Generation of GM-CSF-producing antigen-presenting cells that induce a cytotoxic T cell-mediated antitumor response

References

• Palucka K, Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity. 2013;39:38–16. doi:10.1016/j.immuni.2013.07.004.
   PubMed Web of Science ®Google Scholar
• Anguille S, Smits EL, Lion E, van Tendeloo VF, Berneman ZN. Clinical use of dendritic cells for cancer therapy. Lancet Oncol. 2014;15:e257–e267. doi:10.1016/s1470-2045(13)70585-0.
   PubMed Web of Science ®Google Scholar
• Sprooten J, Ceusters J, Coosemans A, Agostinis P, De Vleeschouwer S, Zitvogel L, Kroemer G, Galluzzi L, Garg AD. Trial watch: dendritic cell vaccination for cancer immunotherapy. Oncoimmunology. 2019;8:e1638212. doi:10.1080/2162402X.2019.1638212.
   PubMed Web of Science ®Google Scholar
• Garg AD, Vara Perez M, Schaaf M, Agostinis P, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: dendritic cell-based anticancer immunotherapy. Oncoimmunology. 2017;6:e1328341. doi:10.1080/2162402X.2017.1328341.
   PubMed Web of Science ®Google Scholar
• Bloy N, Pol J, Aranda F, Eggermont A, Cremer I, Fridman WH, Fucikova J, Galon J, Tartour E, Spisek R, et al. Trial watch: dendritic cell-based anticancer therapy. Oncoimmunology. 2014;3:e963424. doi:10.4161/21624011.2014.963424.
   PubMed Web of Science ®Google Scholar
• Banchereau J, Palucka AK. Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol. 2005;5:296–306. doi:10.1038/nri1592.
   PubMed Web of Science ®Google Scholar
• Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer. 2012;12:265–277. doi:10.1038/nrc3258.
   PubMed Web of Science ®Google Scholar
• Bol KF, Schreibelt G, Gerritsen WR, de Vries IJ, Figdor CG. Dendritic cell-based immunotherapy: state of the art and beyond. Clin Cancer Res. 2016;22:1897–1906. doi:10.1158/1078-0432.CCR-15-1399.
   PubMed Web of Science ®Google Scholar
• Failli A, Legitimo A, Orsini G, Romanini A, Consolini R. Numerical defect of circulating dendritic cell subsets and defective dendritic cell generation from monocytes of patients with advanced melanoma. Cancer Lett. 2013;337:184–192. doi:10.1016/j.canlet.2013.05.013.
   PubMed Web of Science ®Google Scholar
• Orsini G, Legitimo A, Failli A, Ferrari P, Nicolini A, Spisni R, Miccoli P, Consolini R. Defective generation and maturation of dendritic cells from monocytes in colorectal cancer patients during the course of disease. Int J Mol Sci. 2013;14:22022–22041. doi:10.3390/ijms141122022.
   PubMed Web of Science ®Google Scholar
• Verronese E, Delgado A, Valladeau-Guilemond J, Garin G, Guillemaut S, Tredan O, Ray-Coquard I, Bachelot T, N’Kodia A, Bardin-Dit-Courageot C, et al. Immune cell dysfunctions in breast cancer patients detected through whole blood multi-parametric flow cytometry assay. Oncoimmunology. 2016;5:e1100791. doi:10.1080/2162402X.2015.1100791.
   PubMed Web of Science ®Google Scholar
• Guo Y, Lei K, Tang L. Neoantigen vaccine delivery for personalized anticancer immunotherapy. Front Immunol. 2018;9. doi:10.3389/fimmu.2018.01499.
   Web of Science ®Google Scholar
• Jiang Z, Han Y, Cao X. Induced pluripotent stem cell (iPSCs) and their application in immunotherapy. Cell Mol Immunol. 2014;11:17–24. doi:10.1038/cmi.2013.62.
   PubMed Web of Science ®Google Scholar
• Sachamitr P, Hackett S, Fairchild PJ. Induced pluripotent stem cells: challenges and opportunities for cancer immunotherapy. Front Immunol. 2014;5:176. doi:10.3389/fimmu.2014.00176.
