Skin melanoma development in ret transgenic mice despite the depletion of CD25+Foxp3+ regulatory T cells in lymphoid organs

J Immunol. 2009 Nov 15;183(10):6330-7. doi: 10.4049/jimmunol.0900609. Epub 2009 Oct 19.

Abstract

CD4(+)CD25(+)Foxp3(+) regulatory T cells (Treg) known to mediate self-tolerance were also shown to contribute to tumor progression. In mouse melanoma transplantation models, Treg depletion resulted in the stimulation of antitumor immune responses and tumor eradication. To study Treg in conditions close to the clinical situation, we used a ret transgenic mouse spontaneous melanoma model, which, in contrast to transplantation models, resembles human melanoma regarding clinical development. Significantly higher numbers of Treg were found in skin tumors and metastatic lymph nodes at early stages of melanoma progression compared with more advanced stages accompanied by the elevated CCR4 expression on Treg and higher production of its ligand CCL2 in tumor lesions. Numbers of tumor infiltrating Treg inversely correlated with Treg amounts in the bone marrow, suggesting their possible recruitment to melanoma lesions from this organ. The immunosuppressive function of Treg from transgenic tumor-bearing mice was similar to that from transgenic tumor-free mice or nontransgenic littermates. Although anti-CD25 mAb injections resulted in the efficient Treg depletion from lymphoid organs of transgenic mice, melanoma development was not significantly delayed. Furthermore, the treatment of mice with macroscopical tumors also failed to inhibit tumor progression, which correlated with the inability to deplete intratumoral Treg. We suggest that in the autochthonous melanoma genesis, other immunosuppressive cells could play an important role and replace immunosuppressive, tumor-promoting functions of Treg. Therefore, effective melanoma immunotherapy should include the inhibition of Treg migration into the tumor combined with neutralization of other immunosuppressive cells and factors in the tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Movement / immunology
  • Chemokine CCL17 / immunology
  • Chemokine CCL17 / metabolism
  • Chemokine CCL2 / immunology
  • Chemokine CCL2 / metabolism
  • Chemokine CCL22 / immunology
  • Chemokine CCL22 / metabolism
  • Forkhead Transcription Factors / immunology
  • Interleukin-2 Receptor alpha Subunit / immunology
  • Lymphocyte Depletion
  • Melanoma / immunology*
  • Melanoma / metabolism
  • Melanoma / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Proto-Oncogene Proteins c-ret / genetics
  • Receptors, CCR4 / immunology
  • Receptors, CCR4 / metabolism
  • Skin Neoplasms / immunology*
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Ccl17 protein, mouse
  • Ccl2 protein, mouse
  • Ccl22 protein, mouse
  • Chemokine CCL17
  • Chemokine CCL2
  • Chemokine CCL22
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Interleukin-2 Receptor alpha Subunit
  • Receptors, CCR4
  • Proto-Oncogene Proteins c-ret
  • RET protein, human