PRAME as a Potential Target for Immunotherapy in Metastatic Uveal Melanoma

JAMA Ophthalmol. 2017 Jun 1;135(6):541-549. doi: 10.1001/jamaophthalmol.2017.0729.

Abstract

Importance: Uveal melanoma (UM) is an intraocular primary malignant neoplasm that often gives rise to metastatic disease for which there are no effective therapies. A substantial proportion of UMs express the cancer-testis antigen PRAME (preferentially expressed antigen in melanoma), which can potentially be targeted by adoptive T-cell therapy.

Objective: To determine whether there may be a rationale for PRAME-directed T-cell therapy for metastatic UM.

Design, setting, and participants: An experimental study using a retrospective cohort of 64 patients with UM (median follow-up, 62 months) was conducted from January 8, 2015, to November 20, 2016, at the Leiden University Medical Center. Clinical, histopathologic, and genetic parameters were compared between 64 PRAME-positive and PRAME-negative UMs. HLA class I restricted, PRAME-specific T cells were stimulated with UM cell lines to measure their antigen-specific reactivity against these cell lines, which were analyzed for PRAME expression by real-time quantitative polymerase chain reaction. Uveal melanoma metastases from 16 unrelated patients were assessed for PRAME expression by messenger RNA fluorescence in situ hybridization and for HLA class I expression by immunofluorescence staining.

Main outcomes and measures: Interferon γ production for antigen-specific reactivity and detection of PRAME and HLA class I expression in primary and metastatic UM.

Results: Of the 64 patients in the study (31 women and 33 men; mean [SD] age at the time of enucleation, 60.6 [15.6] years), PRAME expression was negative in 35 primary UMs and positive in 29 primary UMs. Positive PRAME expression was associated with a high largest basal diameter (15.0 vs 12.0 mm; P = .005), ciliary body involvement (59% vs 26%; P = .008), and amplification of chromosome 8q (66% vs 23%; P = .002). PRAME-specific T cells reacted against 4 of 7 UM cell lines, demonstrating that T-cell reactivity correlated with PRAME expression. Metastatic UM samples were positive for PRAME messenger RNA in 11 of 16 patients and for HLA class I in 10 of 16 patients, with 8 of 16 patients demonstrating coexpression of both PRAME and HLA class I.

Conclusions and relevance: PRAME is expressed in many primary and metastatic UMs, and about half of the metastatic UMs coexpress PRAME and HLA class I. The finding that PRAME-specific T cells in this study reacted against PRAME-positive UM cell lines suggests a potential role for PRAME-directed immunotherapy for selected patients with metastatic UM.

Publication types

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

MeSH terms

  • Antigens, Neoplasm / biosynthesis
  • Antigens, Neoplasm / genetics*
  • Biomarkers, Tumor / biosynthesis
  • Biomarkers, Tumor / genetics
  • Cell Line, Tumor
  • DNA, Neoplasm / genetics*
  • Female
  • Follow-Up Studies
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Immunotherapy / methods*
  • In Situ Hybridization, Fluorescence
  • Male
  • Melanoma / genetics*
  • Melanoma / secondary
  • Melanoma / therapy
  • Middle Aged
  • Neoplasm Metastasis
  • Retrospective Studies
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Time Factors
  • Uveal Neoplasms / genetics*
  • Uveal Neoplasms / secondary
  • Uveal Neoplasms / therapy

Substances

  • Antigens, Neoplasm
  • Biomarkers, Tumor
  • DNA, Neoplasm
  • PRAME protein, human

Supplementary concepts

  • Uveal melanoma