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Hyperactive gp130/STAT3-driven gastric tumourigenesis promotes submucosal tertiary lymphoid structure development.

David G Hill1, Liang Yu2,3, Hugh Gao2,3

  • 1Division of Infection and Immunity, Systems Immunity Research Institute, School of Medicine, Cardiff University, Cardiff, Wales, United Kingdom.

International Journal of Cancer
|February 9, 2018
PubMed
Summary

Tertiary lymphoid structures (TLSs) form in gastric cancer, driven by gp130-STAT3 signaling. This process, linked to tumor development, was observed in mice and human gastric cancer patients.

Keywords:
STAT3ectopic lymphoid structuresgastric cancerinterleukin-17tertiary lymphoid structures

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Area of Science:

  • Immunology
  • Oncology
  • Gastroenterology

Background:

  • Tertiary lymphoid structures (TLSs) resemble secondary lymphoid organs and are found in chronic inflammation and some cancers, often correlating with better patient outcomes.
  • The mechanisms driving tumor-associated TLS development are not fully understood.
  • Hyperactive signal transducer and activator of transcription 3 (STAT3) signaling via the gp130 receptor is implicated in gastric cancer development.

Purpose of the Study:

  • To investigate the mechanisms governing the development of tumor-associated TLSs in gastric cancer.
  • To determine the role of gp130-STAT3 signaling in TLS formation during gastric tumorigenesis.
  • To compare TLS development in preclinical models with human gastric cancer.

Main Methods:

  • Utilized a preclinical gp130F/F mouse model of gastric cancer.
  • Analyzed submucosal lymphoid aggregates, chemokine expression (Cxcl13, Ccl19, Ccl21), and STAT3 signaling in tumor tissues.
  • Examined TLS presence and gene expression signatures in human intestinal-type gastric cancer samples.
  • Investigated TLS formation in a Helicobacter felis-induced chronic gastritis model.

Main Results:

  • Tumor-associated TLSs, characterized by B and T cells, CD21+ networks, and high endothelial venules, developed in gp130F/F mice during gastric tumorigenesis.
  • TLS formation correlated with gastric adenoma development and the induction of homeostatic chemokines.
  • STAT3 signaling was essential for TLS development in this model, independent of IL-17.
  • TLSs and upregulated chemokine expression were also observed in a chronic gastritis model.
  • TLSs were present in human gastric cancer, and a TLS gene signature associated with advanced disease but not patient survival.

Conclusions:

  • Hyperactive gp130-STAT3 signaling is closely linked to gastric tumor development and lymphoid neogenesis (TLS formation).
  • While TLSs are present in advanced human gastric cancer, their development signature does not predict a favorable prognosis in this context.
  • STAT3-driven lymphoid neogenesis is a key feature of gp130-mediated gastric tumorigenesis.