine protease.

Publication types

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

MeSH terms

  • Absorption, Physiological*
  • Amino Acid Motifs
  • Antibodies, Blocking / metabolism
  • Breast Neoplasms / immunology
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • CRISPR-Cas Systems
  • Cell Line, Tumor
  • Cross-Priming*
  • Female
  • Humans
  • Kinetics
  • Leukocyte Elastase / chemistry
  • Leukocyte Elastase / immunology
  • Leukocyte Elastase / metabolism*
  • Ligands
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / chemistry
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*
  • Neuropilin-1 / antagonists & inhibitors
  • Neuropilin-1 / chemistry
  • Neuropilin-1 / genetics
  • Neuropilin-1 / metabolism*
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Interaction Domains and Motifs
  • RNA Interference
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Solubility
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism

Substances

  • Antibodies, Blocking
  • Ligands
  • Neoplasm Proteins
  • Peptide Fragments
  • Recombinant Proteins
  • Neuropilin-1
  • Leukocyte Elastase

Associated data

  • PDB/3Q76