Cancer testis antigen subfamilies: Attractive targets for therapeutic vaccine (Review)

Cancer-testis antigen (CTA) is a well-accepted optimal target library for cancer diagnosis and treatment. Most CTAs are located on the X chromosome and aggregate into large gene families, such as the melanoma antigen, synovial sarcoma X and G antigen families. Members of the CTA subfamily are usually co-expressed in tumor tissues and share similar structural characteristics and biological functions. As cancer vaccines are recommended to induce specific antitumor responses, CTAs, particularly CTA subfamilies, are widely used in the design of cancer vaccines. To date, DNA, mRNA and peptide vaccines have been commonly used to generate tumor-specific CTAs in vivo and induce anticancer effects. Despite promising results in preclinical studies, the antitumor efficacy of CTA-based vaccines is limited in clinical trials, which may be partially attributed to weak immunogenicity, low efficacy of antigen delivery and presentation processes, as well as a suppressive immune microenvironment. Recently, the development of nanomaterials has enhanced the cancer vaccination cascade, improved the antitumor performance and reduced off-target effects. The present study provided an in-depth review of the structural characteristics and biofunctions of the CTA subfamilies, summarised the design and utilisation of CTA-based vaccine platforms and provided recommendations for developing nanomaterial-derived CTA-targeted vaccines.

[1]  Yaming Zhou,et al.  Hybrid Nanomaterials for Cancer Immunotherapy , 2022, Advanced science.

[2]  Y. Liu,et al.  Safety and Outcomes of a Plasmid DNA Vaccine Encoding the ERBB2 Intracellular Domain in Patients With Advanced-Stage ERBB2-Positive Breast Cancer: A Phase 1 Nonrandomized Clinical Trial. , 2022, JAMA oncology.

[3]  Jingjing Deng,et al.  Phospholipid-Membrane-Based Nanovesicles Acting as Vaccines for Tumor Immunotherapy: Classification, Mechanisms and Applications , 2022, Pharmaceutics.

[4]  Xing Huang,et al.  Personalized pancreatic cancer therapy: from the perspective of mRNA vaccine , 2022, Military Medical Research.

[5]  I. Svane,et al.  Clinical advances and ongoing trials of mRNA vaccines for cancer treatment , 2022, The Lancet Oncology.

[6]  J. Valdés,et al.  Plasmid DNA for Therapeutic Applications in Cancer , 2022, Pharmaceutics.

[7]  Matthew J. Davis,et al.  Individualized, heterologous chimpanzee adenovirus and self-amplifying mRNA neoantigen vaccine for advanced metastatic solid tumors: phase 1 trial interim results , 2022, Nature Medicine.

[8]  M. Akagi,et al.  Clinicopathological assessment of cancer/testis antigens NY-ESO-1 and MAGE-A4 in osteosarcoma , 2022, European journal of histochemistry : EJH.

[9]  Jianxun Song,et al.  mRNA Vaccines: The Dawn of a New Era of Cancer Immunotherapy , 2022, Frontiers in Immunology.

[10]  N. Sobhani,et al.  Therapeutic cancer vaccines: From biological mechanisms and engineering to ongoing clinical trials , 2022, Cancer Treatment Reviews.

[11]  V. Čapkun,et al.  Prognostic Significance of Lymphocyte Infiltrate Localization in Triple-Negative Breast Cancer , 2022, Journal of personalized medicine.

[12]  Dong Yang,et al.  Potentialities and Challenges of mRNA Vaccine in Cancer Immunotherapy , 2022, Frontiers in Immunology.

[13]  J. Futami,et al.  Engineering Cancer/Testis Antigens With Reversible S-Cationization to Evaluate Antigen Spreading , 2022, Frontiers in Oncology.

[14]  Longfei Liang,et al.  Cancer germline antigen gene MAGEB2 promotes cell invasion and correlates with immune microenvironment and immunotherapeutic efficiency in laryngeal cancer. , 2022, Clinical immunology.

[15]  Y. Kodera,et al.  Prognostic significance of NY-ESO-1 antigen and PIGR expression in esophageal tumors of CHP-NY-ESO-1-vaccinated patients as adjuvant therapy , 2022, Cancer Immunology, Immunotherapy.

[16]  C. Poh,et al.  Development of Peptide-Based Vaccines for Cancer , 2022, Journal of oncology.

[17]  Chi Zhang,et al.  Modification of Lipid-Based Nanoparticles: An Efficient Delivery System for Nucleic Acid-Based Immunotherapy , 2022, Molecules.

[18]  D. Tan,et al.  mRNA cancer vaccines: Advances, trends and challenges , 2022, Acta Pharmaceutica Sinica B.

