Enhancing T-cell recruitment in renal cell carcinoma with cytokine-armed adenoviruses

Oncoimmunology. 2024 Sep 25;13(1):2407532. doi: 10.1080/2162402X.2024.2407532. eCollection 2024.

Abstract

Immunotherapy has emerged as a promising approach for cancer treatment, with oncolytic adenoviruses showing power as immunotherapeutic agents. In this study, we investigated the immunotherapeutic potential of an adenovirus construct expressing CXCL9, CXCL10, or IL-15 in clear cell renal cell carcinoma (ccRCC) tumor models. Our results demonstrated robust cytokine secretion upon viral treatment, suggesting effective transgene expression. Subsequent analysis using resistance-based transwell migration and microfluidic chip assays demonstrated increased T-cell migration in response to chemokine secretion by infected cells in both 2D and 3D cell models. Flow cytometry analysis revealed CXCR3 receptor expression across T-cell subsets, with the highest percentage found on CD8+ T-cells, underscoring their key role in immune cell migration. Alongside T-cells, we also detected NK-cells in the tumors of immunocompromised mice treated with cytokine-encoding adenoviruses. Furthermore, we identified potential immunogenic antigens that may enhance the efficacy and specificity of our armed oncolytic adenoviruses in ccRCC. Overall, our findings using ccRCC cell line, in vivo humanized mice, physiologically relevant PDCs in 2D and patient-derived organoids (PDOs) in 3D suggest that chemokine-armed adenoviruses hold promise for enhancing T-cell migration and improving immunotherapy outcomes in ccRCC. Our study contributes to the development of more effective ccRCC treatment strategies by elucidating immune cell infiltration and activation mechanisms within the tumor microenvironment (TME) and highlights the usefulness of PDOs for predicting clinical relevance and validating novel immunotherapeutic approaches. Overall, our research offers insights into the rational design and optimization of viral-based immunotherapies for ccRCC.

Keywords: Cytokines; immunotherapy; oncolytic viruses; renal cell carcinoma; tumor peptides.

MeSH terms

  • Adenoviridae* / genetics
  • Adenoviridae* / immunology
  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • Carcinoma, Renal Cell* / genetics
  • Carcinoma, Renal Cell* / immunology
  • Carcinoma, Renal Cell* / pathology
  • Carcinoma, Renal Cell* / therapy
  • Cell Line, Tumor
  • Cell Movement
  • Chemokine CXCL10 / genetics
  • Chemokine CXCL10 / immunology
  • Chemokine CXCL10 / metabolism
  • Chemokine CXCL9 / genetics
  • Chemokine CXCL9 / immunology
  • Chemokine CXCL9 / metabolism
  • Cytokines / metabolism
  • Humans
  • Immunotherapy / methods
  • Interleukin-15 / genetics
  • Interleukin-15 / immunology
  • Interleukin-15 / metabolism
  • Kidney Neoplasms* / genetics
  • Kidney Neoplasms* / immunology
  • Kidney Neoplasms* / pathology
  • Kidney Neoplasms* / therapy
  • Mice
  • Oncolytic Virotherapy / methods
  • Oncolytic Viruses / genetics
  • Oncolytic Viruses / immunology
  • Receptors, CXCR3 / genetics
  • Receptors, CXCR3 / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Chemokine CXCL9
  • Chemokine CXCL10
  • Cytokines
  • Interleukin-15
  • Receptors, CXCR3

Grants and funding

This work was supported by the iCAN Digital Precision Cancer Medicine platform Academy of Finland (iCAN Flagship); [Magnus Ehrnrooth Foundation]; [Medicinska Understödsföreningen Liv och Hälsa]; [European Research Council under the Horizon 2020 framework] under Grant [681219]; [Finnish Cancer Foundation] under Grants [4706116], [66-7110], [220015], [200082] and [190113]; [Jane and Aatos Erkko Foundation] under Grant [4705796]; and [Helsinki Institute of Life Science (HiLIFE)] under Grant [797011004]. R.M.B thanks the support by the Swedish Cancer Society [CAN 2017/685] and [CAN 2020/1269 PjF], and by the Erling-Persson Family Foundation [12/12-2017] and [22/9-2020].