Database of T cell-defined human tumor antigens: the 2013 update
Nathalie Vigneron1,2, Vincent Stroobant1,2, Benoît J. Van den Eynde1,2, Pierre van der Bruggen1,2
1 Ludwig Institute for Cancer Research, Brussels Branch, Brussels, Belgium
2 WELBIO and de Duve Institute, Université catholique de Louvain, Brussels, Belgium
Address correspondence to: Pierre van der Bruggen, Ph.D., de Duve Institute, Université catholique de Louvain, and Ludwig Institute for Cancer Research, B1.74.03, Avenue Hippocrate 74, B-1200 Brussels, Belgium, Tel.: + 32 0 2 764 74 31, Fax: + 32 0 2 792 94 05, E-mail: email@example.com
Cancer Immunity (15 July 2013) Vol. 13, p. 15
© 2013 by Pierre van der Bruggen
Keywords: peptide, database, HLA, CD4, CD8, T cell
The plethora of tumor antigens that have been—and are still being—defined required systematization to provide a comprehensive overview of those tumor antigens that are the most relevant targets for cancer immunotherapy approaches. Here, we provide a new update of a peptide database resource that we initiated many years ago. This database compiles all human antigenic peptides described in the literature that fulfill a set of strict criteria needed to ascertain their actual “tumor antigen” nature, as we aim at guiding scientists and clinicians searching for appropriate cancer vaccine candidates (www.cancerimmunity.org/peptide). In this review, we revisit those criteria in light of recent findings related to antigen processing. We also introduce the 29 new tumor antigens that were selected for this 2013 update. Two of the new peptides show unusual features, which will be briefly discussed. The database now comprises a total of 403 tumor antigenic peptides.
A tumor antigen database
Since the discovery of the first human T cell defined-tumor antigen in 1991 (1), a growing number of tumor antigens have been described at a regular pace, with dozens of new antigenic peptides reported in the literature every year. In 2001, we started compiling what we think are the most relevant human tumor antigens and created a peptide database, which was posted on the Cancer Immunity website and was regularly updated (2). This tool was primarily designed to provide the scientific community with an open view of the nature and diversity of the tumor antigens available to date for cancer immunotherapy. We selected a classification of peptides based on their tumor specificity because we think it is the most critical factor determining their usefulness for cancer immunotherapy. A first distinction is made between unique antigens, generally derived from point mutations, and shared antigens. The shared antigens are further divided into tumor-specific antigens, differentiation antigens, and overexpressed antigens (3). Various tables are provided on the Cancer Immunity website, recapitulating the sequences of the peptides included in these categories, their position in the protein sequence, a GeneCard link for the encoding gene and/or the parent protein, the HLA presenting molecule and its frequency in Caucasians, the method used to isolate the cytolytic T lymphocyte (CTL) recognizing the antigen, and a PubMed link to the relevant reference. Of note, a number of viruses, such as the Epstein-Barr virus (EBV) and human papilloma virus (HPV), are associated with human malignancies. The antigenic peptides encoded by viral genes have not been included in the database, despite their high potential as targets for immunotherapy.
Inclusion criteria for the peptide database
Because we wanted the database to be useful to clinicians contemplating the development of immunotherapy trials, we included only the peptides that were fully validated, i.e., whose characterization was comprehensive and fully demonstrated the existence, nature, immunogenicity and, most importantly, the natural presentation of these antigenic peptides by tumor cells. Those candidate peptides whose comprehensive characterization was not reported were listed in an additional category of “potential peptides” awaiting further characterization.
