Abstract
Tumour associated antigens recognised by cellular or humoral effectors of the immune system are potential targets for antigen specific cancer immunotherapy. Different categories of cancer antigens have been identified that induce cytotoxic T lymphocyte (CTL) responses in vitro and in vivo, namely: (1) "cancer testis" (CT) antigens, expressed in different tumours and normal testis, (2) melanocyte differentiation antigens, (3) point mutations of normal genes, (4) self antigens that are overexpressed in malignant tissues, and (5) viral antigens. Clinical studies with peptides and proteins derived from these antigens have been initiated to study the efficacy of inducing specific CTL responses in vivo. Immunological and clinical parameters for the assessment of antigen specific immune responses have been defined—delayed type hypersensitivity (DTH), CTL, autoimmmune, and tumour regression responses. Specific DTH and CTL responses and tumour regression have been observed after the intradermal administration of tumour associated peptides alone. Peptide specific immune reactions were enhanced after using granulocyte macrophage stimulating factor (GM-CSF) as a systemic adjuvant by increasing the frequency of dermal antigen presenting Langerhans cells. Complete tumour regression has been observed in the context of measurable peptide specific CTL. However, in single cases with disease progression after an initial tumour response, either a loss of single antigens targeted by CTL or of the presenting major histocompatibility complex (MHC) class I allele was detected, pointing towards immunisation induced immune escape. Cytokines to modulate antigen and MHC class I expression in vivo are being evaluated to prevent immunoselection. Recently, a new CT antigen, NY-ESO-1, has been identified on the basis of spontaneous antibody responses to tumour associated antigens. NY-ESO-1 appears to be one of the most immunogenic antigens known to date, with spontaneous immune responses observed in 50% of patients with NY-ESO-1 expressing cancers. Clinical studies have been initiated to evaluate the immunogenicity of different NY-ESO-1 constructs to induce both humoral and cellular immune responses in vivo.
Key Words: tumour antigens • antigen specific T cell response
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- Alijagic S., Möller P., Artuc M., Jurgovsky K., Czarnetzki B. M., Schadendorf D. Dendritic cells generated from peripheral blood transfected with human tyrosinase induce specific T cell activation. Eur J Immunol. 1995 Nov;25(11):3100–3107. doi: 10.1002/eji.1830251117. [DOI] [PubMed] [Google Scholar]
- Bakker A. B., Schreurs M. W., de Boer A. J., Kawakami Y., Rosenberg S. A., Adema G. J., Figdor C. G. Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J Exp Med. 1994 Mar 1;179(3):1005–1009. doi: 10.1084/jem.179.3.1005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brasseur F., Rimoldi D., Liénard D., Lethé B., Carrel S., Arienti F., Suter L., Vanwijck R., Bourlond A., Humblet Y. Expression of MAGE genes in primary and metastatic cutaneous melanoma. Int J Cancer. 1995 Nov 3;63(3):375–380. doi: 10.1002/ijc.2910630313. [DOI] [PubMed] [Google Scholar]
- Brichard V., Van Pel A., Wölfel T., Wölfel C., De Plaen E., Lethé B., Coulie P., Boon T. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med. 1993 Aug 1;178(2):489–495. doi: 10.1084/jem.178.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Caux C., Dezutter-Dambuyant C., Schmitt D., Banchereau J. GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells. Nature. 1992 Nov 19;360(6401):258–261. doi: 10.1038/360258a0. [DOI] [PubMed] [Google Scholar]
- Chang M. H., Chen C. J., Lai M. S., Hsu H. M., Wu T. C., Kong M. S., Liang D. C., Shau W. Y., Chen D. S. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. N Engl J Med. 1997 Jun 26;336(26):1855–1859. doi: 10.1056/NEJM199706263362602. [DOI] [PubMed] [Google Scholar]
