MHC class II tetramer analyses in AE37-vaccinated prostate cancer patients reveal vaccine-specific polyfunctional and long-lasting CD4⁺ T-cells

References

• Melero I, Gaudernack G, Gerritsen W, Huber C, Parmiani G, Scholl S, Thatcher N, Wagstaff J, Zielinski C, Faulkner I et al. Therapeutic vaccines for cancer: an overview of clinical trials. Nat Rev Clin Oncol 2014; 11:509-24; PMID:25001465; http://dx.doi.org/10.1038/nrclinonc.2014.111
   PubMed Web of Science ®Google Scholar
• Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004; 10:909-15; PMID:15340416; http://dx.doi.org/10.1038/nm1100
   PubMed Web of Science ®Google Scholar
• Galaine J, Borg C, Godet Y, Adotevi O. Interest of Tumor-Specific CD4 T Helper 1 Cells for Therapeutic Anticancer Vaccine. Vaccines (Basel) 2015; 3:490-502; PMID:26350591; http://dx.doi.org/10.3390/vaccines3030490
   PubMed Web of Science ®Google Scholar
• Butterfield LH. Cancer vaccines. BMJ 2015; 350:h988; PMID:25904595; http://dx.doi.org/10.1136/bmj.h988
   PubMed Web of Science ®Google Scholar
• Melief CJ, van der Burg SH. Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat Rev Cancer 2008; 8:351-60; PMID:18418403; http://dx.doi.org/10.1038/nrc2373
   PubMed Web of Science ®Google Scholar
• Slingluff CL, Jr. The present and future of peptide vaccines for cancer: single or multiple, long or short, alone or in combination? Cancer J 2011; 17:343-50; PMID:21952285; http://dx.doi.org/10.1097/PPO.0b013e318233e5b2
   PubMed Web of Science ®Google Scholar
• Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012; 12:298-306; PMID:22419253; http://dx.doi.org/10.1038/nrc3245
   PubMed Web of Science ®Google Scholar
• Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, Lugli A, Zlobec I, Hartmann A, Bifulco C et al. Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumours. J Pathol 2014; 232:199-209; PMID:24122236; http://dx.doi.org/10.1002/path.4287
   PubMed Web of Science ®Google Scholar
• Mueller KL. Cancer immunology and immunotherapy. Realizing the promise. Introduction. Science 2015; 348:54-5; PMID:25838372; http://dx.doi.org/10.1126/science.348.6230.54
   PubMed Web of Science ®Google Scholar
• Baxevanis CN, Papamichail M, Perez SA. Prostate cancer vaccines: the long road to clinical application. Cancer Immunol Immunother 2015; 64:401-8; PMID:25690791; http://dx.doi.org/10.1007/s00262-015-1667-7
   PubMed Web of Science ®Google Scholar
• Ebert LM, MacRaild SE, Zanker D, Davis ID, Cebon J, Chen W. A cancer vaccine induces expansion of NY-ESO-1-specific regulatory T cells in patients with advanced melanoma. PloS One 2012; 7:e48424; PMID:23110239; http://dx.doi.org/10.1371/journal.pone.0048424
   PubMed Web of Science ®Google Scholar
• Oleinika K, Nibbs RJ, Graham GJ, Fraser AR. Suppression, subversion and escape: the role of regulatory T cells in cancer progression. Clin Exp Immunol 2013; 171:36-45; PMID:23199321; http://dx.doi.org/10.1111/j.1365-2249.2012.04657.x
   PubMed Web of Science ®Google Scholar
• deLeeuw RJ, Kost SE, Kakal JA, Nelson BH. The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 2012; 18:3022-9; PMID:22510350; http://dx.doi.org/10.1158/1078-0432.CCR-11-3216
   PubMed Web of Science ®Google Scholar
• Idorn M, Kollgaard T, Kongsted P, Sengelov L, Thor SP. Correlation between frequencies of blood monocytic myeloid-derived suppressor cells, regulatory T cells and negative prognostic markers in patients with castration-resistant metastatic prostate cancer. Cancer Immunol Immunother 2014; 63:1177-87; PMID:25085000; http://dx.doi.org/10.1007/s00262-014-1591-2
   PubMed Web of Science ®Google Scholar
• Keilholz U, Weber J, Finke JH, Gabrilovich DI, Kast WM, Disis ML, Kirkwood JM, Scheibenbogen C, Schlom J, Maino VC et al. Immunologic monitoring of cancer vaccine therapy: results of a workshop sponsored by the Society for Biological Therapy. J Immunother 2002; 25:97-138; PMID:12074049; http://dx.doi.org/10.1097/00002371-200203000-00001
