Two-step enhanced cancer immunotherapy with engineered Salmonella typhimurium secreting heterologous flagellin

Sci Transl Med. 2017 Feb 8;9(376):eaak9537. doi: 10.1126/scitranslmed.aak9537.

Abstract

We report a method of cancer immunotherapy using an attenuated Salmonella typhimurium strain engineered to secrete Vibrio vulnificus flagellin B (FlaB) in tumor tissues. Engineered FlaB-secreting bacteria effectively suppressed tumor growth and metastasis in mouse models and prolonged survival. By using Toll-like receptor 5 (TLR5)-negative colon cancer cell lines, we provided evidence that the FlaB-mediated tumor suppression upon bacterial colonization is associated with TLR5-mediated host reactions in the tumor microenvironment. These therapeutic effects were completely abrogated in TLR4 and MyD88 knockout mice, and partly in TLR5 knockout mice, indicating that TLR4 signaling is a requisite for tumor suppression mediated by FlaB-secreting bacteria, whereas TLR5 signaling augmented tumor-suppressive host reactions. Tumor microenvironment colonization by engineered Salmonella appeared to induce the infiltration of abundant immune cells such as monocytes/macrophages and neutrophils via TLR4 signaling. Subsequent secretion of FlaB from colonizing Salmonella resulted in phenotypic and functional activation of intratumoral macrophages with M1 phenotypes and a reciprocal reduction in M2-like suppressive activities. Together, these findings provide evidence that nonvirulent tumor-targeting bacteria releasing multiple TLR ligands can be used as cancer immunotherapeutics.

MeSH terms

  • Animals
  • Cell Polarity
  • Colonic Neoplasms / pathology
  • Colony Count, Microbial
  • Flagellin / metabolism*
  • Genetic Engineering*
  • HCT116 Cells
  • Humans
  • Immunotherapy*
  • Macrophages / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Nude
  • Neoplasm Metastasis
  • Neoplasms / immunology*
  • Neoplasms / pathology
  • Neoplasms / therapy*
  • Phenotype
  • Salmonella typhimurium / physiology*
  • Signal Transduction
  • Toll-Like Receptor 5 / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Toll-Like Receptor 5
  • Flagellin
  • flaB flagellin