[19]  Jianzhu Chen,et al.  Current Developments and Challenges of mRNA Vaccines. , 2022, Annual review of biomedical engineering.

[20]  M. Hirsch,et al.  Expression of the C‐terminal region of the SSX protein is a useful diagnostic biomarker for spermatocytic tumour , 2021, Histopathology.

[21]  Jingping Li,et al.  Pathogenicity of the MAGE family , 2021, Oncology letters.

[22]  P. Tailor,et al.  Delivery of a Cancer-Testis Antigen-Derived Peptide Using Conformationally Restricted Dipeptide-Based Self-Assembled Nanotubes. , 2021, Molecular pharmaceutics.

[23]  Yanchun Peng,et al.  Distinct tumour antigen-specific T-cell immune response profiles at different hepatocellular carcinoma stages , 2021, BMC cancer.

[24]  T. Tan,et al.  GAGE mediates radio resistance in cervical cancers via the regulation of chromatin accessibility. , 2021, Cell reports.

[25]  A. Ballabio,et al.  Autophagy in major human diseases , 2021, The EMBO journal.

[26]  Aishik Chakraborty,et al.  Biomaterials, biological molecules, and polymers in developing vaccines. , 2021, Trends in pharmacological sciences.

[27]  D. Roy,et al.  Adjuvant oncolytic virotherapy for personalized anti-cancer vaccination , 2021, Nature Communications.

[28]  Xu Wang,et al.  Cancer/Testis Antigens: from Serology to mRNA Cancer Vaccine. , 2021, Seminars in cancer biology.

[29]  L. Pang,et al.  The role of SYT-SSX fusion gene in tumorigenesis of synovial sarcoma. , 2021, Pathology, research and practice.

[30]  Xiangyi Wang,et al.  Peptide‐based therapeutic cancer vaccine: Current trends in clinical application , 2021, Cell proliferation.

[31]  A. Heine,et al.  Clinical and immunological effects of mRNA vaccines in malignant diseases , 2021, Molecular Cancer.

[32]  K. Breckpot,et al.  mRNA in cancer immunotherapy: beyond a source of antigen , 2021, Molecular cancer.

[33]  Leaf Huang,et al.  mRNA vaccine for cancer immunotherapy , 2021, Molecular cancer.

[34]  Xin Zhao,et al.  Biomimetic cytomembrane nanovaccines prevent breast cancer development in the long term. , 2021, Nanoscale.

[35]  Tianliang Li,et al.  Nanobiomaterial-based vaccination immunotherapy of cancer. , 2021, Biomaterials.

[36]  Jie Chen,et al.  Development and Validation of Epigenetic Signature Predict Survival for Patients with Laryngeal Squamous Cell Carcinoma. , 2020, DNA and cell biology.

[37]  M. Takahara,et al.  Expression of placenta-specific 1 and its potential for eliciting anti-tumor helper T-cell responses in head and neck squamous cell carcinoma , 2020, Oncoimmunology.

[38]  A. Abdollahi,et al.  Expression and Prognostic Significance of Cancer/Testis Antigens, MAGE-E1, GAGE, and SOX-6, in Glioblastoma: An Immunohistochemistry Evaluation , 2020, Iranian journal of pathology.

[39]  H. Rammensee,et al.  The peptide vaccine of the future. , 2020, Molecular & cellular proteomics : MCP.

[40]  M. Wadman Public needs to prep for vaccine side effects. , 2020, Science.

[41]  M. de la Guardia,et al.  Strategies in DNA vaccine for melanoma cancer , 2020, Pigment cell & melanoma research.

[42]  K. Fon Tacer,et al.  Emerging roles of the MAGE protein family in stress response pathways , 2020, The Journal of Biological Chemistry.

[43]  Y. Ghasemi,et al.  In Silico Design and Evaluation of PRAME+FliCΔD2D3 as a New Breast Cancer Vaccine Candidate , 2020, Iranian journal of medical sciences.

[44]  Xun Sun,et al.  Engineering nanoparticulate vaccines for enhancing antigen cross-presentation. , 2020, Current opinion in biotechnology.

[45]  J. Utikal,et al.  An RNA vaccine drives immunity in checkpoint-inhibitor-treated melanoma , 2020, Nature.

[46]  D. Kutilin Regulation of Gene Expression of Cancer/Testis Antigens in Colorectal Cancer Patients , 2020, Molecular Biology.

[47]  Y. Wen,et al.  Controllable synthesis of versatile mesoporous organosilica nanoparticles as precision cancer theranostics. , 2020, Biomaterials.

