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Published in: Oral and Maxillofacial Surgery 3/2019

01-09-2019 | Metastasis | Original Article

The expression of melanoma-associated antigen A (MAGE-A) in oral squamous cell carcinoma: an evaluation of the significance for tumor prognosis

Authors: Anna Trippel, Frank Halling, Paul Heymann, Mustafa Ayna, Bilal Al-Nawas, Thomas Ziebart

Published in: Oral and Maxillofacial Surgery | Issue 3/2019

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Abstract

Objectives

Melanoma-associated antigens A had been detected repeatedly in oral squamous cell carcinoma, but not in healthy mucosa. Additionally, patients with MAGE-A expressing cancers are regarded to have a worse survival prognosis, so that MAGE-A are supposed to be part of carcinogenesis. Which role these antigens fulfill within OSCC is still, up today, largely unknown. This study examines the hypothesis that MAGE-A is being produced in OSCC but not in mucosa tissue and if MAGE-A has any correlation to clinical patient’s parameters like tumor size, lymph node metastasis, distant metastasis, overall survival, and recurrence.

Materials and methods

For this purpose, 50 tumor samples and 39 mucosa samples were analyzed by means of PCR and immunohistochemical staining with the antibody 6C1.

Results

Forty of 41 stained tumor samples showed a positive antibody reaction with a maximum staining rate of 53%. Sixteen mucosa samples showed a mild positive reaction. The PCR revealed a linear expression pattern of MAGE-A in which the genes are proportionally expressed in OSCC. We did not find any relationship between MAGE-A and tumor size, overall survival, or recurrence. There was also no connection between MAGE-A and tumor parameters Hif-1 and LDH. Their expression was detected tendentially in tumors with higher staging, advanced lymph node metastasis, and rising age of the patients. The genes MAGE-A3+6 and MAGE-A4 had a statistically significant correlation with lymph node metastasis (p = 0.007 and p = 0.004). Patients got distant metastasis and influence of MAGE-A on metastatic behavior could not be verified. The genes MAGE-A3 and -A4 are consequently qualified as tumor markers in the field of diagnosis and follow-up of OSCC.

