Efficient Identification of Novel Hla-A*0201-Presented Cytotoxic T Lymphocyte Epitopes in the Widely Expressed Tumor Antigen Prame by Proteasome-Mediated Digestion Analysis

doi:10.1084/jem.193.1.73

Published online 1 January 2001.

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© The Rockefeller University Press, 0022-1007/2001/1/73/ $5.00
The Journal of Experimental Medicine, Volume 193, Number 1, January 1, 2001 73-88

Original Article

Efficient Identification of Novel Hla-A*0201–Presented Cytotoxic T Lymphocyte Epitopes in the Widely Expressed Tumor Antigen Prame by Proteasome-Mediated Digestion Analysis

Jan H. Kessler^a, Nico J. Beekman^a, Sandra A. Bres-Vloemans^a, Pauline Verdijk^a, Peter A. van Veelen^a, Antoinette M. Kloosterman-Joosten^a, Debby C.J. Vissers^a, George J.A. ten Bosch^a, Michel G.D. Kester^a, Alice Sijts^b, Jan Wouter Drijfhout^a, Ferry Ossendorp^a, Rienk Offringa^a, and Cornelis J.M. Melief^a

^a Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, 2300 RC Leiden, The Netherlands
^b Institute of Biochemistry, Charité, Humboldt University, D-10117 Berlin, Germany
Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Building 1: E3-Q, P.O. Box 9600, 2300 RC Leiden, The Netherlands.31-71-521-675131-71-526-1671

kesslerj{at}worldonline.nl

We report the efficient identification of four human histocompatibilityleukocyte antigen (HLA)-A*0201–presented cytotoxic T lymphocyte(CTL) epitopes in the tumor-associated antigen PRAME using animproved "reverse immunology" strategy. Next to motif-basedHLA-A*0201 binding prediction and actual binding and stabilityassays, analysis of in vitro proteasome-mediated digestionsof polypeptides encompassing candidate epitopes was incorporatedin the epitope prediction procedure. Proteasome cleavage patternanalysis, in particular determination of correct COOH-terminalcleavage of the putative epitope, allows a far more accurateand selective prediction of CTL epitopes. Only 4 of 19 highaffinity HLA-A*0201 binding peptides (21%) were found to beefficiently generated by the proteasome in vitro. This approachavoids laborious CTL response inductions against high affinitybinding peptides that are not processed and limits the numberof peptides to be assayed for binding. CTL clones induced againstthe four identified epitopes (VLDGLDVLL, PRA^100–108; SLYSFPEPEA,PRA^142–151; ALYVDSLFFL, PRA^300–309; and SLLQHLIGL,PRA^425–433) lysed melanoma, renal cell carcinoma, lungcarcinoma, and mammary carcinoma cell lines expressing PRAMEand HLA-A*0201. This indicates that these epitopes are expressedon cancer cells of diverse histologic origin, making them attractivetargets for immunotherapy of cancer.

Key Words: antigen presentation • antigen processing • cytotoxic T lymphocyte induction • human histocompatibility leukocyte antigen class I binding • tumor immunotherapy

Abbreviations used in this paper: aa, amino acid; B-LCL, B lymphoblastoidcell line; DC, dendritic cell; ER, endoplasmic reticulum; FI,fluorescence index; FL, fluorescein; HBV, hepatitis B virus;MS, mass spectrometry; RT, reverse transcription; TAP, transporter-associatedwith antigen processing.

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