Epigenetic silencing of LDHB promotes hepatocellular carcinoma by remodeling the tumor microenvironment

Cancer Immunol Immunother. 2024 May 13;73(7):127. doi: 10.1007/s00262-024-03717-2.

Abstract

Lactate dehydrogenase B (LDHB) reversibly catalyzes the conversion of pyruvate to lactate or lactate to pyruvate and expressed in various malignancies. However, the role of LDHB in modulating immune responses against hepatocellular carcinoma (HCC) remains largely unknown. Here, we found that down-regulation of lactate dehydrogenase B (LDHB) was coupled with the promoter hypermethylation and knocking down the DNA methyltransferase 3A (DNMT 3A) restored LDHB expression levels in HCC cell lines. Bioinformatics analysis of the HCC cohort from The Cancer Genome Atlas revealed a significant positive correlation between LDHB expression and immune regulatory signaling pathways and immune cell infiltrations. Moreover, immune checkpoint inhibitors (ICIs) have shown considerable promise for HCC treatment and patients with higher LDHB expression responded better to ICIs. Finally, we found that overexpression of LDHB suppressed HCC growth in immunocompetent but not in immunodeficient mice, suggesting that the host immune system was involved in the LDHB-medicated tumor suppression. Our findings indicate that DNMT3A-mediated epigenetic silencing of LDHB may contribute to HCC progression through remodeling the tumor immune microenvironment, and LDHB may become a potential prognostic biomarker and therapeutic target for HCC immunotherapy.

Keywords: DNA methylation; DNMT3A; Hepatocellular carcinoma (HCC); LDHB; Tumor microenvironment.

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / immunology
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Cell Line, Tumor
  • DNA Methylation
  • DNA Methyltransferase 3A* / metabolism
  • Epigenesis, Genetic*
  • Gene Expression Regulation, Neoplastic
  • Gene Silencing
  • Humans
  • Isoenzymes / genetics
  • Isoenzymes / metabolism
  • L-Lactate Dehydrogenase* / genetics
  • L-Lactate Dehydrogenase* / metabolism
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / immunology
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Mice
  • Prognosis
  • Tumor Microenvironment* / immunology

Substances

  • L-Lactate Dehydrogenase
  • DNA Methyltransferase 3A
  • DNMT3A protein, human
  • Isoenzymes
  • lactate dehydrogenase 1