Conclusions and clinical relevance

Two genes have great potential as target proteins in immunotherapy. The genes MAGE-A3+6 and MAGE-A4 had a statistically significant correlation with lymph node metastasis.
Literature
2.
go back to reference Carvalho AL, Singh B, Spiro RH, Kowalski LP, Shah JP (2004) Cancer of the oral cavity: a comparison between institutions in a developing and a developed nation. Head Neck 26:31–38CrossRefPubMed Carvalho AL, Singh B, Spiro RH, Kowalski LP, Shah JP (2004) Cancer of the oral cavity: a comparison between institutions in a developing and a developed nation. Head Neck 26:31–38CrossRefPubMed
3.
go back to reference Warnakulasuriya S (2009) Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 45:309–316CrossRefPubMed Warnakulasuriya S (2009) Global epidemiology of oral and oropharyngeal cancer. Oral Oncol 45:309–316CrossRefPubMed
4.
go back to reference Lo WL, Kao SY, Chi LY, Wong YK, Chang RC (2003) Outcomes of oral squamous cell carcinoma in Taiwan after surgical therapy: factors affecting survival. J Oral Maxillofac Surg 61:751–758CrossRefPubMed Lo WL, Kao SY, Chi LY, Wong YK, Chang RC (2003) Outcomes of oral squamous cell carcinoma in Taiwan after surgical therapy: factors affecting survival. J Oral Maxillofac Surg 61:751–758CrossRefPubMed
6.
go back to reference Bernier J, Domenge C, Ozsahin M, Matuszewska K, Lefèbvre JL, Greiner RH, Giralt J, Maingon P, Rolland F, Bolla M, Cognetti F, Bourhis J, Kirkpatrick A, van Glabbeke M (2004) Postoperative irradiation with or without concomitant chemotherapy for locally advanced head and neck cancer. N Engl J Med 350:1945–1952CrossRefPubMed Bernier J, Domenge C, Ozsahin M, Matuszewska K, Lefèbvre JL, Greiner RH, Giralt J, Maingon P, Rolland F, Bolla M, Cognetti F, Bourhis J, Kirkpatrick A, van Glabbeke M (2004) Postoperative irradiation with or without concomitant chemotherapy for locally advanced head and neck cancer. N Engl J Med 350:1945–1952CrossRefPubMed
7.
go back to reference Kreppel M, Drebber U, Eich HT, Dreiseidler T, Zöller JE, Müller RP, Scheer M (2011) Combined-modality treatment in advanced oral squamous cell carcinoma with primary surgery followed by adjuvant radiochemotherapy. Strahlenther Onkol 187:555–560CrossRefPubMed Kreppel M, Drebber U, Eich HT, Dreiseidler T, Zöller JE, Müller RP, Scheer M (2011) Combined-modality treatment in advanced oral squamous cell carcinoma with primary surgery followed by adjuvant radiochemotherapy. Strahlenther Onkol 187:555–560CrossRefPubMed
8.
go back to reference Lavaf A, Genden E, Cesaretti J et al (2008) Adjuvant radiotherapy improves overall survival for patients with lymph node-positive head and neck squamous cell carcinoma. Cancer 112:535–543CrossRefPubMed Lavaf A, Genden E, Cesaretti J et al (2008) Adjuvant radiotherapy improves overall survival for patients with lymph node-positive head and neck squamous cell carcinoma. Cancer 112:535–543CrossRefPubMed
11.
15.
go back to reference Zhang Q and Su B. Evolutionary origin and human-specific expansion of a cancer/testis antigen gene family. Mol Biol Evol 2014; 31:2365–2375 Zhang Q and Su B. Evolutionary origin and human-specific expansion of a cancer/testis antigen gene family. Mol Biol Evol 2014; 31:2365–2375
16.
go back to reference van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T (1991) A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 254:1643–1647CrossRefPubMed van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T (1991) A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 254:1643–1647CrossRefPubMed
17.
go back to reference Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S (2001) An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 61(14):5544–5551PubMed Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S (2001) An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 61(14):5544–5551PubMed
18.
