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Erschienen in: Cancer Immunology, Immunotherapy 9/2009

01.09.2009 | Original Article

HLA ligand profiles of primary renal cell carcinoma maintained in metastases

verfasst von: Juliane Sarah Stickel, Andreas O. Weinzierl, Nina Hillen, Oliver Drews, Mathias M. Schuler, Jörg Hennenlotter, Dorothee Wernet, Claudia A. Müller, Arnulf Stenzl, Hans-Georg Rammensee, Stefan Stevanović

Erschienen in: Cancer Immunology, Immunotherapy | Ausgabe 9/2009

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Abstract

In recent years, several approaches have been taken in the peptide-based immunotherapy of metastatic renal cell carcinoma (RCC), although little is known about HLA presentation on metastases compared to primary tumor and normal tissue of RCC. In this study we compared primary tumor, normal tissue and metastases with the aim of identifying similarities and differences between these tissues. We performed this comparison for two RCC patients on the level of the HLA ligandome using mass spectrometry and for three patients on the level of the transcriptome using oligonucleotide microarrays. The quantitative results show that primary tumor is more similar to metastasis than to normal tissue, both on the level of HLA ligand presentation and mRNA. We were able to characterize a total of 142 peptides in the qualitative analysis of HLA-presented peptides. Six of them were significantly overpresented on metastasis, among them a peptide derived from CD151; fourteen were overpresented on both primary tumor and metastasis compared to normal tissue, among them an HLA ligand derived from tumor protein p53. Thus, we could demonstrate that peptide-based immunotherapy might affect tumor as well as metastasis of RCC, but not healthy kidney tissue. Furthermore we were able to identify several peptides derived from tumor-associated antigens that are suitable for vaccination of metastatic RCC.
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Literatur
1.
Zurück zum Zitat Ang J, Lijovic M, Ashman LH, Kan K, Frauman AG (2004) CD151 protein expression predicts the clinical outcome of low grade primary prostate cancer better than histological grading: a new prognostic indicator? Cancer Epidemiol Biomarkers Prev 13:1717–1721PubMed Ang J, Lijovic M, Ashman LH, Kan K, Frauman AG (2004) CD151 protein expression predicts the clinical outcome of low grade primary prostate cancer better than histological grading: a new prognostic indicator? Cancer Epidemiol Biomarkers Prev 13:1717–1721PubMed
2.
Zurück zum Zitat Brossart P (2002) Dendritic cells in vaccination therapies of malignant diseases. Transfus Apher Sci 27:183–186PubMedCrossRef Brossart P (2002) Dendritic cells in vaccination therapies of malignant diseases. Transfus Apher Sci 27:183–186PubMedCrossRef
3.
Zurück zum Zitat Burgarolas J (2007) Renal cell carcinoma molecular pathways and therapies. N Engl J Med 356:185–187CrossRef Burgarolas J (2007) Renal cell carcinoma molecular pathways and therapies. N Engl J Med 356:185–187CrossRef
4.
Zurück zum Zitat Costa LJ, Drabkin HA (2007) Renal cell carcinoma: new developments in molecular biology and potential for targeted therapies. Oncologist 12:1404–1415PubMedCrossRef Costa LJ, Drabkin HA (2007) Renal cell carcinoma: new developments in molecular biology and potential for targeted therapies. Oncologist 12:1404–1415PubMedCrossRef
5.
Zurück zum Zitat DeMulder PH, van Herpen CM, Mulders PA (2004) Current treatment of renal cell carcinoma. Ann Oncol Suppl 4:19–28 DeMulder PH, van Herpen CM, Mulders PA (2004) Current treatment of renal cell carcinoma. Ann Oncol Suppl 4:19–28
6.
Zurück zum Zitat Falk K, Rötzschke O, Stevanovic S, Jung G, Rammensee HG (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351:290–296PubMedCrossRef Falk K, Rötzschke O, Stevanovic S, Jung G, Rammensee HG (1991) Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351:290–296PubMedCrossRef
7.
Zurück zum Zitat Glaspy JA (2002) Therapeutic options in the management of renal cell carcinoma. Semin Oncol 29:41–46PubMedCrossRef Glaspy JA (2002) Therapeutic options in the management of renal cell carcinoma. Semin Oncol 29:41–46PubMedCrossRef
8.