[48]  M. Sang,et al.  Epigenetic modulation combined with PD-1/PD-L1 blockade enhances immunotherapy based on MAGE-A11 antigen-specific CD8+ T cells against esophageal carcinoma. , 2020, Carcinogenesis.

[49]  Wei Guo,et al.  Cancer Testis Antigens in Sarcoma: Expression, Function and Immunotherapeutic Application. , 2020, Cancer letters.

[50]  S. Uddin,et al.  Unleashing the immune response to NY-ESO-1 cancer testis antigen as a potential target for cancer immunotherapy , 2020, Journal of Translational Medicine.

[51]  J. Dou,et al.  Decreasing New York esophageal squamous cell carcinoma 1 expression inhibits multiple myeloma growth and osteolytic lesions , 2020, Journal of cellular physiology.

[52]  M. Gjerstorff,et al.  Interaction between Polycomb and SSX Proteins in Pericentromeric Heterochromatin Function and Its Implication in Cancer , 2020, Cells.

[53]  S. Gupta,et al.  Immunogenicity and contraceptive efficacy of recombinant fusion protein encompassing Sp17 spermatozoa‐specific protein and GnRH: Relevance of adjuvants and microparticles based delivery to minimize number of injections , 2019, American journal of reproductive immunology.

[54]  Michael R Hamblin,et al.  Comparison of DNA and mRNA vaccines against cancer. , 2019, Drug discovery today.

[55]  Weiwei Huang,et al.  Development of novel nanoantibiotics using an outer membrane vesicle-based drug efflux mechanism. , 2019, Journal of controlled release : official journal of the Controlled Release Society.

[56]  G. Sethi,et al.  Engineering anti-cancer nanovaccine based on antigen cross-presentation , 2019, Bioscience reports.

[57]  Guizhi Zhu,et al.  Nanovaccines for cancer immunotherapy. , 2019, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[58]  N. Munshi,et al.  BCMA peptide-engineered nanoparticles enhance induction and function of antigen-specific CD8+ cytotoxic T lymphocytes against multiple myeloma: clinical applications , 2019, Leukemia.

[59]  Hang Su,et al.  Cancer stem-like cells with increased expression of NY-ESO-1 initiate breast cancer metastasis , 2019, Oncology letters.

[60]  Jiaming Yu,et al.  Expression of New York esophageal squamous cell carcinoma 1 and its association with Foxp3 and indoleamine‐2,3‐dioxygenase in microenvironment of nonsmall cell lung cancer , 2019, HLA.

[61]  Robin L. Jones,et al.  First-in-Class, First-in-Human Study Evaluating LV305, a Dendritic-Cell Tropic Lentiviral Vector, in Sarcoma and Other Solid Tumors Expressing NY-ESO-1 , 2019, Clinical Cancer Research.

[62]  L. Sellner,et al.  Comparison of IL-2 vs IL-7/IL-15 for the generation of NY-ESO-1-specific T cells , 2019, Cancer Immunology, Immunotherapy.

[63]  Junmin Peng,et al.  Regulation of MAGE‐A3/6 by the CRL4‐DCAF12 ubiquitin ligase and nutrient availability , 2019, EMBO reports.

[64]  Shondra M. Pruett-Miller,et al.  MAGE cancer-testis antigens protect the mammalian germline under environmental stress , 2019, Science Advances.

[65]  G. Vandermeulen,et al.  Cancer DNA vaccines: current preclinical and clinical developments and future perspectives , 2019, Journal of experimental & clinical cancer research : CR.

[66]  A. Farooqi,et al.  Nanoparticle systems for cancer vaccine. , 2019, Nanomedicine.

[67]  D. Atanackovic,et al.  A phase I/IIa study of the mRNA-based cancer immunotherapy CV9201 in patients with stage IIIB/IV non-small cell lung cancer , 2019, Cancer Immunology, Immunotherapy.

[68]  S. Koch,et al.  Phase Ib evaluation of a self-adjuvanted protamine formulated mRNA-based active cancer immunotherapy, BI1361849 (CV9202), combined with local radiation treatment in patients with stage IV non-small cell lung cancer , 2019, Journal of Immunotherapy for Cancer.

[69]  Yu Zeng,et al.  PAGE4 promotes prostate cancer cells survive under oxidative stress through modulating MAPK/JNK/ERK pathway , 2019, Journal of experimental & clinical cancer research : CR.

[70]  Rui Zhang,et al.  Diagnostic value of multiple tumor-associated autoantibodies in lung cancer , 2019, OncoTargets and therapy.

[71]  O. Gordeeva Cancer-testis antigens: Unique cancer stem cell biomarkers and targets for cancer therapy. , 2018, Seminars in cancer biology.