go back to reference Yang B, O’Herrin SM, Wu J, Reagan-Shaw S, Ma Y, Bhat KM, Gravekamp C, Setaluri V, Peters N, Hoffmann FM, Peng H, Ivanov AV, Simpson AJ, Longley BJ (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67:9954–9962CrossRefPubMed Yang B, O’Herrin SM, Wu J, Reagan-Shaw S, Ma Y, Bhat KM, Gravekamp C, Setaluri V, Peters N, Hoffmann FM, Peng H, Ivanov AV, Simpson AJ, Longley BJ (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67:9954–9962CrossRefPubMed
19.
go back to reference Monte M, Simonatto M, Peche LY, Bublik DR, Gobessi S, Pierotti MA, Rodolfo M, Schneider C (2006) MAGE-A tumor antigens target p53 transactivation function through histone deacetylase recruitment and confer resistance to chemotherapeutic agents. Proc Natl Acad Sci U S A 103:11160–11165CrossRefPubMedPubMedCentral Monte M, Simonatto M, Peche LY, Bublik DR, Gobessi S, Pierotti MA, Rodolfo M, Schneider C (2006) MAGE-A tumor antigens target p53 transactivation function through histone deacetylase recruitment and confer resistance to chemotherapeutic agents. Proc Natl Acad Sci U S A 103:11160–11165CrossRefPubMedPubMedCentral
20.
21.
go back to reference Peche LY, Scolz M, Ladelfa MF, Monte M, Schneider C (2012) MageA2 restrains cellular senescence by targeting the function of PMLIV/p53 axis at the PML-NBs. Cell Death Differ 19:926–936CrossRefPubMed Peche LY, Scolz M, Ladelfa MF, Monte M, Schneider C (2012) MageA2 restrains cellular senescence by targeting the function of PMLIV/p53 axis at the PML-NBs. Cell Death Differ 19:926–936CrossRefPubMed
22.
go back to reference Greve KB, Lindgreen JN, Terp MG, Pedersen CB, Schmidt S, Mollenhauer J, Kristensen SB, Andersen RS, Relster MM, Ditzel HJ, Gjerstorff MF (2015) Ectopic expression of cancer/testis antigen SSX2 induces DNA damage and promotes genomic instability. Mol Oncol 9:437–449CrossRefPubMed Greve KB, Lindgreen JN, Terp MG, Pedersen CB, Schmidt S, Mollenhauer J, Kristensen SB, Andersen RS, Relster MM, Ditzel HJ, Gjerstorff MF (2015) Ectopic expression of cancer/testis antigen SSX2 induces DNA damage and promotes genomic instability. Mol Oncol 9:437–449CrossRefPubMed
23.
go back to reference Por E, Byun HJ, Lee EJ, Lim JH, Jung SY, Park I, Kim YM, Jeoung DI, Lee H (2010) The cancer/testis antigen CAGE with oncogenic potential stimulates cell proliferation by up-regulating cyclins D1 and E in an AP-1- and E2Fdependent manner. J Biol Chem 285:14475–14485CrossRefPubMedPubMedCentral Por E, Byun HJ, Lee EJ, Lim JH, Jung SY, Park I, Kim YM, Jeoung DI, Lee H (2010) The cancer/testis antigen CAGE with oncogenic potential stimulates cell proliferation by up-regulating cyclins D1 and E in an AP-1- and E2Fdependent manner. J Biol Chem 285:14475–14485CrossRefPubMedPubMedCentral
24.
go back to reference Kim Y, Park D, Kim H, Choi M, Lee H, Lee YS, Choe J, Kim YM, Jeoung D (2013) miR-200b and cancer/testis antigen CAGE form a feedback loop to regulate the invasion and tumorigenic and angiogenic responses of a cancer cell line to microtubule-targeting drugs. J Biol Chem 288:36502–36518CrossRefPubMedPubMedCentral Kim Y, Park D, Kim H, Choi M, Lee H, Lee YS, Choe J, Kim YM, Jeoung D (2013) miR-200b and cancer/testis antigen CAGE form a feedback loop to regulate the invasion and tumorigenic and angiogenic responses of a cancer cell line to microtubule-targeting drugs. J Biol Chem 288:36502–36518CrossRefPubMedPubMedCentral
25.
go back to reference Barrow C, Browning J, MacGregor D, Davis ID, Sturrock S, Jungbluth AA, Cebon J (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771CrossRefPubMed Barrow C, Browning J, MacGregor D, Davis ID, Sturrock S, Jungbluth AA, Cebon J (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771CrossRefPubMed
26.
go back to reference Yang F, Zhou X, Miao X, Zhang T, Hang X, Tie R, Liu N, Tian F, Wang F, Yuan J (2014) MAGEC2, an epithelial-mesenchymal transition inducer, is associated with breast cancer metastasis. Breast Cancer Res Treat 145:23–32CrossRefPubMedPubMedCentral Yang F, Zhou X, Miao X, Zhang T, Hang X, Tie R, Liu N, Tian F, Wang F, Yuan J (2014) MAGEC2, an epithelial-mesenchymal transition inducer, is associated with breast cancer metastasis. Breast Cancer Res Treat 145:23–32CrossRefPubMedPubMedCentral
