Survivin-targeted immunotherapy drives robust polyfunctional T cell generation and differentiation in advanced ovarian cancer patients

References

• Finke LH, Wentworth K, Blumenstein B, Rudolph NS, Levitsky H, Hoos A. Lessons from randomized phase III studies with active cancer immunotherapies–outcomes from the 2006 meeting of the Cancer Vaccine Consortium (CVC). Vaccine 2007; 25 Suppl 2: B97-B109; PMID:17916465; http://dx.doi.org/10.1016/j.vaccine.2007.06.067
   PubMed Web of Science ®Google Scholar
• Lesterhuis WJ, Haanen JB, Punt CJ. Cancer immunotherapy–revisited. Nat Rev Drug Discov 2011; 10:591-600; PMID:21804596; http://dx.doi.org/10.1038/nrd3500
   PubMed Web of Science ®Google Scholar
• Kyi C, Postow MA. Checkpoint blocking antibodies in cancer immunotherapy. FEBS Lett 2014; 588:368-76; PMID:24161671; http://dx.doi.org/10.1016/j.febslet.2013.10.015
   PubMed Web of Science ®Google Scholar
• Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, Mellman I, Prindiville SA, Viner JL, Weiner LM et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res 2009; 15:5323-37; PMID:19723653; http://dx.doi.org/10.1158/1078-0432.CCR-09-0737
   PubMed Web of Science ®Google Scholar
• Hwang WT, Adams SF, Tahirovic E, Hagemann IS, Coukos G. Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol Oncol 2012; 124:192-8; PMID:22040834; http://dx.doi.org/10.1016/j.ygyno.2011.09.039
   PubMed Web of Science ®Google Scholar
• Restifo NP, Gattinoni L. Lineage relationship of effector and memory T cells. Curr Opin Immunol 2013; 25:556-63; PMID:24148236; http://dx.doi.org/10.1016/j.coi.2013.09.003
   PubMed Web of Science ®Google Scholar
• Machiels JP, Reilly RT, Emens LA, Ercolini AM, Lei RY, Weintraub D, Okoye FI, Jaffee EM. Cyclophosphamide, doxorubicin, and paclitaxel enhance the antitumor immune response of granulocyte/macrophage-colony stimulating factor-secreting whole-cell vaccines in HER-2/neu tolerized mice. Cancer Res 2001; 61:3689-97; PMID:11325840
   PubMed Web of Science ®Google Scholar
• Black CM, Armstrong TD, Jaffee EM. Apoptosis-regulated low-avidity cancer-specific CD8(+) T cells can be rescued to eliminate HER2/neu-expressing tumors by costimulatory agonists in tolerized mice. Cancer Immunol Res 2014; 2:307-19; PMID:24764578; http://dx.doi.org/10.1158/2326-6066.CIR-13-0145
   PubMed Web of Science ®Google Scholar
• Farag MM, Tedjokusumo R, Flechtenmacher C, Asen T, Stremmel W, Muller M, Protzer U, Weigand K. Immune tolerance against HBV can be overcome in HBV transgenic mice by immunization with dendritic cells pulsed by HBVsvp. Vaccine 2012; 30:6034-9; PMID:22867720; http://dx.doi.org/10.1016/j.vaccine.2012.07.057
   PubMed Web of Science ®Google Scholar
• Church SE, Jensen SM, Antony PA, Restifo NP, Fox BA. Tumor-specific CD4+ T cells maintain effector and memory tumor-specific CD8+ T cells. Eur J Immunol 2014; 44:69-79; PMID:24114780; http://dx.doi.org/10.1002/eji.201343718
   PubMed Web of Science ®Google Scholar
• Sharma RK, Yolcu ES, Srivastava AK, Shirwan H. CD4+ T cells play a critical role in the generation of primary and memory antitumor immune responses elicited by SA-4-1BBL and TAA-based vaccines in mouse tumor models. PLoS One 2013; 8: e73145; PMID:24066030; http://dx.doi.org/10.1371/journal.pone.0073145
   PubMed Web of Science ®Google Scholar
• Sallusto F, Lanzavecchia A, Araki K, Ahmed R. From vaccines to memory and back. Immunity 2010; 33:451-63; PMID:21029957; http://dx.doi.org/10.1016/j.immuni.2010.10.008
   PubMed Web of Science ®Google Scholar
• Weir GM, Liwski RS, Mansour M. Immune modulation by chemotherapy or immunotherapy to enhance cancer vaccines. Cancers (Basel) 2011; 3:3114-42; PMID:24212948; http://dx.doi.org/10.3390/cancers3033114
   PubMedGoogle Scholar