- Chen Y. T., Scanlan M. J., Sahin U., Türeci O., Gure A. O., Tsang S., Williamson B., Stockert E., Pfreundschuh M., Old L. J. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc Natl Acad Sci U S A. 1997 Mar 4;94(5):1914–1918. doi: 10.1073/pnas.94.5.1914. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen Y. T., Stockert E., Jungbluth A., Tsang S., Coplan K. A., Scanlan M. J., Old L. J. Serological analysis of Melan-A(MART-1), a melanocyte-specific protein homogeneously expressed in human melanomas. Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5915–5919. doi: 10.1073/pnas.93.12.5915. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen Y. T., Stockert E., Tsang S., Coplan K. A., Old L. J. Immunophenotyping of melanomas for tyrosinase: implications for vaccine development. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8125–8129. doi: 10.1073/pnas.92.18.8125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coulie P. G., Brichard V., Van Pel A., Wölfel T., Schneider J., Traversari C., Mattei S., De Plaen E., Lurquin C., Szikora J. P. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med. 1994 Jul 1;180(1):35–42. doi: 10.1084/jem.180.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coulie P. G., 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 Aug 15;92(17):7976–7980. doi: 10.1073/pnas.92.17.7976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Disis M. L., Cheever M. A. Oncogenic proteins as tumor antigens. Curr Opin Immunol. 1996 Oct;8(5):637–642. doi: 10.1016/s0952-7915(96)80079-3. [DOI] [PubMed] [Google Scholar]
- Feltkamp M. C., Smits H. L., Vierboom M. P., Minnaar R. P., de Jongh B. M., Drijfhout J. W., ter Schegget J., Melief C. J., Kast W. M. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol. 1993 Sep;23(9):2242–2249. doi: 10.1002/eji.1830230929. [DOI] [PubMed] [Google Scholar]
- Fenton R. G., Keller C. J., Hanna N., Taub D. D. Induction of T-cell immunity against Ras oncoproteins by soluble protein or Ras-expressing Escherichia coli. J Natl Cancer Inst. 1995 Dec 20;87(24):1853–1861. doi: 10.1093/jnci/87.24.1853. [DOI] [PubMed] [Google Scholar]
- Gaugler B., Van den Eynde B., van der Bruggen P., Romero P., Gaforio J. J., De Plaen E., Lethé B., Brasseur F., Boon T. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J Exp Med. 1994 Mar 1;179(3):921–930. doi: 10.1084/jem.179.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gjertsen M. K., Bakka A., Breivik J., Saeterdal I., Solheim B. G., Søreide O., Thorsby E., Gaudernack G. Vaccination with mutant ras peptides and induction of T-cell responsiveness in pancreatic carcinoma patients carrying the corresponding RAS mutation. Lancet. 1995 Nov 25;346(8987):1399–1400. doi: 10.1016/s0140-6736(95)92408-6. [DOI] [PubMed] [Google Scholar]
- Gromet M. A., Epstein W. L., Blois M. S. The regressing thin malignant melanoma: a distinctive lesion with metastatic potential. Cancer. 1978 Nov;42(5):2282–2292. doi: 10.1002/1097-0142(197811)42:5<2282::aid-cncr2820420528>3.0.co;2-v. [DOI] [PubMed] [Google Scholar]
- Herr W., Wölfel T., Heike M., Meyer zum Büschenfelde K. H., Knuth A. Frequency analysis of tumor-reactive cytotoxic T lymphocytes in peripheral blood of a melanoma patient vaccinated with autologous tumor cells. Cancer Immunol Immunother. 1994 Aug;39(2):93–99. doi: 10.1007/BF01525314. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jäeger E., Bernhard H., Romero P., Ringhoffer M., Arand M., Karbach J., Ilsemann C., Hagedorn M., Knuth A. Generation of cytotoxic T-cell responses with synthetic melanoma-associated peptides in vivo: implications for tumor vaccines with melanoma-associated antigens. Int J Cancer. 1996 Apr 10;66(2):162–169. doi: 10.1002/(SICI)1097-0215(19960410)66:2<162::AID-IJC4>3.0.CO;2-0. [DOI] [PubMed] [Google Scholar]
- Jäger E., Chen Y. T., Drijfhout J. W., Karbach J., Ringhoffer M., Jäger D., Arand M., Wada H., Noguchi Y., Stockert E. Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J Exp Med. 1998 Jan 19;187(2):265–270. doi: 10.1084/jem.187.2.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jäger E., Jäger D., Karbach J., Chen Y. T., Ritter G., Nagata Y., Gnjatic S., Stockert E., Arand M., Old L. J. Identification of NY-ESO-1 epitopes presented by human histocompatibility antigen (HLA)-DRB4*0101-0103 and recognized by CD4(+) T lymphocytes of patients with NY-ESO-1-expressing melanoma. J Exp Med. 2000 Feb 21;191(4):625–630. doi: 10.1084/jem.191.4.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jäger E., Maeurer M., Höhn H., Karbach J., Jäger D., Zidianakis Z., Bakhshandeh-Bath A., Orth J., Neukirch C., Necker A. Clonal expansion of Melan A-specific cytotoxic T lymphocytes in a melanoma patient responding to continued immunization with melanoma-associated peptides. Int J Cancer. 2000 May 15;86(4):538–547. doi: 10.1002/(sici)1097-0215(20000515)86:4<538::aid-ijc16>3.0.co;2-g. [DOI] [PubMed] [Google Scholar]
