Targeting the atypical chemokine receptor 2 (Ackr2) improves the benefit of anti-PD-1 immunotherapy in melanoma mouse model

Oncoimmunology. 2025 Dec;14(1):2494426. doi: 10.1080/2162402X.2025.2494426. Epub 2025 Apr 18.

Abstract

Immune checkpoint blockade (ICB) therapies, such as anti-PD-1, have transformed cancer treatment, but many patients do not respond due to a non-inflammatory tumor microenvironment (TME). Here, we investigated the impact of targeting Atypical Chemokine Receptor 2 (ACKR2), which scavenges key chemokines involved in immune cell recruitment, on the improvement of anti-PD-1-based therapy. In a melanoma mouse model, we demonstrated that Ackr2 inhibition increases the release of proinflammatory chemokines CCL5 and CXCL10 and enhances the infiltration of NK cells, activated CD8+ and CD4+ effector T cells while reducing regulatory T cells (Tregs) in the TME. Targeting Ackr2 led to tumor growth inhibition, improved survival, and enhanced response to anti-PD-1 therapy. In BRAF- and NRAS-mutant melanoma patients, low ACKR2 expression or high CCL5/CXCL10 levels correlated with improved survival and higher CD8+ T cell markers. Targeting ACKR2 represents a promising approach for developing combination therapies, particularly for 'cold' ICB resistant tumors.

Keywords: ACKR2; CCL5; Cancer immunotherapy; D6; anti-PD-1; combination immunotherapy; immune cell infiltration; immune checkpoint blockade; inflammatory chemokines; melanoma; scavenger receptor; tumor microenvironment.

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • Chemokine CCL5 / metabolism
  • Chemokine CXCL10 / metabolism
  • Disease Models, Animal
  • Female
  • Humans
  • Immune Checkpoint Inhibitors* / pharmacology
  • Immune Checkpoint Inhibitors* / therapeutic use
  • Immunotherapy / methods
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology
  • Melanoma* / drug therapy
  • Melanoma* / immunology
  • Melanoma* / pathology
  • Melanoma, Experimental* / drug therapy
  • Melanoma, Experimental* / immunology
  • Melanoma, Experimental* / pathology
  • Mice
  • Mice, Inbred C57BL
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Receptors, CCR* / antagonists & inhibitors
  • Receptors, CCR* / metabolism
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology

Substances

  • Immune Checkpoint Inhibitors
  • Chemokine CXCL10
  • Receptors, CCR
  • Programmed Cell Death 1 Receptor
  • Chemokine CCL5