Zurück zum Zitat Gouttefangeas C, Stenzl A, Stevanovic S, Rammensee HG (2007) Immunotherapy of renal cell carcinoma. Cancer Immunol Immunother 56:117–128PubMedCrossRef Gouttefangeas C, Stenzl A, Stevanovic S, Rammensee HG (2007) Immunotherapy of renal cell carcinoma. Cancer Immunol Immunother 56:117–128PubMedCrossRef
9.
Zurück zum Zitat Haitel A, Wiener HG, Beathge U, Marberger M, Susani M (2000) mdm2 expression as a prognostic indicator in clear cell renal cell carcinoma: comparison with p53 overexpression and clinicopathological parameters. Clin Cancer Res 6:1840–1844PubMed Haitel A, Wiener HG, Beathge U, Marberger M, Susani M (2000) mdm2 expression as a prognostic indicator in clear cell renal cell carcinoma: comparison with p53 overexpression and clinicopathological parameters. Clin Cancer Res 6:1840–1844PubMed
10.
Zurück zum Zitat Hashida H, Takobayashi A, Tokuhara T, Hatton N, Taki T, Haseqawa H, Satoh S, Kobayashi N, Yamaoka Y, Miyake M (2003) Clinical significance of transmembrane 4 superfamily in colon cancer. Br J Cancer 89:158–167PubMedCrossRef Hashida H, Takobayashi A, Tokuhara T, Hatton N, Taki T, Haseqawa H, Satoh S, Kobayashi N, Yamaoka Y, Miyake M (2003) Clinical significance of transmembrane 4 superfamily in colon cancer. Br J Cancer 89:158–167PubMedCrossRef
11.
Zurück zum Zitat Jones J, Out H, Spentzos D, Kolia S, Inan M, Beecken WD, Fellbaum C, Gu X, Joseph M, Pantuck AJ, Jonas D, Libermann TA (2005) Gene signature of progression and metastasis in renal cell cancer. Clin Cancer Res 11:5730–5739PubMedCrossRef Jones J, Out H, Spentzos D, Kolia S, Inan M, Beecken WD, Fellbaum C, Gu X, Joseph M, Pantuck AJ, Jonas D, Libermann TA (2005) Gene signature of progression and metastasis in renal cell cancer. Clin Cancer Res 11:5730–5739PubMedCrossRef
12.
Zurück zum Zitat Kohno M, Haseqawa H, Miyake M, Yamamoto T, Fujita S (2002) CD151 enhances cell motility and metastasis of cancer cells in the presence of focal adhesion kinase. Int J Cancer 97:336–343PubMedCrossRef Kohno M, Haseqawa H, Miyake M, Yamamoto T, Fujita S (2002) CD151 enhances cell motility and metastasis of cancer cells in the presence of focal adhesion kinase. Int J Cancer 97:336–343PubMedCrossRef
13.
Zurück zum Zitat Krüger T, Schoor O, Lemmel C, Kraemer B, Reichle C, Dengjel J, Weinschenk T, Müller M, Hennenlotter J, Stenzl A, Rammensee HG, Stevanovic S (2005) Lessons to be learned from primary renal cell carcinomas: novel tumor antigens and HLA ligands for immunotherapy. Cancer Immunol Immunother 54:826–836PubMedCrossRef Krüger T, Schoor O, Lemmel C, Kraemer B, Reichle C, Dengjel J, Weinschenk T, Müller M, Hennenlotter J, Stenzl A, Rammensee HG, Stevanovic S (2005) Lessons to be learned from primary renal cell carcinomas: novel tumor antigens and HLA ligands for immunotherapy. Cancer Immunol Immunother 54:826–836PubMedCrossRef
14.
15.
Zurück zum Zitat Lemmel C, Weik S, Eberle U, Dengjel J, Kratt T, Becker HD, Rammensee HG, Stevanovic S (2004) Differential quantitative analysis of MHC ligands by mass spectrometry using stable isotope labeling. Nat Biotechnol 22:450–454PubMedCrossRef Lemmel C, Weik S, Eberle U, Dengjel J, Kratt T, Becker HD, Rammensee HG, Stevanovic S (2004) Differential quantitative analysis of MHC ligands by mass spectrometry using stable isotope labeling. Nat Biotechnol 22:450–454PubMedCrossRef
16.