   PubMed Web of Science ®Google Scholar
• Zhang R, Liu T-Y, Senju S, Haruta M, Hirosawa N, Suzuki M, Tatsumi M, Ueda N, Maki H, Nakatsuka R, et al. Generation of mouse pluripotent stem cell-derived proliferating myeloid cells as an unlimited source of functional antigen-presenting cells. Cancer Immunol Res. 2015;3:668–677. doi:10.1158/2326-6066.CIR-14-0117.
   PubMed Web of Science ®Google Scholar
• Hamilton JA, Achuthan A. Colony stimulating factors and myeloid cell biology in health and disease. Trends Immunol. 2013;34:81–89. doi:10.1016/j.it.2012.08.006.
   PubMed Web of Science ®Google Scholar
• Min L, Mohammad Isa SAB, Shuai W, Piang CB, Nih FW, Kotaka M, Ruedl C. Cutting edge: granulocyte-macrophage colony-stimulating factor is the major CD8+ T cell-derived licensing factor for dendritic cell activation. J Immunol. 2010;184:4625–4629. doi:10.4049/jimmunol.0903873.
   PubMed Web of Science ®Google Scholar
• Kaufman HL, Ruby CE, Hughes T, Slingluff CL Jr. Current status of granulocyte-macrophage colony-stimulating factor in the immunotherapy of melanoma. J Immunother Cancer. 2014;2:11. doi:10.1186/2051-1426-2-11.
   PubMedGoogle Scholar
• Borrello I, Pardoll D. GM-CSF-based cellular vaccines: a review of the clinical experience. Cytokine Growth Factor Rev. 2002;13:185–193. doi:10.1016/S1359-6101(01)00034-X.
   PubMed Web of Science ®Google Scholar
• Shi Y, Liu CH, Roberts AI, Das J, Xu G, Ren G, Zhang Y, Zhang L, Yuan ZR, Tan HSW, et al. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don’t know. Cell Res. 2006;16:126–133. doi:10.1038/sj.cr.7310017.
   PubMed Web of Science ®Google Scholar
• Bezu L, Kepp O, Cerrato G, Pol J, Fucikova J, Spisek R, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: peptide-based vaccines in anticancer therapy. Oncoimmunology. 2018;7:e1511506. doi:10.1080/2162402X.2018.1511506.
   PubMed Web of Science ®Google Scholar
• Joffre OP, Segura E, Savina A, Amigorena S. Cross-presentation by dendritic cells. Nat Rev Immunol. 2012;12:557–569. doi:10.1038/nri3254.
   PubMed Web of Science ®Google Scholar
• Watanabe N, Hanabuchi S, Soumelis V, Yuan W, Ho S, de Waal Malefyt R, Liu Y-J. Human thymic stromal lymphopoietin promotes dendritic cell-mediated CD4+ T cell homeostatic expansion. Nat Immunol. 2004;5:426–434. doi:10.1038/ni1048.
   PubMed Web of Science ®Google Scholar
• Ge Q, Palliser D, Eisen HN, Chen J. Homeostatic T cell proliferation in a T cell-dendritic cell coculture system. Proc Natl Acad Sci U S A. 2002;99:2983–2988. doi:10.1073/pnas.052714199.
   PubMed Web of Science ®Google Scholar
• Gutierrez-Aranda I, Ramos-Mejia V, Bueno C, Munoz-Lopez M, Real PJ, Mácia A, Sanchez L, Ligero G, Garcia-Parez JL, Menendez P, et al. Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells. 2010;28:1568–1570. doi:10.1002/stem.471.
   PubMed Web of Science ®Google Scholar
• Miura K, Okada Y, Aoi T, Okada A, Takahashi K, Okita K, Nakagawa M, Koyanagi M, Tanabe K, Ohnuki M, et al. Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol. 2009;27:743–745. doi:10.1038/nbt.1554.
   PubMed Web of Science ®Google Scholar
• Chen M, Wang YH, Wang Y, Huang L, Sandoval H, Liu YJ, Wang J. Dendritic cell apoptosis in the maintenance of immune tolerance. Science. 2006;311:1160–1164. doi:10.1126/science.1122545.