The “validated peptides” we selected needed to meet the following six requirements:
1. Isolation of stable human T lymphocyte clones or lines recognizing the peptide
2. Identification of the peptide recognized by the T cells
3. Identification of the HLA presenting molecule
4. Evidence that the peptide is processed by tumor cells and presented to the specific CTL
This implies showing recognition of tumor cells expressing the relevant gene and HLA molecule by the T cells. When a polyclonal T cell line is used rather than a clone, it is essential to demonstrate that the CTLs that lyse the tumor cells are the same as those that recognize the peptide. This can be done by “cold target inhibition” experiments using peptide-pulsed cold targets (4). Other means of proof are also possible, such as the testing of stable transfectants of tumor cells with the sequence encoding the parental protein (5) or knocking down the gene encoding the peptide using siRNA or shRNA technology (6).
In some cases, unusual processing features of the peptide (e.g., by only some proteasome subtypes (7-12)) may explain the lack of recognition of some tumor cells by the CTLs, without precluding the “validation” of the peptide, provided it is explained.
When post-translational modifications are involved, characterization of the peptide should include elution of the peptide from the cell surface (13-16). Eluted fractions can then be tested for their ability to activate the CTLs. The CTL-sensitizing fraction should correspond to the fraction able to sensitize the CTLs when the synthetic peptide of interest is fractionated by HPLC in the exact same conditions. Alternatively, the presence of the peptide of interest in the CTL-sensitizing fraction could also be demonstrated by mass spectrometry.
In the case of CD4 T lymphocytes, which may not recognize tumor cells directly, the fact that the peptide is processed can be shown by testing antigen-presenting cells (APCs) loaded with the recombinant protein or a control protein produced in the same organism (17, 18), or loaded with lysates of cells transfected or not with the relevant coding sequence.
5. Report of a peptide sensitization assay
Characterization of peptides recognized by CD8 T cells should generally include the identification of the shortest peptide recognized and a titration showing a clear recognition of this peptide at doses below 1 µM. Putting together this update, we realized that in recent years, fewer investigators perform this control. In the case of peptides that were identified by the “reverse immunology approach” (an approach that consists in raising T cells against specific peptides corresponding to fragments of conventional proteins), we considered that the peptide titration curves might not be mandatory as the CTLs were directly obtained against the peptide of interest. However, we believe that peptide titration curves remain crucial in order to determine the most adequate immunotherapeutic vaccination modalities (cfr. the B*4402-restricted peptide MAGE-A1 KEADPTGHSY example below) and should therefore always be included when describing new potential vaccine candidates.
6. Description of the pattern of antigen expression
A certain level of tumor- or tissue-specificity should be documented, as ubiquitous antigens do not qualify as tumor antigens. This can be done with gene expression, protein expression, or lymphocyte recognition data, which should ideally be corroborative.
New relevant tumor antigens
Among 46 potentially relevant papers considered for the 2013 update, 29 antigens fulfilled the criteria described above and were therefore included in the database, while the other relevant peptides found in the 25 remaining papers did not meet all the requirements and were therefore included in the “potential antigens” list. Table 1 through Table 4 provides the list of new antigens that will be included in the updated database. Most of these peptides were identified using the reverse immunology approach (19), involving either a specific peptide or peptide libraries. The latter technology led, for example, to the mapping of two new antigenic peptides derived from cyclin-A1 and probably representing the most truly leukemia-specific epitopes identified so far (20). Although the reverse immunology approach proved efficient for the identification of many tumor antigens, it will hardly lead to the identification of peptides originating from unexpected events relative to transcription, translation, post-translational modifications or processing. Below, we describe two such peptides, which were included in this year’s update. These peptides were recognized by CTLs and tumor-infiltrating lymphocytes (TILs) raised against autologous tumors and show unexpected properties.
The B*4402-restricted peptide MAGE-A1 KEADPTGHSY
This antigenic peptide is very unusual in the sense that, although it is clearly encoded by MAGE-A1, processed endogenously, and presented by tumor cells, the corresponding synthetic peptide is unable to sensitize target cells to CTL recognition, unless pulsed on paraformaldehyde or acid-treated targets (21). This was shown to result from the lack of binding of the peptide on surface HLA-B*4402, which could originate from the low peptide-receptiveness of this tapasin-dependent HLA molecule. This study exemplifies the importance of doing a peptide titration curve when identifying a potential peptide vaccine candidate. Indeed, peptides such as this MAGE-A1 peptide, which can only be recognized at concentrations higher that 1 µM, might not be adequate to use in a classical synthetic peptide vaccine but might rather require vaccination modalities relying on endogenous presentation such as RNA- or DNA-based vaccines.