• Le DT, Jaffee EM. Regulatory T-cell modulation using cyclophosphamide in vaccine approaches: a current perspective. Cancer Res 2012; 72:3439-44; PMID:22761338; http://dx.doi.org/10.1158/0008-5472.CAN-11-3912
   PubMed Web of Science ®Google Scholar
• Waldron TJ, Quatromoni JG, Karakasheva TA, Singhal S, Rustgi AK. Myeloid derived suppressor cells: Targets for therapy. Oncoimmunology 2013; 2: e24117; PMID:23734336; http://dx.doi.org/10.4161/onci.24117
   PubMed Web of Science ®Google Scholar
• Karkada M, Quinton T, Blackman R, Mansour M. Tumor Inhibition by DepoVax-Based Cancer Vaccine Is Accompanied by Reduced Regulatory/Suppressor Cell Proliferation and Tumor Infiltration. ISRN Oncol 2013; 2013:753427; PMID:23533812; http://dx.doi.org/10.1155/2013/753427
   PubMedGoogle Scholar
• Lladser A, Sanhueza C, Kiessling R, Quest AF. Is survivin the potential Achilles' heel of cancer? Adv Cancer Res 2011; 111:1-37; PMID:21704829; http://dx.doi.org/10.1016/B978-0-12-385524-4.00001-5
   PubMed Web of Science ®Google Scholar
• Vermeij R, Daemen T, de Bock GH, de Graeff P, Leffers N, Lambeck A, ten Hoor KA, Hollema H, van der Zee AG, Nijman HW. Potential target antigens for a universal vaccine in epithelial ovarian cancer. Clin Dev Immunol 2010; 2010:891505; PMID:20885926; http://dx.doi.org/10.1155/2010/891505
   PubMedGoogle Scholar
• Berinstein NL, Karkada M, Morse MA, Nemunaitis JJ, Chatta G, Kaufman H, Odunsi K, Nigam R, Sammatur L, MacDonald LD et al. First-in-man application of a novel therapeutic cancer vaccine formulation with the capacity to induce multi-functional T cell responses in ovarian, breast and prostate cancer patients. J Transl Med 2012; 10:156; PMID:22862954; http://dx.doi.org/10.1186/1479-5876-10-156
   PubMed Web of Science ®Google Scholar
• Karkada M, Weir GM, Quinton T, Sammatur L, MacDonald LD, Grant A, Liwski R, Juskevicius R, Sinnathamby G, Philip R et al. A novel breast/ovarian cancer peptide vaccine platform that promotes specific type-1 but not Treg/Tr1-type responses. J Immunother 2010; 33:250-61; PMID:20445345; http://dx.doi.org/10.1097/CJI.0b013e3181c1f1e9
   PubMed Web of Science ®Google Scholar
• Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, Solary E, Le Cesne A, Zitvogel L, Chauffert B. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother 2007; 56:641-8; PMID:16960692; http://dx.doi.org/10.1007/s00262-006-0225-8
   PubMed Web of Science ®Google Scholar
• Weir GM, Hrytsenko O, Stanford MM, Berinstein NL, Karkada M, Liwski R, Mansour, M. Metronomic cyclophosphamide enhances HPV16E7 peptide vaccine induced antigen-specific and cytotoxic T-cell mediated antitumor immune response. Oncoimmunology 2014; 3: e953407; http://dx.doi.org/10.4161/21624011.2014.953407
   PubMed Web of Science ®Google Scholar
• Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, Jungbluth AA, Frosina D, Gnjatic S, Ambrosone C et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005; 102:18538-43; PMID:16344461; http://dx.doi.org/10.1073/pnas.0509182102
   PubMed Web of Science ®Google Scholar
• Obermajer N, Muthuswamy R, Odunsi K, Edwards RP, Kalinski P. PGE(2)-induced CXCL12 production and CXCR4 expression controls the accumulation of human MDSCs in ovarian cancer environment. Cancer Res 2011; 71:7463-70; PMID:22025564; http://dx.doi.org/10.1158/0008-5472.CAN-11-2449
   PubMed Web of Science ®Google Scholar
• Becker JC, Andersen MH, Hofmeister-Muller V, Wobser M, Frey L, Sandig C, Walter S, Singh-Jasuja H, Kampgen E, Opitz A et al. Survivin-specific T-cell reactivity correlates with tumor response and patient survival: a phase-II peptide vaccination trial in metastatic melanoma. Cancer Immunol Immunother 2012; 61:2091-103; PMID:22565484; http://dx.doi.org/10.1007/s00262-012-1266-9
   PubMed Web of Science ®Google Scholar
