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Original research

Hematopoietic stem cell-derived myeloid and plasmacytoid DC-based vaccines are highly potent inducers of tumor-reactive T cell and NK cell responses ex vivo

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Article: e1285991 | Received 31 Oct 2016, Accepted 18 Jan 2017, Published online: 15 Mar 2017

References

  • Appelbaum FR. Haematopoietic cell transplantation as immunotherapy. Nature 2001; 411:385-9; PMID:11357147; http://dx.doi.org/10.1038/35077251
  • Barrett AJ. Understanding and harnessing the graft-versus-leukaemia effect. Brit J Haematol 2008; 142:877-88; PMID:18564358; http://dx.doi.org/10.1111/j.1365-2141.2008.07260.x
  • Tanaka M, Kobayashi S, Numata A, Tachibana T, Takasaki H, Maruta A, Ishigatsubo Y, Kanamori H. The impact of the dose of natural killer cells in the graft on severe acute graft-versus-host disease after unrelated bone marrow transplantation. Leukemia Res 2012; 36:699-703; PMID:22172462; http://dx.doi.org/10.1016/j.leukres.2011.11.009
  • Baron F, Petersdorf EW, Gooley T, Sandmaier BM, Malkki M, Chauncey TR, Maloney DG, Storb R. What is the role for donor natural killer cells after nonmyeloablative conditioning? Biol Blood Marrow Transplant 2009; 15:580-8; PMID:19361750; http://dx.doi.org/10.1016/j.bbmt.2009.01.018
  • Savani BN, Mielke S, Adams S, Uribe M, Rezvani K, Yong AS, Zeilah J, Kurlander R, Srinivasan R, Childs R et al. Rapid natural killer cell recovery determines outcome after T-cell-depleted HLA-identical stem cell transplantation in patients with myeloid leukemias but not with acute lymphoblastic leukemia. Leukemia 2007; 21:2145-52; PMID:17673900; http://dx.doi.org/10.1038/sj.leu.2404892
  • Banchereau J, Palucka AK. Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol 2005; 5:296-306; PMID:15803149; http://dx.doi.org/10.1038/nri1592
  • 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
  • Liu YJ. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 2001; 106:259-62; PMID:11509173; http://dx.doi.org/10.1016/S0092-8674(01)00456-1
  • Merad M, Sathe P, Helft J, Miller J, Mortha A. The dendritic cell lineage: Ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 2013; 31:563-604; PMID:23516985; http://dx.doi.org/10.1146/annurev-immunol-020711-074950
  • Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, Buck DW, Schmitz J. BDCA-2, BDCA-3, and BDCA-4: Three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 2000; 165:6037-46; PMID:11086035; http://dx.doi.org/10.4049/jimmunol.165.11.6037
  • Nizzoli G, Krietsch J, Weick A, Steinfelder S, Facciotti F, Gruarin P, Bianco A, Steckel B, Moro M, Crosti M et al. Human CD1c+ dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses. Blood 2013; 122:932-42; PMID:23794066; http://dx.doi.org/10.1182/blood-2013-04-495424
  • Wilkinson R, Kassianos AJ, Swindle P, Hart DN, Radford KJ. Numerical and functional assessment of blood dendritic cells in prostate cancer patients. Prostate 2006; 66:180-92; PMID:16173035; http://dx.doi.org/10.1002/pros.20333
  • Colonna M, Trinchieri G, Liu YJ. Plasmacytoid dendritic cells in immunity. Nat Immunol 2004; 5:1219-26; PMID:15549123; http://dx.doi.org/10.1038/ni1141
  • Gerosa F, Gobbi A, Zorzi P, Burg S, Briere F, Carra G, Trinchieri G. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J Immunol 2005; 174:727-34; PMID:15634892; http://dx.doi.org/10.4049/jimmunol.174.2.727
  • Hanabuchi S, Watanabe N, Wang YH, Wang YH, Ito T, Shaw J, Cao W, Qin FX, Liu YJ. Human plasmacytoid predendritic cells activate NK cells through glucocorticoid-induced tumor necrosis factor receptor-ligand (GITRL). Blood 2006; 107:3617-23; PMID:16397134; http://dx.doi.org/10.1182/blood-2005-08-3419