27.
go back to reference Shang B, Gao A, Pan Y, Zhang G, Tu J, Zhou Y, Yang P, Cao Z, Wei Q, Ding Y, Zhang J, Zhao Y, Zhou Q (2014) CT45A1 acts as a new proto-oncogene to trigger tumorigenesis and cancer metastasis. Cell Death Dis 5:e1285CrossRefPubMedPubMedCentral Shang B, Gao A, Pan Y, Zhang G, Tu J, Zhou Y, Yang P, Cao Z, Wei Q, Ding Y, Zhang J, Zhao Y, Zhou Q (2014) CT45A1 acts as a new proto-oncogene to trigger tumorigenesis and cancer metastasis. Cell Death Dis 5:e1285CrossRefPubMedPubMedCentral
28.
go back to reference Caballero OL, Cohen T, Gurung S, Chua R, Lee P, Chen YT, Jat P, Simpson AJ (2013) Effects of CT-Xp gene knock down in melanoma cell lines. Oncotarget 4:531–541CrossRefPubMedPubMedCentral Caballero OL, Cohen T, Gurung S, Chua R, Lee P, Chen YT, Jat P, Simpson AJ (2013) Effects of CT-Xp gene knock down in melanoma cell lines. Oncotarget 4:531–541CrossRefPubMedPubMedCentral
29.
go back to reference De Craene B and Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013; 13:97–110 De Craene B and Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2013; 13:97–110
32.
go back to reference Zhang S, Zhai X, Wang G et al (2015) High expression of MAGE-A9 in tumor and stromal cells of non-small cell lung cancer was correlated with patient poor survival. Int J Clin Exp Pathol 8(1):541–550PubMedPubMedCentral Zhang S, Zhai X, Wang G et al (2015) High expression of MAGE-A9 in tumor and stromal cells of non-small cell lung cancer was correlated with patient poor survival. Int J Clin Exp Pathol 8(1):541–550PubMedPubMedCentral
33.
go back to reference Han L, Jiang B, Wu H, Zhang S, Lu X (2014) Expression and prognostic value of MAGE-A9 in laryngeal squamous cell carcinoma. Int J Clin Exp Pathol 7(10):6734–6742PubMedPubMedCentral Han L, Jiang B, Wu H, Zhang S, Lu X (2014) Expression and prognostic value of MAGE-A9 in laryngeal squamous cell carcinoma. Int J Clin Exp Pathol 7(10):6734–6742PubMedPubMedCentral
36.
go back to reference Laban S, Giebel G, Klümper N, Schröck A, Doescher J, Spagnoli G, Thierauf J, Theodoraki MN, Remark R, Gnjatic S, Krupar R, Sikora AG, Litjens G, Grabe N, Kristiansen G, Bootz F, Schuler PJ, Brunner C, Brägelmann J, Hoffmann TK, Perner S (2017) MAGE expression in head and neck squamous cell carcinoma primary tumors, lymph node metastases and respective recurrences-implications for immunotherapy. Oncotarget 8(9):14719–14735. https://doi.org/10.18632/oncotarget.14830 CrossRefPubMedPubMedCentral Laban S, Giebel G, Klümper N, Schröck A, Doescher J, Spagnoli G, Thierauf J, Theodoraki MN, Remark R, Gnjatic S, Krupar R, Sikora AG, Litjens G, Grabe N, Kristiansen G, Bootz F, Schuler PJ, Brunner C, Brägelmann J, Hoffmann TK, Perner S (2017) MAGE expression in head and neck squamous cell carcinoma primary tumors, lymph node metastases and respective recurrences-implications for immunotherapy. Oncotarget 8(9):14719–14735. https://​doi.​org/​10.​18632/​oncotarget.​14830 CrossRefPubMedPubMedCentral
37.
go back to reference Sharma P, Shen Y, Wen S, Bajorin DF, Reuter VE, Old LJ, Jungbluth AA (2006) Cancer-testis antigens: expression and correlation with survival in human urothelial carcinoma. Clin Cancer Res 12:5442–5447CrossRefPubMed Sharma P, Shen Y, Wen S, Bajorin DF, Reuter VE, Old LJ, Jungbluth AA (2006) Cancer-testis antigens: expression and correlation with survival in human urothelial carcinoma. Clin Cancer Res 12:5442–5447CrossRefPubMed
38.
