Single-Cell Analysis Reveals EP4 as a Target for Restoring T-Cell Infiltration and Sensitizing Prostate Cancer to Immunotherapy

Clin Cancer Res. 2022 Feb 1;28(3):552-567. doi: 10.1158/1078-0432.CCR-21-0299. Epub 2021 Nov 5.

Abstract

Purpose: Immunotherapies targeting immune checkpoint molecules have shown promising treatment for a subset of cancers; however, many "cold" tumors, such as prostate cancer, remain unresponsive. We aimed to identify a potential targetable marker relevant to prostate cancer and develop novel immunotherapy.

Experimental design: Analysis of transcriptomic profiles at single-cell resolution was performed in clinical patients' samples, along with integrated analysis of multiple RNA-sequencing datasets. The antitumor activity of YY001, a novel EP4 antagonist, combined with anti-programmed cell death protein 1 (PD-1) antibody was evaluated both in vitro and in vivo.

Results: We identified EP4 (PTGER4) as expressed in epithelial cells and various immune cells and involved in modulating the prostate cancer immune microenvironment. YY001, a novel EP4 antagonist, inhibited the differentiation, maturation, and immunosuppressive function of myeloid-derived suppressor cells (MDSC) while enhancing the proliferation and anticancer functions of T cells. Furthermore, it reversed the infiltration levels of MDSCs and T cells in the tumor microenvironment by overturning the chemokine profile of tumor cells in vitro and in vivo. The combined immunotherapy demonstrated a robust antitumor immune response as indicated by the robust accumulation and activation of CD8+ cytotoxic T cells, with a significantly decreased MDSC ratio and reduced MDSC immunosuppression function.

Conclusions: Our study identified EP4 as a specific target for prostate cancer immunotherapy and demonstrated that YY001 inhibited the growth of prostate tumors by regulating the immune microenvironment and strongly synergized with anti-PD-1 antibodies to convert completely unresponsive prostate cancers into responsive cancers, resulting in marked tumor regression, long-term survival, and lasting immunologic memory.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents, Immunological / therapeutic use
  • CD8-Positive T-Lymphocytes / immunology*
  • Cell Line, Tumor
  • Gene Expression
  • Humans
  • Immunotherapy / methods*
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Male
  • Mice
  • Molecular Targeted Therapy
  • Programmed Cell Death 1 Receptor / immunology
  • Prostatic Neoplasms / immunology*
  • Prostatic Neoplasms / therapy*
  • Receptors, Prostaglandin E, EP4 Subtype / antagonists & inhibitors*
  • Receptors, Prostaglandin E, EP4 Subtype / genetics*
  • Single-Cell Analysis*
  • Tumor Microenvironment / immunology

Substances

  • Antineoplastic Agents, Immunological
  • PDCD1 protein, human
  • PTGER4 protein, human
  • Programmed Cell Death 1 Receptor
  • Receptors, Prostaglandin E, EP4 Subtype