Cancer testis antigens in sarcoma: Expression, function and immunotherapeutic application
Abstract
Sarcomas are a group of heterogeneous malignancies of mesenchymal origin. Patient outcomes remain especially grim for those with recurrent or metastatic disease, and current therapeutic strategies have not significantly improved outcomes over the past few decades. This has led to a number of studies assessing novel therapies. Cancer testis antigens (CTAs) are tumor-associated antigens with physiologic expression in the testis and various malignancies, including sarcomas. Genes encoding CTAs include MAGE, NY-ESO-1, PRAME, TRAG-3/CSAGE, and SSX. The importance and function of CTAs in tumorigenesis have gained recognition in recent years. They are also proving as robust diagnostic and prognostic biomarkers. Therapeutically, antigens derived from CTAs are highly recognizable by T lymphocytes and therefore capable of generating a potent antitumor immune response. CTAs are, therefore, promising targets for novel immunotherapies. Here we review the emerging works on expression, function, and immunotherapeutic application of CTAs in sarcoma therapy.
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Cancer-testis antigens comprise ubiquitin ligases that have restricted expression in normal testis but are highly overexpressed across multiple cancer types.
“Finally, cancer-testis antigens (CTAs) also comprise ubiquitin ligases that have restricted expression in the normal testis but are highly overexpressed across multiple cancer types154,155.”
From PROTAC targeted protein degraders: the past is prologue (2022) · cites this paper as [154]
Cites
Chimeric Antigen Receptor T Cells for Sustained Remissions in Leukemia
Maude, S. L., Frey, N., Shaw, P. A., Aplenc, R., Barrett, D. M., Bunin, N. J., Chew, A., Gonzalez, V. E., Zheng, Z., Lacey, S. F., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1407222 · Cited by 5,413 · see citing works
A Gene Encoding an Antigen Recognized by Cytolytic T Lymphocytes on a Human Melanoma
van der Bruggen, P., Traversari, C., Chomez, P., Lurquin, C., Plaen, E. D., den Eynde, B. J. V., Knuth, A. K., & Boon, T. (1991) · Science · doi:10.1126/science.1840703 · Cited by 3,548 · see citing works
Robbins, P. F., Morgan, R. A., Feldman, S. A., Yang, J. C.-H., Sherry, R. M., Dudley, M. E., Wunderlich, J. R., Nahvi, A. V., Helman, L. J., Mackall, C. L., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.32.2537 · Cited by 1,635 · see citing works
Cancer/testis antigens, gametogenesis and cancer
Simpson, A. J. G., Caballero, O. L., Jungbluth, A. A., Chen, Y., & Old, L. J. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1669 · Cited by 1,587 · see citing works
A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening
Chen, Y., Scanlan, M. J., Şahin, U., Türeci, Ö., Gure, A. O., Tsang, S., Williamson, B., Stockert, E., Pfreundschuh, M. G., & Old, L. J. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.5.1914 · Cited by 1,247 · see citing works
Cancer Regression and Neurological Toxicity Following Anti-MAGE-A3 TCR Gene Therapy
Morgan, R. A., Chinnasamy, N., Abate‐Daga, D., Gros, A., Robbins, P. F., Zheng, Z., Dudley, M. E., Feldman, S. A., Yang, J. C., Sherry, R. M., et al. (2013) · Journal of Immunotherapy · doi:10.1097/cji.0b013e3182829903 · Cited by 1,155 · see citing works
Ahmed, N., Brawley, V. S., Hegde, M., Robertson, C., Ghazi, A., Gerken, C., Liu, E., Dakhova, O., Ashoori, A., Corder, A., et al. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2014.58.0225 · Cited by 1,004 · see citing works
Rapoport, A. P., Stadtmauer, E. A., Binder-Scholl, G. K., Goloubeva, O. G., Vogl, D. T., Lacey, S. F., Badros, A. Z., Garfall, A. L., Weiss, B. M., Finklestein, J. M., et al. (2015) · Nature Medicine · doi:10.1038/nm.3910 · Cited by 857 · see citing works
Robbins, P. F., Kassim, S. H., Tran, T. L. N., Crystal, J. S., Morgan, R. A., Feldman, S. A., Yang, J. C., Dudley, M. E., Wunderlich, J. R., Sherry, R. M., et al. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-2708 · Cited by 807 · see citing works
Ikeda, H., Lethé, B., Lehmann, F. F., van Baren, N., Baurain, J., Smet, C. D., Chambost, H., Vitale, M., Moretta, A., Boon, T., et al. (1997) · Immunity · doi:10.1016/s1074-7613(00)80426-4 · Cited by 763 · see citing works
A Survey of the Humoral Immune Response of Cancer Patients to a Panel of Human Tumor Antigens
Stockert, E., Jäger, E., Chen, Y., Scanlan, M. J., Gout, I. T., Karbach, J., Arand, M., Knuth, A. K., & Old, L. J. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.8.1349 · Cited by 697 · see citing works
Vansteenkiste, J., Cho, B. C., Vanakesa, T., Pas, T. M. D., Zielinski, M., Kim, M. S., Jassem, J., Yoshimura, M., Dahabreh, J., Nakayama, H., et al. (2016) · The Lancet Oncology · doi:10.1016/s1470-2045(16)00099-1 · Cited by 512 · see citing works
An overview of the MAGE gene family with the identification of all human members of the family.