An antigenic peptide produced after reverse splicing and double asparagine deamidation
While peptides recognized by CTLs are generally derived from fragments of conventional proteins, an increasing variety of non-classical events were shown to contribute to the production of these peptides. Antigenic peptides were produced by the aberrant transcription of intronic or reverse strand sequences (22-25). Other peptides arise from the translation of alternative open-reading frames or pseudogenes (26-32). Peptides produced from post-translational modifications such as deamidation of asparagine residues (15, 33), serine/threonine phosphorylation (34, 35), or peptide splicing were also described (14, 16, 36, 37). One of the peptides added in the current release of the database was found, surprisingly, to combine several post-translational modifications (13). It is first composed of two tyrosinase fragments that are spliced in the reverse order to that in which they appear in the parental protein. In addition, each of the splicing partners contains an aspartic acid residue, originating from the post-translational conversion of a genetically encoded asparagine. Studying the processing of this usual peptide, Dalet et al. showed that it requires translation of tyrosinase into the endoplasmic reticulum (ER) and retrotranslocation into the cytosol, where the two asparagines are deglycosylated by peptide-N-glycanase, resulting in their conversion into aspartates by deamidation. This is followed by cleavage and splicing of the appropriate fragments by the standard proteasome, and further transport of the resulting peptide into the ER through the TAP transporter.
We intend to keep updating the database on a regular basis, as a service to the scientific community. We welcome any suggestions regarding the inclusion of other peptides, or the revision of some inclusion criteria or any other aspect of the database.
CTL, cytolytic T lymphocyte; TIL, tumor-infiltrating lymphocyte
N.V. is supported by a postdoctoral fellowship from the F.R.S.-FNRS.
- van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 1991; 254: 1643-1647. (PMID: 1840703)
- van der Bruggen P, Stroobant V, Vigneron N, Van den Eynde B. Peptide database: T cell-defined tumor antigens. Cancer Immun 2013. URL: http://www.cancerimmunity.org/peptide/
- Vigneron N, Van den Eynde BJ. Insights into the processing of MHC class I ligands gained from the study of human tumor epitopes. Cell Mol Life Sci 2011; 68: 1503-1520. (PMID: 21387143)
- Schultz ES, Lethé B, Cambiaso CL, Van Snick J, Chaux P, Corthals J, Heirman C, Thielemans K, Boon T, van der Bruggen P. A MAGE-A3 peptide presented by HLA-DP4 is recognized on tumor cells by CD4+ cytolytic T lymphocytes. Cancer Res 2000; 60: 6272-6275. (PMID: 11103782)
- Vigneron N, Ooms A, Morel S, Ma W, Degiovanni G, Van den Eynde B. A peptide derived from melanocytic protein gp100 and presented by HLA-B35 is recognized by autologous cytolytic T lymphocytes on melanoma cells. Tissue Antigens 2005; 65: 156-162. (PMID: 15713214)
