DMXAA causes tumor site-specific vascular disruption in murine non-small cell lung cancer, and like the endogenous non-canonical cyclic dinucleotide STING agonist, 2'3'-cGAMP, induces M2 macrophage repolarization

PLoS One. 2014 Jun 18;9(6):e99988. doi: 10.1371/journal.pone.0099988. eCollection 2014.

Abstract

The vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid (DMXAA), a murine agonist of the stimulator of interferon genes (STING), appears to target the tumor vasculature primarily as a result of stimulating pro-inflammatory cytokine production from tumor-associated macrophages (TAMs). Since there were relatively few reports of DMXAA effects in genetically-engineered mutant mice (GEMM), and models of non-small cell lung cancer (NSCLC) in particular, we examined both the effectiveness and macrophage dependence of DMXAA in various NSCLC models. The DMXAA responses of primary adenocarcinomas in K-rasLA1/+ transgenic mice, as well as syngeneic subcutaneous and metastatic tumors, generated by a p53R172HΔg/+; K-rasLA1/+ NSCLC line (344SQ-ELuc), were assessed both by in vivo bioluminescence imaging as well as by histopathology. Macrophage-dependence of DMXAA effects was explored by clodronate liposome-mediated TAM depletion. Furthermore, a comparison of the vascular structure between subcutaneous tumors and metastases was carried out using micro-computed tomography (micro-CT). Interestingly, in contrast to the characteristic hemorrhagic necrosis produced by DMXAA in 344SQ-ELuc subcutaneous tumors, this agent failed to cause hemorrhagic necrosis of either 344SQ-ELuc-derived metastases or autochthonous K-rasLA1/+ NSCLCs. In addition, we found that clodronate liposome-mediated depletion of TAMs in 344SQ-ELuc subcutaneous tumors led to non-hemorrhagic necrosis due to tumor feeding-vessel occlusion. Since NSCLC were comprised exclusively of TAMs with anti-inflammatory M2-like phenotype, the ability of DMXAA to re-educate M2-polarized macrophages was examined. Using various macrophage phenotypic markers, we found that the STING agonists, DMXAA and the non-canonical endogenous cyclic dinucleotide, 2'3'-cGAMP, were both capable of re-educating M2 cells towards an M1 phenotype. Our findings demonstrate that the choice of preclinical model and the anatomical site of a tumor can determine the vascular disrupting effectiveness of DMXAA, and they also support the idea of STING agonists having therapeutic utility as TAM repolarizing agents.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / blood supply
  • Adenocarcinoma / drug therapy
  • Animals
  • Carcinoma, Non-Small-Cell Lung / blood supply*
  • Carcinoma, Non-Small-Cell Lung / drug therapy*
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Membrane Permeability / drug effects
  • Cell Polarity / drug effects*
  • Clodronic Acid / pharmacology
  • Clodronic Acid / therapeutic use
  • Humans
  • Inflammation / pathology
  • Liposomes / chemistry
  • Lung Neoplasms / blood supply
  • Lung Neoplasms / drug therapy
  • Macrophages / drug effects
  • Macrophages / pathology*
  • Male
  • Membrane Proteins / agonists*
  • Mice, Transgenic
  • Necrosis
  • Neovascularization, Pathologic / drug therapy*
  • Neovascularization, Pathologic / pathology
  • Nucleotides, Cyclic / pharmacology
  • Nucleotides, Cyclic / therapeutic use*
  • Phenotype
  • Subcutaneous Tissue / drug effects
  • Tumor Suppressor Protein p53 / metabolism
  • Xanthones / pharmacology
  • Xanthones / therapeutic use*
  • Xenograft Model Antitumor Assays
  • ras Proteins / metabolism

Substances

  • Liposomes
  • Membrane Proteins
  • Nucleotides, Cyclic
  • Sting1 protein, mouse
  • Tumor Suppressor Protein p53
  • Xanthones
  • cyclic guanosine monophosphate-adenosine monophosphate
  • Clodronic Acid
  • vadimezan
  • ras Proteins