   PubMed Web of Science ®Google Scholar
• Altman JD, Davis MM. MHC-peptide tetramers to visualize antigen-specific T cells. In Current protocols in immunology. eds. John E Coligan et al 2003; Chapter 17:Unit 17.3; Page 1-33
   Google Scholar
• Ayyoub M, Dojcinovic D, Pignon P, Raimbaud I, Schmidt J, Luescher I, Valmori D. Monitoring of NY-ESO-1 specific CD4+ T cells using molecularly defined MHC class II/His-tag-peptide tetramers. Proc Natl Acad Sci U S A 2010; 107:7437-42; PMID:20368442; http://dx.doi.org/10.1073/pnas.1001322107
   PubMed Web of Science ®Google Scholar
• Francois V, Ottaviani S, Renkvist N, Stockis J, Schuler G, Thielemans K, Colau D, Marchand M, Boon T, Lucas S et al. The CD4(+) T-cell response of melanoma patients to a MAGE-A3 peptide vaccine involves potential regulatory T cells. Cancer Res 2009; 69:4335-45; PMID:19435913; http://dx.doi.org/10.1158/0008-5472.CAN-08-3726
   PubMed Web of Science ®Google Scholar
• Schmidt HH, Ge Y, Hartmann FJ, Conrad H, Klug F, Nittel S, Bernhard H, Domschke C, Schuetz F, Sohn C et al. HLA Class II tetramers reveal tissue-specific regulatory T cells that suppress T-cell responses in breast carcinoma patients. Onco immunol 2013; 2:e24962; PMID:23894725; http://dx.doi.org/10.4161/onci.24962
   Google Scholar
• Gajewski TF. Monitoring Specific T-Cell Responses to Melanoma Vaccines: ELISPOT, Tetramers, and Beyond. Clinical and Diagnostic Laboratory Immunology 2000; 7(2):141-144; PMID:10702484
   PubMedGoogle Scholar
• Perez SA, Kallinteris NL, Bisias S, Tzonis PK, Georgakopoulou K, Varla-Leftherioti M, Papamichail M, Thanos A, von Hofe E, Baxevanis CN. Results from a phase I clinical study of the novel Ii-Key/HER-2/neu(776-790) hybrid peptide vaccine in patients with prostate cancer. Clin Cancer Res 2010; 16:3495-506; PMID:20466887; http://dx.doi.org/10.1158/1078-0432.CCR-10-0085
   PubMed Web of Science ®Google Scholar
• Perez SA, Anastasopoulou EA, Papamichail M, Baxevanis CN. AE37 peptide vaccination in prostate cancer: identification of biomarkers in the context of prognosis and prediction. Cancer Immunol Immunother 2014; 63:1141-50; PMID:25052849; http://dx.doi.org/10.1007/s00262-014-1582-3
   PubMed Web of Science ®Google Scholar
• Perez SA, Anastasopoulou EA, Tzonis P, Gouttefangeas C, Kalbacher H, Papamichail M, Baxevanis CN. AE37 peptide vaccination in prostate cancer: a 4-year immunological assessment updates on a phase I trial. Cancer Immunol Immunother 2013; 62:1599-608; PMID:23934022; http://dx.doi.org/10.1007/s00262-013-1461-3
   PubMed Web of Science ®Google Scholar
• Perez SA, Peoples GE, Papamichail M, Baxevanis CN. Invariant chain-peptide fusion vaccine using HER-2/neu. Methods Mol Biol 2014; 1139:321-36; PMID:24619690; http://dx.doi.org/10.1007/978-1-4939-0345-0_26
   PubMedGoogle Scholar
• Anastasopoulou EA, Voutsas IF, Keramitsoglou T, Gouttefangeas C, Kalbacher H, Thanos A, Papamichail M, Perez SA, Baxevanis CN. A pilot study in prostate cancer patients treated with the AE37 Ii-key-HER-2/neu polypeptide vaccine suggests that HLA-A*24 and HLA-DRB1*11 alleles may be prognostic and predictive biomarkers for clinical benefit. Cancer Immunol Immunother 2015; 64:1123-36; PMID:26026288; http://dx.doi.org/10.1007/s00262-015-1717-1
   PubMed Web of Science ®Google Scholar
• Amyes E, McMichael AJ, Callan MF. Human CD4+ T cells are predominantly distributed among six phenotypically and functionally distinct subsets. J Immunol 2005; 175:5765-73; PMID:16237068; http://dx.doi.org/10.4049/jimmunol.175.9.5765
   PubMed Web of Science ®Google Scholar
• Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004; 22:745-63; PMID:15032595; http://dx.doi.org/10.1146/annurev.immunol.22.012703.104702
   PubMed Web of Science ®Google Scholar
