Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth

J Immunol. 2012 Dec 15;189(12):5602-11. doi: 10.4049/jimmunol.1201018. Epub 2012 Nov 14.

Abstract

Myeloid-derived suppressor cells (MDSCs) represent a heterogeneous population of myeloid cells in cancer patients and tumor-bearing mice that potently inhibits T cell responses. During tumor progression, MDSCs accumulate in several organs, including the tumor tissue. So far, tumor-infiltrating MDSC subpopulations remain poorly explored. In this study, we performed global gene expression profiling of mouse tumor-infiltrating granulocytic and monocytic (MO-MDSC) subsets compared with MDSCs from peripheral blood. RMA-S lymphoma-infiltrating MO-MDSCs not only produced high levels of NO and arginase-1, but also greatly increased levels of chemokines comprising the CCR5 ligands CCL3, CCL4, and CCL5. MO-MDSCs isolated from B16 melanoma and from skin tumor-bearing ret transgenic mice also expressed high levels of CCL3, CCL4, and CCL5. Expression of CCR5 was preferentially detected on regulatory T cells (Tregs). Accordingly, tumor-infiltrating MO-MDSCs directly attracted high numbers of Tregs via CCR5 in vitro. Intratumoral injection of CCL4 or CCL5 increased tumor-infiltrating Tregs, and deficiency of CCR5 led to their profound decrease. Moreover, in CCR5-deficient mice, RMA-S and B16 tumor growth was delayed emphasizing the importance of CCR5 in the control of antitumor immune responses. Overall, our data demonstrate that chemokines secreted by tumor-infiltrating MO-MDSCs recruit high numbers of Tregs revealing a novel suppressive role of MDSCs with potential clinical implications for the development of cancer immunotherapies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chemokine CCL3 / biosynthesis
  • Chemokine CCL3 / genetics
  • Chemokine CCL3 / metabolism
  • Chemokine CCL4 / biosynthesis
  • Chemokine CCL4 / genetics
  • Chemokine CCL4 / metabolism
  • Chemokine CCL5 / biosynthesis
  • Chemokine CCL5 / genetics
  • Chemokine CCL5 / metabolism
  • Chemotaxis, Leukocyte / genetics
  • Chemotaxis, Leukocyte / immunology*
  • Disease Models, Animal
  • Immune Tolerance / genetics
  • Immune Tolerance / immunology*
  • Ligands
  • Lymphoma / immunology
  • Lymphoma / metabolism
  • Lymphoma / pathology
  • Melanoma, Experimental / immunology*
  • Melanoma, Experimental / metabolism
  • Melanoma, Experimental / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Monocytes / immunology*
  • Monocytes / metabolism
  • Monocytes / pathology
  • Myeloid Cells / immunology*
  • Myeloid Cells / metabolism
  • Myeloid Cells / pathology
  • Receptors, CCR5 / deficiency
  • Receptors, CCR5 / metabolism
  • Receptors, CCR5 / physiology*
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism
  • T-Lymphocytes, Regulatory / pathology

Substances

  • Chemokine CCL3
  • Chemokine CCL4
  • Chemokine CCL5
  • Ligands
  • Receptors, CCR5

Associated data

  • GEO/GSE41620