- Jäger E., Ringhoffer M., Altmannsberger M., Arand M., Karbach J., Jäger D., Oesch F., Knuth A. Immunoselection in vivo: independent loss of MHC class I and melanocyte differentiation antigen expression in metastatic melanoma. Int J Cancer. 1997 Apr 10;71(2):142–147. doi: 10.1002/(sici)1097-0215(19970410)71:2<142::aid-ijc3>3.0.co;2-0. [DOI] [PubMed] [Google Scholar]
- Jäger E., Ringhoffer M., Arand M., Karbach J., Jäger D., Ilsemann C., Hagedorn M., Oesch F., Knuth A. Cytolytic T cell reactivity against melanoma-associated differentiation antigens in peripheral blood of melanoma patients and healthy individuals. Melanoma Res. 1996 Dec;6(6):419–425. doi: 10.1097/00008390-199612000-00003. [DOI] [PubMed] [Google Scholar]
- Jäger E., Ringhoffer M., Dienes H. P., Arand M., Karbach J., Jäger D., Ilsemann C., Hagedorn M., Oesch F., Knuth A. Granulocyte-macrophage-colony-stimulating factor enhances immune responses to melanoma-associated peptides in vivo. Int J Cancer. 1996 Jul 3;67(1):54–62. doi: 10.1002/(SICI)1097-0215(19960703)67:1<54::AID-IJC11>3.0.CO;2-C. [DOI] [PubMed] [Google Scholar]
- Jäger E., Ringhoffer M., Karbach J., Arand M., Oesch F., Knuth A. Inverse relationship of melanocyte differentiation antigen expression in melanoma tissues and CD8+ cytotoxic-T-cell responses: evidence for immunoselection of antigen-loss variants in vivo. Int J Cancer. 1996 May 16;66(4):470–476. doi: 10.1002/(SICI)1097-0215(19960516)66:4<470::AID-IJC10>3.0.CO;2-C. [DOI] [PubMed] [Google Scholar]
- Jäger E., Stockert E., Zidianakis Z., Chen Y. T., Karbach J., Jäger D., Arand M., Ritter G., Old L. J., Knuth A. Humoral immune responses of cancer patients against "Cancer-Testis" antigen NY-ESO-1: correlation with clinical events. Int J Cancer. 1999 Oct 22;84(5):506–510. doi: 10.1002/(sici)1097-0215(19991022)84:5<506::aid-ijc10>3.0.co;2-6. [DOI] [PubMed] [Google Scholar]
- Kang X., Kawakami Y., el-Gamil M., Wang R., Sakaguchi K., Yannelli J. R., Appella E., Rosenberg S. A., Robbins P. F. Identification of a tyrosinase epitope recognized by HLA-A24-restricted, tumor-infiltrating lymphocytes. J Immunol. 1995 Aug 1;155(3):1343–1348. [PubMed] [Google Scholar]
- Kawakami Y., Eliyahu S., Delgado C. H., Robbins P. F., Rivoltini L., Topalian S. L., Miki T., Rosenberg S. A. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3515–3519. doi: 10.1073/pnas.91.9.3515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawakami Y., Eliyahu S., Delgado C. H., Robbins P. F., Sakaguchi K., Appella E., Yannelli J. R., Adema G. J., Miki T., Rosenberg S. A. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6458–6462. doi: 10.1073/pnas.91.14.6458. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawakami Y., Eliyahu S., Jennings C., Sakaguchi K., Kang X., Southwood S., Robbins P. F., Sette A., Appella E., Rosenberg S. A. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J Immunol. 1995 Apr 15;154(8):3961–3968. [PubMed] [Google Scholar]
- Knuth A., Danowski B., Oettgen H. F., Old L. J. T-cell-mediated cytotoxicity against autologous malignant melanoma: analysis with interleukin 2-dependent T-cell cultures. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3511–3515. doi: 10.1073/pnas.81.11.3511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knuth A., Wölfel T., Klehmann E., Boon T., Meyer zum Büschenfelde K. H. Cytolytic T-cell clones against an autologous human melanoma: specificity study and definition of three antigens by immunoselection. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2804–2808. doi: 10.1073/pnas.86.8.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knuth A., Wölfel T., Meyer zum Büschenfelde K. H. Cellular and humoral immune responses against cancer: implications for cancer vaccines. Curr Opin Immunol. 1991 Oct;3(5):659–664. doi: 10.1016/0952-7915(91)90093-g. [DOI] [PubMed] [Google Scholar]