  • Benlahrech A, Donaghy H, Rozis G, Goodier M, Klavinskis L, Gotch F, Patterson S. Human NK cell Up-regulation of CD69, HLA-DR, interferon gamma secretion and cytotoxic activity by plasmacytoid dendritic cells is regulated through overlapping but different pathways. Sensors 2009; 9:386-403; PMID:22389607; http://dx.doi.org/10.3390/s90100386
  • Persson CM, Chambers BJ. Plasmacytoid dendritic cell-induced migration and activation of NK cells in vivo. Eur J Immunol 2010; 40:2155-64; PMID:20540112; http://dx.doi.org/10.1002/eji.200940098
  • Rajagopal D, Paturel C, Morel Y, Uematsu S, Akira S, Diebold SS. Plasmacytoid dendritic cell-derived type I interferon is crucial for the adjuvant activity of toll-like receptor 7 agonists. Blood 2010; 115:1949-57; PMID:20065291; http://dx.doi.org/10.1182/blood-2009-08-238543
  • Nierkens S, den Brok MH, Garcia Z, Togher S, Wagenaars J, Wassink M, Boon L, Ruers TJ, Figdor CG, Schoenberger SP et al. Immune adjuvant efficacy of CpG oligonucleotide in cancer treatment is founded specifically upon TLR9 function in plasmacytoid dendritic cells. Cancer Res 2011; 71:6428-37; PMID:21788345; http://dx.doi.org/10.1158/0008-5472.CAN-11-2154
  • Lou Y, Liu C, Kim GJ, Liu YJ, Hwu P, Wang G. Plasmacytoid dendritic cells synergize with myeloid dendritic cells in the induction of antigen-specific antitumor immune responses. J Immunol 2007; 178:1534-41; PMID:17237402; http://dx.doi.org/10.4049/jimmunol.178.3.1534
  • Kuwajima S, Sato T, Ishida K, Tada H, Tezuka H, Ohteki T. Interleukin 15-dependent crosstalk between conventional and plasmacytoid dendritic cells is essential for CpG-induced immune activation. Nat Immunol 2006; 7:740-6; PMID:16715101; http://dx.doi.org/10.1038/ni1348
  • Liu C, Lou Y, Lizee G, Qin H, Liu S, Rabinovich B, Kim GJ, Wang YH, Ye Y, Sikora AG et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J Clin Invest 2008; 118:1165-75; PMID:18259609; http://dx.doi.org/10.1172/JCI33583
  • Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, Lee H, Arthur CD, White JM, Kalinke U et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011; 208:1989-2003; PMID:21930769; http://dx.doi.org/10.1084/jem.20101158
  • Thordardottir S, Hangalapura BN, Hutten T, Cossu M, Spanholtz J, Schaap N, Radstake TR, van der Voort R, Dolstra H. The aryl hydrocarbon receptor antagonist StemRegenin 1 promotes human plasmacytoid and myeloid dendritic cell development from CD34+ hematopoietic progenitor cells. Stem Cells Dev 2014; 23:955-67; PMID:24325394; http://dx.doi.org/10.1089/scd.2013.0521
  • Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005; 6:769-76; PMID:15995707; http://dx.doi.org/10.1038/ni1223
  • Gautier G, Humbert M, Deauvieau F, Scuiller M, Hiscott J, Bates EE, Trinchieri G, Caux C, Garrone P. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 2005; 201:1435-46; PMID:15851485; http://dx.doi.org/10.1084/jem.20041964
  • Kerkmann M, Rothenfusser S, Hornung V, Towarowski A, Wagner M, Sarris A, Giese T, Endres S, Hartmann G. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J Immunol 2003; 170:4465-74; PMID:12707322; http://dx.doi.org/10.4049/jimmunol.170.9.4465
  • Gibson SJ, Lindh JM, Riter TR, Gleason RM, Rogers LM, Fuller AE, Oesterich JL, Gorden KB, Qiu X, McKane SW et al. Plasmacytoid dendritic cells produce cytokines and mature in response to the TLR7 agonists, imiquimod and resiquimod. Cell Immunol 2002; 218:74-86; PMID:12470615; http://dx.doi.org/10.1016/S0008-8749(02)00517-8
  • den Haan JM, Meadows LM, Wang W, Pool J, Blokland E, Bishop TL, Reinhardus C, Shabanowitz J, Offringa R, Hunt DF et al. The minor histocompatibility antigen HA-1: A diallelic gene with a single amino acid polymorphism. Science 1998; 279:1054-7; PMID:9461441; http://dx.doi.org/10.1126/science.279.5353.1054
