Blocking IL1 Beta Promotes Tumor Regression and Remodeling of the Myeloid Compartment in a Renal Cell Carcinoma Model: Multidimensional Analyses

Clin Cancer Res. 2021 Jan 15;27(2):608-621. doi: 10.1158/1078-0432.CCR-20-1610. Epub 2020 Nov 4.

Abstract

Purpose: Intratumoral immunosuppression mediated by myeloid-derived suppressor cells (MDSC) and tumor-associated macrophages (TAM) represents a potential mechanism of immune checkpoint inhibitor (ICI) resistance in solid tumors. By promoting TAM and MDSC infiltration, IL1β may drive adaptive and innate immune resistance in renal cell carcinoma (RCC) and in other tumor types.

Experimental design: Using the RENCA model of RCC, we evaluated clinically relevant combinations of anti-IL1β plus either anti-PD-1 or the multitargeted tyrosine kinase inhibitor (TKI), cabozantinib. We performed comprehensive immune profiling of established RENCA tumors via multiparameter flow cytometry, tumor cytokine profiling, and single-cell RNA sequencing (RNA-seq). Similar analyses were extended to the MC38 tumor model.

Results: Analyses via multiparameter flow cytometry, tumor cytokine profiling, and single-cell RNA-seq showed that anti-IL1β reduces infiltration of polymorphonuclear MDSCs and TAMs. Combination treatment with anti-IL1β plus anti-PD-1 or cabozantinib showed increased antitumor activity that was associated with decreases in immunosuppressive MDSCs and increases in M1-like TAMs.

Conclusions: Single-cell RNA-seq analyses show that IL1β blockade and ICI or TKI remodel the myeloid compartment through nonredundant, relatively T-cell-independent mechanisms. IL1β is an upstream mediator of adaptive myeloid resistance and represents a potential target for kidney cancer immunotherapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anilides / administration & dosage
  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Carcinoma, Renal Cell / drug therapy*
  • Carcinoma, Renal Cell / genetics
  • Carcinoma, Renal Cell / metabolism
  • Cell Line, Tumor
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal*
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Immune Checkpoint Inhibitors / administration & dosage
  • Interleukin-1beta / antagonists & inhibitors*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Kidney Neoplasms / drug therapy*
  • Kidney Neoplasms / genetics
  • Kidney Neoplasms / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Myeloid-Derived Suppressor Cells / drug effects*
  • Myeloid-Derived Suppressor Cells / metabolism
  • Pyridines / administration & dosage
  • RNA-Seq / methods
  • Single-Cell Analysis / methods
  • Treatment Outcome
  • Tumor Burden / drug effects
  • Tumor Burden / genetics
  • Tumor-Associated Macrophages / classification
  • Tumor-Associated Macrophages / drug effects
  • Tumor-Associated Macrophages / metabolism

Substances

  • Anilides
  • Cytokines
  • Immune Checkpoint Inhibitors
  • Interleukin-1beta
  • Pyridines
  • cabozantinib