Immunomodulatory effects of antiangiogenic tyrosine kinase inhibitors in renal cell carcinoma models: Impact on following anti-PD-1 treatments

Biochem Pharmacol. 2024 Aug:226:116397. doi: 10.1016/j.bcp.2024.116397. Epub 2024 Jun 27.

Abstract

The approval of immune checkpoint inhibitors (ICIs) has revolutionized the management of metastatic renal cell carcinoma (RCC), introducing several ICI-based combinations as the new standard of care for affected patients. Nonetheless, monotherapy with antiangiogenic tyrosine kinase inhibitors (TKIs), such as pazopanib or sunitinib, still represents a first-line treatment option for selected patients belonging to the favorable risk group according to the International mRCC Database Consortium (IMDC) model. After TKI monotherapy, the main second-line option is represented by ICI monotherapy with the anti-Programmed Death Receptor 1(PD-1) nivolumab. To date, the expected clinical outcomes are similar with pazopanib or sunitinib and there is no clear indication for selecting one TKI over the other. Moreover, their impact on subsequent ICI treatment outcomes is not well defined, yet. Based on these premises, we investigated the immunomodulatory activity of these drugs in vitro and in vivo.Both TKIs induced Programmed Cell Death Ligand-1 (PD-L1) expression and soluble PD-L1 release in RCC cells, and hampered T cell activation, reducing cytokine production and the proportion of activated T cells. Nevertheless, in a syngeneic co-culture system with peripheral blood mononuclear cells (PBMCs) and tumor cells, incubation with anti-PD-1 antibody following TKIs treatment significantly restored T cell function, potentiating the cytotoxic effects against tumor cells. Pazopanib and sunitinib followed by anti-PD-1 antibody produced a comparable inhibition of tumor growth in a RCC syngeneic mouse model. Our findings suggest that pazopanib and sunitinib, showing similar immunomodulatory effects, may have a comparable impact on the subsequent effectiveness of PD-1/PD-L1 blockade.

Keywords: Antiangiogenic drugs; Immunotherapy; PD-1/PD-L1; Pazopanib; Renal cell carcinoma; Sunitinib.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inhibitors* / administration & dosage
  • Angiogenesis Inhibitors* / pharmacology
  • Angiogenesis Inhibitors* / therapeutic use
  • Animals
  • B7-H1 Antigen / antagonists & inhibitors
  • B7-H1 Antigen / metabolism
  • Carcinoma, Renal Cell* / drug therapy
  • Carcinoma, Renal Cell* / pathology
  • Cell Line, Tumor
  • Female
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Indazoles / administration & dosage
  • Indazoles / pharmacology
  • Indazoles / therapeutic use
  • Kidney Neoplasms* / drug therapy
  • Kidney Neoplasms* / pathology
  • Mice
  • Nivolumab / administration & dosage
  • Nivolumab / pharmacology
  • Nivolumab / therapeutic use
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism
  • Protein Kinase Inhibitors* / pharmacology
  • Protein Kinase Inhibitors* / therapeutic use
  • Pyrimidines* / pharmacology
  • Pyrimidines* / therapeutic use
  • Sulfonamides* / pharmacology
  • Sulfonamides* / therapeutic use
  • Sunitinib* / pharmacology
  • Sunitinib* / therapeutic use
  • Tyrosine Kinase Inhibitors
  • Xenograft Model Antitumor Assays / methods

Substances

  • pazopanib
  • Angiogenesis Inhibitors
  • Protein Kinase Inhibitors
  • Sunitinib
  • Pyrimidines
  • Sulfonamides
  • Programmed Cell Death 1 Receptor
  • Indazoles
  • Immune Checkpoint Inhibitors
  • PDCD1 protein, human
  • Nivolumab
  • B7-H1 Antigen
  • Tyrosine Kinase Inhibitors