Chomez, P., Backer, O. D., Bertrand, M. J. M., Plaen, E. D., Boon, T., & Lucas, S. (2001) · PubMed · Cited by 485 · see citing works
CTdatabase: a knowledge-base of high-throughput and curated data on cancer-testis antigens
de Almeida, L. G. P., Sakabe, N. J., deOliveira, A. R., da Silva, M. C. C., Mundstein, A. S., Cohen, T., Chen, Y., Chua, R., Gurung, S., Gnjatic, S., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn673 · Cited by 436 · see citing works
The Human Tumor Antigen PRAME Is a Dominant Repressor of Retinoic Acid Receptor Signaling
Epping, M. T., Wang, L., Edel, M. J., Carlée, L., Hernandez, M., & Bernards, R. (2005) · Cell · doi:10.1016/j.cell.2005.07.003 · Cited by 432 · see citing works
D’Angelo, S. P., Melchiori, L., Merchant, M. S., Bernstein, D. B., Glod, J. W., Kaplan, R. N., Grupp, S. A., Tap, W. D., Chagin, K., Binder, G. K., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-1417 · Cited by 432 · see citing works
Monitoring CD8 T cell responses to NY-ESO-1: Correlation of humoral and cellular immune responses
Jäger, E., Nagata, Y., Gnjatic, S., Wada, H., Stockert, E., Karbach, J., Dunbar, P. R., Lee, S. Y., Jungbluth, A. A., Jäger, D., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4760 · Cited by 398 · see citing works
Single and Dual Amino Acid Substitutions in TCR CDRs Can Enhance Antigen-Specific T Cell Functions
Robbins, P. F., Li, Y. F., El‐Gamil, M., Zhao, Y., Wargo, J. A., Zheng, Z., Xu, H., Morgan, R. A., Feldman, S. A., Johnson, L. A., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.9.6116 · Cited by 385 · see citing works
Surgery in reference centers improves survival of sarcoma patients: a nationwide study
Blay, J., Honoré, C., Stoeckle, E., Méeus, P., Jafari, M., Gouin, F., Anract, P., Ferron, G., Rochwerger, A., ROPARS, M., et al. (2019) · Annals of Oncology · doi:10.1093/annonc/mdz124 · Cited by 338 · see citing works
Lu, Y., Parker, L. L., Lu, T., Zheng, Z., Toomey, M. A., White, D. E., Yao, X., Li, Y. F., Robbins, P. F., Feldman, S. A., et al. (2017) · Journal of Clinical Oncology · doi:10.1200/jco.2017.74.5463 · Cited by 278 · see citing works
Yang, B., O’Herrin, S. M., Wu, J., Reagan‐Shaw, S., Ma, Y., Bhat, K. M. R., Gravekamp, C., Setaluri, V., Peters, N. R., Hoffmann, F. M., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1478 · Cited by 272 · see citing works
Trama, A., Botta, L., Foschi, R., Ferrari, A., Stiller, C. A., Désandes, E., Maule, M. M., Merletti, F., & Gatta, G. (2016) · The Lancet Oncology · doi:10.1016/s1470-2045(16)00162-5 · Cited by 265 · see citing works
Türeci, Ö., Şahin, U., Schobert, I., Koslowski, M., Scmitt, H., Schild, H., Stenner, F., Seitz, G., Rammensee, H., & Pfreundschuh, M. G. (1996) · PubMed · Cited by 249 · see citing works
Expression of MAGE-antigens in normal tissues and cancer
Jungbluth, A. A., BUSAM, K. J., Kolb, D., Iversen, K., Coplan, K. A., Chen, Y., Spagnoli, G. C., & Old, L. J. (2000) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(20000215)85:4 · Cited by 214 · see citing works
Dréno, B., Thompson, J. F., Smithers, B. M., Santinami, M., Jouary, T., Gutzmer, R., Levchenko, E., Rutkowski, P. L., Grob, J., Korovin, S. I., et al. (2018) · The Lancet Oncology · doi:10.1016/s1470-2045(18)30254-7 · Cited by 204 · see citing works
Cancer/Testis Antigens: Expression, Regulation, Tumor Invasion, and Use in Immunotherapy of Cancers
Salmaninejad, A., Modarressi, M. H., Pourvahedi, M., Golchehre, Z., Bereshneh, A. H., & Rezaei, N. (2016) · Immunological Investigations · doi:10.1080/08820139.2016.1197241 · Cited by 193 · see citing works
Krishnadas, D. K., Shusterman, S., Bai, F., Diller, L., Sullivan, J. E., Cheerva, A. C., George, R. E., & Lucas, K. G. (2015) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-015-1731-3 · Cited by 176 · see citing works
Advances in immune checkpoint inhibitors for bone sarcoma therapy
Thanindratarn, P., Dean, D. C., Nelson, S. D., Hornicek, F. J., & Duan, Z. (2019) · Journal of bone oncology · doi:10.1016/j.jbo.2019.100221 · Cited by 166 · see citing works
Self-citationMage-A Cancer/Testis Antigens Inhibit p53 Function by Blocking Its Interaction with Chromatin
Marcar, L., MacLaine, N. J., Hupp, T. R., & Meek, D. W. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1341 · Cited by 158 · see citing works
Zhang, S., Kohli, K., Black, G., Lu, Y., Spadinger, S. M., He, Q., Pillarisetty, V. G., Cranmer, L. D., Tine, B. A. V., Yee, C., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0940 · Cited by 155 · see citing works
Cronwright, G., Blanc, K. L., Gotherstrom, C. O. T., D’Arcy, P., Ehnman, M., & Brodin, B. A. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-1882 · Cited by 138 · see citing works
Overexpression of MAGE/GAGE genes in paclitaxel/doxorubicin-resistant human cancer cell lines.