Zurück zum Zitat Mombini H, Givi M, Rashidi I (2006) Relationship between expression of p53 protein and tumor subtype and grade in renal cell carcinoma. Urol J 3:79–81PubMed Mombini H, Givi M, Rashidi I (2006) Relationship between expression of p53 protein and tumor subtype and grade in renal cell carcinoma. Urol J 3:79–81PubMed
17.
18.
Zurück zum Zitat Pomara G, Salinitri G, Nesi G, Maio E, Minervini A, Gammazza AM, Francesca T, Cappello F, Selli C (2008) p53 and Ki-67 expression in renal cell carcinoma of pregnant women and their correlation with prognosis: a pilot study. Int J Gynecol 18:132–135CrossRef Pomara G, Salinitri G, Nesi G, Maio E, Minervini A, Gammazza AM, Francesca T, Cappello F, Selli C (2008) p53 and Ki-67 expression in renal cell carcinoma of pregnant women and their correlation with prognosis: a pilot study. Int J Gynecol 18:132–135CrossRef
19.
Zurück zum Zitat Rammensee HG, Weinschenk T, Gouttefangeas C, Stevanovic S (2002) Towards patient-specific tumor antigen selection for vaccination. Immunol Rev 188:164–176PubMedCrossRef Rammensee HG, Weinschenk T, Gouttefangeas C, Stevanovic S (2002) Towards patient-specific tumor antigen selection for vaccination. Immunol Rev 188:164–176PubMedCrossRef
20.
Zurück zum Zitat Schmidt SM, Schag K, Müller MR, Weinschenk T, Appel S, Schoor O, Weck MM, Grünebach F, Kanz L, Stevanovic S, Rammensee HG, Brossart P (2004) Induction of adipophilin-specific cytotoxic T lymphocytes using a novel HLA-A2-binding peptide that mediates tumor cell lysis. Cancer Res 64:1164–1170PubMedCrossRef Schmidt SM, Schag K, Müller MR, Weinschenk T, Appel S, Schoor O, Weck MM, Grünebach F, Kanz L, Stevanovic S, Rammensee HG, Brossart P (2004) Induction of adipophilin-specific cytotoxic T lymphocytes using a novel HLA-A2-binding peptide that mediates tumor cell lysis. Cancer Res 64:1164–1170PubMedCrossRef
21.
Zurück zum Zitat Stevanovic S (2002) Identification of tumor-associated T-cell epitopes for vaccine development. Nat Rev Cancer 2:514–520PubMedCrossRef Stevanovic S (2002) Identification of tumor-associated T-cell epitopes for vaccine development. Nat Rev Cancer 2:514–520PubMedCrossRef
22.
Zurück zum Zitat Testa JE, Brooks PC, Lin JM, Quiqley JP (1999) Eukaryotic expression cloning with an antimetastatic monoclonal antibody identifies a tetraspanin (PETA-3/CD151) as an effector of human tumor cell migration and metastasis. Cancer Res 59:3812–3820PubMed Testa JE, Brooks PC, Lin JM, Quiqley JP (1999) Eukaryotic expression cloning with an antimetastatic monoclonal antibody identifies a tetraspanin (PETA-3/CD151) as an effector of human tumor cell migration and metastasis. Cancer Res 59:3812–3820PubMed
23.
Zurück zum Zitat Tokuhara T, Haseqawa H, Hatton N, Ishida H, Taki T, Tachibana S, Sasaki S, Miyake M (2001) Clinical significance of CD151 gene expression in non-small cell lung cancer. Clin Cancer Res 7:4109–4114PubMed Tokuhara T, Haseqawa H, Hatton N, Ishida H, Taki T, Tachibana S, Sasaki S, Miyake M (2001) Clinical significance of CD151 gene expression in non-small cell lung cancer. Clin Cancer Res 7:4109–4114PubMed
24.
Zurück zum Zitat Uzunlar AK, Sahin H, Yilmaz F, Ozekinci S (2005) Expression of p53 oncoprotein and bcl-2 in renal cell carcinoma. Saudi Med J 26:37–41PubMed Uzunlar AK, Sahin H, Yilmaz F, Ozekinci S (2005) Expression of p53 oncoprotein and bcl-2 in renal cell carcinoma. Saudi Med J 26:37–41PubMed
26.
