Manganese is a potent inducer of lysosomal activity that inhibits de novo HBV infection

PLoS Pathog. 2025 Jan 2;21(1):e1012800. doi: 10.1371/journal.ppat.1012800. eCollection 2025 Jan.

Abstract

Sodium taurocholate co-transporting polypeptide (NTCP) has been identified as an entry receptor for hepatitis B virus (HBV), but the molecular events of the viral post-endocytosis steps remain obscure. In this study, we discovered that manganese (Mn) could strongly inhibit HBV infection in NTCP-reconstituted HepG2 cells without affecting viral replication. We therefore profiled the antiviral effects of Mn2+ in an attempt to elucidate the regulatory mechanisms involved in early HBV infection. Intriguingly, Mn2+ conspicuously stimulated lysosomal activity, as evidenced by hyperactivation of mTORC1 and increased endo/lysosomal acidity. After HBV-triggered internalization, the NTCP receptor was sorted to late endosomal compartments by the ESCRT machinery in concert with the invading virion. The establishment of HBV infection was found to be independent of lysosomal fusion-driven late endosome maturation; Mn2+-induced lysosomal hyperfunction virtually impaired infection, suggesting that virions may gain cytosolic access directly from late endosomes. In contrast, suppression of lysosomal activity substantially enhanced HBV infection. Prolonged mTORC1 inactivation facilitated viral infection by depleting lysosomes and accelerating endocytic transport of virions. Notably, treatment with the natural steroidal alkaloid tomatidine recapitulated the effects of Mn2+ in stimulating lysosomal activity and exhibited potent anti-HBV activity in HepG2-NTCP cells and in proliferating human hepatocyte organoids. These findings provide new insights into the post-endocytosis events of HBV infection. The negative regulation of early HBV infection by endo/lysosomal activity makes it a promising target for antiviral therapies.

MeSH terms

  • Antiviral Agents / pharmacology
  • Hep G2 Cells
  • Hepatitis B virus* / drug effects
  • Hepatitis B virus* / physiology
  • Hepatitis B* / drug therapy
  • Hepatitis B* / metabolism
  • Hepatitis B* / virology
  • Humans
  • Lysosomes* / drug effects
  • Lysosomes* / metabolism
  • Manganese* / metabolism
  • Mechanistic Target of Rapamycin Complex 1 / metabolism
  • Organic Anion Transporters, Sodium-Dependent / metabolism
  • Symporters / metabolism
  • Virus Replication / drug effects

Substances

  • Manganese
  • Symporters
  • Mechanistic Target of Rapamycin Complex 1
  • Antiviral Agents
  • sodium-bile acid cotransporter
  • Organic Anion Transporters, Sodium-Dependent

Grants and funding

This work was supported by the Shanghai Municipal Science and Technology Major Project (ZD2021CY001 to QD), the National Natural Science Foundation grants of China (82072279 to QD; 82372233 to QD; 81871647 to QD) and the Innovation Fund for Medical Sciences from Chinese Academy of Medical Sciences (2019-I2M-5-040 to QD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.