Duan, Z., Duan, Y., Lamendola, D. E., Yusuf, R. Z., Naeem, R., Penson, R. T., & Seiden, M. V. (2003) · PubMed · Cited by 134 · see citing works
Self-citationPollack, S. M., Jungbluth, A. A., Hoch, B. L., Farrar, E. A., Bleakley, M., Schneider, D. J., Loggers, E. T., Rodler, E. T., Eary, J. F., Conrad, E. U., et al. (2012) · Cancer · doi:10.1002/cncr.27446 · Cited by 126 · see citing works
Emerging Contributions of Cancer/Testis Antigens to Neoplastic Behaviors
Gibbs, Z. A., & Whitehurst, A. W. (2018) · Trends in cancer · doi:10.1016/j.trecan.2018.08.005 · Cited by 124 · see citing works
Lai, J.-P., Robbins, P. F., Raffeld, M. A., Aung, P. P., Tsokos, M., Rosenberg, S. A., Miettinen, M., & Lee, C. R. (2012) · Modern Pathology · doi:10.1038/modpathol.2012.31 · Cited by 122 · see citing works
Maxfield, K., Taus, P., Corcoran, K., Wooten, J., Macion, J., Zhou, Y., Borromeo, M. D., Kollipara, R. K., Yan, J., Xie, Y., et al. (2015) · Nature Communications · doi:10.1038/ncomms9840 · Cited by 120 · see citing works
Nicholaou, T., Ebert, L. M., Davis, I. D., McArthur, G. A., Jackson, H. M., Dimopoulos, N., Tan, B. S., Maraskovsky, E., Miloradovic, L., Hopkins, W., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-2484 · Cited by 119 · see citing works
Cancer-testis antigen expression in synovial sarcoma: NY-ESO-1, PRAME, MAGEA4, and MAGEA1
Iura, K., Maekawa, A., Kohashi, K., Ishii, T., Bekki, H., Otsuka, H., Yamada, Y., Yamamoto, H., Harimaya, K., Iwamoto, Y., et al. (2016) · Human Pathology · doi:10.1016/j.humpath.2016.12.006 · Cited by 110 · see citing works
Cancer/testis tumour-associated antigens: immunohistochemical detection with monoclonal antibodies
Juretić, A., Spagnoli, G. C., Schultz‐Thater, E., & Šarčević, B. (2003) · The Lancet Oncology · doi:10.1016/s1470-2045(03)00982-3 · Cited by 105 · see citing works
Nowicki, T. S., Berent-Maoz, B., Cheung-Lau, G. C., Huang, R., Wang, X., Tsoi, J., Kaplan‐Lefko, P. J., Cabrera, P. V., Tran, J., Pang, J., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-3496 · Cited by 104 · see citing works
Cyclin-dependent kinase 9 (CDK9) is a novel prognostic marker and therapeutic target in osteosarcoma
Ma, H., Seebacher, N. A., Hornicek, F. J., & Duan, Z. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.12.022 · Cited by 98 · see citing works
Self-citationBerghuis, D., de Hooge, A. S. K., Santos, S. J., Horst, D., Wiertz, E. J. H. J., van Eggermond, M. C. J. A., van den Elsen, P. J., Taminiau, A. H. M., Ottaviano, L., Schaefer, K., et al. (2009) · The Journal of Pathology · doi:10.1002/path.2537 · Cited by 94 · see citing works
NY-ESO-1 (CTAG1B) expression in mesenchymal tumors
Endo, M., de Graaff, M. A., Ingram, D. R., Lim, S., Lev, D. C., Bruijn, I. H. B., Somaiah, N., Bovée, J. V. M. G., Lazar, A. J., & Nielsen, T. O. (2014) · Modern Pathology · doi:10.1038/modpathol.2014.155 · Cited by 90 · see citing works
Multiepitope CD8+ T cell response to a NY-ESO-1 peptide vaccine results in imprecise tumor targeting
Dutoit, V., Taub, R. N., Papadopoulos, K. P., Talbot, S. M., Keohan, M. L., Brehm, M., Gnjatic, S., Harris, P. E., Bisikirska, B. C., Guillaume, P., et al. (2002) · Journal of Clinical Investigation · doi:10.1172/jci16428 · Cited by 88 · see citing works
Somaiah, N., Block, M. S., Kim, J. W., Shapiro, G. I., Do, K. T., Hwu, P., Eder, J. P., Jones, R. L., Lu, H., ter Meulen, J. H., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-1025 · Cited by 87 · see citing works
TRAG-3, a novel gene, isolated from a taxol-resistant ovarian carcinoma cell line
Duan, Z., Feller, A. J., Toh, H. C., Makastorsis, T., & Seiden, M. V. (1999) · Gene · doi:10.1016/s0378-1119(99)00042-6 · Cited by 81 · see citing works
Self-citationXAGE-1, a new gene that is frequently expressed in Ewing's sarcoma.