  • Oostvogels R, Minnema MC, van Elk M, Spaapen RM, te Raa GD, Giovannone B, Buijs A, van Baarle D, Kater AP, Griffioen M et al. Towards effective and safe immunotherapy after allogeneic stem cell transplantation: Identification of hematopoietic-specific minor histocompatibility antigen UTA2-1. Leukemia 2013; 27:642-9; PMID:23079962; http://dx.doi.org/10.1038/leu.2012.277
  • Brickner AG, Warren EH, Caldwell JA, Akatsuka Y, Golovina TN, Zarling AL, Shabanowitz J, Eisenlohr LC, Hunt DF, Engelhard VH et al. The immunogenicity of a new human minor histocompatibility antigen results from differential antigen processing. J Exp Med 2001; 193:195-206; PMID:11148223; http://dx.doi.org/10.1084/jem.193.2.195
  • Kijima M, Yamaguchi T, Ishifune C, Maekawa Y, Koyanagi A, Yagita H, Chiba S, Kishihara K, Shimada M, Yasutomo K. Dendritic cell-mediated NK cell activation is controlled by Jagged2-Notch interaction. Proc Natl Acad Sci U S A 2008; 105:7010-5; PMID:18458347; http://dx.doi.org/10.1073/pnas.0709919105
  • Karimi K, Karimi Y, Chan J, Boudreau JE, Basset J, Chew MV, Reid S, Bramson JL, Wan Y, Ashkar AA. Type I IFN signaling on dendritic cells is required for NK cell-mediated anti-tumor immunity. Innate Immun 2015; 21:626-34; PMID:25749844; http://dx.doi.org/10.1177/1753425915575078
  • Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, Perricaudet M, Tursz T, Maraskovsky E, Zitvogel L. Dendritic cells directly trigger NK cell functions: Cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 1999; 5:405-11; PMID:10202929; http://dx.doi.org/10.1038/7403
  • Boudreau JE, Stephenson KB, Wang F, Ashkar AA, Mossman KL, Lenz LL, Rosenthal KL, Bramson JL, Lichty BD, Wan Y. IL-15 and type I interferon are required for activation of tumoricidal NK cells by virus-infected dendritic cells. Cancer Res 2011; 71:2497-506; PMID:21307131; http://dx.doi.org/10.1158/0008-5472.CAN-10-3025
  • Stegmann KA, Bjorkstrom NK, Veber H, Ciesek S, Riese P, Wiegand J, Hadem J, Suneetha PV, Jaroszewicz J, Wang C et al. Interferon-alpha-induced TRAIL on natural killer cells is associated with control of hepatitis C virus infection. Gastroenterology 2010; 138:1885-97; PMID:20334827; http://dx.doi.org/10.1053/j.gastro.2010.01.051
  • Cordeau M, Belounis A, Lelaidier M, Cordeiro P, Sartelet H, Herblot S, Duval M. Efficient killing of high risk neuroblastoma using natural killer cells activated by plasmacytoid dendritic cells. PloS One 2016; 11:e0164401; PMID:27716850; http://dx.doi.org/10.1371/journal.pone.0164401
  • Lelaidier M, Diaz-Rodriguez Y, Cordeau M, Cordeiro P, Haddad E, Herblot S, Duval M. TRAIL-mediated killing of acute lymphoblastic leukemia by plasmacytoid dendritic cell-activated natural killer cells. Oncotarget 2015; 6:29440-55; PMID:26320191; http://dx.doi.org/10.18632/oncotarget.4984
  • Wimmers F, Schreibelt G, Skold AE, Figdor CG, De Vries IJ. Paradigm shift in dendritic cell-based immunotherapy: From in vitro generated monocyte-derived DCs to naturally circulating DC subsets. Front Immunol 2014; 5:165; PMID:24782868; http://dx.doi.org/10.3389/fimmu.2014.00165
  • Esashi E, Wang YH, Perng O, Qin XF, Liu YJ, Watowich SS. The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor IRF8. Immunity 2008; 28:509-20; PMID:18342552; http://dx.doi.org/10.1016/j.immuni.2008.02.013
  • Holloway PA, Kaldenhoven N, van Dijk M, Bloem AC, de Lau W, van der Zee R, Kircher-Eibl B, Mutis T, Lokhorst HM. Susceptibility of malignant plasma cells to HA-1(H) specific lysis suggests a role for the minor histocompatibility antigen HA-1 in the graft-versus-myeloma effect. Leukemia 2004; 18:1543-5; PMID:15322561; http://dx.doi.org/10.1038/sj.leu.2403445
