Lactate accumulation drives hepatocellular carcinoma metastasis through facilitating tumor-derived exosome biogenesis by Rab7A lactylation

Cancer Lett. 2025 Sep 1:627:217636. doi: 10.1016/j.canlet.2025.217636. Epub 2025 Mar 21.

Abstract

Previous studies have demonstrated that lactate accumulation, a common hallmark for metabolic deprivation in solid tumors, could actively drive tumor invasion and metastasis. However, whether lactate influences the biogenesis of tumor-derived exosomes (TDEs), the prerequisite for distant metastasis formation, remains unknown. Here, we demonstrated that extracellular lactate, after taken up by tumor cells via lactate transporter MCT1, drove the release of TDE mainly through facilitating multivesicular body (MVB) trafficking towards plasma membrane instead of lysosome. Mechanistically, lactate promoted p300-mediated Rab7A lactylation, which hereafter inhibited its GTPase activity and promoted MVB docking with plasma membrane. Moreover, lactate administration enriched integrin β4 and ECM remodeling-related proteins in TDE cargos, which promoted pulmonary pre-metastatic niche formation. Combinatorial inhibition of MCT1 and p300 significantly abrogated HCC metastasis in a clinical-relevant PDX model. In summary, we demonstrated that lactate promote TDE biogenesis and HCC pulmonary metastasis, and proposed a potential clinical strategy targeting TDEs to prevent HCC metastasis.

Keywords: Extracellular vesicle; HCC; Lactylation; Metastasis; Small GTPases.

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Carcinoma, Hepatocellular* / secondary
  • Cell Line, Tumor
  • E1A-Associated p300 Protein / metabolism
  • Exosomes* / metabolism
  • Exosomes* / pathology
  • Humans
  • Lactic Acid* / metabolism
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Lung Neoplasms* / metabolism
  • Lung Neoplasms* / secondary
  • Male
  • Mice
  • Mice, Nude
  • Monocarboxylic Acid Transporters / metabolism
  • Neoplasm Metastasis
  • Symporters / metabolism
  • rab GTP-Binding Proteins* / genetics
  • rab GTP-Binding Proteins* / metabolism
  • rab7 GTP-Binding Proteins

Substances

  • rab GTP-Binding Proteins
  • Lactic Acid
  • Monocarboxylic Acid Transporters
  • rab7 GTP-Binding Proteins
  • monocarboxylate transport protein 1
  • E1A-Associated p300 Protein
  • EP300 protein, human
  • Symporters