[72]  Margaret M. Billingsley,et al.  Biomaterials for vaccine‐based cancer immunotherapy , 2018, Journal of controlled release : official journal of the Controlled Release Society.

[73]  N. Chao,et al.  Cancer-testis antigen GAGE-1 expression and serum immunoreactivity in hepatocellular carcinoma , 2018, Nigerian journal of clinical practice.

[74]  Angelique W Whitehurst,et al.  Emerging Contributions of Cancer/Testis Antigens to Neoplastic Behaviors. , 2018, Trends in cancer.

[75]  Xiaowei Xu,et al.  A Designer Cross-reactive DNA Immunotherapeutic Vaccine that Targets Multiple MAGE-A Family Members Simultaneously for Cancer Therapy , 2018, Clinical Cancer Research.

[76]  F. Pontén,et al.  Detection of autoantibodies against cancer-testis antigens in non-small cell lung cancer. , 2018, Lung cancer.

[77]  M. Sang,et al.  Epigenetic regulation of MAGE family in human cancer progression-DNA methylation, histone modification, and non-coding RNAs , 2018, Clinical Epigenetics.

[78]  O. H. Iwenofu,et al.  NY-ESO-1: a promising cancer testis antigen for sarcoma immunotherapy and diagnosis. , 2018, Chinese clinical oncology.

[79]  Y. Lei,et al.  Antitumor effect of recombinant Mycobacterium smegmatis expressing MAGEA3 and SSX2 fusion proteins. , 2018, Experimental and therapeutic medicine.

[80]  Sepideh Parvizpour,et al.  In silico design of a triple-negative breast cancer vaccine by targeting cancer testis antigens , 2018, BioImpacts : BI.

[81]  Abeer M. Mahmoud Cancer testis antigens as immunogenic and oncogenic targets in breast cancer. , 2018, Immunotherapy.

[82]  Hannah C. Beird,et al.  The SS18-SSX Fusion Oncoprotein Hijacks BAF Complex Targeting and Function to Drive Synovial Sarcoma. , 2018, Cancer cell.

[83]  J. Orban,et al.  Prostate-Associated Gene 4 (PAGE4): Leveraging the Conformational Dynamics of a Dancing Protein Cloud as a Therapeutic Target , 2018, Journal of clinical medicine.

[84]  Ü. Maiväli,et al.  Antibody response against cancer-testis antigens MAGEA4 and MAGEA10 in patients with melanoma , 2018, Oncology letters.

[85]  D. Bedognetti,et al.  NY-ESO-1 Based Immunotherapy of Cancer: Current Perspectives , 2018, Front. Immunol..

[86]  A. Shafei,et al.  Computational prediction of vaccine potential epitopes and 3-dimensional structure of XAGE-1b for non-small cell lung cancer immunotherapy , 2018, Biomedical journal.

[87]  Ö. Türeci,et al.  Personalized vaccines for cancer immunotherapy , 2018, Science.

[88]  Darjus F. Tschaharganeh,et al.  The SS18-SSX Oncoprotein Hijacks KDM2B-PRC1.1 to Drive Synovial Sarcoma. , 2018, Cancer cell.

[89]  E. Nelson,et al.  Co-delivery of human cancer-testis antigens with adjuvant in protein nanoparticles induces higher cell-mediated immune responses. , 2018, Biomaterials.

[90]  S. Pollack The potential of the CMB305 vaccine regimen to target NY-ESO-1 and improve outcomes for synovial sarcoma and myxoid/round cell liposarcoma patients , 2017, Expert review of vaccines.

[91]  M. Zago,et al.  Expression of cancer/testis antigens MAGE-A, MAGE-C1, GAGE and CTAG1B in benign and malignant thyroid diseases , 2017, Oncology letters.

[92]  Xin Li,et al.  High expression of MAGE-A9 is associated with unfavorable survival in esophageal squamous cell carcinoma , 2017, Oncology letters.

[93]  M. Amagai,et al.  Lack of XAGE‐1b and NY‐ESO‐1 in metastatic lymph nodes may predict the potential survival of stage III melanoma patients , 2017, The Journal of dermatology.

[94]  C. Schneider,et al.  Functional interaction between co-expressed MAGE-A proteins , 2017, PloS one.

[95]  Anna K. Lee,et al.  A Comprehensive Guide to the MAGE Family of Ubiquitin Ligases. , 2017, Journal of molecular biology.

[96]  M. O. Olde Rikkert,et al.  Effects of tetrahydrocannabinol on balance and gait in patients with dementia: A randomised controlled crossover trial , 2017, Journal of psychopharmacology.

