Dysbiosis of Gut Microbiota Promotes Hepatocellular Carcinoma Progression by Regulating the Immune Response

J Immunol Res. 2021 Oct 20:2021:4973589. doi: 10.1155/2021/4973589. eCollection 2021.

Abstract

Method: This study included 74 Chinese male patients with HCC. They were divided into early (n = 19), intermediate (n = 37), and terminal (n = 18) groups, referred to as Barcelona Clinic Liver Cancer stage 0+A, B, and C+D, respectively. Paired fecal and plasma samples were collected. Microbial composition and profiles were analyzed by 16S rRNA gene sequencing. The levels of gut damage marker (regenerating islet-derived protein 3α (REG3α)) and microbial translocation markers (soluble CD14 (sCD14), lipopolysaccharide-binding protein (LBP), peptidoglycan recognition proteins (PGRPs)) were determined in plasma samples of patients by ELISA. Twenty plasma cytokine and chemokines were determined by Luminex.

Results: In early, intermediate, and terminal groups, the abundance of the Bifidobacteriaceae family decreased significantly (3.52%, 1.55%, and 0.56%, respectively, P = 0.003), while the abundance of the Enterococcaceae family increased significantly (1.6%, 2.9%, and 13.4%, respectively, P = 0.022). Levels of REG3α and sCD14 were markedly elevated only in the terminal group compared with the early (P = 0.025 and P = 0.048) and intermediate groups (P = 0.023 and P = 0.046). The level of LBP significantly increased in the intermediate (P = 0.035) and terminal (P = 0.025) groups compared with the early group. The PGRP levels were elevated only in the terminal group compared with the early group (P = 0.018). The ratio of Enterococcaceae to Bifidobacteriaceae was significantly associated with the levels of REG3α, LBP, sCD14, and PGRPs. With HCC progression, increased levels of inflammatory cytokines accompanied by a T cell-immunosuppressive response and microbial translocation were observed.

Conclusion: Gut microbiota compositional and functional shift, together with elevated gut damage and microbial translocation, may promote HCC development by stimulating inflammatory response and suppressing T cell response.

Publication types

  • Observational Study

MeSH terms

  • Actinobacteria / genetics
  • Actinobacteria / immunology
  • Actinobacteria / isolation & purification
  • Aged
  • Bacterial Translocation / immunology*
  • Carcinoma, Hepatocellular / diagnosis
  • Carcinoma, Hepatocellular / immunology*
  • Carcinoma, Hepatocellular / microbiology
  • Carcinoma, Hepatocellular / pathology
  • DNA, Bacterial / isolation & purification
  • Disease Progression
  • Dysbiosis / complications*
  • Dysbiosis / diagnosis
  • Dysbiosis / immunology
  • Dysbiosis / microbiology
  • Enterococcaceae / genetics
  • Enterococcaceae / immunology
  • Enterococcaceae / isolation & purification
  • Feces / microbiology
  • Gastrointestinal Microbiome / genetics
  • Gastrointestinal Microbiome / immunology*
  • Humans
  • Liver Neoplasms / diagnosis
  • Liver Neoplasms / immunology*
  • Liver Neoplasms / microbiology
  • Liver Neoplasms / pathology
  • Male
  • Middle Aged
  • RNA, Ribosomal, 16S

Substances

  • DNA, Bacterial
  • RNA, Ribosomal, 16S