Liu, X. F., Helman, L. J., Yeung, C., Bera, T. K., Lee, B., & Pastan, I. H. (2000) · PubMed · Cited by 78 · see citing works
Overexpressed PRAME is a potential immunotherapy target in sarcoma subtypes
Roszik, J., Wang, W., Livingston, J. A., Roland, C. L., Ravi, V., Yee, C., Hwu, P., Futreal, P. A., Lazar, A. J., PATEL, S. R., et al. (2017) · Clinical Sarcoma Research · doi:10.1186/s13569-017-0077-3 · Cited by 78 · see citing works
Iura, K., Kohashi, K., Hotokebuchi, Y., Ishii, T., Maekawa, A., Yamada, Y., Yamamoto, H., Iwamoto, Y., & Oda, Y. (2015) · The Journal of Pathology Clinical Research · doi:10.1002/cjp2.16 · Cited by 77 · see citing works
Zendman, A. J. W., van Kraats, A. A., Weidle, U. H., Ruiter, D. J., & van Muijen, G. N. P. (2002) · International Journal of Cancer · doi:10.1002/ijc.10371 · Cited by 77 · see citing works
Immunomodulatory activity of SGI-110, a 5-aza-2′-deoxycytidine-containing demethylating dinucleotide
Coral, S., Parisi, G., Nicolay, H. J. M., Colizzi, F., Danielli, R., Fratta, E., Covre, A., Taverna, P., Sigalotti, L., & Maio, M. (2012) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-012-1365-7 · Cited by 76 · see citing works
Schultz‐Thater, E., Noppen, C., Gudat, F. G., Dürmüller, U., Zajac, P., Kocher, T., Heberer, M., & Spagnoli, G. C. (2000) · British Journal of Cancer · doi:10.1054/bjoc.2000.1251 · Cited by 75 · see citing works
Ayyoub, M., Taub, R. N., Keohan, M. L., Hesdorffer, M. E., Metthez, G., Memeo, L., MANSUKHANI, M. M., Hibshoosh, H. H., Hesdorffer, C. S., & Valmori, D. (2004) · PubMed · Cited by 75 · see citing works
Radiotherapy of Human Sarcoma Promotes an Intratumoral Immune Effector Signature
Sharma, A., Bode, B., Studer, G., Moch, H., Okoniewski, M. J., Knuth, A. K., von Boehmer, L., & van den Broek, M. F. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-0352 · Cited by 70 · see citing works
Cancer‐germline gene expression in pediatric solid tumors using quantitative real‐time PCR
Jacobs, J. F. M., Brasseur, F., de Kaa, C. A. H., van de Rakt, M. W. M. M., Figdor, C. G., Adema, G. J., Hoogerbrugge, P. M., Coulie, P. G., & de Vries, I. J. M. (2006) · International Journal of Cancer · doi:10.1002/ijc.22118 · Cited by 69 · see citing works
Hemminger, J. A., Toland, A. E., Scharschmidt, T. J., Mayerson, J. L., D, D. C. G., & Iwenofu, O. H. (2014) · Modern Pathology · doi:10.1038/modpathol.2013.244 · Cited by 64 · see citing works
Bolli, M., Kocher, T., Adamina, M., Güller, U., Dalquen, P., Haas, P., Mirlacher, M., Gambazzi, F., Harder, F. H., Heberer, M., et al. (2002) · PubMed Central · doi:10.1097/01.sla.0000036266.09823.6c · Cited by 63 · see citing works
Targeting mutant TP53 as a potential therapeutic strategy for the treatment of osteosarcoma
Tang, F., Min, L., Seebacher, N. A., Li, X., Zhou, Y., Hornicek, F. J., Wei, Y., Tu, C., & Duan, Z. (2019) · Journal of Orthopaedic Research® · doi:10.1002/jor.24227 · Cited by 63 · see citing works
Self-citationPollack, S. M., Li, Y., Blaisdell, M. J., Farrar, E. A., Chou, J., Hoch, B. L., Loggers, E. T., Rodler, E. T., Eary, J. F., Conrad, E. U., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032165 · Cited by 61 · see citing works
Expression and prognostic relevance of PRAME in primary osteosarcoma
Tan, P., Zou, C., Yong, B., Han, J., Zhang, L., Su, Q., Yin, J., Wang, J., Huang, G., Peng, T., et al. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.02.110 · Cited by 60 · see citing works
Expression of MAGE genes in osteosarcoma
Sudo, T., Kuramoto, T., Komiya, S., Inoue, A., & Itoh, K. (1997) · Journal of Orthopaedic Research® · doi:10.1002/jor.1100150119 · Cited by 57 · see citing works
Tissue Microarray Evaluation of Melanoma Antigen E (MAGE) Tumor-Associated Antigen Expression
Bolli, M., Kocher, T., Adamina, M., Güller, U., Dalquen, P., Haas, P., Mirlacher, M., Gambazzi, F., Harder, F. H., Heberer, M., et al. (2002) · Annals of Surgery · doi:10.1097/00000658-200212000-00011 · Cited by 57 · see citing works
Hemminger, J. A., Toland, A. E., Scharschmidt, T. J., Mayerson, J. L., Kraybill, W. G., D, D. C. G., & Iwenofu, O. H. (2012) · Modern Pathology · doi:10.1038/modpathol.2012.133 · Cited by 56 · see citing works
Krishnadas, D. K., Bao, L., Bai, F., Chencheri, S. C., & Lucas, K. G. (2014) · Tumor Biology · doi:10.1007/s13277-014-1764-9 · Cited by 54 · see citing works
Expression and Therapeutic Potential of SOX9 in Chordoma
Chen, H., Garbutt, C. C., Spentzos, D., Choy, E., Hornicek, F. J., & Duan, Z. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0177 · Cited by 54 · see citing works
Self-citationZou, C., Shen, J., Tang, Q., Zheng, Y., Yin, J., Li, Z., Xie, X., Huang, G., Lev, D. C., & Wang, J. (2011) · Cancer · doi:10.1002/cncr.26486 · Cited by 52 · see citing works
