Antigen targeting to dendritic cells combined with transient regulatory T cell inhibition results in long-term tumor regression

References

• 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
• Menetrier-Caux C, Curiel T, Faget J, Manuel M, Caux C, Zou W. Targeting regulatory T cells. Target Oncol 2012; 7:15-28; PMID:22327882; http://dx.doi.org/10.1007/s11523-012-0208-y
   PubMed Web of Science ®Google Scholar
• Nishikawa H, S Sakaguchi. Regulatory T cells in tumor immunity. Int J Cancer 2010; 127:759-67; PMID:20518016; http://dx.doi.org/10.1002/ijc.25429
   PubMed Web of Science ®Google Scholar
• Chen DS, I Mellman. Oncology meets immunology: the cancer-immunity cycle. Immunity 2013; 39:1-10; PMID:23890059; http://dx.doi.org/10.1016/j.immuni.2013.07.012
   PubMed Web of Science ®Google Scholar
• Belkaid Y, G Oldenhove. Tuning microenvironments: induction of regulatory T cells by dendritic cells. Immunity 2008; 29: 362-71.; PMID:18799144; http://dx.doi.org/10.1016/j.immuni.2008.08.005
   PubMed Web of Science ®Google Scholar
• Mayer CT, Berod L, Sparwasser T. Layers of dendritic cell-mediated T cell tolerance, their regulation and the prevention of autoimmunity. Front Immunol 2012; 3:183; PMID:22783257; http://dx.doi.org/10.3389/fimmu.2012.00183
   PubMed Web of Science ®Google Scholar
• Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10:942-9; PMID:15322536; http://dx.doi.org/10.1038/nm1093
   PubMed Web of Science ®Google Scholar
• Kryczek I, Liu R, Wang G, Wu K, Shu X, Szeliga W, Vatan L, Finlayson E, Huang E, Simeone D et al. FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res 2009; 69:3995-4000; PMID:19383912; http://dx.doi.org/10.1158/0008-5472.CAN-08-3804
   PubMed Web of Science ®Google Scholar
• Hindley JP, Ferreira C, Jones E, Lauder SN, Ladell K, Wynn KK, Betts GJ, Singh Y, Price DA, Godkin AJ et al. Analysis of the T-cell receptor repertoires of tumor-infiltrating conventional and regulatory T cells reveals no evidence for conversion in carcinogen-induced tumors. Cancer Res 2011; 71:736-46; PMID:21156649; http://dx.doi.org/10.1158/0008-5472.CAN-10-1797
   PubMed Web of Science ®Google Scholar
• Haen SP, HG Rammensee. The repertoire of human tumor-associated epitopes - identification and selection of antigens and their application in clinical trials. Curr Opin Immunol 2013; 25:277-83; PMID:23619309; http://dx.doi.org/10.1016/j.coi.2013.03.007
   PubMed Web of Science ®Google Scholar
• Sosman JA, Carrillo C, Urba WJ, Flaherty L, Atkins MB, Clark JI, Dutcher J, Margolin KA, Mier J, Gollob J et al. Three phase II cytokine working group trials of gp100 (210M) peptide plus high-dose interleukin-2 in patients with HLA-A2-positive advanced melanoma. J Clin Oncol 2008; 26:2292-8; PMID:18467720; http://dx.doi.org/10.1200/JCO.2007.13.3165
   PubMed Web of Science ®Google Scholar
• Di Pucchio T, Pilla L, Capone I, Ferrantini M, Montefiore E, Urbani F, Patuzzo R, Pennacchioli E, Santinami M, Cova A, et al. Immunization of stage IV melanoma patients with Melan-A/MART-1 and gp100 peptides plus IFN-alpha results in the activation of specific CD8(+) T cells and monocyte/dendritic cell precursors. Cancer Res 2006; 66: 4943-51; PMID:16651452; http://dx.doi.org/10.1158/0008-5472.CAN-05-3396
   PubMed Web of Science ®Google Scholar
• Schwartzentruber DJ, Lawson DH, Richards JM, Conry RM, Miller DM, Treisman J, Gailani F, Riley L, Conlon K, Pockaj B et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N Engl J Med 2011; 364:2119-27; PMID:21631324; http://dx.doi.org/10.1056/NEJMoa1012863
   PubMed Web of Science ®Google Scholar