- Tomita Y, Imai K, Senju S, Irie A, Inoue M, Hayashida Y, Shiraishi K, Mori T, Daigo Y, Tsunoda T, Ito T, Nomori H, Nakamura Y, Kohrogi H, Nishimura Y. A novel tumor-associated antigen, cell division cycle 45-like can induce cytotoxic T-lymphocytes reactive to tumor cells. Cancer Sci 2011; 102: 697-705. (PMID: 21231984)
- Vigneron N, Van den Eynde BJ. Proteasome subtypes and the processing of tumor antigens: increasing antigenic diversity. Curr Opin Immunol 2012; 24: 84-91. (PMID: 22206698)
- Ma W, Vigneron N, Chapiro J, Stroobant V, Germeau C, Boon T, Coulie PG, Van den Eynde BJ. A MAGE-C2 antigenic peptide processed by the immunoproteasome is recognized by cytolytic T cells isolated from a melanoma patient after successful immunotherapy. Int J Cancer 2011; 129: 2427-2434. (PMID: 21207413)
- Corbière V, Chapiro J, Stroobant V, Ma W, Lurquin C, Lethé B, van Baren N, Van den Eynde BJ, Boon T, Coulie PG. Antigen spreading contributes to MAGE vaccination-induced regression of melanoma metastases. Cancer Res 2011; 71: 1253-1262. (PMID: 21216894)
- Dalet A, Stroobant V, Vigneron N, Van den Eynde BJ. Differences in the production of spliced antigenic peptides by the standard proteasome and the immunoproteasome. Eur J Immunol 2011; 41: 39-46. (PMID: 21182075)
- Chapiro J, Claverol S, Piette F, Ma W, Stroobant V, Guillaume B, Gairin J-E, Morel S, Burlet-Schiltz O, Monsarrat B, Boon T, Van den Eynde B. Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J Immunol 2006; 176: 1053-1061. (PMID: 16393993)
- Guillaume B, Chapiro J, Stroobant V, Colau D, Van Holle B, Parvizi G, Bousquet-Dubouch MP, Theate I, Parmentier N, Van den Eynde BJ. Two abundant proteasome subtypes that uniquely process some antigens presented by HLA class I molecules. Proc Natl Acad Sci U S A 2010; 107: 18599-18604. (PMID: 20937868)
- Dalet A, Robbins PF, Stroobant V, Vigneron N, Li YF, El-Gamil M, Hanada K, Yang JC, Rosenberg SA, Van den Eynde BJ. An antigenic peptide produced by reverse splicing and double asparagine deamidation. Proc Natl Acad Sci U S A 2011; 108: E323-331. (PMID: 21670269)
- Vigneron N, Stroobant V, Chapiro J, Ooms A, Degiovanni G, Morel S, van der Bruggen P, Boon T, Van den Eynde B. An antigenic peptide produced by peptide splicing in the proteasome. Science 2004; 304: 587-590. (PMID: 15001714)
- Skipper JCA, Hendrickson RC, Gulden PH, Brichard V, Van Pel A, Chen Y, Shabanowitz J, Wölfel T, Slingluff CL Jr, Boon T, Hunt DF, Engelhard VH. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J Exp Med 1996; 183: 527-534. (PMID: 8627164)
- Hanada K, Yewdell JW, Yang JC. Immune recognition of a human renal cancer antigen through post-translational protein splicing. Nature 2004; 427: 252-256. (PMID: 14724640)
- Chaux P, Vantomme V, Stroobant V, Thielemans K, Corthals J, Luiten R, Eggermont AM, Boon T, van der Bruggen P. Identification of MAGE-3 epitopes presented by HLA-DR molecules to CD4+ T lymphocytes. J Exp Med 1999; 189: 767-777. (PMID: 10049940)
- Zarour HM, Storkus WJ, Brusic V, Williams E, Kirkwood JM. NY-ESO-1 encodes DRB1*0401-restricted epitopes recognized by melanoma-reactive CD4+ T cells. Cancer Res 2000; 60: 4946-4952. (PMID: 10987311)
- Boon T, van der Bruggen P. Human tumor antigens recognized by T lymphocytes. J Exp Med 1996; 183: 725-729. (PMID: 8642276)