Iura, K., Kohashi, K., Ishii, T., Maekawa, A., Bekki, H., Otsuka, H., Yamada, Y., Yamamoto, H., Matsumoto, Y., Iwamoto, Y., et al. (2017) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-017-2206-z · Cited by 50 · see citing works
Peptide Vaccine Induces Enhanced Tumor Growth Associated with Apoptosis Induction in CD8+ T Cells
Muraoka, D., Kato, T., Wang, L., Maeda, Y., Noguchi, T., Harada, N., Takeda, K., Yagita∥, H., Guillaume, P., Luescher, I. F., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903649 · Cited by 49 · see citing works
Hemminger, J. A., & Iwenofu, O. H. (2013) · Modern Pathology · doi:10.1038/modpathol.2013.65 · Cited by 47 · see citing works
D’Arcy, P., Maruwge, W., Wolahan, B., Ma, L., & Brodin, B. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0095136 · Cited by 44 · see citing works
Marcar, L., Ihrig, B., Hourihan, J. M., Bray, S. E., Quinlan, P., Jordan, L. B., Thompson, A. M., Hupp, T. R., & Meek, D. W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127713 · Cited by 42 · see citing works
Membrane‐associated phospholipase A1 beta (LIPI) Is an Ewing tumour‐associated cancer/testis antigen
Foell, J. L., Hesse, M., Volkmer, I., Schmiedel, B. J., Neumann, I., & Staege, M. S. (2008) · Pediatric Blood & Cancer · doi:10.1002/pbc.21602 · Cited by 40 · see citing works
Luk, S. J., van der Steen, D. M., Hagedoorn, R. S., Jordanova, E. S., Schilham, M. W., Bovée, J. V. M. G., Cleven, A. H. G., Falkenburg, J. H. F., Szuhai, K., & Heemskerk, M. H. M. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1507600 · Cited by 40 · see citing works
Ectopic expression of cancer/testis antigen SSX2 induces DNA damage and promotes genomic instability
Greve, K. B. V., Lindgreen, J., Terp, M. G., Pedersen, C. B., Schmidt, S., Mollenhauer, J., Kristensen, S. B., Andersen, R. S., Relster, M. M., Ditzel, H. J., et al. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.09.001 · Cited by 36 · see citing works
Cancer/testis antigen CSAGE is concurrently expressed with MAGE in chondrosarcoma
Lin, C., Mak, S., Meitner, P. A., Wolf, J. M., Bluman, E. M., Block, J. A., & Terek, R. M. (2002) · Gene · doi:10.1016/s0378-1119(02)00395-5 · Cited by 33 · see citing works
Identification of HLA-A*0201-restricted cytotoxic T lymphocyte epitope from TRAG-3 antigen.
Zhu, B., Chen, Z., Cheng, X., Lin, Z., Guo, J., Jia, Z., Zou, L., Wang, Z., Hu, Y., Wang, D., et al. (2003) · PubMed · Cited by 33 · see citing works
Feller, A. J., Duan, Z., Penson, R. T., Toh, H., & Seiden, M. V. (2000) · PubMed · Cited by 32 · see citing works
Self-citationExpression of SSX genes in human osteosarcomas
Naka, N., Araki, N., Nakanishi, H., Itoh, K., Mano, M., Ishiguro, S., de Bruijn, D. R. H., Myoui, A., Ueda, T., & Yoshikawa, H. (2002) · International Journal of Cancer · doi:10.1002/ijc.10277 · Cited by 30 · see citing works
Fujiwara, H. (2014) · Pharmaceuticals · doi:10.3390/ph7121049 · Cited by 25 · see citing works
Characterization of Ewing sarcoma associated cancer/testis antigens
Mahlendorf, D. E., & Staege, M. S. (2013) · Cancer Biology & Therapy · doi:10.4161/cbt.23298 · Cited by 24 · see citing works
Effects of CT-Xp Gene Knock down in Melanoma Cell Lines
Caballero, O. L., Cohen, T., Gurung, S., Chua, R. A., Lee, P., Chen, Y., Jat, P., & Simpson, A. J. G. (2013) · Oncotarget · doi:10.18632/oncotarget.921 · Cited by 24 · see citing works
Li, X., Seebacher, N. A., Xiao, T., Hornicek, F. J., & Duan, Z. (2018) · Journal of Orthopaedic Research® · doi:10.1002/jor.24189 · Cited by 24 · see citing works
Self-citationMAGE antigen expression in monophasic and biphasic synovial sarcoma
Antonescu, C. R., BUSAM, K. J., Iversen, K., Kolb, D., Coplan, K. A., Spagnoli, G. C., Ladanyi, M., Old, L. J., & Jungbluth, A. A. (2002) · Human Pathology · doi:10.1053/hupa.2002.31295 · Cited by 23 · see citing works
Immunotherapy in Sarcoma: Future Horizons
Burgess, M. A., Gorantla, V. C., Weiss, K. R., & Tawbi, H. A. (2015) · Current Oncology Reports · doi:10.1007/s11912-015-0476-7 · Cited by 21 · see citing works
Materna, V., Surowiak, P., Kaplenko, I., Spaczyński, M., Duan, Z., Zabel, M., Dietel, M., & Lage, H. (2007) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-006-0346-7 · Cited by 21 · see citing works
Self-citationSpontaneous CD4+ T Cell Responses against TRAG-3 in Patients with Melanoma and Breast Cancers
Janjic, B. M., Andrade, P., Wang, X., Fourcade, J. J., Almunia, C., Kudela, P., Brufsky, A., Jacobs, S. A., Friedland, D., Stoller, R. G., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.4.2717 · Cited by 20 · see citing works