[97]  E. Wilson,et al.  Melanoma antigen-A11 regulates substrate-specificity of Skp2-mediated protein degradation , 2017, Molecular and Cellular Endocrinology.

[98]  Arash Salmaninejad,et al.  Cancer/Testis Antigens: Expression, Regulation, Tumor Invasion, and Use in Immunotherapy of Cancers , 2016, Immunological investigations.

[99]  K. Safranow,et al.  Expression of Cancer Testis Antigens in Colorectal Cancer: New Prognostic and Therapeutic Implications , 2016, Disease markers.

[100]  A. Dunker,et al.  Prostate-associated gene 4 (PAGE4), an intrinsically disordered cancer/testis antigen, is a novel therapeutic target for prostate cancer , 2016, Asian journal of andrology.

[101]  Moon Soo Kim,et al.  Efficacy of the MAGE-A3 cancer immunotherapeutic as adjuvant therapy in patients with resected MAGE-A3-positive non-small-cell lung cancer (MAGRIT): a randomised, double-blind, placebo-controlled, phase 3 trial. , 2016, The Lancet. Oncology.

[102]  K. Patel,et al.  MAGE-A is More Highly Expressed Than NY-ESO-1 in a Systematic Immunohistochemical Analysis of 3668 Cases , 2016, Journal of immunotherapy.

[103]  N. Petrovsky,et al.  Molecular mechanisms for enhanced DNA vaccine immunogenicity , 2016, Expert review of vaccines.

[104]  V. Uversky Dancing Protein Clouds: The Strange Biology and Chaotic Physics of Intrinsically Disordered Proteins* , 2016, The Journal of Biological Chemistry.

[105]  M. Sang,et al.  Expression of MAGE-A1, -A9, -A11 in laryngeal squamous cell carcinoma and their prognostic significance: a retrospective clinical study , 2016, Acta oto-laryngologica.

[106]  S. Senju,et al.  An oncofetal antigen, IMP-3-derived long peptides induce immune responses of both helper T cells and CTLs , 2016, Oncoimmunology.

[107]  J. Déjardin Switching between Epigenetic States at Pericentromeric Heterochromatin. , 2015, Trends in genetics : TIG.

[108]  S. Ghafouri-Fard,et al.  Immunotherapy in Multiple Myeloma Using Cancer-Testis Antigens , 2015, Iranian journal of cancer prevention.

[109]  S. H. van der Burg,et al.  Local and systemic XAGE-1b-specific immunity in patients with lung adenocarcinoma , 2015, Cancer Immunology, Immunotherapy.

[110]  A. Muzikansky,et al.  Increased NY-ESO-1 Expression and Reduced Infiltrating CD3+ T Cells in Cutaneous Melanoma , 2015, Journal of immunology research.

[111]  Y. Iwamoto,et al.  Cancer‐testis antigens PRAME and NY‐ESO‐1 correlate with tumour grade and poor prognosis in myxoid liposarcoma , 2015, The journal of pathology. Clinical research.

[112]  Guo-min Wang,et al.  XAGE-1b Cancer/Testis Antigen Is a Potential Target for Immunotherapy in Prostate Cancer , 2015, Urologia Internationalis.

[113]  B. Longley,et al.  MAGE proteins regulate KRAB zinc finger transcription factors and KAP1 E3 ligase activity. , 2014, Archives of biochemistry and biophysics.

[114]  Yusuke Nakamura,et al.  Phase II Clinical Trial of Multiple Peptide Vaccination for Advanced Head and Neck Cancer Patients Revealed Induction of Immune Responses and Improved OS , 2014, Clinical Cancer Research.

[115]  Yuan Yang,et al.  XAGE-1b expression is associated with the diagnosis and early recurrence of hepatocellular carcinoma. , 2014, Molecular and clinical oncology.

[116]  D. Mavroudis,et al.  A phase II trial evaluating the clinical and immunologic response of HLA-A2(+) non-small cell lung cancer patients vaccinated with an hTERT cryptic peptide. , 2014, Lung cancer.

[117]  Sreeparna Banerjee,et al.  Epigenetic Mechanisms Underlying the Dynamic Expression of Cancer-Testis Genes, PAGE2, -2B and SPANX-B, during Mesenchymal-to-Epithelial Transition , 2014, PloS one.

[118]  Yusuke Nakamura,et al.  Phase I clinical study of multiple epitope peptide vaccine combined with chemoradiation therapy in esophageal cancer patients , 2014, Journal of Translational Medicine.

[119]  D. McNeel,et al.  DNA vaccines encoding altered peptide ligands for SSX2 enhance epitope-specific CD8+ T-cell immune responses. , 2014, Vaccine.