- Ochsenreither S, Majeti R, Schmitt T, Stirewalt D, Keilholz U, Loeb KR, Wood B, Choi YE, Bleakley M, Warren EH, Hudecek M, Akatsuka Y, Weissman IL, Greenberg PD. Cyclin-A1 represents a new immunogenic targetable antigen expressed in acute myeloid leukemia stem cells with characteristics of a cancer-testis antigen. Blood 2012; 119: 5492-5501. (PMID: 22529286)
- Stroobant V, Demotte N, Luiten RM, Leonhardt RM, Cresswell P, Bonehill A, Michaux A, Ma W, Mulder A, Van den Eynde BJ, van der Bruggen P, Vigneron N. Inefficient exogenous loading of a tapasin-dependent peptide onto HLA-B*44:02 can be improved by acid treatment or fixation of target cells. Eur J Immunol 2012; 42: 1417-1428. (PMID: 22678898)
- Coulie PG, Lehmann F, Lethé B, Herman J, Lurquin C, Andrawiss M, Boon T. A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma. Proc Natl Acad Sci U S A 1995; 92: 7976-7980. (PMID: 7644523)
- Guilloux Y, Lucas S, Brichard VG, Van Pel A, Viret C, De Plaen E, Brasseur F, Lethé B, Jotereau F, Boon T. A peptide recognized by human cytolytic T lymphocytes on HLA-A2 melanomas is encoded by an intron sequence of the N-acetylglucosaminyltransferase V gene. J Exp Med 1996; 183: 1173-1183. (PMID: 8642259)
- Robbins PF, El-Gamil M, Li YF, Fitzgerald EB, Kawakami Y, Rosenberg SA. The intronic region of an incompletely spliced gp100 gene transcript encodes an epitope recognized by melanoma-reactive tumor-infiltrating lymphocytes. J Immunol 1997; 159: 303-308. (PMID: 9200467)
- Van den Eynde BJ, Gaugler B, Probst-Kepper M, Michaux L, Devuyst O, Lorge F, Weynants P, Boon T. A new antigen recognized by cytolytic T lymphocytes on a human kidney tumor results from reverse strand transcription. J Exp Med 1999; 190: 1793-1799. (PMID: 10601354)
- Probst-Kepper M, Stroobant V, Kridel R, Gaugler B, Landry C, Brasseur F, Cosyns J-P, Weynand B, Boon T, Van den Eynde BJ. An alternative open reading frame of the human macrophage colony-stimulating factor gene is independently translated and codes for an antigenic peptide of 14 amino acids recognized by tumor-infiltrating CD8 T lymphocytes. J Exp Med 2001; 193: 1189-1198. (PMID: 11369790)
- Malarkannan S, Horng T, Shih PP, Schwab S, Shastri N. Presentation of out-of-frame peptide/MHC class I complexes by a novel translation initiation mechanism. Immunity 1999; 10: 681-690. (PMID: 10403643)
- Wang R-F, Parkhurst MR, Kawakami Y, Robbins PF, Rosenberg SA. Utilization of an alternative open reading frame of a normal gene in generating a novel human cancer antigen. J Exp Med 1996; 183: 1131-1140. (PMID: 8642255)
- Ronsin C, Chung-Scott V, Poullion I, Aknouche N, Gaudin C, Triebel F. A non-AUG-defined alternative open reading frame of the intestinal carboxyl esterase mRNA generates an epitope recognized by renal cell carcinoma-reactive tumor-infiltrating lymphocytes in situ. J Immunol 1999; 163: 483-490. (PMID: 10384152)
- Godet Y, Moreau-Aubry A, Guilloux Y, Vignard V, Khammari A, Dreno B, Jotereau F, Labarrière N. MELOE-1 is a new antigen overexpressed in melanomas and involved in adoptive T cell transfer efficiency. J Exp Med 2008; 205: 2673-2682. (PMID: 18936238)