Altvater, B., Kailayangiri, S., Theimann, N., Ahlmann, M., Farwick, N., Chen, C. I.-U., Pscherer, S., Neumann, I., Mrachatz, G., Hansmeier, A., et al. (2014) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-014-1574-3 · Cited by 20 · see citing works
Schmiedel, B. J., Hutter, C., Hesse, M., & Staege, M. S. (2010) · Molecular Biology Reports · doi:10.1007/s11033-010-0595-z · Cited by 19 · see citing works
Liu, S., Liu, F., Huang, W., Gu, L., Meng, L., Ju, Y., Wu, Y., Li, J., Liu, L., & Sang, M. (2017) · Oncotarget · doi:10.18632/oncotarget.22973 · Cited by 19 · see citing works
Xu, J. H., Guo, W., & Xie, L. (2018) · BMC Cancer · doi:10.1186/s12885-018-4872-x · Cited by 19 · see citing works
Self-citationShurell, E., Vergara‐Lluri, M., Li, Y., Crompton, J. G., Singh, A. S., Bernthal, N. M., Wu, H., Eilber, F. C., & Dry, S. (2016) · Oncotarget · doi:10.18632/oncotarget.12096 · Cited by 18 · see citing works
Naka, N., Joyama, S., Tsukamoto, Y., Yoshioka, K., Hashimoto, N., Ujiiye, T., Hayashi, T., Kawase, M., Mano, M., Ishiguro, S., et al. (2005) · Journal of Molecular Diagnostics · doi:10.1016/s1525-1578(10)60545-4 · Cited by 16 · see citing works
Insights on PRAME and osteosarcoma by means of gene expression profiling
de Toledo, S. R. C., Oliveira, I. D., Tesser‐Gamba, F., Torre, C. A. D., Alves, M. T. D. S., Jesús-García, R., Petrilli, A. S., Zago, M. A., Proto‐Siqueira, R., Silva, W. A., et al. (2011) · Journal of Orthopaedic Science · doi:10.1007/s00776-011-0106-7 · Cited by 15 · see citing works
MAGEA1 inhibits the expression of BORIS via increased promoter methylation
Zhao, J., Wang, Y., Liang, Q., Xu, Y., & Sang, J. (2018) · Journal of Cell Science · doi:10.1242/jcs.218628 · Cited by 15 · see citing works
Chawla, S. P., Tine, B. A. V., Pollack, S. M., Ganjoo, K. N., ELIAS, A. D., Riedel, R. F., Attia, S., Choy, E., Okuno, S. H., Agulnik, M., et al. (2017) · Annals of Oncology · doi:10.1093/annonc/mdx387.007 · Cited by 13 · see citing works
Ohta, M., Tanaka, F., Sadanaga, N., Yamaguchi, H., INOUE, H. K., & Mori, M. (2006) · Oncology Reports · doi:10.3892/or.15.6.1529 · Cited by 11 · see citing works
Expression of TRAG‐3 in breast cancer
Wu, Y., Zhao, T., Ni, B., Zou, L., Liu, H., & Zhu, B. (2003) · International Journal of Cancer · doi:10.1002/ijc.11349 · Cited by 7 · see citing works
Flagged first, then by citations
7 of the 104 references couldn’t be matched to a known paper.
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Sorted by citations
PROTAC targeted protein degraders: the past is prologue
Békés, M., Langley, D. R., & Crews, C. M. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00371-6 · Cited by 3,395 · see citing works
Dugage, M. R., Nassif, E. F., Italiano, A., & Bahleda, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.775761 · Cited by 96 · see citing works
Virus-like Particle (VLP) Vaccines for Cancer Immunotherapy
Ruzzi, F., Semprini, M. S., Scalambra, L., Palladini, A., Angelicola, S., Cappello, C., Pittino, O. M., Nanni, P., & Lollini, P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241612963 · Cited by 46 · see citing works
The potential and promise for clinical application of adoptive T cell therapy in cancer
Li, Y., Zheng, Y., Liu, T., Liao, C., Shen, G., & He, Z. (2024) · Journal of Translational Medicine · doi:10.1186/s12967-024-05206-7 · Cited by 39 · see citing works
Albertsmeier, M., Altendorf-Hofmann, A., Lindner, L. H., Issels, R. D., Kampmann, E., Dürr, H. R., Schubert-Fritschle, G., Angele, M. K., Kirchner, T., Jungbluth, A. A., et al. (2020) · Cancers · doi:10.3390/cancers12123612 · Cited by 36 · see citing works
Nakata, E., Fujiwara, T., Kunisada, T., Ito, T., Takihira, S., & Ozaki, T. (2021) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyab005 · Cited by 35 · see citing works
Cancer testis antigen subfamilies: Attractive targets for therapeutic vaccine (Review)
Ren, S., Zhang, Z., Li, M., Wang, D., Guo, R., Fang, X., & Chen, F. (2023) · International Journal of Oncology · doi:10.3892/ijo.2023.5519 · Cited by 30 · see citing works
Li, X., Ren, P., Shen, W.-Z., Jin, X., & Zhang, J. (2020) · PubMed Central · Cited by 29 · see citing works
Immunotherapy and Biomarkers in Sarcoma
Dajsakdipon, T., Siripoon, T., Ngamphaiboon, N., Ativitavas, T., & Dejthevaporn, T. S. (2022) · Current Treatment Options in Oncology · doi:10.1007/s11864-022-00944-6 · Cited by 29 · see citing works
Tertiary lymphoid structures in cancer: immune mechanisms and clinical implications
Wang, S., Wang, H., Li, C., Liu, B., He, S., & Tu, C. (2024) · MedComm · doi:10.1002/mco2.489 · Cited by 25 · see citing works
CAR T-cells to treat brain tumors
Guzman, G., Pellot, K., Reed, M. R., & Rodriguez, A. (2023) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2023.02.014 · Cited by 27 · see citing works