[120]  K. Rajagopalan,et al.  The Stress-response protein prostate-associated gene 4, interacts with c-Jun and potentiates its transactivation. , 2014, Biochimica et biophysica acta.

[121]  Prakash Kulkarni,et al.  Prostate-associated gene 4 (PAGE4) protects cells against stress by elevating p21 and suppressing reactive oxygen species production. , 2013, American journal of clinical and experimental urology.

[122]  Masakazu Yamamoto,et al.  Immunological responses to a multi-peptide vaccine targeting cancer-testis antigens and VEGFRs in advanced pancreatic cancer patients , 2013, Oncoimmunology.

[123]  Yang Liu,et al.  Preliminary study on XAGE-1b gene and its mechanism for promoting tumor cell growth. , 2013, Biomedical reports.

[124]  A. Eggermont,et al.  Selection of immunostimulant AS15 for active immunization with MAGE-A3 protein: results of a randomized phase II study of the European Organisation for Research and Treatment of Cancer Melanoma Group in Metastatic Melanoma. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[125]  M. McNutt,et al.  Subnuclear distribution of SSX regulates its function , 2013, Molecular and Cellular Biochemistry.

[126]  M. Sang,et al.  The expression and clinical significance of melanoma-associated antigen-A1, -A3 and -A11 in glioma , 2013, Oncology letters.

[127]  K. Takeda,et al.  Multiple therapeutic peptide vaccines consisting of combined novel cancer testis antigens and anti-angiogenic peptides for patients with non-small cell lung cancer , 2013, Journal of Translational Medicine.

[128]  E. Morenghi,et al.  Preliminary evidence for high anti-PLAC1 antibody levels in infertile patients with repeated unexplained implantation failure. , 2013, Placenta.

[129]  Zhijian J. Chen,et al.  Regulation of WASH-Dependent Actin Polymerization and Protein Trafficking by Ubiquitination , 2013, Cell.

[130]  A. Lladser,et al.  Harnessing DNA-induced immune responses for improving cancer vaccines , 2012, Human vaccines & immunotherapeutics.

[131]  Christian Ruiz,et al.  PAGE4 positivity is associated with attenuated AR signaling and predicts patient survival in hormone-naive prostate cancer. , 2012, The American journal of pathology.

[132]  H. Ditzel,et al.  GAGE Cancer-Germline Antigens Are Recruited to the Nuclear Envelope by Germ Cell-Less (GCL) , 2012, PloS one.

[133]  Yusuke Nakamura,et al.  Multicenter, phase II clinical trial of cancer vaccination for advanced esophageal cancer with three peptides derived from novel cancer-testis antigens , 2012, Journal of Translational Medicine.

[134]  J. Heino,et al.  Characterization of Intrinsically Disordered Prostate Associated Gene (PAGE5) at Single Residue Resolution by NMR Spectroscopy , 2011, PloS one.

[135]  D. McNeel,et al.  Vaccines Targeting the Cancer-testis Antigen SSX-2 Elicit HLA-A2 Epitope-specific Cytolytic T Cells , 2011, Journal of immunotherapy.

[136]  J. Lang,et al.  Expression and immunotherapeutic targeting of the SSX family of cancer-testis antigens in prostate cancer. , 2011, Cancer research.

[137]  S. Stevanović,et al.  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 , 2011, Cancer Immunology, Immunotherapy.

[138]  Ling Wang,et al.  Melanoma-associated antigen genes - an update. , 2011, Cancer letters.

[139]  R. Vessella,et al.  Expression of cancer/testis antigens in prostate cancer is associated with disease progression , 2010, The Prostate.

[140]  Jirun Peng,et al.  Hepatocellular carcinoma patients highly and specifically expressing XAGE-1 exhibit prolonged survival. , 2010, Oncology letters.

[141]  Maojun Yang,et al.  MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. , 2010, Molecular cell.

[142]  Xiaoliang Zhou,et al.  Expression of tumor-specific antigen MAGE, GAGE and BAGE in ovarian cancer tissues and cell lines , 2010, BMC Cancer.

[143]  Ru-fu Chen,et al.  Preparation and antitumor effects of nanovaccines with MAGE-3 peptides in transplanted gastric cancer in mice. , 2010, Chinese journal of cancer.

[144]  Qiang Yu,et al.  Combinatorial pharmacologic approaches target EZH2-mediated gene repression in breast cancer cells , 2009, Molecular Cancer Therapeutics.

[145]  N. Brünner,et al.  High frequency of tumor cells with nuclear Egr-1 protein expression in human bladder cancer is associated with disease progression , 2009, BMC Cancer.