- Rosenberg SA, Tong-On P, Li Y, Riley JP, El-Gamil M, Parkhurst MR, Robbins PF. Identification of BING-4 cancer antigen translated from an alternative open reading frame of a gene in the extended MHC class II region using lymphocytes from a patient with a durable complete regression following immunotherapy. J Immunol 2002; 168: 2402-2407. (PMID: 11859131)
- Moreau-Aubry A, Le Guiner S, Labarrière N, Gesnel MC, Jotereau F, Breathnach R. A processed pseudogene codes for a new antigen recognized by a CD8(+) T cell clone on melanoma. J Exp Med 2000; 191: 1617-1624. (PMID: 10790436)
- Selby M, Erickson A, Dong C, Cooper S, Parham P, Houghton M, Walker CM. Hepatitis C virus envelope glycoprotein E1 originates in the endoplasmic reticulum and requires cytoplasmic processing for presentation by class I MHC molecules. J Immunol 1999; 162: 669-676. (PMID: 9916684)
- Zarling AL, Ficarro SB, White FM, Shabanowitz J, Hunt DF, Engelhard VH. Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. J Exp Med 2000; 192: 1755-1762. (PMID: 17001009)
- Zarling AL, Polefrone JM, Evans AM, Mikesh LM, Shabanowitz J, Lewis ST, Engelhard VH, Hunt DF. Identification of class I MHC-associated phosphopeptides as targets for cancer immunotherapy. Proc Natl Acad Sci U S A 2006; 103: 14889-14894. (PMID: 17001009)
- Warren EH, Vigneron NJ, Gavin MA, Coulie PG, Stroobant V, Dalet A, Tykodi SS, Xuereb SM, Mito JK, Riddell SR, Van den Eynde BJ. An antigen produced by splicing of noncontiguous peptides in the reverse order. Science 2006; 313: 1444-1447. (PMID: 16960008)
- Dalet A, Vigneron N, Stroobant V, Hanada K, Van den Eynde BJ. Splicing of distant peptide fragments occurs in the proteasome by transpeptidation and produces the spliced antigenic peptide derived from fibroblast growth factor-5. J Immunol 2010; 184: 3016-3024. (PMID: 20154207)
- Goodyear OC, Pearce H, Pratt G, Moss P. Dominant responses with conservation of T-cell receptor usage in the CD8+ T-cell recognition of a cancer testis antigen peptide presented through HLA-Cw7 in patients with multiple myeloma. Cancer Immunol Immunother 2011; 60: 1751-1761. (PMID: 21785964)
- Anderson LD Jr, Cook DR, Yamamoto TN, Berger C, Maloney DG, Riddell SR. Identification of MAGE-C1 (CT-7) epitopes for T-cell therapy of multiple myeloma. Cancer Immunol Immunother 2011; 60: 985-997. (PMID: 21461886)
- Wen W, Zhang L, Peng J, Chen J, Hao J, Li X, Qian X, Zeng P, Zhang Y, Yin Y. Identification of promiscuous HLA-DR-restricted CD4(+) T-cell epitopes on the cancer-testis antigen HCA587. Cancer Sci 2011; 102: 1455-1461. (PMID: 21595801)
- Neumann F, Kubuschok B, Ertan K, Schormann C, Stevanovic S, Preuss KD, Schmidt W, Pfreundschuh M. A peptide epitope derived from the cancer testis antigen HOM-MEL-40/SSX2 capable of inducing CD4(+) and CD8(+) T-cell as well as B-cell responses. Cancer Immunol Immunother 2011; 60: 1333-1346. (PMID: 21630107)
- Ohue Y, Eikawa S, Okazaki N, Mizote Y, Isobe M, Uenaka A, Fukuda M, Old LJ, Oka M, Nakayama E. Spontaneous antibody, and CD4 and CD8 T-cell responses against XAGE-1b (GAGED2a) in non-small cell lung cancer patients. Int J Cancer 2012; 131: E649-658. (PMID: 22109656)