Wang, W.-L., Gökgöz, N., Samman, B., Andrulis, I. L., Wunder, J. S., & Demicco, E. G. (2020) · Modern Pathology · doi:10.1038/s41379-020-00687-5 · Cited by 24 · see citing works
Exploring the landscape of immunotherapy approaches in sarcomas
Pilavaki, P., Panagi, M., Arifi, S., Jones, R. L., Stylianopoulos, T., & Constantinidou, A. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2022.1069963 · Cited by 17 · see citing works
PRAME protein expression in DICER1 ‐related tumours
Thorner, P. S., Chong, A., Nadaf, J., Benlimame, N., Marrano, P. M., Chami, R., Fu, L., & Foulkes, W. D. (2022) · The Journal of Pathology Clinical Research · doi:10.1002/cjp2.264 · Cited by 15 · see citing works
Sarcoma Immunotherapy: Confronting Present Hurdles and Unveiling Upcoming Opportunities
Jeong, S., Afroz, S., Kang, D., Noh, J., Suh, J., Kim, J. H., You, H. J., Kang, H. G., Kim, Y., & Kim, J. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.0079 · Cited by 15 · see citing works
Baldi, G. G., Gronchi, A., Tazzari, M., & Stacchiotti, S. (2022) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2022.2065986 · Cited by 15 · see citing works
Cancer-Associated B Cells in Sarcoma
Kendal, J. K., Shehata, M. S., Lofftus, S. Y., & Crompton, J. G. (2023) · Cancers · doi:10.3390/cancers15030622 · Cited by 11 · see citing works
Advances in the Molecular Biology of Chondrosarcoma for Drug Discovery and Precision Medicine
Walker, R. L., Hornicek, F. J., & Duan, Z. (2025) · Cancers · doi:10.3390/cancers17162689 · Cited by 10 · see citing works
Self-citationCadwell, C. R., Yuksek, G. E., Hirbe, A. C., Srihari, D., LeBoit, P., Dahiya, S. M., & Pekmezci, M. (2020) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlaa125 · Cited by 10 · see citing works
Inhibiting ALK-TOPK signaling pathway promotes cell apoptosis of ALK-positive NSCLC
Xiao, J., Zhang, L., Yi, H., Zou, L., Mo, J., Xue, F., Zheng, J., Huang, Y., Lü, H., Wu, H., et al. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05260-3 · Cited by 9 · see citing works
Avdonkina, N. A., Danilova, A. B., Misyurin, V. A., Prosekina, E. A., Girdyuk, D. V., Emelyanova, N. V., Нехаева, Т. Л., Гафтон, Г. И., & Балдуева, И. А. (2020) · Pathology - Research and Practice · doi:10.1016/j.prp.2020.153214 · Cited by 8 · see citing works
Leveraging Cancer Phenotypic Plasticity for Novel Treatment Strategies
Ramisetty, S. K., Subbalakshmi, A. R., Pareek, S., Mirzapoiazova, T., Do, D., Prabhakar, D., Pisick, E. P., Shrestha, S., Achuthan, S., Bhattacharya, S., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13113337 · Cited by 8 · see citing works
SCAN-ACT: adoptive T cell therapy target discovery through single-cell transcriptomics
Testa, S., Pal, A., Subramanian, A., Varma, S., Tang, J. P., Graham, D., Arfan, S., Pan, M., Bui, N. Q., Ganjoo, K. N., et al. (2025) · Genome Medicine · doi:10.1186/s13073-025-01514-9 · Cited by 6 · see citing works
Sapozhnikova, K. A., Misyurin, A. V., Pestov, N. B., Мелешкина, Е. Г., Oreshkov, S. D., Ganzhula, E. P., Mikhailova, A. S., Аркадьевич, К. В., Misyurin, V. A., & Brylev, V. A. (2021) · Russian Journal of Bioorganic Chemistry · doi:10.1134/s1068162021050332 · Cited by 6 · see citing works
Nishio, J., Nakayama, S., & Aoki, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021127 · Cited by 6 · see citing works
Esperança‐Martins, M., Vasques, H., Ravasqueira, M. S., Lemos, M. M., Fonseca, F., Coutinho, D., López, J. A., Huang, R. S. P., Dias, S., Gallego-Paez, L. M., et al. (2025) · Cancers · doi:10.3390/cancers17172861 · Cited by 5 · see citing works
Oliva, J., Milewski, D., Banks, L. B., Bailey, K. M., Moding, E. J., Lake, J. A., Chen, A. P., Daley, J. D., Resch, E. E., Kaplan, R. N., et al. (2025) · Cancers · doi:10.3390/cancers17183068 · Cited by 5 · see citing works
Vanacker, H., Connacher, R., Meurgey, A., Bollard, J., Attignon, V., Tirode, F., Jean‐Denis, M., Brahmi, M., Blay, J., Wang, R., et al. (2024) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000541 · Cited by 5 · see citing works
Zainodini, N., Abolhasani, M., Mohsenzadegan, M., Farajollahi, M. M., & Rismani, E. (2024) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-024-05694-6 · Cited by 4 · see citing works
Chen, A., Qiu, Y., Yen, Y., Chun, W., Wang, X., Li, C., Wei, Z., Li, L., Yu, L., Liu, F., et al. (2025) · Cancer Medicine · doi:10.1002/cam4.70750 · Cited by 4 · see citing works
Evaluation of Production Protocols for the Generation of NY-ESO-1-Specific T Cells
Gong, W., Wang, L., Stock, S., Ni, M., Schubert, M., Neuber, B., Kleist, C., Hückelhoven‐Krauss, A., Wu, D., Müller‐Tidow, C., et al. (2021) · Cells · doi:10.3390/cells10010152 · Cited by 4 · see citing works