go back to reference Cabezón T, Gromova I, Gromov P, Serizawa R, Timmermans Wielenga V, Kroman N, Celis JE, Moreira JMA (2013) Proteomic profiling of triple-negative breast carcinomas in combination with a three-tier orthogonal technology approach identifies Mage-A4 as potential therapeutic target in estrogen receptor negative breast cancer. Mol Cell Proteomics 12(2):381–394. https://doi.org/10.1074/mcp.M112.019786 CrossRefPubMed Cabezón T, Gromova I, Gromov P, Serizawa R, Timmermans Wielenga V, Kroman N, Celis JE, Moreira JMA (2013) Proteomic profiling of triple-negative breast carcinomas in combination with a three-tier orthogonal technology approach identifies Mage-A4 as potential therapeutic target in estrogen receptor negative breast cancer. Mol Cell Proteomics 12(2):381–394. https://​doi.​org/​10.​1074/​mcp.​M112.​019786 CrossRefPubMed
39.
go back to reference Cuffel C, Rivals JP, Zaugg Y, Salvi S, Seelentag W, Speiser DE, Liénard D, Monnier P, Romero P, Bron L, Rimoldi D (2011) Pattern and clinical significance of cancer-testis gene expression in head and neck squamous cell carcinoma. Int J Cancer 128:2625–2634CrossRefPubMed Cuffel C, Rivals JP, Zaugg Y, Salvi S, Seelentag W, Speiser DE, Liénard D, Monnier P, Romero P, Bron L, Rimoldi D (2011) Pattern and clinical significance of cancer-testis gene expression in head and neck squamous cell carcinoma. Int J Cancer 128:2625–2634CrossRefPubMed
40.
go back to reference Atanackovic D, Blum I, Cao Y, Wenzel S, Bartels K, Faltz C, Hossfeld DK, Hegewisch-Becker S, Bokemeyer C, Leuwer R (2006) Expression of cancer-testis antigens as possible targets for antigen-specific immunotherapy in head and neck squamous cell carcinoma. Cancer Biol Ther 5:1218–1225CrossRefPubMed Atanackovic D, Blum I, Cao Y, Wenzel S, Bartels K, Faltz C, Hossfeld DK, Hegewisch-Becker S, Bokemeyer C, Leuwer R (2006) Expression of cancer-testis antigens as possible targets for antigen-specific immunotherapy in head and neck squamous cell carcinoma. Cancer Biol Ther 5:1218–1225CrossRefPubMed
41.
go back to reference Kienstra MA, Neel HB, Strome SE, Roche P (2003) Identification of NY-ESO-1, MAGE-1, and MAGE-3 in head and neck squamous cell carcinoma. Head Neck 25:457–463CrossRefPubMed Kienstra MA, Neel HB, Strome SE, Roche P (2003) Identification of NY-ESO-1, MAGE-1, and MAGE-3 in head and neck squamous cell carcinoma. Head Neck 25:457–463CrossRefPubMed
42.
go back to reference Pastorcic-Grgic M, Sarcevic B, Dosen D, Juretic A, Spagnoli GC, Grgic M (2009) Prognostic value of MAGE-A and NYESO-1 expression in pharyngeal cancer. Head Neck 22:22 Pastorcic-Grgic M, Sarcevic B, Dosen D, Juretic A, Spagnoli GC, Grgic M (2009) Prognostic value of MAGE-A and NYESO-1 expression in pharyngeal cancer. Head Neck 22:22
43.
go back to reference Lee KD, Chang HK, Jo YK, Kim BS, Lee BH, Lee YW, Lee HK, Huh MH, Min YG, Spagnoli GC, Yu TH (1999) Expression of the MAGE 3 gene product in squamous cell carcinomas of the head and neck. Anticancer Res 19:5037–5042PubMed Lee KD, Chang HK, Jo YK, Kim BS, Lee BH, Lee YW, Lee HK, Huh MH, Min YG, Spagnoli GC, Yu TH (1999) Expression of the MAGE 3 gene product in squamous cell carcinomas of the head and neck. Anticancer Res 19:5037–5042PubMed
44.
go back to reference Chen X, Wang L, Liu J, Huang L, Yang L, Gao Q, Zhang Y (2017) Expression and prognostic relevance of MAGE-A3 and MAGE-C2 in non-small cell lung cancer. Oncol Lett 13:1609–1628CrossRefPubMedPubMedCentral Chen X, Wang L, Liu J, Huang L, Yang L, Gao Q, Zhang Y (2017) Expression and prognostic relevance of MAGE-A3 and MAGE-C2 in non-small cell lung cancer. Oncol Lett 13:1609–1628CrossRefPubMedPubMedCentral
45.
go back to reference Kocher T, Zheng M, Bolli M, Simon R, Forster T, Schultz-Thater E, Remmel E, Noppen C, Schmid U, Ackermann D, Mihatsch MJ, Gasser T, Heberer M, Sauter G, Spagnoli GC (2002) Prognostic relevance of MAGE-A4 tumor antigen expression in transitional cell carcinoma of the urinary bladder: a tissue microarray study. Int J Cancer 100:702–705. https://doi.org/10.1002/ijc.10540 CrossRefPubMed Kocher T, Zheng M, Bolli M, Simon R, Forster T, Schultz-Thater E, Remmel E, Noppen C, Schmid U, Ackermann D, Mihatsch MJ, Gasser T, Heberer M, Sauter G, Spagnoli GC (2002) Prognostic relevance of MAGE-A4 tumor antigen expression in transitional cell carcinoma of the urinary bladder: a tissue microarray study. Int J Cancer 100:702–705. https://​doi.​org/​10.​1002/​ijc.​10540 CrossRefPubMed