Zurück zum Zitat Wang L, Zhu JS, Song MQ, Chen GQ, Chen JL (2006) Comparison of gene expression profiles between primary tumor and metastatic lesions in gastric cancer patients using laser microdissection and cDNA microarray. World J Gastroenerol 12:6949–6954 Wang L, Zhu JS, Song MQ, Chen GQ, Chen JL (2006) Comparison of gene expression profiles between primary tumor and metastatic lesions in gastric cancer patients using laser microdissection and cDNA microarray. World J Gastroenerol 12:6949–6954
27.
Zurück zum Zitat Warburton HE, Brady M, Vlathovic N, Lenihan WM, Parsons K, Boyd MT (2005) p53 regulation and function in renal cell carcinoma. Cancer Res 65:6498–6503PubMedCrossRef Warburton HE, Brady M, Vlathovic N, Lenihan WM, Parsons K, Boyd MT (2005) p53 regulation and function in renal cell carcinoma. Cancer Res 65:6498–6503PubMedCrossRef
28.
Zurück zum Zitat Weidanz JA, Nguyen T, Woodburn T, Neethling FA, Chiriva-Internati M, Hildebrand WH, Lustgarten J (2006) Levels of specific peptide-HLA class I complex predicts tumor cell susceptibility to CTL killing. J Immunol 177:5088–5097PubMed Weidanz JA, Nguyen T, Woodburn T, Neethling FA, Chiriva-Internati M, Hildebrand WH, Lustgarten J (2006) Levels of specific peptide-HLA class I complex predicts tumor cell susceptibility to CTL killing. J Immunol 177:5088–5097PubMed
29.
Zurück zum Zitat Weigelt B, Glas A, Wessels LF, Witteveen AT, Peterse JL, van`t Veer LJ (2003) Gene expression profiles of primary breast tumor maintained in distant metastases. Proc Natl Acad Sci USA 100:15901–15905PubMedCrossRef Weigelt B, Glas A, Wessels LF, Witteveen AT, Peterse JL, van`t Veer LJ (2003) Gene expression profiles of primary breast tumor maintained in distant metastases. Proc Natl Acad Sci USA 100:15901–15905PubMedCrossRef
30.
Zurück zum Zitat Weinschenk T, Gouttefangeas C, Schirle M, Obermayr F, Walter S, Schoor O, Kurek R, Loeser W, Bichler KH, Wernet D, Stevanovic S, Rammensee HG (2002) Integrated functional genomics approach for the design of patient-individual antitumor vaccines. Cancer Res 62:5818–5827PubMed Weinschenk T, Gouttefangeas C, Schirle M, Obermayr F, Walter S, Schoor O, Kurek R, Loeser W, Bichler KH, Wernet D, Stevanovic S, Rammensee HG (2002) Integrated functional genomics approach for the design of patient-individual antitumor vaccines. Cancer Res 62:5818–5827PubMed
31.
Zurück zum Zitat Weinzierl AO, Lemmel C, Schoor O, Müller M, Krüger T, Wernet D, Hennenlotter J, Stenzl A, Klingel K, Rammensee HG, Stevanovic S (2007) Distorted relation between mRNA copy number and corresponding major histocompatibility complex ligand density on the cell surface. Moll Cell Proteomics 6:102–113CrossRef Weinzierl AO, Lemmel C, Schoor O, Müller M, Krüger T, Wernet D, Hennenlotter J, Stenzl A, Klingel K, Rammensee HG, Stevanovic S (2007) Distorted relation between mRNA copy number and corresponding major histocompatibility complex ligand density on the cell surface. Moll Cell Proteomics 6:102–113CrossRef
32.
Zurück zum Zitat Weinzierl AO, Maurer D, Altenberend F, Schneiderhan-Marra N, Klingel K, Schoor O, Wernet D, Joos T, Rammensee HG, Stevanović S (2008) A cryptic vascular endothelial growth factor T-cell epitope: identification and characterization by mass spectrometry and T-cell assays. Cancer Res 68:2447–2454PubMedCrossRef Weinzierl AO, Maurer D, Altenberend F, Schneiderhan-Marra N, Klingel K, Schoor O, Wernet D, Joos T, Rammensee HG, Stevanović S (2008) A cryptic vascular endothelial growth factor T-cell epitope: identification and characterization by mass spectrometry and T-cell assays. Cancer Res 68:2447–2454PubMedCrossRef
33.