• Lennerz V, Gross S, Gallerani E, Sessa C, Mach N, Boehm S, Hess D, von Boehmer L, Knuth A, Ochsenbein AF et al. Immunologic response to the survivin-derived multi-epitope vaccine EMD640744 in patients with advanced solid tumors. Cancer Immunol Immunother 2014; 63:381-94; PMID:24487961; http://dx.doi.org/10.1007/s00262-013-1516-5
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, Finkelstein SE, Theoret MR, Rosenberg SA, Restifo NP. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest 2005; 115:1616-26; PMID:15931392; http://dx.doi.org/10.1172/JCI24480
   PubMed Web of Science ®Google Scholar
• Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE, Palmer DC, Antony PA, Hwang ST, Rosenberg SA et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A 2005; 102:9571-6; PMID:15980149; http://dx.doi.org/10.1073/pnas.0503726102
   PubMed Web of Science ®Google Scholar
• Gomez CE, Najera JL, Perdiguero B, Garcia-Arriaza J, Sorzano CO, Jimenez V, Gonzalez-Sanz R, Jimenez JL, Munoz-Fernandez MA, Lopez Bernaldo de Quiros JC et al. The HIV/AIDS vaccine candidate MVA-B administered as a single immunogen in humans triggers robust, polyfunctional, and selective effector memory T cell responses to HIV-1 antigens. J Virol 2011; 85:11468-78; PMID:21865377; http://dx.doi.org/10.1128/JVI.05165-11
   PubMed Web of Science ®Google Scholar
• Hailemichael Y, Dai Z, Jaffarzad N, Ye Y, Medina MA, Huang XF, Dorta-Estremera SM, Greeley NR, Nitti G, Peng W et al. Persistent antigen at vaccination sites induces tumor-specific CD8(+) T cell sequestration, dysfunction and deletion. Nat Med 2013; 19:465-72; PMID:23455713; http://dx.doi.org/10.1038/nm.3105
   PubMed Web of Science ®Google Scholar
• Salerno EP, Shea SM, Olson WC, Petroni GR, Smolkin ME, McSkimming C, Chianese-Bullock KA, Slingluff CL, Jr. Activation, dysfunction and retention of T cells in vaccine sites after injection of incomplete Freund's adjuvant, with or without peptide. Cancer Immunol Immunother 2013; 62:1149-59; PMID:23657629; http://dx.doi.org/10.1007/s00262-013-1435-5
   PubMed Web of Science ®Google Scholar
• Brewer KD, Lake K, Pelot N, Stanford MM, DeBay DR, Penwell A, Weir GM, Karkada M, Mansour M, Bowen CV. Clearance of depot vaccine SPIO-labeled antigen and substrate visualized using MRI. Vaccine 2014; 32:6956-62; PMID:25444822; http://dx.doi.org/10.1016/j.vaccine.2014.10.058
   PubMed Web of Science ®Google Scholar
• Slingluff CL Jr, Yamshchikov G, Neese P, Galavotti H, Eastham S, Engelhard VH, Kittlesen D, Deacon D, Hibbitts S, Grosh WW et al. Phase I trial of a melanoma vaccine with gp100(280-288) peptide and tetanus helper peptide in adjuvant: immunologic and clinical outcomes. Clin Cancer Res 2001; 7:3012-24; PMID:11595689
   PubMed Web of Science ®Google Scholar
• Galecki A, Burzykowski T. Linear Mixed-Effect Models Using R. Vol. 10. 2013, New York: Springer.
   Google Scholar
• Galecki A. General class of covariance structures for two or more repeated factors in longitudinal data analysis. Commun Statist Theory Methods 1994; 23:3105-3119; http://dx.doi.org/10.1080/03610929408831436
   Web of Science ®Google Scholar
• Kenward M, Small RJ. Small sample inference for fixed ffects from restricted maximum likelihood. Biometrics 1997; 53:983-997; PMID:9333350; http://dx.doi.org/10.2307/2533558
   PubMed Web of Science ®Google Scholar
• Dmitrienko A, Tamhane AC, Bretz, F, Multiple testing problems in pharamceutical statistics. 2010, Boca Raton: Chapman & Hall/ CRC Press.
   Google Scholar
• Ellebaek E, Engell-Boerregaard L, Iversen TZ, Froesig TM, Munir S, Hadrup SR, Andersen MH, Svane IM. Metastatic melanoma patients treated with dendritic cell vaccination, interleukin-2 and metronomic cyclophosphamide: results from a phase II trial. Cancer Immunol Immunother 2012; 61:1791-804; PMID:22426890; http://dx.doi.org/10.1007/s00262-012-1242-4
   PubMed Web of Science ®Google Scholar