  • van der Waart AB, van de Weem NM, Maas F, Kramer CS, Kester MG, Falkenburg JH, Schaap N, Jansen JH, van der Voort R, Gattinoni L et al. Inhibition of Akt signaling promotes the generation of superior tumor-reactive T cells for adoptive immunotherapy. Blood 2014; 124:3490-500; PMID:25336630; http://dx.doi.org/10.1182/blood-2014-05-578583
  • Norde WJ, Overes IM, Maas F, Fredrix H, Vos JC, Kester MG, van der Voort R, Jedema I, Falkenburg JH, Schattenberg AV et al. Myeloid leukemic progenitor cells can be specifically targeted by minor histocompatibility antigen LRH-1-reactive cytotoxic T cells. Blood 2009; 113:2312-23; PMID:19074734; http://dx.doi.org/10.1182/blood-2008-04-153825
  • Gillespie G, Mutis T, Schrama E, Kamp J, Esendam B, Falkenburg JF, Goulmy E, Moss P. HLA class I-minor histocompatibility antigen tetramers select cytotoxic T cells with high avidity to the natural ligand. Hematol J 2000; 1:403-10; PMID:11920221; http://dx.doi.org/10.1038/sj.thj.6200065
  • Swann JB, Hayakawa Y, Zerafa N, Sheehan KC, Scott B, Schreiber RD, Hertzog P, Smyth MJ. Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J Immunol 2007; 178:7540-9; PMID:17548588; http://dx.doi.org/10.4049/jimmunol.178.12.7540
  • Della Chiesa M, Romagnani C, Thiel A, Moretta L, Moretta A. Multidirectional interactions are bridging human NK cells with plasmacytoid and monocyte-derived dendritic cells during innate immune responses. Blood 2006; 108:3851-8; PMID:16873676; http://dx.doi.org/10.1182/blood-2006-02-004028
  • Pelus LM. Peripheral blood stem cell mobilization: New regimens, new cells, where do we stand. Curr Opin Hematol 2008; 15:285-92; PMID:18536564; http://dx.doi.org/10.1097/MOH.0b013e328302f43a
  • Hobo W, Maas F, Adisty N, de Witte T, Schaap N, van der Voort R, Dolstra H. siRNA silencing of PD-L1 and PD-L2 on dendritic cells augments expansion and function of minor histocompatibility antigen-specific CD8+ T cells. Blood 2010; 116:4501-11; PMID:20682852; http://dx.doi.org/10.1182/blood-2010-04-278739
  • Hobo W, Novobrantseva TI, Fredrix H, Wong J, Milstein S, Epstein-Barash H, Liu J, Schaap N, van der Voort R, Dolstra H. Improving dendritic cell vaccine immunogenicity by silencing PD-1 ligands using siRNA-lipid nanoparticles combined with antigen mRNA electroporation. Cancer Immunol Immunother: CII 2013; 62:285-97; PMID:22903385; http://dx.doi.org/10.1007/s00262-012-1334-1
  • Roeven MW, Hobo W, van der Voort R, Fredrix H, Norde WJ, Teijgeler K, Ruiters MH, Schaap N, Dolstra H. Efficient nontoxic delivery of PD-L1 and PD-L2 siRNA into dendritic cell vaccines using the cationic lipid SAINT-18. J Immunother 2015; 38:145-54; PMID:25839440; http://dx.doi.org/10.1097/CJI.0000000000000071
  • van der Waart AB, Fredrix H, van der Voort R, Schaap N, Hobo W, Dolstra H. siRNA silencing of PD-1 ligands on dendritic cell vaccines boosts the expansion of minor histocompatibility antigen-specific CD8(+) T cells in NOD/SCID/IL2Rg(null) mice. Cancer Immunol Immunother: CII 2015; 64:645-54; PMID:25724840; http://dx.doi.org/10.1007/s00262-015-1668-6
  • Markovic SN, Dietz AB, Greiner CW, Maas ML, Butler GW, Padley DJ, Bulur PA, Allred JB, Creagan ET, Ingle JN et al. Preparing clinical-grade myeloid dendritic cells by electroporation-mediated transfection of in vitro amplified tumor-derived mRNA and safety testing in stage IV malignant melanoma. J Transl Med 2006; 4:35; PMID:16911798; http://dx.doi.org/10.1186/1479-5876-4-35
