Epitope-Specific Antitumor Immunity Suppresses Tumor Spread in Papillary Thyroid Cancer

J Clin Endocrinol Metab. 2017 Jul 1;102(7):2154-2161. doi: 10.1210/jc.2016-2469.

Abstract

Context: Papillary thyroid cancer (PTC) is characterized by a lymphocytic infiltration. PTC patients with lymphocytic infiltration may have a better clinical outcome.

Objective: Characterization of tumor epitope-specific immunity and correlation analyses with the clinical outcome.

Patients: 150 PTC patients; 40 Hashimoto thyroiditis (HT) patients; 21 healthy controls; 27,239 healthy whites (for HLA typing).

Main outcome measures: HLA class I restricted thyroperoxidase (TPO) and thyroglobulin (Tg) epitope-specific T cells (tetramer analyses), correlation analyses between HLA class II phenotypes, T cell immunity, and the clinical course.

Results: The frequency of TPO- and Tg-specific CD8+ T cells in PTC patients was largely increased compared with healthy controls (TPO and Tg, P < 0.005 and P < 0.005) and was similar to those in HT patients. HLA-DQB1*03-positive PTC patients had a significantly lower risk [risk ratio (RR), 0.170; 95% confidence interval (CI), 0.037 to 0.755; P < 0.05] and HLA-DRB1*03-positive and HLA-DQB1*02-positive PTC patients a significantly higher risk (HLA-DRB1*03: RR, 4.400; 95% CI, 1.378 to 14.05; P < 0.05; HLA-DQB1*02: RR, 3.692; 95% CI, 1.102 to 12.38; P < 0.05) for distant metastases, compared with patients with other haplotypes. HLA-DQB1*03-positive PTC patients revealed an increased responsiveness of tumor epitopes in vitro. These tumor epitope-specific CD8+ T cells were also found in lymph node metastases of HLA-DQB1*03-positive PTC patients.

Conclusion: We demonstrate a tumor epitope-specific immunity in PTC patients and the protective role of HLA-DQB1*03 against metastatic spread. These results have direct implications for new treatment options with immune checkpoint inhibitors.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Antigens, Neoplasm / immunology*
  • CD8-Positive T-Lymphocytes / immunology
  • Carcinoma / immunology*
  • Carcinoma / pathology
  • Carcinoma / secondary
  • Carcinoma, Papillary
  • Case-Control Studies
  • Epitopes / immunology
  • Epitopes, T-Lymphocyte / immunology*
  • Female
  • Hashimoto Disease / immunology
  • Histocompatibility Antigens Class II / immunology
  • Histocompatibility Testing / methods
  • Humans
  • Immunity, Cellular
  • Lymphatic Metastasis
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Male
  • Middle Aged
  • Prognosis
  • T-Lymphocyte Subsets / immunology
  • Thyroid Cancer, Papillary
  • Thyroid Neoplasms / immunology*
  • Thyroid Neoplasms / pathology
  • Thyroid Neoplasms / secondary
  • Young Adult

Substances

  • Antigens, Neoplasm
  • Epitopes
  • Epitopes, T-Lymphocyte
  • Histocompatibility Antigens Class II