46.
go back to reference Jiang CQ, Fan LF, Liu ZS, Qian Q, Xia D, Diao LM, He YM, Ai ZL (2004 Oct) Expression levels and significance of hypoxia inducible factor-1 alpha and vascular endothelial growth factor in human colorectal adenocarcinoma. Chin Med J 117(10):1541–1546PubMed Jiang CQ, Fan LF, Liu ZS, Qian Q, Xia D, Diao LM, He YM, Ai ZL (2004 Oct) Expression levels and significance of hypoxia inducible factor-1 alpha and vascular endothelial growth factor in human colorectal adenocarcinoma. Chin Med J 117(10):1541–1546PubMed
48.
go back to reference Ries J, Mollaoglu N, Vairaktaris E, Neukam FW, Nkenke E (2009) Diagnostic and therapeutic relevance of NY-ESO-1 expression in oral squamous cell carcinoma. Anticancer Res 29(12):5125–5130PubMed Ries J, Mollaoglu N, Vairaktaris E, Neukam FW, Nkenke E (2009) Diagnostic and therapeutic relevance of NY-ESO-1 expression in oral squamous cell carcinoma. Anticancer Res 29(12):5125–5130PubMed
49.
go back to reference Duan Z, Duan Y, Lamendola DE, Yusuf RZ, Naeem R, Penson RT, Seiden MV (2003) Over-expression of MAGE/GAGE genes in paclitaxel/doxorubicin-resistant human cancer cell lines. Clin Cancer Res 9:2778–2785PubMed Duan Z, Duan Y, Lamendola DE, Yusuf RZ, Naeem R, Penson RT, Seiden MV (2003) Over-expression of MAGE/GAGE genes in paclitaxel/doxorubicin-resistant human cancer cell lines. Clin Cancer Res 9:2778–2785PubMed
51.
go back to reference Hartmann S, Kriegebaum U, Küchler N, Lessner G, Brands RC, Linz C, Schneider T, Kübler AC, Müller-Richter UD (2013) Efficacy of cetuximab and panitumumab in oral squamous cell carcinoma cell lines: prognostic value of MAGE-A subgroups for treatment success. J Craniomaxillofac Surg 41:623–629CrossRefPubMed Hartmann S, Kriegebaum U, Küchler N, Lessner G, Brands RC, Linz C, Schneider T, Kübler AC, Müller-Richter UD (2013) Efficacy of cetuximab and panitumumab in oral squamous cell carcinoma cell lines: prognostic value of MAGE-A subgroups for treatment success. J Craniomaxillofac Surg 41:623–629CrossRefPubMed
53.
go back to reference Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, Kammula US, Hughes MS, Restifo NP, Raffeld M, Lee CCR, Levy CL, Li YF, el-Gamil M, Schwarz SL, Laurencot C, Rosenberg SA (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29(7):917–924. https://doi.org/10.1200/JCO.2010.32.2537 CrossRefPubMedPubMedCentral Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, Kammula US, Hughes MS, Restifo NP, Raffeld M, Lee CCR, Levy CL, Li YF, el-Gamil M, Schwarz SL, Laurencot C, Rosenberg SA (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29(7):917–924. https://​doi.​org/​10.​1200/​JCO.​2010.​32.​2537 CrossRefPubMedPubMedCentral
54.
go back to reference Szmania S, Gnjatic S, Tricot G, Stone K, Zhan F, Moreno A, Thuro B, Melenhorst J, Barrett J, Shaughnessy J, Old LJ, Barlogie B, Brichard VG, van Rhee F (2007) Immunization with a recombinant MAGE-A3 protein after high-dose therapy for myeloma. J Immunother 30(8):847–854CrossRefPubMed Szmania S, Gnjatic S, Tricot G, Stone K, Zhan F, Moreno A, Thuro B, Melenhorst J, Barrett J, Shaughnessy J, Old LJ, Barlogie B, Brichard VG, van Rhee F (2007) Immunization with a recombinant MAGE-A3 protein after high-dose therapy for myeloma. J Immunother 30(8):847–854CrossRefPubMed
Metadata
Title
The expression of melanoma-associated antigen A (MAGE-A) in oral squamous cell carcinoma: an evaluation of the significance for tumor prognosis
Authors
Anna Trippel
Frank Halling
Paul Heymann
Mustafa Ayna
Bilal Al-Nawas
Thomas Ziebart
Publication date
01-09-2019
Publisher
Springer Berlin Heidelberg
Published in
Oral and Maxillofacial Surgery / Issue 3/2019
Print ISSN: 1865-1550
Electronic ISSN: 1865-1569
DOI
https://doi.org/10.1007/s10006-019-00778-x

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