T cell neoepitope discovery in colorectal cancer by high throughput profiling of somatic mutations in expressed genes

Gut. 2017 Mar;66(3):454-463. doi: 10.1136/gutjnl-2015-309453. Epub 2015 Dec 17.

Abstract

Objective: Patient-specific (unique) tumour antigens, encoded by somatically mutated cancer genes, generate neoepitopes that are implicated in the induction of tumour-controlling T cell responses. Recent advancements in massive DNA sequencing combined with robust T cell epitope predictions have allowed their systematic identification in several malignancies.

Design: We undertook the identification of unique neoepitopes in colorectal cancers (CRCs) by using high-throughput sequencing of cDNAs expressed by standard cancer cell cultures, and by related cancer stem/initiating cells (CSCs) cultures, coupled with a reverse immunology approach not requiring human leukocyte antigen (HLA) allele-specific epitope predictions.

Results: Several unique mutated antigens of CRC, shared by standard cancer and related CSC cultures, were identified by this strategy. CD8+ and CD4+ T cells, either autologous to the patient or derived from HLA-matched healthy donors, were readily expanded in vitro by peptides spanning different cancer mutations and specifically recognised differentiated cancer cells and CSC cultures, expressing the mutations. Neoepitope-specific CD8+ T cell frequency was also increased in a patient, compared with healthy donors, supporting the occurrence of clonal expansion in vivo.

Conclusions: These results provide a proof-of-concept approach for the identification of unique neoepitopes that are immunogenic in patients with CRC and can also target T cells against the most aggressive CSC component.

Keywords: ANTIGENS; CANCER IMMUNOBIOLOGY; COLORECTAL CANCER; GENE MUTATION; IMMUNE RESPONSE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenomatous Polyposis Coli Protein / genetics
  • CD4-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / immunology*
  • Cell Cycle Proteins / genetics
  • Class I Phosphatidylinositol 3-Kinases
  • Colorectal Neoplasms / genetics*
  • Colorectal Neoplasms / immunology*
  • DNA Mutational Analysis
  • DNA, Complementary / analysis*
  • Epitopes, T-Lymphocyte / genetics*
  • Epitopes, T-Lymphocyte / immunology
  • F-Box Proteins / genetics
  • F-Box-WD Repeat-Containing Protein 7
  • Gene Expression
  • HLA Antigens / genetics
  • HLA Antigens / immunology
  • High-Throughput Screening Assays
  • Humans
  • Neoplastic Stem Cells / immunology
  • Phosphatidylinositol 3-Kinases / genetics
  • Proto-Oncogene Proteins p21(ras) / genetics
  • Smad4 Protein / genetics
  • Smad4 Protein / immunology
  • Tumor Cells, Cultured
  • Tumor Suppressor Protein p53 / genetics
  • Ubiquitin-Protein Ligases / genetics

Substances

  • APC protein, human
  • Adenomatous Polyposis Coli Protein
  • Cell Cycle Proteins
  • DNA, Complementary
  • Epitopes, T-Lymphocyte
  • F-Box Proteins
  • F-Box-WD Repeat-Containing Protein 7
  • FBXW7 protein, human
  • HLA Antigens
  • KRAS protein, human
  • SMAD4 protein, human
  • Smad4 Protein
  • Tumor Suppressor Protein p53
  • Ubiquitin-Protein Ligases
  • Phosphatidylinositol 3-Kinases
  • Class I Phosphatidylinositol 3-Kinases
  • PIK3CA protein, human
  • Proto-Oncogene Proteins p21(ras)