NLRP6 deficiency enhances macrophage-mediated phagocytosis via E-Syt1 to inhibit hepatocellular carcinoma progression

Gut. 2025 Oct 8;74(11):1883-1895. doi: 10.1136/gutjnl-2024-334448.

Abstract

Background: Current treatments with tyrosine kinase inhibitors and immune checkpoint inhibitors have limited efficacy for hepatocellular carcinoma (HCC) due to drug resistance. Emerging therapies such as chimeric antigen receptor T (CAR-T) and macrophage-based cell therapies are promising but need to be improved.

Objectives: This study investigates the role of macrophage NOD-like receptor family pyrin domain containing 6 (NLRP6) in HCC progression and its therapeutic potential.

Design: Immunofluorescence staining was performed in patient samples. Liver tumour models (autonomous, orthotopic, subcutaneous) were developed, and RNA sequencing, flow cytometry and immunohistochemistry were performed in wild-type, Nlrp6 -/- mice, and cell-specific Nlrp6 knockout mice. Phagocytosis was assessed using particles or tumour cells. Multiomics, immunoprecipitation mass spectrometry, western blot and co-immunoprecipitation were performed to examine the interaction between NLRP6's PYD domain and E-Syt1's SMP domain.

Results: CD68 (a macrophage marker) and NLRP6 expression were detected in patient HCC tissues, and patients with lower macrophage NLRP6 expression had longer survival. Compared with their wild-type mice, Nlrp6 -/- mice and macrophage cell-specific Nlrp6 knockout mice showed delayed tumour growth. Adoptive transfer of Nlrp6 -/- macrophages reduced tumour growth in vivo. Macrophages from Nlrp6 -/- mice were more abundant and exhibited enhanced phagocytosis compared with those from wild-type mice. Co-immunoprecipitation and phagocytosis experiments revealed E-Syt1 promoted phagocytosis, which was negatively regulated by NLRP6 through interaction with its PYD domain.

Conclusions: NLRP6 promotes HCC progression by inhibiting macrophage infiltration and suppressing phagocytosis via the interaction between its PYD domain and E-Syt1's SMP domain. Transfer of Nlrp6 -/- macrophages is a promising therapeutic strategy for reducing HCC tumour growth.

Keywords: CANCER; HEPATOCELLULAR CARCINOMA; LIVER IMMUNOLOGY; MACROPHAGES.

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular* / genetics
  • Carcinoma, Hepatocellular* / immunology
  • Carcinoma, Hepatocellular* / metabolism
  • Carcinoma, Hepatocellular* / pathology
  • Disease Progression
  • Humans
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / immunology
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Macrophages* / metabolism
  • Mice
  • Mice, Knockout
  • Phagocytosis*
  • Receptors, Cell Surface

Substances

  • Nod-like receptor pyrin domain-containing protein 6, mouse
  • Receptors, Cell Surface