Multi-omics-driven discovery of invasive patterns and treatment strategies in CA19-9 positive intrahepatic cholangiocarcinoma

J Transl Med. 2024 Nov 15;22(1):1031. doi: 10.1186/s12967-024-05854-9.

Abstract

Background: Intrahepatic cholangiocarcinoma (ICC) is a malignant tumor with a poor prognosis, predominantly CA19-9 positive. High CA19-9 levels correlate with increased aggressiveness and worse outcomes. This study employs multi-omics analysis to reveal molecular features and identify therapeutic targets of CA19-9 positive ICC, aiming to support individualized treatment.

Methods: Data from seven clinical cohorts, two whole-exome sequencing cohorts, six RNA sequencing/microarray cohorts, one proteomic cohort, 20 single-cell RNA sequencing samples, and one spatial transcriptome sample were analyzed. Key findings were validated on tissue microarrays from 52 ICC samples.

Results: CA19-9 positive ICC exhibited poorer OS (median 24.1 v.s. 51.5 months) and RFS (median 11.7 v.s. 28.2 months) compared to negative group (all P < 0.05). Genomic analysis revealed a higher KRAS mutation frequency in the positive group and a greater prevalence of IDH1/2 mutations in the negative group (all P < 0.05). Transcriptomic analysis indicated upregulated glycolysis pathways in CA19-9 positive ICC. Single-cell analysis identified specific glycolysis-related cell subclusters associated with poor prognosis, including Epi_SLC2A1, CAF_VEGFA, and Mph_SPP1. Higher hypoxia in the CA19-9 positive group led to metabolic reprogramming and promoted these cells' formation. These cells formed interactive communities promoting epithelial-mesenchymal transition (EMT) and angiogenesis. Drug sensitivity analysis identified six potential therapeutic drugs.

Conclusions: This study systematically elucidated the clinical, genomic, transcriptomic, and immune features of CA19-9 positive ICC. It reveals glycolysis-associated cellular communities and their cancer-promoting mechanisms, enhancing our understanding of ICC and laying the groundwork for individualized therapeutic strategies.

Keywords: CA19-9; Glycolysis; Hypoxia; Intrahepatic cholangiocarcinoma; Multi-omics.

MeSH terms

  • Aged
  • Bile Duct Neoplasms / blood
  • Bile Duct Neoplasms / genetics
  • Bile Duct Neoplasms / pathology
  • CA-19-9 Antigen / blood
  • Cholangiocarcinoma* / blood
  • Cholangiocarcinoma* / genetics
  • Cholangiocarcinoma* / pathology
  • Cohort Studies
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Genomics
  • Humans
  • Male
  • Middle Aged
  • Multiomics
  • Mutation / genetics
  • Neoplasm Invasiveness
  • Prognosis
  • Proteomics
  • Transcriptome / genetics

Substances

  • CA-19-9 Antigen