A novel liver zonation phenotype-associated molecular classification of hepatocellular carcinoma

Front Immunol. 2023 Mar 2:14:1140201. doi: 10.3389/fimmu.2023.1140201. eCollection 2023.

Abstract

Background: Liver zonation is a unique phenomenon in which the liver exhibits distinct functions among hepatocytes along the radial axis of the lobule. This phenomenon can cause the sectionalized initiation of several liver diseases, including hepatocellular carcinoma (HCC). However, few studies have explored the zonation features of HCC.

Methods: Four single-cell RNA sequencing datasets were used to identify hepatocyte-specific zonation markers. Integrative analysis was then performed with a training RNA-seq cohort (616 HCC samples) and an external validating microarray cohort (285 HCC samples) from the International Cancer Genome Consortium, The Cancer Genome Atlas, Gene Expression Omnibus, and EMBL's European Bioinformatics Institute for clustering using non-negative matrix factorization consensus clustering based on zonation genes. Afterward, we evaluated the prognostic value, clinical characteristics, transcriptome and mutation features, immune infiltration, and immunotherapy response of the HCC subclasses.

Results: A total of 94 human hepatocyte-specific zonation markers (39 central markers and 55 portal markers) were identified for the first time. Subsequently, three subgroups of HCC, namely Cluster1, Cluster2, and Cluster3 were identified. Cluster1 exhibited a non-zonational-like signature with the worst prognosis. Cluster2 was intensively associated with a central-like signature and exhibited low immune infiltration and sensitivity toward immune blockade therapy. Cluster3 was intensively correlated with a portal-like signature with the best prognosis. Finally, we identified candidate therapeutic targets and agents for Cluster1 HCC samples.

Conclusion: The current study established a novel HCC classification based on liver zonation signature. By classifying HCC into three clusters with non-zonational-like (Cluster1), central-like (Cluster2), and portal-like (Cluster3) features, this study provided new perspectives on the heterogeneity of HCC and shed new light on delivering precision medicine for HCC patients.

Keywords: classification; drug sensitivity; hepatocellular carcinoma; immunotherapy; liver zonation; precision medicine; prognosis; single-cell sequencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms
  • Animals
  • Biomarkers*
  • Carcinoma, Hepatocellular* / classification
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / immunology
  • Carcinoma, Hepatocellular* / therapy
  • Cohort Studies
  • Datasets as Topic
  • Hepatocytes / immunology
  • Hepatocytes / metabolism
  • Hepatocytes / pathology
  • Humans
  • Immunotherapy
  • Liver Neoplasms* / classification
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / immunology
  • Liver Neoplasms* / therapy
  • Liver* / immunology
  • Liver* / metabolism
  • Liver* / pathology
  • Mice
  • Molecular Targeted Therapy
  • Mutation
  • Phenotype*
  • Precision Medicine
  • Prognosis
  • Reproducibility of Results
  • Sequence Analysis, RNA
  • Single-Cell Gene Expression Analysis
  • Transcriptome

Substances

  • Biomarkers

Grants and funding

This work was supported by the National Natural Science Foundation of China (NO. 82200972 to TZ, NO. 82070647 to JW, and 82071251 to XC).