Intratumoral microbiome promotes liver metastasis and dampens adjuvant imatinib treatment in gastrointestinal stromal tumor

Cancer Lett. 2024 Oct 1:601:217149. doi: 10.1016/j.canlet.2024.217149. Epub 2024 Aug 8.

Abstract

Understanding the determinants of long-term liver metastasis (LM) outcomes in gastrointestinal stromal tumor (GIST) patients is crucial. We established the feature selection model of intratumoral microbiome at the surgery, achieving robust predictive accuracies of 0.953 and 0.897 AUCs in discovery (n = 74) and validation (n = 34) cohorts, respectively. Notably, despite the significant reduction in LM occurrence with adjuvant imatinib (AI) treatment, intratumoral microbiome exerted independently stronger effects on post-operative LM. Employing both 16S and full-length rRNA sequencing, we pinpoint intracellular Shewanella algae as a foremost LM risk factor in both AI- and non-AI-treated patients. Experimental validation confirmed S. algae's intratumoral presence in GIST, along with migration/invasion-promoting effects on GIST cells. Furthermore, S. algae promoted LM and impeded AI treatment in metastatic mouse models. Our findings advocate for incorporating intratumoral microbiome evaluation at surgery, and propose S. algae as a therapeutic target for LM suppression in GIST.

Keywords: Gastrointestinal stromal tumor; Imatinib; Intratumoral microbiome; Liver metastasis; Machine learning algorithm.

MeSH terms

  • Aged
  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • Cell Line, Tumor
  • Chemotherapy, Adjuvant / methods
  • Female
  • Gastrointestinal Neoplasms* / drug therapy
  • Gastrointestinal Neoplasms* / microbiology
  • Gastrointestinal Neoplasms* / pathology
  • Gastrointestinal Stromal Tumors* / drug therapy
  • Gastrointestinal Stromal Tumors* / microbiology
  • Gastrointestinal Stromal Tumors* / pathology
  • Humans
  • Imatinib Mesylate* / pharmacology
  • Imatinib Mesylate* / therapeutic use
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / microbiology
  • Liver Neoplasms* / secondary
  • Male
  • Mice
  • Microbiota / drug effects
  • Middle Aged

Substances

  • Imatinib Mesylate
  • Antineoplastic Agents