Primary tumors induce neutrophil extracellular traps with targetable metastasis promoting effects

JCI Insight. 2019 Jul 25;5(16):e128008. doi: 10.1172/jci.insight.128008.

Abstract

Targeting the dynamic tumor immune microenvironment (TIME) can provide effective therapeutic strategies for cancer. Neutrophils are the predominant leukocyte population in mice and humans, and mounting evidence implicates these cells during tumor growth and metastasis. Neutrophil extracellular traps (NETs) are networks of extracellular neutrophil DNA fibers that are capable of binding tumor cells to support metastatic progression. Here we demonstrate for the first time that circulating NET levels are elevated in advanced esophageal, gastric and lung cancer patients compared to healthy controls. Using pre-clinical murine models of lung and colon cancer in combination with intravital video microscopy, we show that NETs functionally regulate disease progression and that blocking NETosis through multiple strategies significantly inhibits spontaneous metastasis to the lung and liver. Further, we visualize how inhibiting tumor-induced NETs decreases cancer cell adhesion to liver sinusoids following intrasplenic injection - a mechanism previously thought to be driven primarily by exogenous stimuli. Thus, in addition to neutrophil abundance, the functional contribution of NETosis within the TIME has critical translational relevance and represents a promising target to impede metastatic dissemination.

Keywords: Gastric cancer; Lung cancer; Neutrophils; Oncology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • Apoptosis / drug effects
  • Apoptosis / immunology*
  • Cell Adhesion / drug effects
  • Cell Adhesion / immunology
  • Cell Line, Tumor / transplantation
  • Disease Models, Animal
  • Disease Progression
  • Extracellular Traps / drug effects
  • Extracellular Traps / metabolism*
  • Female
  • Humans
  • Intravital Microscopy
  • Male
  • Mice
  • Middle Aged
  • Neoplasm Metastasis / immunology*
  • Neoplasm Metastasis / prevention & control
  • Neoplasms / blood
  • Neoplasms / drug therapy
  • Neoplasms / immunology
  • Neoplasms / pathology*
  • Neutrophils / drug effects
  • Neutrophils / immunology
  • Neutrophils / pathology*
  • Primary Cell Culture
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology
  • Young Adult

Substances

  • Antineoplastic Agents

Grants and funding