APOBEC3B interaction with PRC2 modulates microenvironment to promote HCC progression

Gut. 2019 Oct;68(10):1846-1857. doi: 10.1136/gutjnl-2018-317601. Epub 2019 Jun 1.

Abstract

Objective: APOBEC3B (A3B), a cytidine deaminase acting as a contributor to the APOBEC mutation pattern in many kinds of tumours, is upregulated in patients with hepatocellular carcinoma (HCC). However, APOBEC mutation patterns are absent in HCC. The mechanism of how A3B affects HCC progression remains elusive.

Design: A3B -promoter luciferase reporter and other techniques were applied to elucidate mechanisms of A3B upregulation in HCC. A3B overexpression and knockdown cell models, immunocompetent and immune-deficient mouse HCC model were conducted to investigate the influence of A3B on HCC progression. RNA-seq, flow cytometry and other techniques were conducted to analyse how A3B modulated the cytokine to enhance the recruitment of myeloid--derived suppressor cells (MDSCs) and tumour--associated macrophages (TAMs).

Results: A3B upregulation through non-classical nuclear factor-κB (NF-κB)signalling promotes HCC growth in immunocompetent mice, associated with an increase of MDSCs, TAMs and programmed cell death1 (PD1) exprssed CD8+ T cells. A CCR2 antagonist suppressed TAMs and MDSCs infiltration and delayed tumour growth in A3B and A3BE68Q/E255Q- expressing mouse tumours. Mechanistically, A3B upregulation in HCC depresses global H3K27me3 abundance via interaction with polycomb repressor complex 2 (PRC2) and reduces an occupancy of H3K27me3 on promoters of the chemokine CCL2 to recruit massive TAMs and MDSCs.

Conclusion: Our observations uncover a deaminase-independent role of the A3B in modulating the HCC microenvironment and demonstrate a proof for the concept of targeting A3B in HCC immunotherapy.

Keywords: cancer immunobiology; chemotaxis; hepatobiliary cancer; macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular / genetics*
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / pathology
  • Cytidine Deaminase / biosynthesis
  • Cytidine Deaminase / genetics*
  • DNA, Neoplasm / genetics
  • Disease Progression
  • Gene Expression Regulation, Neoplastic*
  • Liver Neoplasms, Experimental / genetics*
  • Liver Neoplasms, Experimental / metabolism
  • Liver Neoplasms, Experimental / pathology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Minor Histocompatibility Antigens / biosynthesis
  • Minor Histocompatibility Antigens / genetics*
  • Promoter Regions, Genetic
  • Tumor Microenvironment / physiology*

Substances

  • DNA, Neoplasm
  • Minor Histocompatibility Antigens
  • APOBEC3B protein, human
  • Cytidine Deaminase