• Smith JW, Walker EB, Fox BA, Haley D, Wisner KP, Doran T, Fisher B, Justice L, Wood W, Vetto J et al. Adjuvant immunization of HLA-A2-positive melanoma patients with a modified gp100 peptide induces peptide-specific CD8+ T-cell responses. J Clin Oncol 2003; 21:1562-73; PMID:12697882; http://dx.doi.org/10.1200/JCO.2003.09.020
   PubMed Web of Science ®Google Scholar
• Walker EB, Haley D, Miller W, Floyd K, Wisner KP, Sanjuan N, Maecker H, Romero P, Hu HM, Alvord WG, et al. gp100(209-2M) peptide immunization of human lymphocyte antigen-A2+ stage I-III melanoma patients induces significant increase in antigen-specific effector and long-term memory CD8+ T cells. Clin Cancer Res 2004; 10:668-0; PMID:14760090
   PubMed Web of Science ®Google Scholar
• Caminschi I, Maraskovsky E, Heath WR. Targeting dendritic cells in vivo for cancer therapy. Front Immunol 2012; 3:13; PMID:22566899; http://dx.doi.org/10.3389/fimmu.2012.00013
   PubMed Web of Science ®Google Scholar
• Engering A, Geijtenbeek TB, van Vliet SJ, Wijers M, van Liempt E, Demaurex N, Lanzavecchia A, Fransen J, Figdor CG, Piguet V. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 2002; 168:2118-26; PMID:11859097; http://dx.doi.org/10.4049/jimmunol.168.5.2118
   PubMed Web of Science ®Google Scholar
• Kretz-Rommel A, Qin F, Dakappagari N, Torensma R, Faas S, Wu D, Bowdish KS. In vivo targeting of antigens to human dendritic cells through DC-SIGN elicits stimulatory immune responses and inhibits tumor growth in grafted mouse models. J Immunother 2007; 30:715-26; PMID:17893564; http://dx.doi.org/10.1097/CJI.0b013e318135472c
   PubMed Web of Science ®Google Scholar
• Tacken PJ, de Vries IJ, Gijzen K, Joosten B, Wu D, Rother RP, Faas SJ, Punt CJ, Torensma R, Adema GJ et al. Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 2005; 106:1278-85; PMID:15878980; http://dx.doi.org/10.1182/blood-2005-01-0318
   PubMed Web of Science ®Google Scholar
• Garcia-Vallejo JJ, Y van Kooyk. The physiological role of DC-SIGN: a tale of mice and men. Trends Immunol 2013; 34:482-6; PMID:23608151; http://dx.doi.org/10.1016/j.it.2013.03.001
   PubMed Web of Science ®Google Scholar
• Schaefer M, Reiling N, Fessler C, Stephani J, Taniuchi I, Hatam F, Yildirim AO, Fehrenbach H, Walter K, Ruland J et al. Decreased pathology and prolonged survival of human DC-SIGN transgenic mice during mycobacterial infection. J Immunol 2008; 180:6836-45; PMID:18453604; http://dx.doi.org/10.4049/jimmunol.180.10.6836
   PubMed Web of Science ®Google Scholar
• Cruz LJ, Tacken PJ, Fokkink R, Joosten B, Stuart MC, Albericio F, Torensma R, Figdor CG. Targeted PLGA nano- but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J Control Release 2010; 144:118-26; PMID:20156497; http://dx.doi.org/10.1016/j.jconrel.2010.02.013
   PubMed Web of Science ®Google Scholar
• Hesse C, Ginter W, Förg T, Mayer CT, Baru AM, Arnold-Schrauf C, Unger WW, Kalay H, van Kooyk Y, Berod L et al. In vivo targeting of human DC-SIGN drastically enhances CD8+ T-cell-mediated protective immunity. Eur J Immunol 2013; 43:2543-53; PMID:23784881; http://dx.doi.org/10.1002/eji.201343429
   PubMed Web of Science ®Google Scholar
• Appelmelk BJ, van Die I, van Vliet SJ, Vandenbroucke-Grauls CM, Geijtenbeek TB, van Kooyk Y. Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells. J Immunol 2003; 170:1635-9; PMID:12574325; http://dx.doi.org/10.4049/jimmunol.170.4.1635
   PubMed Web of Science ®Google Scholar
• Garcia-Vallejo JJ, Ambrosini M, Overbeek A, van Riel WE, Bloem K, Unger WW, Chiodo F, Bolscher JG, Nazmi K, Kalay H et al. Multivalent glycopeptide dendrimers for the targeted delivery of antigens to dendritic cells. Mol Immunol 2013; 53:387-97; PMID:23103377; http://dx.doi.org/10.1016/j.molimm.2012.09.012