   PubMed Web of Science ®Google Scholar
• Johansson-Percival A, He B, Li Z-J, Kjellén A, Russell K, Li J, Larma I, Ganss R. De novo induction of intratumoral lymphoid structures and vessel normalization enhances immunotherapy in resistant tumors. Nat Immunol. 2017;18:1207–1217. doi:10.1038/ni.3836.
   PubMed Web of Science ®Google Scholar
• Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56–61. doi:10.1126/science.aaa8172.
   PubMed Web of Science ®Google Scholar
• Yang P, Song H, Qin Y, Huang P, Zhang C, Kong D, Wang W. Engineering dendritic-cell-based vaccines and PD-1 blockade in self-assembled peptide nanofibrous hydrogel to amplify antitumor T-cell immunity. Nano Lett. 2018;18:4377–4385. doi:10.1021/acs.nanolett.8b01406.
   PubMed Web of Science ®Google Scholar
• Wilgenhof S, Corthals J, Heirman C, van Baren N, Lucas S, Kvistborg P, Thielemans K, Neyns B. Phase II study of autologous monocyte-derived mRNA electroporated dendritic cells (TriMixDC-MEL) plus ipilimumab in patients with pretreated advanced melanoma. J Clin Oncol. 2016;34:1330–1338. doi:10.1200/JCO.2015.63.4121.
   PubMed Web of Science ®Google Scholar
• Chen S, Lee L-F, Fisher TS, Jessen B, Elliott M, Evering W, Logronio K, Tu GH, Tsaparikos K, Li X, et al. Combination of 4-1BB agonist and PD-1 antagonist promotes antitumor effector/memory CD8 T cells in a poorly immunogenic tumor model. Cancer Immunol Res. 2015;3:149–160. doi:10.1158/2326-6066.CIR-14-0118.
   PubMed Web of Science ®Google Scholar
• Juneja VR, McGuire KA, Manguso RT, LaFleur MW, Collins N, Haining WN, Freeman GJ, Sharpe AH. PD-L1 on tumor cells is sufficient for immune evasion in immunogenic tumors and inhibits CD8 T cell cytotoxicity. J Exp Med. 2017;214:895–904. doi:10.1084/jem.20160801.
   PubMed Web of Science ®Google Scholar
• Zhu G, Mei L, Vishwasrao HD, Jacobson O, Wang Z, Liu Y, Yung BC, Fu X, Jin A, Niu G, et al. Intertwining DNA-RNA nanocapsules loaded with tumor neoantigens as synergistic nanovaccines for cancer immunotherapy. Nat Commun. 2017;8:1482. doi:10.1038/s41467-017-01386-7.
   PubMed Web of Science ®Google Scholar
• Li L, Goedegebuure SP, Gillanders WE. Preclinical and clinical development of neoantigen vaccines. Ann Oncol. 2017;28:xii11–xii17. doi:10.1093/annonc/mdx681.
   PubMed Web of Science ®Google Scholar
• Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348:69–74. doi:10.1126/science.aaa4971.
   PubMed Web of Science ®Google Scholar
• Gautam S, Fioravanti J, Zhu W, Le Gall JB, Brohawn P, Lacey NE, Hu J, Hocker JD, Hawk NV, Kapoor V, et al. The transcription factor c-Myb regulates CD8+ T cell stemness and antitumor immunity. Nat Immunol. 2019;20:337–349. doi:10.1038/s41590-018-0311-z.
   PubMed Web of Science ®Google Scholar
• Siddiqui I, Schaeuble K, Chennupati V, Fuertes Marraco SA, Calderon-Copete S, Pais Ferreira D, Carmona SJ, Scarpellino L, Gfeller D, Pradervand S, et al. Intratumoral Tcf1(+)PD-1(+)CD8(+) T cells with stem-like properties promote tumor control in response to vaccination and checkpoint blockade immunotherapy. Immunity. 2019;50:195–211 e110. doi:10.1016/j.immuni.2018.12.021.
   PubMed Web of Science ®Google Scholar
• Sachamitr P, Leishman AJ, Davies TJ, Fairchild PJ. Directed differentiation of human induced pluripotent stem cells into dendritic cells displaying tolerogenic properties and resembling the CD141(+) subset. Front Immunol. 2017;8:1935. doi:10.3389/fimmu.2017.01935.