- Knuth A., Wölfel T., Meyer zum Büschenfelde K. H. T cell responses to human malignant tumours. Cancer Surv. 1992;13:39–52. [PubMed] [Google Scholar]
- Koenig S., Woods R. M., Brewah Y. A., Newell A. J., Jones G. M., Boone E., Adelsberger J. W., Baseler M. W., Robinson S. M., Jacobson S. Characterization of MHC class I restricted cytotoxic T cell responses to tax in HTLV-1 infected patients with neurologic disease. J Immunol. 1993 Oct 1;151(7):3874–3883. [PubMed] [Google Scholar]
- Koziel M. J., Dudley D., Afdhal N., Grakoui A., Rice C. M., Choo Q. L., Houghton M., Walker B. D. HLA class I-restricted cytotoxic T lymphocytes specific for hepatitis C virus. Identification of multiple epitopes and characterization of patterns of cytokine release. J Clin Invest. 1995 Nov;96(5):2311–2321. doi: 10.1172/JCI118287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kugler A., Stuhler G., Walden P., Zöller G., Zobywalski A., Brossart P., Trefzer U., Ullrich S., Müller C. A., Becker V. Regression of human metastatic renal cell carcinoma after vaccination with tumor cell-dendritic cell hybrids. Nat Med. 2000 Mar;6(3):332–336. doi: 10.1038/73193. [DOI] [PubMed] [Google Scholar]
- Mandelboim O., Berke G., Fridkin M., Feldman M., Eisenstein M., Eisenbach L. CTL induction by a tumour-associated antigen octapeptide derived from a murine lung carcinoma. Nature. 1994 May 5;369(6475):67–71. doi: 10.1038/369067a0. [DOI] [PubMed] [Google Scholar]
- Marchand M., Weynants P., Rankin E., Arienti F., Belli F., Parmiani G., Cascinelli N., Bourlond A., Vanwijck R., Humblet Y. Tumor regression responses in melanoma patients treated with a peptide encoded by gene MAGE-3. Int J Cancer. 1995 Dec 11;63(6):883–885. doi: 10.1002/ijc.2910630622. [DOI] [PubMed] [Google Scholar]
- Marchand M., Weynants P., Rankin E., Arienti F., Belli F., Parmiani G., Cascinelli N., Bourlond A., Vanwijck R., Humblet Y. Tumor regression responses in melanoma patients treated with a peptide encoded by gene MAGE-3. Int J Cancer. 1995 Dec 11;63(6):883–885. doi: 10.1002/ijc.2910630622. [DOI] [PubMed] [Google Scholar]
- Marchand M., van Baren N., Weynants P., Brichard V., Dréno B., Tessier M. H., Rankin E., Parmiani G., Arienti F., Humblet Y. Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE-3 and presented by HLA-A1. Int J Cancer. 1999 Jan 18;80(2):219–230. doi: 10.1002/(sici)1097-0215(19990118)80:2<219::aid-ijc10>3.0.co;2-s. [DOI] [PubMed] [Google Scholar]
- Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol. 1994;12:991–1045. doi: 10.1146/annurev.iy.12.040194.005015. [DOI] [PubMed] [Google Scholar]
- Murray R. J., Kurilla M. G., Brooks J. M., Thomas W. A., Rowe M., Kieff E., Rickinson A. B. Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies. J Exp Med. 1992 Jul 1;176(1):157–168. doi: 10.1084/jem.176.1.157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nestle F. O., Alijagic S., Gilliet M., Sun Y., Grabbe S., Dummer R., Burg G., Schadendorf D. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med. 1998 Mar;4(3):328–332. doi: 10.1038/nm0398-328. [DOI] [PubMed] [Google Scholar]
- Noguchi Y., Richards E. C., Chen Y. T., Old L. J. Influence of interleukin 12 on p53 peptide vaccination against established Meth A sarcoma. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2219–2223. doi: 10.1073/pnas.92.6.2219. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ogg G. S., Rod Dunbar P., Romero P., Chen J. L., Cerundolo V. High frequency of skin-homing melanocyte-specific cytotoxic T lymphocytes in autoimmune vitiligo. J Exp Med. 1998 Sep 21;188(6):1203–1208. doi: 10.1084/jem.188.6.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rehermann B., Fowler P., Sidney J., Person J., Redeker A., Brown M., Moss B., Sette A., Chisari F. V. The cytotoxic T lymphocyte response to multiple hepatitis B virus polymerase epitopes during and after acute viral hepatitis. J Exp Med. 1995 Mar 1;181(3):1047–1058. doi: 10.1084/jem.181.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rivoltini L., Kawakami Y., Sakaguchi K., Southwood S., Sette A., Robbins P. F., Marincola F. M., Salgaller M. L., Yannelli J. R., Appella E. Induction of tumor-reactive CTL from peripheral blood and tumor-infiltrating lymphocytes of melanoma patients by in vitro stimulation with an immunodominant peptide of the human melanoma antigen MART-1. J Immunol. 1995 Mar 1;154(5):2257–2265. [PubMed] [Google Scholar]