  • Tavernier G, Andries O, Demeester J, Sanders NN, De Smedt SC, Rejman J. mRNA as gene therapeutic: How to control protein expression. J Control Release 2011; 150:238-47; PMID:20970469; http://dx.doi.org/10.1016/j.jconrel.2010.10.020
  • Met O, Eriksen J, Svane IM. Studies on mRNA electroporation of immature and mature dendritic cells: Effects on their immunogenic potential. Mol Biotechnol 2008; 40:151-60; PMID:18543130; http://dx.doi.org/10.1007/s12033-008-9071-6
  • de Haar C, Plantinga M, Blokland NJ, van Til NP, Flinsenberg TW, Van Tendeloo VF, Smits EL, Boon L, Spel L, Boes M et al. Generation of a cord blood-derived Wilms Tumor 1 dendritic cell vaccine for AML patients treated with allogeneic cord blood transplantation. Oncoimmunology 2015; 4:e1023973; PMID:26451309; http://dx.doi.org/10.1080/2162402X.2015.1023973
  • Millrud CR, Bergenfelz C, Leandersson K. On the origin of myeloid-derived suppressor cells. Oncotarget 2017; 8:3649–65; PMID:27690299; http://dx.doi.org/10.18632/oncotarget.12278
  • Hobo W, Broen K, van der Velden WJ, Greupink-Draaisma A, Adisty N, Wouters Y, Kester M, Fredrix H, Jansen JH, van der Reijden B et al. Association of disparities in known minor histocompatibility antigens with relapse-free survival and graft-versus-host disease after allogeneic stem cell transplantation. Biol Blood Marrow Transplant 2013; 19:274-82; PMID:23022467; http://dx.doi.org/10.1016/j.bbmt.2012.09.008
  • Hobo W, Norde WJ, Schaap N, Fredrix H, Maas F, Schellens K, Falkenburg JH, Korman AJ, Olive D, van der Voort R et al. B and T lymphocyte attenuator mediates inhibition of tumor-reactive CD8+ T cells in patients after allogeneic stem cell transplantation. J Immunol 2012; 189:39-49; PMID:22634623; http://dx.doi.org/10.4049/jimmunol.1102807
  • Hassan C, Chabrol E, Jahn L, Kester MG, de Ru AH, Drijfhout JW, Rossjohn J, Falkenburg JH, Heemskerk MH, Gras S et al. Naturally processed non-canonical HLA-A*02:01 presented peptides. J Biol Chem 2015; 290:2593-603; PMID:25505266; http://dx.doi.org/10.1074/jbc.M114.607028
  • de Rijke B, van Horssen-Zoetbrood A, Beekman JM, Otterud B, Maas F, Woestenenk R, Kester M, Leppert M, Schattenberg AV, de Witte T et al. A frameshift polymorphism in P2×5 elicits an allogeneic cytotoxic T lymphocyte response associated with remission of chronic myeloid leukemia. J Clin Invest 2005; 115:3506-16; PMID:16322791; http://dx.doi.org/10.1172/JCI24832
  • Wills MR, Carmichael AJ, Mynard K, Jin X, Weekes MP, Plachter B, Sissons JG. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: Frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol 1996; 70:7569-79; PMID:8892876; http://jvi.asm.org/content/70/11/7569.long
  • Roeven MW, Thordardottir S, Kohela A, Maas F, Preijers F, Jansen JH, Blijlevens NM, Cany J, Schaap N, Dolstra H. The aryl hydrocarbon receptor antagonist StemRegenin1 improves in vitro generation of highly functional natural killer cells from CD34(+) hematopoietic stem and progenitor cells. Stem Cells Dev 2015; 24:2886-98; PMID:26414401; http://dx.doi.org/10.1089/scd.2014.0597
  • Cany J, van der Waart AB, Spanholtz J, Tordoir M, Jansen JH, van der Voort R, Schaap NM, Dolstra H. Combined IL-15 and IL-12 drives the generation of CD34-derived natural killer cells with superior maturation and alloreactivity potential following adoptive transfer. Oncoimmunology 2015; 4:e1017701; PMID:26140247; http://dx.doi.org/10.1080/2162402X.2015.1017701
  • Spanholtz J, Tordoir M, Eissens D, Preijers F, van der Meer A, Joosten I, Schaap N, de Witte TM, Dolstra H. High log-scale expansion of functional human natural killer cells from umbilical cord blood CD34-positive cells for adoptive cancer immunotherapy. PloS One 2010; 5:e9221; PMID:20169160; http://dx.doi.org/10.1371/journal.pone.0009221