Oral Presentation 24th Annual Lorne Proteomics Symposium 2019

Spliced HLA peptides, a novel source for immunotherapy (#10)

Pouya Faridi 1 , Patricia T. Illing 1 , Chen Li 1 , Sri H. Ramarathinam 1 , Julian P. Vivian 1 , Nicole A. Mifsud 1 , Rochelle Ayala 1 , Jiangning Song 1 , Linden J. Gearing 2 , Nicola Ternette 3 , Jamie Rossjohn 1 , Katherine Woods 4 , Ralf Schittenhelm 1 , Andreas Behren 4 , Nathan P. Croft 1 , Anthony W. Purcell 1
  1. Infection and Immunity Program, Biomedicine Discovery Institute & Department of Biochemistry and Molecular Biology, Monash University, Melbourne, VIC, Australia
  2. Centre for Innate Immunity and Infectious Diseases, Hudson Institute of Medical Research and Department of Molecular and Translational Science, School of Clinical Science, Monash University, Melbourne, Victoria, Australia
  3. Jenner Institute, University of Oxford, Oxford , UK
  4. Olivia Newton-John Cancer Research Institute, Melbourne, Australia

Human leukocyte antigen class I (HLA-I) molecules sample the proteome following the degradation of intracellular proteins via the proteasome and other proteolytic mechanisms. These complexes of HLA-I and peptide (pHLA) are then recognized by T cells and the nature of the bound peptide ligand is the key driver of adaptive immunity. We have developed a sophisticated data-driven workflow for the identification of distal and proximal cis-spliced as well as trans-spliced (where distinct proteins contribute peptide segments) peptide antigens. We have shown for 17 different monoallelic cell lines, that up to 40% of pHLA are generated through post-translational splicing mechanisms. We also found that spliced peptides display canonical HLA-binding sequence features (1). To understand the biological relevance of spliced peptides, we have interrogated the immunopeptidome of HLA-I molecules immunoaffinity purified from influenza-infected cells using LC-MS/MS and the novel bioinformatic pipeline. We have found around 42% of influenza derived p-HLAs (83 out of 198 peptides) are spliced peptides. We have also applied our approach to p-HLA derived from melanoma cell lines and identified 38766 peptides of which 6% were cis-spliced and 21% trans-spliced. Of note, more than more 100 spliced peptides were derived from melanoma-associated antigens (MAA) and ~40% of known MAA were only represented by spliced peptides. Immunogenicity studies of a subset of the MAA shown that multiple of the tested spliced peptides were highly immunogenic, compared to a smaller fraction of linear peptides. Our results highlight the complexity and diversity of HLA peptide antigen presentation and identify a mechanism whereby the available peptidome is diversified to enhance immunity. We found spliced peptides may yield more immunogenic epitopes than are available from the viral/cancer genome. Moreover, some antigens lack high-affinity HLA-ligands and the peptide splicing mechanism can generate higher affinity neoepitopes for interaction with host HLA allomorphs. Understanding the nature and abundance of spliced peptides has a high relevance for our understanding of potential novel targets of T cell immunity and will have significant implications for further immunotherapeutic approaches.

  1. P. Faridi et al., A subset of HLA-I peptides are not genomically templated: Evidence for cis- and trans-spliced peptide ligands. Science Immunology 3, (2018).