[146]  F. Yehiely,et al.  GAGE, an antiapoptotic protein binds and modulates the expression of nucleophosmin/B23 and interferon regulatory factor 1. , 2009, Journal of interferon & cytokine research : the official journal of the International Society for Interferon and Cytokine Research.

[147]  Martin A. Cheever,et al.  The Prioritization of Cancer Antigens: A National Cancer Institute Pilot Project for the Acceleration of Translational Research , 2009, Clinical Cancer Research.

[148]  Yusuke Nakamura,et al.  Vaccination with multiple peptides derived from novel cancer‐testis antigens can induce specific T‐cell responses and clinical responses in advanced esophageal cancer , 2009, Cancer science.

[149]  J. E. Eid,et al.  The Synovial Sarcoma-Associated SYT-SSX2 Oncogene Antagonizes the Polycomb Complex Protein Bmi1 , 2009, PloS one.

[150]  E. Tartour,et al.  Functions of Anti-MAGE T-cells induced in melanoma patients under different vaccination modalities. , 2008, Cancer research.

[151]  M. Gjerstorff,et al.  An overview of the GAGE cancer/testis antigen family with the inclusion of newly identified members. , 2008, Tissue antigens.

[152]  D. Schadendorf,et al.  Expression of GAGE family proteins in malignant melanoma. , 2007, Cancer letters.

[153]  H. Ditzel,et al.  MAGE-A1, GAGE and NY-ESO-1 cancer/testis antigen expression during human gonadal development. , 2007, Human reproduction.

[154]  P. Chomez,et al.  A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. , 2007, Journal of immunology.

[155]  C. Bokemeyer,et al.  Cancer-testis antigens are commonly expressed in multiple myeloma and induce systemic immunity following allogeneic stem cell transplantation. , 2007, Blood.

[156]  Guido Ferrari,et al.  Durable HIV-1 antibody and T-cell responses elicited by an adjuvanted multi-protein recombinant vaccine in uninfected human volunteers. , 2007, Vaccine.

[157]  O. Nielsen,et al.  Restriction of GAGE protein expression to subpopulations of cancer cells is independent of genotype and may limit the use of GAGE proteins as targets for cancer immunotherapy , 2006, British Journal of Cancer.

[158]  K. Pantel,et al.  Promoter Demethylation and Histone Acetylation Mediate Gene Expression of MAGE-A1, -A2, -A3, and -A12 in Human Cancer Cells , 2006, Molecular Cancer Research.

[159]  Richard Bourgon,et al.  Genome-wide analysis of Polycomb targets in Drosophila melanogaster , 2006, Nature Genetics.

[160]  M. Pfreundschuh,et al.  Prospective study on the expression of cancer testis genes and antibody responses in 100 consecutive patients with primary breast cancer , 2006, International journal of cancer.

[161]  I. Davis,et al.  Tumor Antigen Expression in Melanoma Varies According to Antigen and Stage , 2006, Clinical Cancer Research.

[162]  A. Simpson,et al.  Cancer-Testis Genes Are Coordinately Expressed and Are Markers of Poor Outcome in Non–Small Cell Lung Cancer , 2005, Clinical Cancer Research.

[163]  M. Aoe,et al.  XAGE-1 Expression in Non–Small Cell Lung Cancer and Antibody Response in Patients , 2005, Clinical Cancer Research.

[164]  Lloyd J. Old,et al.  Cancer/testis antigens, gametogenesis and cancer , 2005, Nature Reviews Cancer.

[165]  F. Pijpers,et al.  Therapeutic cancer vaccines , 2005, Nature Reviews Drug Discovery.

[166]  F. Zhan,et al.  NY-ESO-1 is highly expressed in poor-prognosis multiple myeloma and induces spontaneous humoral and cellular immune responses. , 2005, Blood.

[167]  H. Kumon,et al.  XAGE‐1 mRNA Expression in Prostate Cancer and Antibody Response in Patients , 2005, Microbiology and immunology.

[168]  B. Brodin,et al.  Cancer/testis antigen expression in human mesenchymal stem cells: down-regulation of SSX impairs cell migration and matrix metalloproteinase 2 expression. , 2005, Cancer research.

[169]  T. Boon,et al.  Promoter-Dependent Mechanism Leading to Selective Hypomethylation within the 5′ Region of Gene MAGE-A1 in Tumor Cells , 2004, Molecular and Cellular Biology.

[170]  István Simon,et al.  Preformed structural elements feature in partner recognition by intrinsically unstructured proteins. , 2004, Journal of molecular biology.