   PubMedGoogle Scholar
• Unger WW, van Beelen AJ, Bruijns SC, Joshi M, Fehres CM, van Bloois L, Verstege MI, Ambrosini M, Kalay H, Nazmi K et al. Glycan-modified liposomes boost CD4+ and CD8+ T-cell responses by targeting DC-SIGN on dendritic cells. J Control Release 2012; 160:88-95; PMID:22366522; http://dx.doi.org/10.1016/j.jconrel.2012.02.007
   PubMed Web of Science ®Google Scholar
• Aarnoudse CA, Bax M, Sánchez-Hernández M, García-Vallejo JJ, van Kooyk Y. Glycan modification of the tumor antigen gp100 targets DC-SIGN to enhance dendritic cell induced antigen presentation to T cells. Int J Cancer 2008; 122:839-46; PMID:17957800; http://dx.doi.org/10.1002/ijc.23101
   PubMed Web of Science ®Google Scholar
• Singh SK, Stephani J, Schaefer M, Kalay H, García-Vallejo JJ, den Haan J, Saeland E, Sparwasser T, van Kooyk Y. Targeting glycan modified OVA to murine DC-SIGN transgenic dendritic cells enhances MHC class I and II presentation. Mol Immunol 2009; 47:164-74; PMID:19818504; http://dx.doi.org/10.1016/j.molimm.2009.09.026
   PubMed Web of Science ®Google Scholar
• Yang L, Yang H, Rideout K, Cho T, Joo KI, Ziegler L, Elliot A, Walls A, Yu D, Baltimore D et al. Engineered lentivector targeting of dendritic cells for in vivo immunization. Nat Biotechnol 2008; 26:326-34; PMID:18297056; http://dx.doi.org/10.1038/nbt1390
   PubMed Web of Science ®Google Scholar
• Klages K, Mayer CT, Lahl K, Loddenkemper C, Teng MW, Ngiow SF, Smyth MJ, Hamann A, Huehn J, Sparwasser T. Selective depletion of Foxp3+ regulatory T cells improves effective therapeutic vaccination against established melanoma. Cancer Res 2010; 70:7788-99; PMID:20924102; http://dx.doi.org/10.1158/0008-5472.CAN-10-1736
   PubMed Web of Science ®Google Scholar
• Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155:1151-64; PMID:7636184
   PubMed Web of Science ®Google Scholar
• Quezada SA, Peggs KS, Simpson TR, Shen Y, Littman DR, Allison JP. Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J Exp Med 2008; 205:2125-38; PMID:18725522; http://dx.doi.org/10.1084/jem.20080099
   PubMed Web of Science ®Google Scholar
• Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor Rejection by in Vivo Administration of Anti-CD25 (Interleukin-2 Receptor +¦) Monoclonal Antibody. Cancer Res 1999; 59:3128-33; PMID:10397255
   PubMed Web of Science ®Google Scholar
• Dannull J, Su Z, Rizzieri D, Yang BK, Coleman D, Yancey D, Zhang A, Dahm P, Chao N, Gilboa E et al. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 2005; 115:3623-33; PMID:16308572; http://dx.doi.org/10.1172/JCI25947
   PubMed Web of Science ®Google Scholar
• Morse MA, Hobeika AC, Osada T, Serra D, Niedzwiecki D, Lyerly HK, Clay TM. Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines. Blood 2008; 112:610-8; PMID:18519811; http://dx.doi.org/10.1182/blood-2008-01-135319
   PubMed Web of Science ®Google Scholar
• Baur AS, Lutz MB, Schierer S, Beltrame L, Theiner G, Zinser E, Ostalecki C, Heidkamp G, Haendle I, Erdmann M et al. Denileukin diftitox (ONTAK) induces a tolerogenic phenotype in dendritic cells and stimulates survival of resting Treg. Blood 2013; 122:2185-94; PMID:23958949; http://dx.doi.org/10.1182/blood-2012-09-456988
   PubMed Web of Science ®Google Scholar
• Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G, Hamann A, Wagner H, Huehn J, Sparwasser T. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med 2007; 204:57-63; PMID:17200412; http://dx.doi.org/10.1084/jem.20061852
   PubMed Web of Science ®Google Scholar
• Janssen EM, Lemmens EE, Wolfe T, Christen U, von Herrath MG, Schoenberger SP. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 2003; 421:852-6; PMID:12594515; http://dx.doi.org/10.1038/nature01441
