Impaired STAT phosphorylation in T cells from melanoma patients in response to IL-2: association with clinical stage

Clin Cancer Res. 2009 Jun 15;15(12):4085-94. doi: 10.1158/1078-0432.CCR-08-3323. Epub 2009 Jun 9.

Abstract

Purpose: To assess the extent of signal transducer and activator of transcription (STAT) activation in response to interleukin 2 (IL-2) in melanoma patients' T cells, along with clinical stage of tumor progression.

Experimental design: T lymphocytes from peripheral blood of healthy donors and of American Joint Committee on Cancer stage I to IV melanoma patients, as well as from metastatic lymph nodes of patients, were evaluated for responsiveness to IL-2. CFSE assays and single-cell phospho-STAT-specific flow cytometry screening were used. Results. T cells from advanced melanoma patients, in comparison with healthy donors, showed reduced proliferation to IL-2 and IL-15, but not to anti-CD3 monoclonal antibody. Impaired response occurred in CCR7(+) and CCR7(-) T-cell subsets, but not in CD3(-) CD8(+) natural killer (NK) cells, and was not explained by induction of apoptosis, increased cytokine consumption, or altered IL-2R subunit expression in patients' T lymphocytes. By phospho-specific flow cytometry, defective STAT1 and STAT5 activation in response to IL-2 was found mainly in T lymphocytes from peripheral blood and/or tumor site of American Joint Committee on Cancer stage III and IV patients, compared with stage I and II patients and to donors, and in melanoma antigen-specific T cells isolated from metastatic lymph nodes. At tumor site, impaired STAT activation in T cells did not correlate with frequency of CD4(+) CD25(+) Foxp3(+) T cells. Serum from advanced melanoma patients inhibited IL-2-dependent STAT activation in donors' T cells and a neutralizing monoclonal antibody to transforming growth factor beta1 counteracted such inhibition.

Conclusions: These results provide evidence for development of impaired STAT signaling in response to IL-2, along with clinical evolution of the disease, in melanoma patients' T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CD3 Complex / immunology
  • CD3 Complex / metabolism
  • Cell Proliferation / drug effects
  • Humans
  • Interleukin-15 / pharmacology
  • Interleukin-2 / pharmacology*
  • Janus Kinase 3 / immunology
  • Janus Kinase 3 / metabolism
  • Killer Cells, Natural / drug effects*
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / metabolism
  • Melanoma / immunology*
  • Melanoma / pathology
  • Neoplasm Staging
  • Phosphorylation / drug effects
  • Receptors, Cytokine / immunology
  • Receptors, Cytokine / metabolism
  • STAT1 Transcription Factor / metabolism*
  • STAT5 Transcription Factor / metabolism*
  • Skin Neoplasms / immunology*
  • Skin Neoplasms / pathology
  • T-Lymphocytes / drug effects*
  • T-Lymphocytes / metabolism

Substances

  • CD3 Complex
  • Interleukin-15
  • Interleukin-2
  • Receptors, Cytokine
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • STAT5 Transcription Factor
  • JAK3 protein, human
  • Janus Kinase 3