[171]  Yao-Tseng Chen,et al.  The SSX gene family: Characterization of 9 complete genes , 2002, International journal of cancer.

[172]  U. Weidle,et al.  The XAGE family of cancer/testis‐associated genes: Alignment and expression profile in normal tissues, melanoma lesions and Ewing's sarcoma , 2002, International journal of cancer.

[173]  P. Barker,et al.  The MAGE proteins: Emerging roles in cell cycle progression, apoptosis, and neurogenetic disease , 2002, Journal of neuroscience research.

[174]  D. Schadendorf,et al.  Tumor-associated Antigens as Possible Targets for Immune Therapy in Head and Neck Cancer: Comparative mRNA Expression Analysis of RAGE and GAGE Genes , 2002, Acta oto-laryngologica.

[175]  M. Bertrand,et al.  An overview of the MAGE gene family with the identification of all human members of the family. , 2001, Cancer research.

[176]  D. Jäger,et al.  Induction of primary NY-ESO-1 immunity: CD8+ T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[177]  A. V. van Kessel,et al.  Delineation of the protein domains responsible for SYT, SSX, and SYT-SSX nuclear localization. , 2000, Experimental cell research.

[178]  A. V. van Kessel,et al.  Heterogeneous expression of the SSX cancer/testis antigens in human melanoma lesions and cell lines. , 2000, Cancer research.

[179]  G. Nilsson,et al.  A novel fusion gene, SYT-SSX4, in synovial sarcoma. , 1999, Journal of the National Cancer Institute.

[180]  F. Brasseur,et al.  Cytolytic T lymphocytes recognize an antigen encoded by MAGE-A10 on a human melanoma. , 1999, Journal of immunology.

[181]  P. Coulie,et al.  Tumor regressions observed in patients with metastatic melanoma treated with an antigenic peptide encoded by gene MAGE‐3 and presented by HLA‐A1 , 1999, International journal of cancer.

[182]  F. Lim,et al.  A KRAB-related domain and a novel transcription repression domain in proteins encoded by SSX genes that are disrupted in human sarcomas , 1998, Oncogene.

[183]  I. Pastan,et al.  PAGE-1, an X chromosome-linked GAGE-like gene that is expressed in normal and neoplastic prostate, testis, and uterus. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[184]  Yao-Tseng Chen,et al.  Expression of SSX genes in human tumors , 1998, International Journal of Cancer.

[185]  P. Jones,et al.  Altered DNA methylation and genome instability: a new pathway to cancer? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[186]  Yao-Tseng Chen,et al.  A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[187]  W. Gerald,et al.  Molecular diagnosis of synovial sarcoma and characterization of a variant SYT-SSX2 fusion transcript. , 1995, The American journal of pathology.

[188]  A. Poustka,et al.  The melanoma antigen gene (MAGE) family is clustered in the chromosomal band Xq28. , 1995, Genomics.

[189]  B. Gusterson,et al.  Fusion of SYT to two genes, SSX1 and SSX2, encoding proteins with homology to the Kruppel‐associated box in human synovial sarcoma. , 1995, The EMBO journal.

[190]  P. Chomez,et al.  A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. , 1991, Science.

[191]  Kyung-Ja Cho,et al.  NY-ESO-1 as a diagnostic and prognostic marker for myxoid liposarcoma. , 2022, American journal of translational research.

[192]  Sepideh Dashti,et al.  Humoral immune responses against cancer-testis antigens in human malignancies. , 2019, Human antibodies.

[193]  D. Jäger,et al.  Monitoring CD 8 T cell responses to NY-ESO-1 : correlation of humoral and cellular immune responses , 2017 .

[194]  C. Slingluff,et al.  A randomized pilot trial testing the safety and immunologic effects of a MAGE-A3 protein plus AS15 immunostimulant administered into muscle or into dermal/subcutaneous sites , 2015, Cancer Immunology, Immunotherapy.

[195]  Jian Feng,et al.  High expression of MAGE-A9 in tumor and stromal cells of non-small cell lung cancer was correlated with patient poor survival. , 2015, International journal of clinical and experimental pathology.

[196]  M. Sang,et al.  Expressions of MAGE-A9 and MAGE-A11 in breast cancer and their expression mechanism. , 2014, Archives of medical research.

[197]  Yao-Tseng Chen,et al.  NY-ESO-1: review of an immunogenic tumor antigen. , 2006, Advances in cancer research.

[198]  Pierre van der Bruggen,et al.  Structure, chromosomal localization, and expression of 12 genes of the MAGE family , 2005, Immunogenetics.

[199]  A. Hongo,et al.  SSX expression in gynecological cancers and antibody response in patients. , 2004, Cancer immunity.