Immune activation underlies a sustained clinical response to Yttrium-90 radioembolisation in hepatocellular carcinoma

Gut. 2019 Feb;68(2):335-346. doi: 10.1136/gutjnl-2017-315485. Epub 2018 Feb 13.

Abstract

Objectives: Yttrium-90 (Y90)-radioembolisation (RE) significantly regresses locally advanced hepatocellular carcinoma and delays disease progression. The current study is designed to deeply interrogate the immunological impact of Y90-RE, which elicits a sustained therapeutic response.

Design: Time-of-flight mass cytometry and next-generation sequencing (NGS) were used to analyse the immune landscapes of tumour-infiltrating leucocytes (TILs), tumour tissues and peripheral blood mononuclear cells (PBMCs) at different time points before and after Y90-RE.

Results: TILs isolated after Y90-RE exhibited signs of local immune activation: higher expression of granzyme B (GB) and infiltration of CD8+ T cells, CD56+ NK cells and CD8+ CD56+ NKT cells. NGS confirmed the upregulation of genes involved in innate and adaptive immune activation in Y90-RE-treated tumours. Chemotactic pathways involving CCL5 and CXCL16 correlated with the recruitment of activated GB+CD8+ T cells to the Y90-RE-treated tumours. When comparing PBMCs before and after Y90-RE, we observed an increase in tumour necrosis factor-α on both the CD8+ and CD4+ T cells as well as an increase in percentage of antigen-presenting cells after Y90-RE, implying a systemic immune activation. Interestingly, a high percentage of PD-1+/Tim-3+CD8+ T cells coexpressing the homing receptors CCR5 and CXCR6 denoted Y90-RE responders. A prediction model was also built to identify sustained responders to Y90-RE based on the immune profiles from pretreatment PBMCs.

Conclusion: High-dimensional analysis of tumour and systemic immune landscapes identified local and systemic immune activation that corresponded to the sustained response to Y90-RE. Potential biomarkers associated with a positive clinical response were identified and a prediction model was built to identify sustained responders prior to treatment.

Keywords: Time-of-flight Mass Cytometry (CyTOF); Y90 radioembolization; biomarkers; chemotaxis; hepatocellular carcinoma; immune activation; tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigen-Presenting Cells / immunology
  • Biomarkers, Tumor / immunology
  • Carcinoma, Hepatocellular / immunology*
  • Carcinoma, Hepatocellular / radiotherapy*
  • Chemokine CCL5 / immunology
  • Chemokine CXCL16 / immunology
  • Disease Progression
  • Female
  • Flow Cytometry / methods
  • Granzymes / immunology
  • Humans
  • Leukocytes, Mononuclear / immunology*
  • Liver Neoplasms / immunology*
  • Liver Neoplasms / radiotherapy*
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Male
  • Singapore
  • Treatment Outcome
  • Tumor Necrosis Factor-alpha / immunology
  • Yttrium Radioisotopes*

Substances

  • Biomarkers, Tumor
  • CXCL16 protein, human
  • Chemokine CCL5
  • Chemokine CXCL16
  • Tumor Necrosis Factor-alpha
  • Yttrium Radioisotopes
  • Yttrium-90
  • Granzymes