Zurück zum Zitat Wierecky J, Müller MR, Wirths S, Halder-Oehler E, Dörfel D, Schmidt SM, Häntschel M, Brugger W, Schröder S, Horger MS, Kanz L, Brossart P (2006) Immunologic and clinical responses after vaccinations with peptide-pulsed dendritic cells in metastatic renal cancer patients. Cancer Res 66:5910–5918PubMedCrossRef Wierecky J, Müller MR, Wirths S, Halder-Oehler E, Dörfel D, Schmidt SM, Häntschel M, Brugger W, Schröder S, Horger MS, Kanz L, Brossart P (2006) Immunologic and clinical responses after vaccinations with peptide-pulsed dendritic cells in metastatic renal cancer patients. Cancer Res 66:5910–5918PubMedCrossRef
34.
Zurück zum Zitat Yanez-Mo M, Alfranca A, Cabanas C, Marazuela M, Tejedor R, Ursa MA, Ashman LK, de Landazuri MO, Sanchez-Madrid F (1998) Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA1 and CD151/PETA-3 with alpha3beta1 integrin localized at endothelial lateral junctions. J Cell Biol 141:791–804PubMedCrossRef Yanez-Mo M, Alfranca A, Cabanas C, Marazuela M, Tejedor R, Ursa MA, Ashman LK, de Landazuri MO, Sanchez-Madrid F (1998) Regulation of endothelial cell motility by complexes of tetraspan molecules CD81/TAPA1 and CD151/PETA-3 with alpha3beta1 integrin localized at endothelial lateral junctions. J Cell Biol 141:791–804PubMedCrossRef
35.
Zurück zum Zitat Yao M, Tabuchi H, Nagashima Y, Baba M, Nakaiqawa N, Ishquro H, Hamada K, Inayama Y, Kishida T, Hatton K, Yamada-Okatse H, Kubotaya Y (2005) Gene expression analysis of renal cell carcinoma: adipose differentiation related protein as a potential diagnostic and prognostic biomarker for clear-cell renal carcinoma. J Pathol 205:377–387PubMedCrossRef Yao M, Tabuchi H, Nagashima Y, Baba M, Nakaiqawa N, Ishquro H, Hamada K, Inayama Y, Kishida T, Hatton K, Yamada-Okatse H, Kubotaya Y (2005) Gene expression analysis of renal cell carcinoma: adipose differentiation related protein as a potential diagnostic and prognostic biomarker for clear-cell renal carcinoma. J Pathol 205:377–387PubMedCrossRef
36.
Zurück zum Zitat Zigeuner R, Ratschek M, Rehak P, Schips L, Langner C (2004) Value of p53 as a prognostic marker in histologic subtypes of renal cell carcinoma: a systematic analysis of primary and metastatic tumor tissue. Urology 63:651–655PubMedCrossRef Zigeuner R, Ratschek M, Rehak P, Schips L, Langner C (2004) Value of p53 as a prognostic marker in histologic subtypes of renal cell carcinoma: a systematic analysis of primary and metastatic tumor tissue. Urology 63:651–655PubMedCrossRef
37.
Zurück zum Zitat Zöller M (2006) Gastrointestinal tumor: metastasis and tetraspanins. Z Gastroenterol 44:573–586PubMedCrossRef Zöller M (2006) Gastrointestinal tumor: metastasis and tetraspanins. Z Gastroenterol 44:573–586PubMedCrossRef
Metadaten
Titel
HLA ligand profiles of primary renal cell carcinoma maintained in metastases
verfasst von
Juliane Sarah Stickel
Andreas O. Weinzierl
Nina Hillen
Oliver Drews
Mathias M. Schuler
Jörg Hennenlotter
Dorothee Wernet
Claudia A. Müller
Arnulf Stenzl
Hans-Georg Rammensee
Stefan Stevanović
Publikationsdatum
01.09.2009
Verlag
Springer-Verlag
Erschienen in
Cancer Immunology, Immunotherapy / Ausgabe 9/2009
Print ISSN: 0340-7004
Elektronische ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-008-0655-6

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