Murine B16 melanomas expressing high levels of the chemokine stromal-derived factor-1/CXCL12 induce tumor-specific T cell chemorepulsion and escape from immune control

J Immunol. 2006 Mar 1;176(5):2902-14. doi: 10.4049/jimmunol.176.5.2902.

Abstract

The chemokine, stromal-derived factor-1/CXCL12, is expressed by normal and neoplastic tissues and is involved in tumor growth, metastasis, and modulation of tumor immunity. T cell-mediated tumor immunity depends on the migration and colocalization of CTL with tumor cells, a process regulated by chemokines and adhesion molecules. It has been demonstrated that T cells are repelled by high concentrations of the chemokine CXCL12 via a concentration-dependent and CXCR4 receptor-mediated mechanism, termed chemorepulsion or fugetaxis. We proposed that repulsion of tumor Ag-specific T cells from a tumor expressing high levels of CXCL12 allows the tumor to evade immune control. Murine B16/OVA melanoma cells (H2b) were engineered to constitutively express CXCL12. Immunization of C57BL/6 mice with B16/OVA cells lead to destruction of B16/OVA tumors expressing no or low levels of CXCL12 but not tumors expressing high levels of the chemokine. Early recruitment of adoptively transferred OVA-specific CTL into B16/OVA tumors expressing high levels of CXCL12 was significantly reduced in comparison to B16/OVA tumors, and this reduction was reversed when tumor-specific CTLs were pretreated with the specific CXCR4 antagonist, AMD3100. Memory OVA-specific CD8+ T cells demonstrated antitumor activity against B16/OVA tumors but not B16/OVA.CXCL12-high tumors. Expression of high levels of CXCL12 by B16/OVA cells significantly reduced CTL colocalization with and killing of target cells in vitro in a CXCR4-dependent manner. The repulsion of tumor Ag-specific T cells away from melanomas expressing CXCL12 confirms the chemorepellent activity of high concentrations of CXCL12 and may represent a novel mechanism by which certain tumors evade the immune system.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cancer Vaccines / immunology
  • Cell Line, Tumor
  • Cell Migration Inhibition*
  • Cell Proliferation
  • Chemokine CXCL12
  • Chemokines, CXC / biosynthesis*
  • Chemokines, CXC / genetics
  • Chemokines, CXC / physiology
  • Chemotaxis, Leukocyte / immunology*
  • Cytotoxicity, Immunologic
  • Dose-Response Relationship, Immunologic
  • Epitopes, T-Lymphocyte
  • Immunotherapy, Adoptive
  • Melanoma, Experimental / immunology*
  • Melanoma, Experimental / metabolism*
  • Melanoma, Experimental / pathology
  • Melanoma, Experimental / therapy
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Ovalbumin / immunology
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, CCR5 / metabolism
  • Receptors, CXCR4 / physiology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes, Cytotoxic / immunology

Substances

  • Cancer Vaccines
  • Chemokine CXCL12
  • Chemokines, CXC
  • Cxcl12 protein, mouse
  • Epitopes, T-Lymphocyte
  • Receptors, Antigen, T-Cell
  • Receptors, CCR5
  • Receptors, CXCR4
  • Ovalbumin