Autophagy-induced RelB/p52 activation mediates tumour-associated macrophage repolarisation and suppression of hepatocellular carcinoma by natural compound baicalin

Cell Death Dis. 2015 Oct 22;6(10):e1942. doi: 10.1038/cddis.2015.271.

Abstract

The plasticity of tumour-associated macrophages (TAMs) has implicated an influential role in hepatocellular carcinoma (HCC). Repolarisation of TAM towards M1 phenotype characterises an immune-competent microenvironment that favours tumour regression. To investigate the role and mechanism of TAM repolarisation in suppression of HCC by a natural compound baicalin, Orthotopic HCC implantation model was used to investigate the effect of baicalin on HCC; liposome-clodronate was introduced to suppress macrophage populations in mice; bone marrow-derived monocytes (BMDMs) were induced to unpolarised, M1-like, M2-like macrophages and TAM using different conditioned medium. We observed that oral administration of baicalin (50 mg/kg) completely blocked orthotopic growth of implanted HCC. Suppression of HCC by baicalin was diminished when mice macrophage was removed by clodronate treatment. Baicalin induced repolarisation of TAM to M1-like phenotype without specific toxicity to either phenotype of macrophages. Baicalin initiated TAM reprogramming to M1-like macrophage, and promoted pro-inflammatory cytokines production. Co-culturing of HCC cells with baicalin-treated TAMs resulted in reduced proliferation and motility in HCC. Baicalin had minimal effect on derivation of macrophage polarisation factors by HCC cells, while directly induced repolarisation of TAM and M2-like macrophage. This effect was associated with elevated autophagy, and transcriptional activation of RelB/p52 pathway. Suppression of autophagy or RelB abolished skewing of baicalin-treated TAM. Autophagic degradation of TRAF2 in baicalin-treated TAM might be responsible for RelB/p52 activation. Our findings unveil the essential role of TAM repolarisation in suppressive effect of baicalin on HCC, which requires autophagy-associated activation of RelB/p52.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy / drug effects
  • Carcinoma, Hepatocellular / drug therapy
  • Carcinoma, Hepatocellular / pathology*
  • Cell Polarity / drug effects
  • Flavonoids / pharmacology*
  • Flavonoids / therapeutic use
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Interleukin-12 / genetics
  • Interleukin-12 / metabolism
  • Liver Neoplasms, Experimental / drug therapy
  • Liver Neoplasms, Experimental / pathology*
  • Macrophages / drug effects
  • Macrophages / pathology
  • Mice
  • NF-kappa B p52 Subunit / metabolism
  • NF-kappa B p52 Subunit / physiology*
  • Signal Transduction
  • Transcription Factor RelB / metabolism
  • Transcription Factor RelB / physiology*
  • Tumor Microenvironment
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Flavonoids
  • NF-kappa B p52 Subunit
  • Relb protein, mouse
  • Tumor Necrosis Factor-alpha
  • Transcription Factor RelB
  • Interleukin-12
  • baicalin