Tumor-infiltrating plasmacytoid dendritic cells promote immunosuppression by Tr1 cells in human liver tumors

References

• Mazzanti R, Gramantieri L, Bolondi L. Hepatocellular carcinoma: epidemiology and clinical aspects. Mol Aspects Med 2008; 29:130-43; PMID:18061252; http://dx.doi.org/10.1016/j.mam.2007.09.008
   PubMedGoogle Scholar
• Kemeny N. The management of resectable and unresectable liver metastases from colorectal cancer. Curr Opin Oncol 2010; 22:364-73; PMID: 20520544; http://dx.doi.org/10.1097/CCO.0b013e32833a6c8a
   PubMed Web of Science ®Google Scholar
• Pardee AD, Butterfield LH. Immunotherapy of hepatocellular carcinoma: Unique challenges and clinical opportunities. Oncoimmunology 2012; 1:48-55; PMID:22720211; http://dx.doi.org/10.4161/onci.1.1.18344
   PubMed Web of Science ®Google Scholar
• Mazzolini G, Ochoa MC, Morales-Kastresana A, Sanmamed MF, Melero I. The liver, liver metastasis and liver cancer: a special case for immunotherapy with cytokines and immunostimulatory monoclonal antibodies. Immunotherapy 2012; 4:1081-5; PMID:23194355; http://dx.doi.org/10.2217/imt.12.99
   PubMedGoogle Scholar
• Pedroza-Gonzalez A, Xu K, Wu TC, Aspord C, Tindle S, Marches F, Gallegos M, Burton EC, Savino D, Hori T, et al. Thymic stromal lymphopoietin fosters human breast tumor growth by promoting type 2 inflammation. J Exp Med 2011; 208:479-90; PMID:21339324; http://dx.doi.org/10.1084/jem.20102131
   PubMed Web of Science ®Google Scholar
• Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012; 12:265-77; PMID:22437871; http://dx.doi.org/10.1038/nrc3258
   PubMed Web of Science ®Google Scholar
• Pedroza-Gonzalez A, Verhoef C, Ijzermans JN, Peppelenbosch MP, Kwekkeboom J, Verheij J, Janssen HL, Sprengers D. Activated tumor-infiltrating CD4+ regulatory T cells restrain antitumor immunity in patients with primary or metastatic liver cancer. Hepatology 2013; 57:183-94; PMID:22911397; http://dx.doi.org/10.1002/hep.26013
   PubMed Web of Science ®Google Scholar
• Pedroza-Gonzalez A, Kwekkeboom J, Sprengers D. T-cell suppression mediated by regulatory T cells infiltrating hepatic tumors can be overcome by GITRL treatment. Oncoimmunology 2013; 2:e22450; PMID:23483229; http://dx.doi.org/10.4161/onci.22450
   PubMedGoogle Scholar
• Gregori S, Goudy KS, Roncarolo MG. The cellular and molecular mechanisms of immuno-suppression by human type 1 regulatory T cells. Front Immunol 2012; 3:30; PMID:22566914; http://dx.doi.org/10.3389/fimmu.2012.00030
   PubMed Web of Science ®Google Scholar
• Roncarolo MG, Gregori S, Lucarelli B, Ciceri F, Bacchetta R. Clinical tolerance in allogeneic hematopoietic stem cell transplantation. Immunol Rev 2011; 241:145-63; PMID:21488896; http://dx.doi.org/10.1111/j.1600-065X.2011.01010.x
   PubMed Web of Science ®Google Scholar
• Kakita N, Kanto T, Itose I, Kuroda S, Inoue M, Matsubara T, Higashitani K, Miyazaki M, Sakakibara M, Hiramatsu N, et al. Comparative analyses of regulatory T cell subsets in patients with hepatocellular carcinoma: a crucial role of CD25(−) FOXP3(−) T cells. Int J Cancer 2012; 131:2573-83; PMID:22419479; http://dx.doi.org/10.1002/ijc.27535
   PubMedGoogle Scholar
• Marshall NA, Christie LE, Munro LR, Culligan DJ, Johnston PW, Barker RN, Vickers MA. Immunosuppressive regulatory T cells are abundant in the reactive lymphocytes of Hodgkin lymphoma. Blood 2004; 103:1755-62; PMID:14604957; http://dx.doi.org/10.1182/blood-2003-07-2594
   PubMed Web of Science ®Google Scholar
• Lundqvist A, Palmborg A, Pavlenko M, Levitskaya J, Pisa P. Mature dendritic cells induce tumor-specific type 1 regulatory T cells. J Immunother 2005; 28:229-35; PMID:15838379; http://dx.doi.org/10.1097/01.cji.0000158854.15664.c2
   PubMedGoogle Scholar
• Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside TL. Expansion of human T regulatory type 1 cells in the microenvironment of cyclooxygenase 2 overexpressing head and neck squamous cell carcinoma. Cancer Res 2007; 67:8865-73; PMID:17875728; http://dx.doi.org/10.1158/0008-5472.CAN-07-0767
   PubMed Web of Science ®Google Scholar
• Gagliani N, Magnani CF, Huber S, Gianolini ME, Pala M, Licona-Limon P, Guo B, Herbert DR, Bulfone A, Trentini F, et al. Coexpression of CD49b and LAG-3 identifies human and mouse T regulatory type 1 cells. Nat Med 2013; 19:739-46; PMID:23624599; http://dx.doi.org/10.1038/nm.3179