   PubMed Web of Science ®Google Scholar
• Bos R, LA Sherman. CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 2010; 70:8368-77; PMID:20940398; http://dx.doi.org/10.1158/0008-5472.CAN-10-1322
   PubMed Web of Science ®Google Scholar
• Li X, Kostareli E, Suffner J, Garbi N, Hämmerling GJ. Efficient Treg depletion induces T-cell infiltration and rejection of large tumors. Eur J Immunol 2010; 40:3325-35; PMID:21072887; http://dx.doi.org/10.1002/eji.201041093
   PubMed Web of Science ®Google Scholar
• Bos PD, Plitas G, Rudra D, Lee SY, Rudensky AY. Transient regulatory T cell ablation deters oncogene-driven breast cancer and enhances radiotherapy. J Exp Med 2013; 210: 2435-66; PMID:24127486; http://dx.doi.org/10.1084/jem.20130762
   PubMed Web of Science ®Google Scholar
• Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 2007; 8:191-7; PMID:17136045; http://dx.doi.org/10.1038/ni1428
   PubMed Web of Science ®Google Scholar
• Mayer CT, Ghorbani P, Kühl AA, Stüve P, Hegemann M, Berod L, Gershwin ME, Sparwasser T. Few Foxp3 regulatory T cells are sufficient to protect adult mice from lethal autoimmunity. Eur J Immunol 2014; 44:2990-3002 (epub ahead of print)PMID:25042334; http://dx.doi.org/10.1002/eji.201344315
   PubMed Web of Science ®Google Scholar
• Fisher DT, Chen Q, Skitzki JJ, Muhitch JB, Zhou L, Appenheimer MM, Vardam TD, Weis EL, Passanese J, Wang WC et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest 2011; 121:3846-59; PMID:21926464; http://dx.doi.org/10.1172/JCI44952
   PubMed Web of Science ®Google Scholar
• Teng MW, Ngiow SF, von Scheidt B, McLaughlin N, Sparwasser T, Smyth MJ. Conditional regulatory T-cell depletion releases adaptive immunity preventing carcinogenesis and suppressing established tumor growth. Cancer Res 2010; 70:7800-9; PMID:20924111; http://dx.doi.org/10.1158/0008-5472.CAN-10-1681
   PubMed Web of Science ®Google Scholar
• Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998; 393:480-3; PMID:9624005; http://dx.doi.org/10.1038/31002
   PubMed Web of Science ®Google Scholar
• Ossendorp F, Mengedé E, Camps M, Filius R, Melief CJ. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med 1998; 187:693-702; PMID:9480979; http://dx.doi.org/10.1084/jem.187.5.693
   PubMed Web of Science ®Google Scholar
• Haen SP, HG Rammensee. The repertoire of human tumor-associated epitopes - identification and selection of antigens and their application in clinical trials. Curr Opin Immunol 2013; 25:277-83; PMID:23619309; http://dx.doi.org/10.1016/j.coi.2013.03.007
   PubMed Web of Science ®Google Scholar
• Peggs KS, Quezada SA, Chambers CA, Korman AJ, Allison JP. Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med 2009; 206:1717-25; PMID:19581407; http://dx.doi.org/10.1084/jem.20082492
   PubMed Web of Science ®Google Scholar
• Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID:20525992; http://dx.doi.org/10.1056/NEJMoa1003466
   PubMed Web of Science ®Google Scholar
• Hodge JW, Chakraborty M, Kudo-Saito C, Garnett CT, Schlom J. Multiple costimulatory modalities enhance CTL avidity. J Immunol 2005; 174:5994-6004; PMID:15879092; http://dx.doi.org/10.4049/jimmunol.174.10.5994
   PubMed Web of Science ®Google Scholar
• Topalian SL, Drake CG, Pardoll DM. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol 2012; 24:207-12; PMID:22236695; http://dx.doi.org/10.1016/j.coi.2011.12.009
   PubMed Web of Science ®Google Scholar
• Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A 2010; 107:4275-80; PMID:20160101; http://dx.doi.org/10.1073/pnas.0915174107
   PubMed Web of Science ®Google Scholar