- Meng Z, Wang Y, Zhang G, Ke Y, Yan Y, Wu L, Huang Q, Zeng G, Ying H, Jiao S. Identification of an HLA-DPB1*0501 restricted Melan-A/MART-1 epitope recognized by CD4+ T lymphocytes: prevalence for immunotherapy in Asian populations. J Immunother 2011; 34: 525-534. (PMID: 21760531)
- Osen W, Soltek S, Song M, Leuchs B, Steitz J, Tuting T, Eichmuller SB, Nguyen XD, Schadendorf D, Paschen A. Screening of human tumor antigens for CD4 T cell epitopes by combination of HLA-transgenic mice, recombinant adenovirus and antigen peptide libraries. PLoS One 2010; 5: e14137. (PMID: 21152437)
- Komori H, Nakatsura T, Senju S, Yoshitake Y, Motomura Y, Ikuta Y, Fukuma D, Yokomine K, Harao M, Beppu T, Matsui M, Torigoe T, Sato N, Baba H, Nishimura Y. Identification of HLA-A2- or HLA-A24-restricted CTL epitopes possibly useful for glypican-3-specific immunotherapy of hepatocellular carcinoma. Clin Cancer Res 2006; 12: 2689-2697. (PMID: 16675560)
- Tomita Y, Harao M, Senju S, Imai K, Hirata S, Irie A, Inoue M, Hayashida Y, Yoshimoto K, Shiraishi K, Mori T, Nomori H, Kohrogi H, Nishimura Y. Peptides derived from human insulin-like growth factor-II mRNA binding protein 3 can induce human leukocyte antigen-A2-restricted cytotoxic T lymphocytes reactive to cancer cells. Cancer Sci 2011; 102: 71-78. (PMID: 21087352)
- Wilkinson R, Woods K, D’Rozario R, Prue R, Vari F, Hardy MY, Dong Y, Clements JA, Hart DN, Radford KJ. Human kallikrein 4 signal peptide induces cytotoxic T cell responses in healthy donors and prostate cancer patients. Cancer Immunol Immunother 2012; 61: 169-179. (PMID: 21874303)
- Imai K, Hirata S, Irie A, Senju S, Ikuta Y, Yokomine K, Harao M, Inoue M, Tomita Y, Tsunoda T, Nakagawa H, Nakamura Y, Baba H, Nishimura Y. Identification of HLA-A2-restricted CTL epitopes of a novel tumour-associated antigen, KIF20A, overexpressed in pancreatic cancer. Br J Cancer 2011; 104: 300-307. (PMID: 21179034)
- Nakatsugawa M, Horie K, Yoshikawa T, Shimomura M, Kikuchi Y, Sakemura N, Suzuki S, Nobuoka D, Hirohashi Y, Torigoe T, Harada K, Takasu H, Sato N, Nakatsura T. Identification of an HLA-A*0201-restricted cytotoxic T lymphocyte epitope from the lung carcinoma antigen, Lengsin. Int J Oncol 2011; 39: 1041-1049. (PMID: 21687943)
- Rogel A, Vignard V, Bobinet M, Labarrière N, Lang F. A long peptide from MELOE-1 contains multiple HLA class II T cell epitopes in addition to the HLA-A*0201 epitope: an attractive candidate for melanoma vaccination. Cancer Immunol Immunother 2011; 60: 327-337. (PMID: 21080167)
- Yamazoe S, Tanaka H, Iwauchi T, Yoshii M, Ito G, Amano R, Yamada N, Sawada T, Ohira M, Hirakawa K. Identification of HLA-A*0201- and A*2402-restricted epitopes of mucin 5AC expressed in advanced pancreatic cancer. Pancreas 2011; 40: 896-904. (PMID: 21697763)
- Widenmeyer M, Griesemann H, Stevanovic S, Feyerabend S, Klein R, Attig S, Hennenlotter J, Wernet D, Kuprash DV, Sazykin AY, Pascolo S, Stenzl A, Gouttefangeas C, Rammensee HG. Promiscuous survivin peptide induces robust CD4+ T-cell responses in the majority of vaccinated cancer patients. Int J Cancer 2012; 131: 140-149. (PMID: 21858810)