MHC-restricted phosphopeptide antigens: preclinical validation and first-in-humans clinical trial in participants with high-risk melanoma

J Immunother Cancer. 2020 May;8(1):e000262. doi: 10.1136/jitc-2019-000262.

Abstract

Background: Phosphorylated peptides presented by MHC molecules represent a new class of neoantigens expressed on cancer cells and recognized by CD8 T-cells. These peptides are promising targets for cancer immunotherapy. Previous work identified an HLA-A*0201-restricted phosphopeptide from insulin receptor substrate 2 (pIRS2) as one such target. The purpose of this study was to characterize a second phosphopeptide, from breast cancer antiestrogen resistance 3 (BCAR3), and to evaluate safety and immunogenicity of a novel immunotherapic vaccine comprising either or both of these phosphorylated peptides.

Methods: Phosphorylated BCAR3 protein was evaluated in melanoma and breast cancer cell lines by Western blot, and recognition by T-cells specific for HLA-A*0201-restricted phosphorylated BCAR3 peptide (pBCAR3126-134) was determined by 51Cr release assay and intracellular cytokine staining. Human tumor explants were also evaluated by mass spectrometry for presentation of pIRS2 and pBCAR3 peptides. For the clinical trial, participants with resected stage IIA-IV melanoma were vaccinated 6 times over 12 weeks with one or both peptides in incomplete Freund's adjuvant and Hiltonol (poly-ICLC). Adverse events (AEs) were coded based on National Cancer Institute (NCI) Common Terminology Criteria for Adverse Events (CTCAE) V.4.03, with provision for early study termination if dose-limiting toxicity (DLT) rates exceeded 33%. The enrollment target was 12 participants evaluable for immune response to each peptide. T-cell responses were assessed by interferon-γ ELISpot assay.

Results: pBCAR3 peptides were immunogenic in vivo in mice, and in vitro in normal human donors, and T-cells specific for pBCAR3126-134 controlled outgrowth of a tumor xenograft. The pIRS21097-1105 peptide was identified by mass spectrometry from human hepatocellular carcinoma tumors. In the clinical trial, 15 participants were enrolled. All had grade 1 or 2 treatment-related AEs, but there were no grade 3-4 AEs, DLTs or deaths on study. T-cell responses were induced to the pIRS21097-1105 peptide in 5/12 patients (42%, 90% CI 18% to 68%) and to the pBCAR3126-134 peptide in 2/12 patients (17%, 90% CI 3% to 44%).

Conclusion: This study supports the safety and immunogenicity of vaccines containing the cancer-associated phosphopeptides pBCAR3126-134 and pIRS21097-1105, and the data support continued development of immune therapy targeting phosphopeptides. Future studies will define ways to further enhance the magnitude and durability of phosphopeptide-specific immune responses.

Trial registration number: NCT01846143.

Keywords: antigens; immunogenicity; immunotherapy; melanoma; neoplasm; vaccination; vaccine.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Antigens, Neoplasm / genetics
  • Antigens, Neoplasm / immunology*
  • CD8-Positive T-Lymphocytes / immunology
  • Cancer Vaccines / administration & dosage
  • Cancer Vaccines / adverse effects*
  • Cancer Vaccines / genetics
  • Cancer Vaccines / immunology
  • Cell Line, Tumor
  • Female
  • Guanine Nucleotide Exchange Factors / genetics
  • Guanine Nucleotide Exchange Factors / immunology
  • HLA-A2 Antigen / genetics
  • HLA-A2 Antigen / immunology
  • Humans
  • Immunogenicity, Vaccine
  • Immunotherapy / adverse effects*
  • Immunotherapy / methods
  • Insulin Receptor Substrate Proteins / genetics
  • Insulin Receptor Substrate Proteins / immunology
  • Male
  • Melanoma / immunology
  • Melanoma / therapy*
  • Mice
  • Mice, Transgenic
  • Middle Aged
  • Phosphopeptides / genetics
  • Phosphopeptides / immunology
  • Pilot Projects
  • Proof of Concept Study
  • Skin Neoplasms / immunology
  • Skin Neoplasms / therapy*
  • Vaccines, Subunit / administration & dosage
  • Vaccines, Subunit / adverse effects
  • Vaccines, Subunit / genetics
  • Vaccines, Subunit / immunology
  • Xenograft Model Antitumor Assays

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, Neoplasm
  • BCAR3 protein, human
  • Cancer Vaccines
  • Guanine Nucleotide Exchange Factors
  • HLA-A*02:01 antigen
  • HLA-A2 Antigen
  • IRS2 protein, human
  • Insulin Receptor Substrate Proteins
  • Phosphopeptides
  • Vaccines, Subunit

Associated data

  • ClinicalTrials.gov/NCT01846143