• Attig S, Hennenlotter J, Pawelec G, Klein G, Koch SD, Pircher H, Feyerabend S, Wernet D, Stenzl A, Rammensee HG et al. Simultaneous infiltration of polyfunctional effector and suppressor T cells into renal cell carcinomas. Cancer Res 2009; 69:8412-9; PMID:19843860; http://dx.doi.org/10.1158/0008-5472.CAN-09-0852
   PubMed Web of Science ®Google Scholar
• Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8:247-58; PMID:18323851; http://dx.doi.org/10.1038/nri2274
   PubMed Web of Science ®Google Scholar
• Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S, Gottlieb PA, Kapranov P, Gingeras TR, Fazekas de St GB et al. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med 2006; 203:1701-11; PMID:16818678; http://dx.doi.org/10.1084/jem.20060772
   PubMed Web of Science ®Google Scholar
• Sun J, Tang DN, Fu T, Sharma P. Identification of human regulatory T cells in the setting of T-cell activation and anti-CTLA-4 immunotherapy on the basis of expression of latency-associated peptide. Cancer Discov 2012; 2:122-30; PMID:22585857; http://dx.doi.org/10.1158/2159-8290.CD-11-0236
   PubMed Web of Science ®Google Scholar
• Yu N, Li X, Song W, Li D, Yu D, Zeng X, Li M, Leng X, Li X. CD4(+)CD25 (+)CD127 (low/-) T cells: a more specific Treg population in human peripheral blood. Inflammation 2012; 35:1773-80; PMID:22752562; http://dx.doi.org/10.1007/s10753-012-9496-8
   PubMed Web of Science ®Google Scholar
• Mahalingam J, Lin YC, Chiang JM, Su PJ, Fang JH, Chu YY, Huang CT, Chiu CT, Lin CY. LAP+CD4+ T cells are suppressors accumulated in the tumor sites and associated with the progression of colorectal cancer. Clin Cancer Res 2012; 18:5224-33; PMID:22879386; http://dx.doi.org/10.1158/1078-0432.CCR-12-0211
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, Almeida JR, Gostick E, Yu Z, Carpenito C et al. A human memory T cell subset with stem cell-like properties. Nat Med 2011; 17:1290-7; PMID:21926977; http://dx.doi.org/10.1038/nm.2446
   PubMed Web of Science ®Google Scholar
• Restifo NP. Big bang theory of stem-like T cells confirmed. Blood 2014; 124:476-7; PMID:25061170; http://dx.doi.org/10.1182/blood-2014-06-578989
   PubMed Web of Science ®Google Scholar
• Humphreys RE, Adams S, Koldzic G, Nedelescu B, von HE, Xu M. Increasing the potency of MHC class II-presented epitopes by linkage to Ii-Key peptide. Vaccine 2000; 18:2693-7; PMID:10781856; http://dx.doi.org/10.1016/S0264-410X(00)00067-0
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer 2012; 12:671-84; PMID:22996603; http://dx.doi.org/10.1038/nrc3322
   PubMed Web of Science ®Google Scholar
• Lugli E, Dominguez MH, Gattinoni L, Chattopadhyay PK, Bolton DL, Song K, Klatt NR, Brenchley JM, Vaccari M, Gostick E et al. Superior T memory stem cell persistence supports long-lived T cell memory. J Clin Invest 2013; 123:594-9; PMID:23281401; http://dx.doi.org/10.1172/JCI66327
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Restifo NP. Moving T memory stem cells to the clinic. Blood 2013; 121:567-8; PMID:23349370; http://dx.doi.org/10.1182/blood-2012-11-468660
   PubMed Web of Science ®Google Scholar
• Mitchell MS, Harel W, Groshen S. Association of HLA phenotype with response to active specific immunotherapy of melanoma. J Clin Oncol 1992; 10:1158-64; PMID:1607920
   PubMed Web of Science ®Google Scholar
• Sonpavde G, Wang M, Peterson LE, Wang HY, Joe T, Mims MP, Kadmon D, Ittmann MM, Wheeler TM, Gee AP et al. HLA-restricted NY-ESO-1 peptide immunotherapy for metastatic castration resistant prostate cancer. Invest New Drugs 2014; 32:235-42; PMID:23609828; http://dx.doi.org/10.1007/s10637-013-9960-9
   PubMed Web of Science ®Google Scholar
• Sosman JA, Unger JM, Liu PY, Flaherty LE, Park MS, Kempf RA, Thompson JA, Terasaki PI, Sondak VK. Adjuvant immunotherapy of resected, intermediate-thickness, node-negative melanoma with an allogeneic tumor vaccine: impact of HLA class I antigen expression on outcome. J Clin Oncol 2002; 20:2067-75; PMID:11956267; http://dx.doi.org/10.1200/JCO.2002.08.072
