Enhanced CCR2 expression by ACKR2-deficient NK cells increases tumoricidal cell therapy efficacy

J Leukoc Biol. 2024 Nov 27;116(6):1544-1553. doi: 10.1093/jleuko/qiae162.

Abstract

Chemokines regulate leukocyte navigation to inflamed sites and specific tissue locales and may therefore be useful for ensuring accurate homing of cell therapeutic products. We, and others, have shown that atypical chemokine receptor 2 (ACKR2)-deficient mice (ACKR2-/-) are protected from metastasis development in cell line and spontaneous mouse models. We have shown that this relates to enhanced CCR2 expression on ACKR2-/- natural killer cells, allowing them to home more effectively to CCR2 ligand-expressing metastatic deposits. Here we demonstrate that the metastatic-suppression phenotype in ACKR2-/- mice is not a direct effect of the absence of ACKR2. Instead, enhanced natural killer cell CCR2 expression is caused by passenger mutations that originate from the creation of the ACKR2-/- mouse strain in 129 embryonic stem cells. We further demonstrate that simple selection of CCR2+ natural killer cells enriches for a population of cells with enhanced antimetastatic capabilities. Given the widespread expression of CCR2 ligands by tumors, our study highlights CCR2 as a potentially important contributor to natural killer cell tumoricidal cell therapy.

Keywords: atypical chemokine receptor; metastasis; passenger mutation.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chemokine Receptor D6
  • Cytotoxicity, Immunologic
  • Killer Cells, Natural* / immunology
  • Killer Cells, Natural* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasm Metastasis
  • Receptors, CCR2* / genetics
  • Receptors, CCR2* / metabolism
  • Receptors, Chemokine / genetics
  • Receptors, Chemokine / metabolism

Substances

  • Receptors, CCR2
  • Ackr2 protein, mouse
  • Ccr2 protein, mouse
  • Receptors, Chemokine
  • Chemokine Receptor D6