- Robbins P. F., el-Gamil M., Kawakami Y., Stevens E., Yannelli J. R., Rosenberg S. A. Recognition of tyrosinase by tumor-infiltrating lymphocytes from a patient responding to immunotherapy. Cancer Res. 1994 Jun 15;54(12):3124–3126. [PubMed] [Google Scholar]
- Sahin U., Türeci O., Schmitt H., Cochlovius B., Johannes T., Schmits R., Stenner F., Luo G., Schobert I., Pfreundschuh M. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11810–11813. doi: 10.1073/pnas.92.25.11810. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schirmbeck R., Melber K., Reimann J. Hepatitis B virus small surface antigen particles are processed in a novel endosomal pathway for major histocompatibility complex class I-restricted epitope presentation. Eur J Immunol. 1995 Apr;25(4):1063–1070. doi: 10.1002/eji.1830250431. [DOI] [PubMed] [Google Scholar]
- Schlichtholz B., Legros Y., Gillet D., Gaillard C., Marty M., Lane D., Calvo F., Soussi T. The immune response to p53 in breast cancer patients is directed against immunodominant epitopes unrelated to the mutational hot spot. Cancer Res. 1992 Nov 15;52(22):6380–6384. [PubMed] [Google Scholar]
- Stockert E., Jäger E., Chen Y. T., Scanlan M. J., Gout I., Karbach J., Arand M., Knuth A., Old L. J. A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J Exp Med. 1998 Apr 20;187(8):1349–1354. doi: 10.1084/jem.187.8.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilkin A. F., Lubin R., Soussi T., Lazar V., Janin N., Mathieu M. C., Lefrère I., Carlu C., Roy M., Kayibanda M. Primary proliferative T cell response to wild-type p53 protein in patients with breast cancer. Eur J Immunol. 1995 Jun;25(6):1765–1769. doi: 10.1002/eji.1830250642. [DOI] [PubMed] [Google Scholar]
- Traversari C., van der Bruggen P., Luescher I. F., Lurquin C., Chomez P., Van Pel A., De Plaen E., Amar-Costesec A., Boon T. A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J Exp Med. 1992 Nov 1;176(5):1453–1457. doi: 10.1084/jem.176.5.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van den Eynde B., Peeters O., De Backer O., Gaugler B., Lucas S., Boon T. A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma. J Exp Med. 1995 Sep 1;182(3):689–698. doi: 10.1084/jem.182.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Visseren M. J., van Elsas A., van der Voort E. I., Ressing M. E., Kast W. M., Schrier P. I., Melief C. J. CTL specific for the tyrosinase autoantigen can be induced from healthy donor blood to lyse melanoma cells. J Immunol. 1995 Apr 15;154(8):3991–3998. [PubMed] [Google Scholar]
- Wölfel T., Hauer M., Schneider J., Serrano M., Wölfel C., Klehmann-Hieb E., De Plaen E., Hankeln T., Meyer zum Büschenfelde K. H., Beach D. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science. 1995 Sep 1;269(5228):1281–1284. doi: 10.1126/science.7652577. [DOI] [PubMed] [Google Scholar]
- Wölfel T., Klehmann E., Müller C., Schütt K. H., Meyer zum Büschenfelde K. H., Knuth A. Lysis of human melanoma cells by autologous cytolytic T cell clones. Identification of human histocompatibility leukocyte antigen A2 as a restriction element for three different antigens. J Exp Med. 1989 Sep 1;170(3):797–810. doi: 10.1084/jem.170.3.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wölfel T., Schneider J., Meyer Zum Büschenfelde K. H., Rammensee H. G., Rötzschke O., Falk K. Isolation of naturally processed peptides recognized by cytolytic T lymphocytes (CTL) on human melanoma cells in association with HLA-A2.1. Int J Cancer. 1994 May 1;57(3):413–418. doi: 10.1002/ijc.2910570320. [DOI] [PubMed] [Google Scholar]
- 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 Dec 13;254(5038):1643–1647. doi: 10.1126/science.1840703. [DOI] [PubMed] [Google Scholar]