   PubMed Web of Science ®Google Scholar
• Choi KD, Vodyanik M, Slukvin II. Hematopoietic differentiation and production of mature myeloid cells from human pluripotent stem cells. Nat Protoc. 2011;6:296–313. doi:10.1038/nprot.2010.184.
   PubMed Web of Science ®Google Scholar
• Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004;427:154–159. doi:10.1038/nature02238.
   PubMed Web of Science ®Google Scholar
• Veglia F, Tyurin VA, Blasi M, De Leo A, Kossenkov AV, Donthireddy L, To TKJ, Schug Z, Basu S, Wang F, et al. Fatty acid transport protein 2 reprograms neutrophils in cancer. Nature. 2019;569:73–78. doi:10.1038/s41586-019-1118-2.
   PubMed Web of Science ®Google Scholar
• Parmiani G, Castelli C, Pilla L, Santinami M, Colombo MP, Rivoltini L. Opposite immune functions of GM-CSF administered as vaccine adjuvant in cancer patients. Ann Oncol. 2007;18:226–232. doi:10.1093/annonc/mdl158.
   PubMed Web of Science ®Google Scholar
• Serafini P, Carbley R, Noonan KA, Tan G, Bronte V, Borrello I. High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells. Cancer Res. 2004;64:6337–6343. doi:10.1158/0008-5472.CAN-04-0757.
   PubMed Web of Science ®Google Scholar
• Tsuchiya N, Zhang R, Iwama T, Ueda N, Liu T, Tatsumi M, Sasaki Y, Shimoda R, Osako Y, Sawada Y, et al. Type I interferon delivery by iPSC-derived myeloid cells elicits antitumor immunity via XCR1+ dendritic cells. Cell Rep. 2019;29:162–175.e169. doi:10.1016/j.celrep.2019.08.086.
   PubMed Web of Science ®Google Scholar
• Heckler M, Dougan SK. Unmasking pancreatic cancer: epitope spreading after single antigen chimeric antigen receptor T-cell therapy in a human Phase I trial. Gastroenterology. 2018;155:11–14. doi:10.1053/j.gastro.2018.06.023.
   PubMed Web of Science ®Google Scholar
• O’Donnell JS, Teng MWL, Smyth MJ. Cancer immunoediting and resistance to T cell-based immunotherapy. Nat Rev Clin Oncol. 2019;16:151–167. doi:10.1038/s41571-018-0142-8.
   PubMed Web of Science ®Google Scholar
• Kooreman NG, Kim Y, de Almeida PE, Termglinchan V, Diecke S, Shao N-Y, Wei -T-T, Yi H, Dey D, Nelakanti R, et al. Autologous iPSC-based vaccines elicit anti-tumor responses in vivo. Cell Stem Cell. 2018;22:501–513 e507. doi:10.1016/j.stem.2018.01.016.
   PubMed Web of Science ®Google Scholar
• McCormick F. Cancer gene therapy: fringe or cutting edge? Nat Rev Cancer. 2001;1:130–141. doi:10.1038/35101008.
   PubMed Web of Science ®Google Scholar
• Di Stasi A, Tey S-K, Dotti G, Fujita Y, Kennedy-Nasser A, Martinez C, Straathof K, Liu E, Durett AG, Grilley B, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med. 2011;365:1673–1683. doi:10.1056/NEJMoa1106152.
   PubMed Web of Science ®Google Scholar
• Umekage M, Sato Y, Takasu N. Overview: an iPS cell stock at CiRA. Inflamm Regen. 2019;39:17. doi:10.1186/s41232-019-0106-0.
   PubMed Web of Science ®Google Scholar
• Xu H, Wang B, Ono M, Kagita A, Fujii K, Sasakawa N, Ueda T, Gee P, Nishikawa M, Nomura M, et al. Targeted disruption of HLA genes via CRISPR-cas9 generates iPSCs with enhanced immune compatibility. Cell Stem Cell. 2019;24:566–578 e567. doi:10.1016/j.stem.2019.02.005.
   PubMed Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi:10.1186/s13059-014-0550-8.
   PubMed Web of Science ®Google Scholar
• da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44–57. doi:10.1038/nprot.2008.211.
   PubMed Web of Science ®Google Scholar