Identification of tumor-associated, MHC class II-restricted phosphopeptides as targets for immunotherapy

Proc Natl Acad Sci U S A. 2009 Jul 21;106(29):12073-8. doi: 10.1073/pnas.0903852106. Epub 2009 Jul 6.

Abstract

The activation and recruitment of CD4(+) T cells are critical for the development of efficient antitumor immunity and may allow for the optimization of current cancer immunotherapy strategies. Searching for more optimal and selective targets for CD4(+) T cells, we have investigated phosphopeptides, a new category of tumor-derived epitopes linked to proteins with vital cellular functions. Although MHC I-restricted phosphopeptides have been identified, it was previously unknown whether human MHC II molecules present phosphopeptides for specific CD4(+) T cell recognition. We first demonstrated the fine specificity of human CD4(+) T cells to discriminate a phosphoresidue by using cells raised against the candidate melanoma antigen mutant B-Raf or its phosphorylated counterpart. Then, we assessed the presence and complexity of human MHC II-associated phosphopeptides by analyzing 2 autologous pairs of melanoma and EBV-transformed B lymphoblastoid lines. By using sequential affinity isolation, biochemical enrichment, mass spectrometric sequencing, and comparative analysis, a total of 175 HLA-DR-associated phosphopeptides were characterized. Many were derived from source proteins that may have roles in cancer development, growth, and metastasis. Most were expressed exclusively by either melanomas or transformed B cells, suggesting the potential to define cell type-specific phosphatome "fingerprints." We then generated HLA-DRbeta1*0101-restricted CD4(+) T cells specific for a phospho-MART-1 peptide identified in both melanoma cell lines. These T cells showed specificity for phosphopeptide-pulsed antigen-presenting cells as well as for intact melanoma cells. This previously undescribed demonstration of MHC II-restricted phosphopeptides recognizable by human CD4(+) T cells provides potential new targets for cancer immunotherapy.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Antigens, Neoplasm / immunology
  • CD4-Positive T-Lymphocytes / immunology
  • HLA-DR Antigens / immunology
  • Histocompatibility Antigens Class II / immunology*
  • Humans
  • Immunotherapy*
  • MART-1 Antigen
  • Melanoma / immunology*
  • Molecular Sequence Data
  • Mutation / genetics
  • Neoplasm Proteins / immunology
  • Phosphopeptides / chemistry
  • Phosphopeptides / immunology*
  • Proto-Oncogene Proteins B-raf / genetics

Substances

  • Antigens, Neoplasm
  • HLA-DR Antigens
  • Histocompatibility Antigens Class II
  • MART-1 Antigen
  • MLANA protein, human
  • Neoplasm Proteins
  • Phosphopeptides
  • Proto-Oncogene Proteins B-raf