Lin, L., Zou, X., Nong, W., Ge, Y., Li, F., Luo, B., Zhang, Q., & Xie, X. (2024) · Immunity Inflammation and Disease · doi:10.1002/iid3.1284 · Cited by 4 · see citing works
Kido, T., & Lau, Y. C. (2025) · Cell & Bioscience · doi:10.1186/s13578-025-01432-8 · Cited by 3 · see citing works
Exploring CX3CR1 as a prognostic biomarker and immunotherapeutic target in sarcoma
Li, T., Li, X., Kang, P., & Zhao, J. (2025) · Translational Oncology · doi:10.1016/j.tranon.2025.102283 · Cited by 3 · see citing works
Murata, K., Minowa, T., Tsukahara, T., Yoshida, T., Minami, A., Nakatsugawa, M., Mizue, Y., Murai, A., Tokita, S., Sasaki, K., et al. (2025) · OncoImmunology · doi:10.1080/2162402x.2025.2528110 · Cited by 3 · see citing works
miRNAs as Biomarkers and Possible Therapeutic Strategies in Synovial Sarcoma
Jiang, S., Hu, Y., Zhou, Y., Tang, G., Cui, W., Wang, X., Chen, B., Hu, Z., & Xu, B. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.881007 · Cited by 3 · see citing works
Corbin, H., Neyaz, A., Jones, T. E., Clark, B. Z., Yu, J., Fine, J. L., John, I., & Bhargava, R. (2025) · American Journal of Clinical Pathology · doi:10.1093/ajcp/aqaf084 · Cited by 2 · see citing works
Lack of PRAME Expression in Cutaneous T-Cell Lymphomas
Bui, C. M., Kitahara, S., Shon, W., Pukhalskaya, T., & Smoller, B. R. (2021) · Dermatopathology · doi:10.3390/dermatopathology9010002 · Cited by 1 · see citing works
Enhanced immune responses are accompanied by increased MAGEA expression in osteosarcoma metastases
Meijer, D. M., van Oost, S., Roelands, J. P., Ruano, D., Bruijn, I. H. B., van den Akker, B. E., Kruisselbrink, A. B., Wijers‐Koster, P. M., van der Ploeg, M., Ijsselsteijn, M. E., et al. (2024) · BMJ Oncology · doi:10.1136/bmjonc-2024-000472 · Cited by 1 · see citing works
Liang, S.-X., Fang, H., Chen, W., & Yan, Y. (2021) · Journal of Hard Tissue Biology · doi:10.2485/jhtb.30.283 · Cited by 1 · see citing works
Lin, X., Huo, J., Su, H., Xu, Y., & Zhang, F. (2023) · Clinical Breast Cancer · doi:10.1016/j.clbc.2023.09.017 · Cited by 1 · see citing works
Esperança‐Martins, M., Vasques, H., Ravasqueira, M. S., Lemos, M. M., Fonseca, F., Coutinho, D., López, J. A., Huang, R. S. P., Dias, S., Gallego-Paez, L. M., et al. (2025) · medRxiv · doi:10.1101/2025.01.31.25321492 · Cited by 1 · see citing works
Advances in the Molecular Biology of Chondrosarcoma
Duan, Z., Dean, D. C., Bukata, S. V., & Hornicek, F. J. (2021) · Springer eBooks · doi:10.1007/978-3-030-74572-1_2
Self-citationZNF165 as a potential novel immunotherapeutic target for gastric cancerPreprint
Zhang, F., Shao, K., He, P., Xiang, L., Wu, W., Zhang, P., Maswikiti, E. P., Wei, Y., Wang, F., Tang, F., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1942312/v1
Gallas, L. F., Pacca, A. M., & Natal, R. D. A. (2024) · Surgical and Experimental Pathology · doi:10.1186/s42047-024-00168-y
Role of adoptive cell therapy in cancer immunotherapy
Puri, G., Singh, B. K., & Ranjan, P. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-41551-7.00004-7
The evolution of cellular therapies in sarcoma: Breakthroughs, challenges, and future directions
Wannaphut, C., Thirasastr, P., Livingston, J., Araujo, D. M., Conley, A. P., Keung, E. Z.-Y., Roland, C. L., & Somaiah, N. (2026) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2026.2708435
Torrado, C., & Conley, A. P. (2026) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2026.2734584
- Authors
- Wei, R., Dean, D. C., Thanindratarn, P., Hornicek, F. J., Guo, W., & Duan, Z.
- Affiliations
- University of California, Los Angeles (US)
- Peking University People's Hospital (CN)
- Corresponding author
- Guo, Wei
- Duan, Zhenfeng
- Venue
- Cancer Letters
- Publisher
- Elsevier BV
- Published
- 2020-06
- Volume
- 479
- Pages
- 54-60
- ISSN
- 0304-3835 (ISSN-L)
- OpenAlex
- W2980627006
- Cited by
- 48
- References
- 104
- Citations by year
- 2026: 3 · 2025: 10 · 2024: 9 · 2023: 7 · 2022: 7 · 2021: 7 · 2020: 5
- FWCI
- 0.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cancer Letters (publishedVersion)
- PubMed (publishedVersion)
- Funders
- UCLA
- Sarcoma Foundation of America (222433)
- National Cancer Institute
- National Institutes of Health (UO1, CA151452-01)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- cancer-testis antigens, sarcoma, MAGE, NY-ESO-1, PRAME, SSX, tumor-associated antigens, cancer immunotherapy, diagnostic biomarkers, prognostic factors, antitumor immunity, carcinogenesis
- MeSH terms
- Antigens, Neoplasm, Humans, Immunotherapy, Sarcoma, T-Lymphocytes, Biomarkers, Tumor, Gene Expression Regulation, Neoplastic
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