Analysis of the HLA class I immunopeptidome in health and in cancer
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1 Research Collection Doctoral Thesis Analysis of the HLA class I immunopeptidome in health and in cancer Author(s): Gloger, Andreas Publication Date: 2016 Permanent Link: This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library
2 DISS. ETH NO Analysis of the HLA class I immunopeptidome in health and in cancer A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) Presented by Andreas Gloger Diplom Biologe (Dipl.Biol.) born on citizen of Germany Accepted on the recommendation of Prof. Dr. Dario Neri, examiner Prof. Dr. Cornelia Halin Winter, co-examiner 2016
3 1. Summary Human leukocyte antigen class I (HLA class I) molecules are protein complexes that present peptides from the cytosolic degradation of proteins on the surface of virtually all nucleated cells in the human body. The entirety of peptides presented on HLA class I molecules is termed the HLA class I peptidome or immunopeptidome. Cytotoxic T lymphocytes, cells of the adaptive immune system, can bind through their T cell receptors to HLA class I proteins in complex with suitable peptides. This recognition event is biased towards peptides, which are not present in normal tissues ( non self ), such as viral antigens and mutated peptides in cancer. By this mechanism, T cells are able to combat intracellular pathogens and cancer. In this thesis, we analyzed the HLA class I peptidome of cancer cell lines as well as peptides bound to soluble HLA (shla) class I molecules in the plasma of healthy donors and patients with metastatic melanoma using a combination of immune capturing and mass spectrometry (MS). In the MS analysis of the immunopeptidome of cancer cell lines we were able to refine and further develop experimental methodologies, leading to high confidence identification of thousands of HLA class I-bound peptides. In addition, the identification of hundreds of HLA peptides from the serum of melanoma patients helped to shed light on the shla immunopeptidome in cancer, revealing the presence of peptides originating from melanoma-associated antigens. The HLA class I peptidome analysis of melanoma cell lines and of patients sera allowed the compilation of an extensive list of HLA bound peptides. This list included prominent previously identified T cell epitopes, as well as peptides from melanoma-associated antigens which had not been described before. In addition, by utilizing publically available exome sequencing data we could 5
4 identify one so called neo-epitope, an HLA bound peptide originating from a mutated protein, via mass spectrometry. This observation suggests that neo-epitopes are indeed presented on HLA class I molecules, albeit at low frequency. Lastly, by extending our analysis to blood sera and plasma of healthy donors, we could improve the existing methodologies, leading to high confidence peptide identification of ~ peptides per sample. This refined and simplified procedure may be routinely used for the profiling of cancer patients, potentially serving as biomarker for the prediction of response to therapy. 2. Zusammenfassung Moleküle des humanen Leukozytenantigens der Klasse I (HLA Klasse I) sind Proteinkomplexe, die Peptide aus der zytosolischen Degradation von Proteinen auf der Oberfläche von beinahe allen kernhaltigen Zellen des menschlichen Körpers präsentieren. Die Gesamtheit aller auf HLA Klasse I präsentierten Peptide bezeichnet man als das HLA Klasse I Peptidom oder Immuno- Peptidom. Zytotoxische T Lymphozyten, Zellen des adaptiven Immunsystems, können durch ihren T-Zell-Rezeptor den Komplex aus HLA Klasse I Proteinen und den darauf präsentierten Peptiden binden. Dieser Prozess hat eine Tendenz dazu, Peptide zu erkennen, die im Normalfall nicht in gesunden Geweben präsentiert werden, wie z.b. virale Antigene oder mutierte Peptide in Krebserkrankungen. Durch ebendiesen Mechanismus sind T Zellen in der Lage intrazelluläre Krankheitserreger sowie Krebserkrankungen zu bekämpfen. In dieser Doktorarbeit analysierten wir HLA Klasse I Peptidome von Krebszelllinien sowie Peptide von löslichen HLA Klasse I Molekülen (shla, von engl.: soluble) aus dem Blutplasma und Blutserum von gesunden Spendern und Patienten mit metastasierenden Melanomen mit Hilfe einer Kombination aus 6
5 Immuno-Affinitäts-Chromatographie und Massenspektrometrie (MS). In der MS-Analyse von Immunopeptidomen von Krebs-Zelllinien konnte es uns gelingen, durch von uns verbesserte und weiterentwickelte experimentelle Methoden tausende von HLA Klasse I gebundenen Peptiden mit hoher Zuverlässigkeit zu identifizieren. Zusätzlich verhalf die Identifikation von hunderten Peptiden aus den Blutseren von Melanom-Patienten bei der Aufklärung des shla Immunopeptidoms in Krebserkrankungen, wobei Peptide von Melanom-assoziierten Antigenen nachgewiesen werden konnten. Die HLA Klasse I Peptidom-analyse erlaubte es, eine ausführliche Liste von HLA Klasse I gebundenen Peptiden zusammenzustellen, welche sowohl aus der Literatur bekannte T-Zell-Epitope als auch bisher unbeschriebe Peptide von Melanom-assoziierten Antigenen enthielt. Zusätzlich konnten wir durch öffentlich zugängliche Exom-Sequenzdaten ein Peptid eines mutierten Proteins identifizieren. Diese Beobachtung legt nahe, dass Neo-Epitope tatsächlich von HLA Klasse I Moleküle präsentiert werden, jedoch in seltenen Fällen. Schlussendlich übertrugen wir unsere weiterentwickelten experimentellen Methoden auf die Analyse von Blutserum und -plasma, wobei wir zwei-, bis dreitausend Peptide mit hoher Zuverlässigkeit aus einzelnen Proben identifizieren konnten. Diese verbesserte und simplifizierte Verfahrensweise könnte routinemäßig für die Fallanalyse von Krebspatienten eingesetzt werden, wobei sie zur Identifizierung von Biomarkern zur Vorhersage des Therapieerfolgs genutzt werden könnte. 7
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