Macrophage Elastase Induces TRAIL-mediated Tumor Cell Death through Its Carboxy-Terminal Domain

Am J Respir Crit Care Med. 2017 Aug 1;196(3):353-363. doi: 10.1164/rccm.201606-1150OC.

Abstract

Rationale: Macrophage elastase (matrix metalloproteinase [MMP]-12) is a potent protease that contributes to the lung destruction that accompanies cigarette smoking; it simultaneously inhibits lung tumor angiogenesis and metastasis by catalyzing the formation of antiangiogenic peptides. Recent studies have revealed novel nonproteolytic functions of MMP12, including antimicrobial activity through a peptide within its C-terminal domain (CTD).

Objectives: To determine whether the MMP12 CTD contributes to its antitumor activity in lung cancer.

Methods: We used recombinant MMP12 peptide fragments, including its catalytic domain, CTD, and a 20 amino acid peptide within the CTD (SR20), in an in vitro system to delineate their effects on non-small cell lung cancer cell proliferation and apoptosis. We translated our findings to two murine models of lung cancer, including orthotopic human xenograft and KrasLSL/G12D mouse models of lung cancer.

Measurements and main results: We show that SR20 triggers tumor apoptosis by up-regulation of gene expression of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and its receptor, death receptor 4, sensitizing cells to an autocrine loop of TRAIL-mediated cell death. We then demonstrate the therapeutic efficacy of SR20 against two murine models of lung cancer.

Conclusions: The MMP12 CTD initiates TRAIL-mediated tumor cell death through its conserved SR20 peptide.

Keywords: apoptosis; lung cancer; matrix metalloproteinase-12; proteases; tumor necrosis factor–related apoptosis-inducing ligand.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Carcinoma, Non-Small-Cell Lung / metabolism*
  • Cell Death
  • Cell Line, Tumor
  • Cell Proliferation
  • Disease Models, Animal
  • Humans
  • Lung Neoplasms / metabolism*
  • Matrix Metalloproteinase 12 / metabolism*
  • Mice
  • Receptors, TNF-Related Apoptosis-Inducing Ligand / metabolism*
  • TNF-Related Apoptosis-Inducing Ligand / metabolism*
  • Up-Regulation

Substances

  • Receptors, TNF-Related Apoptosis-Inducing Ligand
  • TNF-Related Apoptosis-Inducing Ligand
  • Matrix Metalloproteinase 12