   PubMed Web of Science ®Google Scholar
• Kemper C, Chan AC, Green JM, Brett KA, Murphy KM, Atkinson JP. Activation of human CD4+ cells with CD3 and CD46 induces a T-regulatory cell 1 phenotype. Nature 2003; 421:388-92; PMID:12540904; http://dx.doi.org/10.1038/nature01315
   PubMed Web of Science ®Google Scholar
• Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, Kroczek RA. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999; 397:263-6; PMID:9930702; http://dx.doi.org/10.1038/16717
   PubMed Web of Science ®Google Scholar
• Ito T, Yang M, Wang YH, Lande R, Gregorio J, Perng OA, Qin XF, Liu YJ, Gilliet M. Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J Exp Med 2007; 204:105-15; PMID:17200410; http://dx.doi.org/10.1084/jem.20061660
   PubMed Web of Science ®Google Scholar
• Conrad C, Gregorio J, Wang YH, Ito T, Meller S, Hanabuchi S, Anderson S, Atkinson N, Ramirez PT, Liu YJ, et al. Plasmacytoid dendritic cells promote immunosuppression in ovarian cancer via ICOS costimulation of Foxp3(+) T-regulatory cells. Cancer Res 2012; 72:5240-9; PMID:22850422; http://dx.doi.org/10.1158/0008-5472.CAN-12-2271
   PubMed Web of Science ®Google Scholar
• Labidi-Galy SI, Sisirak V, Meeus P, Gobert M, Treilleux I, Bajard A, Combes JD, Faget J, Mithieux F, Cassignol A, et al. Quantitative and functional alterations of plasmacytoid dendritic cells contribute to immune tolerance in ovarian cancer. Cancer Res 2011; 71:5423-34; PMID:21697280; http://dx.doi.org/10.1158/0008-5472.CAN-11-0367
   PubMed Web of Science ®Google Scholar
• Faget J, Bendriss-Vermare N, Gobert M, Durand I, Olive D, Biota C, Bachelot T, Treilleux I, Goddard-Leon S, Lavergne E, et al. ICOS-ligand expression on plasmacytoid dendritic cells supports breast cancer progression by promoting the accumulation of immunosuppressive CD4+ T cells. Cancer Res 2012; 72:6130-41; PMID:23026134; http://dx.doi.org/10.1158/0008-5472.CAN-12-2409
   PubMed Web of Science ®Google Scholar
• Sisirak V, Faget J, Gobert M, Goutagny N, Vey N, Treilleux I, Renaudineau S, Poyet G, Labidi-Galy SI, Goddard-Leon S, et al. Impaired IFN-alpha production by plasmacytoid dendritic cells favors regulatory T-cell expansion that may contribute to breast cancer progression. Cancer Res 2012; 72:5188-97; PMID:22836755; http://dx.doi.org/10.1158/0008-5472.CAN-11-3468
   PubMed Web of Science ®Google Scholar
• Chen KJ, Lin SZ, Zhou L, Xie HY, Zhou WH, Taki-Eldin A, Zheng SS. Selective recruitment of regulatory T cell through CCR6-CCL20 in hepatocellular carcinoma fosters tumor progression and predicts poor prognosis. PLoS One 2011; 6:e24671; PMID:21935436; http://dx.doi.org/10.1371/journal.pone.0024671
   PubMed Web of Science ®Google Scholar
• Nishikawa H, Sakaguchi S. Regulatory T cells in tumor immunity. Int J Cancer 2010; 127:759-67; PMID:20518016
   PubMed Web of Science ®Google Scholar
• Yang XH, Yamagiwa S, Ichida T, Matsuda Y, Sugahara S, Watanabe H, Sato Y, Abo T, Horwitz DA, Aoyagi Y. Increase of CD4+ CD25+ regulatory T-cells in the liver of patients with hepatocellular carcinoma. J Hepatol 2006; 45:254-62; PMID:16600416; http://dx.doi.org/10.1016/j.jhep.2006.01.036
   PubMed Web of Science ®Google Scholar
• Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009; 27:186-92; PMID:19064967; http://dx.doi.org/10.1200/JCO.2008.18.7229
   PubMed Web of Science ®Google Scholar
• Bergmann C, Strauss L, Wang Y, Szczepanski MJ, Lang S, Johnson JT, Whiteside TL. T regulatory type 1 cells in squamous cell carcinoma of the head and neck: mechanisms of suppression and expansion in advanced disease. Clin Cancer Res 2008; 14:3706-15; PMID:18559587; http://dx.doi.org/10.1158/1078-0432.CCR-07-5126
   PubMed Web of Science ®Google Scholar
• Akbari O, Freeman GJ, Meyer EH, Greenfield EA, Chang TT, Sharpe AH, Berry G, DeKruyff RH, Umetsu DT. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med 2002; 8:1024-32; PMID:12145647; http://dx.doi.org/10.1038/nm745
   PubMed Web of Science ®Google Scholar
• Le Mercier I, Poujol D, Sanlaville A, Sisirak V, Gobert M, Durand I, Dubois B, Treilleux I, Marvel J, Vlach J, et al. Tumor promotion by intratumoral plasmacytoid dendritic cells is reversed by TLR7 ligand treatment. Cancer Res 2013; 73:4629-40; PMID:23722543; http://dx.doi.org/10.1158/0008-5472.CAN-12-3058
   PubMed Web of Science ®Google Scholar