   PubMed Web of Science ®Google Scholar
• Xu M, Kallinteris NL, Von HE. CD4+ T-cell activation for immunotherapy of malignancies using Ii-Key/MHC class II epitope hybrid vaccines. Vaccine 2012; 30:2805-10; PMID:22386748; http://dx.doi.org/10.1016/j.vaccine.2012.02.031
   PubMed Web of Science ®Google Scholar
• Brown DM. Cytolytic CD4 cells: Direct mediators in infectious disease and malignancy. Cell Immunol 2010; 262:89-95; PMID:20236628; http://dx.doi.org/10.1016/j.cellimm.2010.02.008
   PubMed Web of Science ®Google Scholar
• van de Berg PJ, van Leeuwen EM, ten Berge IJ, van LR. Cytotoxic human CD4(+) T cells. Curr Opin Immunol 2008; 20:339-43; PMID:18440213; http://dx.doi.org/10.1016/j.coi.2008.03.007
   PubMed Web of Science ®Google Scholar
• Inderberg-Suso EM, Trachsel S, Lislerud K, Rasmussen AM, Gaudernack G. Widespread CD4+ T-cell reactivity to novel hTERT epitopes following vaccination of cancer patients with a single hTERT peptide GV1001. Onco Immunol 2012; 1:670-86; PMID:22934259; http://dx.doi.org/10.4161/onci.20426
   Web of Science ®Google Scholar
• Fu J, Zhang Z, Zhou L, Qi Z, Xing S, Lv J, Shi J, Fu B, Liu Z, Zhang JY et al. Impairment of CD4+ cytotoxic T cells predicts poor survival and high recurrence rates in patients with hepatocellular carcinoma. Hepatol 2013; 58:139-49; PMID:22961630; http://dx.doi.org/10.1002/hep.26054
   PubMed Web of Science ®Google Scholar
• Coler R, Hudson T, Hughes S, Huang P, Beebe E, Orr M. Vaccination Produces CD4 T Cells with a Novel CD154-CD40-Dependent Cytolytic Mechanism. J Immunol 2015; 195:3190-7; PMID:26297758; http://dx.doi.org/10.4049/jimmunol.1501118
   PubMed Web of Science ®Google Scholar
• Gross S, Lennerz V, Gallerani E, Mach N, Bohm S, Hess D, von BL, Knuth A, Ochsenbein A, Gnad-Vogt U et al. Short Peptide Vaccine Induces CD4+ T Helper Cells in Patients with Different Solid Cancers. Cancer Immunol Res 2016; 4:18-25; PMID:26563311; http://dx.doi.org/10.1158/2326-6066.CIR-15-0105
   PubMed Web of Science ®Google Scholar
• Atanackovic D, Altorki NK, Stockert E, Williamson B, Jungbluth AA, Ritter E, Santiago D, Ferrara CA, Matsuo M, Selvakumar A et al. Vaccine-induced CD4+ T cell responses to MAGE-3 protein in lung cancer patients. J Immunol 2004; 172:3289-96; PMID:14978137; http://dx.doi.org/10.4049/jimmunol.172.5.3289
   PubMed Web of Science ®Google Scholar
• Reissfelder C, Stamova S, Gossmann C, Braun M, Bonertz A, Walliczek U, Grimm M, Rahbari NN, Koch M, Saadati M et al. Tumor-specific cytotoxic T lymphocyte activity determines colorectal cancer patient prognosis. J Clin Invest 2015; 125:739-51; PMID:25562322; http://dx.doi.org/10.1172/JCI74894
   PubMed Web of Science ®Google Scholar
• Bonertz A, Weitz J, Pietsch DH, Rahbari NN, Schlude C, Ge Y, Juenger S, Vlodavsky I, Khazaie K, Jaeger D et al. Antigen-specific Tregs control T cell responses against a limited repertoire of tumor antigens in patients with colorectal carcinoma. J Clin Invest 2009; 119:3311-21; PMID:19809157; http://dx.doi.org/10.1172/JCI39608
   PubMed Web of Science ®Google Scholar
• Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007; 37:129-38; PMID:17154262; http://dx.doi.org/10.1002/eji.200636435
   PubMed Web of Science ®Google Scholar
• Welters MJ, Kenter GG, Piersma SJ, Vloon AP, Lowik MJ, Berends-van der Meer DM, Drijfhout JW, Valentijn AR, Wafelman AR, Oostendorp J et al. Induction of tumor-specific CD4+ and CD8+ T-cell immunity in cervical cancer patients by a human papillomavirus type 16 E6 and E7 long peptides vaccine. Clin Cancer Res 2008; 14:178-87; PMID:18172269; http://dx.doi.org/10.1158/1078-0432.CCR-07-1880
   PubMed Web of Science ®Google Scholar
• Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van LM, Buckner JH, Ziegler SF. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+. J Clin Invest 2003; 112:1437-43; PMID:14597769; http://dx.doi.org/10.1172/JCI19441
   PubMed Web of Science ®Google Scholar