Trojan-Horse Strategy Targeting the Gut-Liver Axis Modulates Gut Microbiome and Reshapes Microenvironment for Orthotopic Hepatocellular Carcinoma Therapy

Adv Sci (Weinh). 2024 Nov;11(44):e2310002. doi: 10.1002/advs.202310002. Epub 2024 Oct 7.

Abstract

Reversing the hepatic inflammatory and immunosuppressive microenvironment caused by gut microbiota-derived lipopolysaccharides (LPS), accumulating to the liver through the gut-liver axis, is crucial for suppressing hepatocellular carcinoma (HCC) and metastasis. However, synergistically manipulating LPS-induced inflammation and gut microbiota remains a daunting task. Herein, a Trojan-horse strategy is proposed using an oral dextran-carbenoxolone (DEX-CBX) conjugate, which combines prebiotic and glycyrrhetinic acid (GA) homologs, to targeted delivery GA to HCC through the gut-liver axis for simultaneous modulation of hepatic inflammation and gut microbiota. In the orthotopic HCC model, a 95-45% reduction in the relative abundances of LPS-associated microbiota is observed, especially Helicobacter, caused by DEX-CBX treatment over phosphate-buffered saline (PBS) treatment. Notably, a dramatic increase (37-fold over PBS) in the abundance of Akkermansia, which is known to strengthen systemic immune response, is detected. Furthermore, DEX-CBX significantly increased natural killer T cells (5.7-fold) and CD8+ T cells (3.9-fold) as well as decreased M2 macrophages (59% reduction) over PBS treatment, resulting in a tumor suppression rate of 85.4%. DEX-CBX is anticipated to offer a novel strategy to precisely modulate hepatic inflammation and the gut microbiota to address both the symptoms and root causes of LPS-induced immunosuppression in HCC.

Keywords: gut microbiota; hepatic inflammation; hepatocellular carcinoma; immunotherapy; oral nanomedicine.

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / drug therapy
  • Carcinoma, Hepatocellular* / immunology
  • Disease Models, Animal*
  • Gastrointestinal Microbiome* / drug effects
  • Lipopolysaccharides / metabolism
  • Liver
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / immunology
  • Mice
  • Tumor Microenvironment* / drug effects
  • Tumor Microenvironment* / immunology

Substances

  • Lipopolysaccharides