Targeting CXCR4 impaired T regulatory function through PTEN in renal cancer patients

Br J Cancer. 2024 Jun;130(12):2016-2026. doi: 10.1038/s41416-024-02702-x. Epub 2024 May 4.

Abstract

Background: Tregs trafficking is controlled by CXCR4. In Renal Cell Carcinoma (RCC), the effect of the new CXCR4 antagonist, R54, was explored in peripheral blood (PB)-Tregs isolated from primary RCC patients.

Methods: PB-Tregs were isolated from 77 RCC patients and 38 healthy donors (HDs). CFSE-T effector-Tregs suppression assay, IL-35, IFN-γ, IL-10, TGF-β1 secretion, and Nrp-1+Tregs frequency were evaluated. Tregs were characterised for CTLA-4, PD-1, CD40L, PTEN, CD25, TGF-β1, FOXP3, DNMT1 transcriptional profile. PTEN-pAKT signalling was evaluated in the presence of R54 and/or triciribine (TCB), an AKT inhibitor. Methylation of TSDR (Treg-Specific-Demethylated-Region) was conducted.

Results: R54 impaired PB-RCC-Tregs function, reduced Nrp-1+Tregs frequency, the release of IL-35, IL-10, and TGF-β1, while increased IFN-γ Teff-secretion. The CXCR4 ligand, CXCL12, recruited CD25+PTEN+Tregs in RCC while R54 significantly reduced it. IL-2/PMA activates Tregs reducing pAKT+Tregs while R54 increases it. The AKT inhibitor, TCB, prevented the increase in pAKT+Tregs R54-mediated. Moreover, R54 significantly reduced FOXP3-TSDR demethylation with DNMT1 and FOXP3 downregulation.

Conclusion: R54 impairs Tregs function in primary RCC patients targeting PTEN/PI3K/AKT pathway, reducing TSDR demethylation and FOXP3 and DNMT1 expression. Thus, CXCR4 targeting is a strategy to inhibit Tregs activity in the RCC tumour microenvironment.

MeSH terms

  • Adult
  • Aged
  • Carcinoma, Renal Cell* / drug therapy
  • Carcinoma, Renal Cell* / immunology
  • Carcinoma, Renal Cell* / metabolism
  • Carcinoma, Renal Cell* / pathology
  • Female
  • Forkhead Transcription Factors / metabolism
  • Humans
  • Kidney Neoplasms* / drug therapy
  • Kidney Neoplasms* / immunology
  • Kidney Neoplasms* / metabolism
  • Kidney Neoplasms* / pathology
  • Male
  • Middle Aged
  • PTEN Phosphohydrolase* / metabolism
  • Receptors, CXCR4* / metabolism
  • Signal Transduction
  • T-Lymphocytes, Regulatory* / immunology

Substances

  • PTEN Phosphohydrolase
  • Receptors, CXCR4
  • PTEN protein, human
  • CXCR4 protein, human
  • Forkhead Transcription Factors
  • FOXP3 protein, human