Targeting of HPV-16+ Epithelial Cancer Cells by TCR Gene Engineered T Cells Directed against E6

Clin Cancer Res. 2015 Oct 1;21(19):4431-9. doi: 10.1158/1078-0432.CCR-14-3341.

Abstract

Purpose: The E6 and E7 oncoproteins of HPV-associated epithelial cancers are in principle ideal immunotherapeutic targets, but evidence that T cells specific for these antigens can recognize and kill HPV(+) tumor cells is limited. We sought to determine whether TCR gene engineered T cells directed against an HPV oncoprotein can successfully target HPV(+) tumor cells.

Experimental design: T-cell responses against the HPV-16 oncoproteins were investigated in a patient with an ongoing 22-month disease-free interval after her second resection of distant metastatic anal cancer. T cells genetically engineered to express an oncoprotein-specific TCR from this patient's tumor-infiltrating T cells were tested for specific reactivity against HPV(+) epithelial tumor cells.

Results: We identified, from an excised metastatic anal cancer tumor, T cells that recognized an HLA-A*02:01-restricted epitope of HPV-16 E6. The frequency of the dominant T-cell clonotype from these cells was approximately 400-fold greater in the patient's tumor than in her peripheral blood. T cells genetically engineered to express the TCR from this clonotype displayed high avidity for an HLA-A*02:01-restricted epitope of HPV-16, and they showed specific recognition and killing of HPV-16(+) cervical, and head and neck cancer cell lines.

Conclusions: These findings demonstrate that HPV-16(+) tumors can be targeted by E6-specific TCR gene engineered T cells, and they provide the foundation for a novel cellular therapy directed against HPV-16(+) malignancies, including cervical, oropharyngeal, anal, vulvar, vaginal, and penile cancers.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Anus Neoplasms / etiology
  • Anus Neoplasms / pathology
  • Carcinoma / etiology*
  • Carcinoma / metabolism
  • Carcinoma / therapy
  • Cell Line, Tumor
  • Cross Reactions / immunology
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Epitopes, T-Lymphocyte / genetics
  • Epitopes, T-Lymphocyte / immunology
  • Female
  • Gene Expression
  • Genes, T-Cell Receptor*
  • HLA-A2 Antigen / immunology
  • HLA-A2 Antigen / metabolism
  • Human papillomavirus 16 / genetics
  • Human papillomavirus 16 / immunology*
  • Humans
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / metabolism
  • Lymphocytes, Tumor-Infiltrating / pathology
  • Neoplasm Metastasis
  • Oncogene Proteins, Viral / genetics
  • Oncogene Proteins, Viral / immunology*
  • Oncogene Proteins, Viral / metabolism
  • Protein Binding / immunology
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / immunology
  • Repressor Proteins / genetics
  • Repressor Proteins / immunology*
  • Repressor Proteins / metabolism
  • T-Cell Antigen Receptor Specificity / immunology
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism*
  • Transduction, Genetic
  • Uterine Cervical Neoplasms / etiology

Substances

  • E6 protein, Human papillomavirus type 16
  • Epitopes, T-Lymphocyte
  • HLA-A2 Antigen
  • Oncogene Proteins, Viral
  • Recombinant Fusion Proteins
  • Repressor Proteins