T-cells with a single tumor antigen-specific T-cell receptor can be generated in vitro from clinically relevant stem cell sources

References

• Locke FL, Neelapu SS, Bartlett NL, Siddiqi T, Chavez JC, Hosing CM, Ghobadi A, Budde LE, Bot A, Rossi JM, et al. Phase 1 results of ZUMA-1: a multicenter study of KTE-C19 anti-CD19 CAR T cell therapy in refractory aggressive lymphoma. Mol Ther. 2017;25(1):285–12. doi:10.1016/j.ymthe.2016.10.020.
   PubMed Web of Science ®Google Scholar
• Turtle CJ, Hanafi LA, Berger C, Gooley TA, Cherian S, Hudecek M, Sommermeyer D, Melville K, Pender B, Budiarto TM, et al. CD19 CAR-T cells of defined CD4(+): CD8(+) composition in adult B cell ALL patients. J Clin Invest. 2016;126(6):2123–2138. doi:10.1172/JCI85309.
   PubMed Web of Science ®Google Scholar
• Shlush LI, Mitchell A, Heisler L, Abelson S, Ng SWK, Trotman-Grant A, Medeiros JJF, Rao-Bhatia A, Jaciw-Zurakowsky I, Marke R, et al. Tracing the origins of relapse in acute myeloid leukaemia to stem cells. Nature. 2017;547(7661):104-+. doi:10.1038/nature22993.
   PubMed Web of Science ®Google Scholar
• Casucci M, Di Robilant BN, Falcone L, Camisa B, Norelli M, Genovese P, Gentner B, Gullotta F, Ponzoni M, Bernardi M, et al. CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood. 2013;122(20):3461–3472. doi:10.1182/blood-2013-04-493361.
   PubMed Web of Science ®Google Scholar
• Wang J, Chen S, Xiao W, Li W, Wang L, Yang S, Wang W, Xu L, Liao S, Liu W, et al. CAR-T cells targeting CLL-1 as an approach to treat acute myeloid leukemia. J Hematol Oncol. 2018;11(1):7. doi:10.1186/s13045-017-0553-5.
   PubMedGoogle Scholar
• Chien CD, Sauter CT, Ishii K, Nguyen SM, Shen F, Tasian SK, Chen W, Dimitrov DS, Fry TJ. Preclinical development of FLT3-redirected chimeric antigen receptor T cell immunotherapy for acute myeloid leukemia. Blood. 2016;128(22):1072. doi:10.1182/blood.V128.22.1072.1072.
   Web of Science ®Google Scholar
• Peinert S, Prince HM, Guru PM, Kershaw MH, Smyth MJ, Trapani JA, Gambell P, Harrison S, Scott AM, Smyth FE, et al. Gene-modified T cells as immunotherapy for multiple myeloma and acute myeloid leukemia expressing the Lewis Y antigen. Gene Ther. 2010;17(5):678–686. doi:10.1038/gt.2010.21.
   PubMed Web of Science ®Google Scholar
• Chang YH, Connolly J, Shimasaki N, Mimura K, Kono K, Campana D. A chimeric receptor with NKG2D specificity enhances natural killer cell activation and killing of tumor cells. Cancer Res. 2013;73(6):1777–1786. doi:10.1158/0008-5472.CAN-12-3558.
   PubMed Web of Science ®Google Scholar
• VanSeggelen H, Hammill JA, Dvorkin-Gheva A, Tantalo DG, Kwiecien JM, Denisova GF, Rabinovich B, Wan Y, Bramson JL. T cells engineered with chimeric antigen receptors targeting NKG2D ligands display lethal toxicity in mice. Mol Ther. 2015;23(10):1600–1610. doi:10.1038/mt.2015.119.
   PubMed Web of Science ®Google Scholar
• Kenderian SS, Ruella M, Shestova O, Klichinsky M, Aikawa V, Morrissette JJD, Scholler J, Song D, Porter DL, Carroll M, et al. CD33-specific chimeric antigen receptor T cells exhibit potent preclinical activity against human acute myeloid leukemia. Leukemia. 2015;29(8):1637–1647. doi:10.1038/leu.2015.52.
   PubMed Web of Science ®Google Scholar
• Mardiros A, Dos Santos C, McDonald T, Brown CE, Wang XL, Budde LE, Hoffman L, Aguilar B, Chang W-C, Bretzlaff W, et al. T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia. Blood. 2013;122(18):3138–3148. doi:10.1182/blood-2012-12-474056.
   PubMed Web of Science ®Google Scholar
• Pizzitola I, Anjos-Afonso F, Rouault-Pierre K, Lassailly F, Tettamanti S, Spinelli O, Biondi A, Biagi E, Bonnet D. Chimeric antigen receptors against CD33/CD123 antigens efficiently target primary acute myeloid leukemia cells in vivo. Leukemia. 2014;28(8):1596–1605. doi:10.1038/leu.2014.62.
   PubMed Web of Science ®Google Scholar
• Maude SL, Frey N, Shaw PA, Aplenc R, Barrett DM, Bunin NJ, Chew A, Gonzalez VE, Zheng Z, Lacey SF, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16):1507–1517. doi:10.1056/NEJMoa1407222.
   PubMed Web of Science ®Google Scholar
• Topp MS, Gokbuget N, Zugmaier G, Degenhard E, Goebeler ME, Klinger M, Neumann SA, Horst HA, Raff T, Viardot A, et al. Long-term follow-up of hematologic relapse-free survival in a phase 2 study of blinatumomab in patients with MRD in B-lineage ALL. Blood. 2012;120(26):5185–5187. doi:10.1182/blood-2012-07-441030.
   PubMed Web of Science ®Google Scholar
• Rosenfeld C, Cheever MA, Gaiger A. WT1 in acute leukemia, chronic myelogenous leukemia and myelodysplastic syndrome: therapeutic potential of WT1 targeted therapies. Leukemia. 2003;17(7):1301–1312. doi:10.1038/sj.leu.2402988.
   PubMed Web of Science ®Google Scholar
• Chapuis AG, Egan DN, Bar M, Schmitt TM, McAfee MS, Paulson KG, Voillet V, Gottardo R, Ragnarsson GB, Bleakley M, et al. T cell receptor gene therapy targeting WT1 prevents acute myeloid leukemia relapse post-transplant. Nat Med. 2019;25(7):1064–1072. doi:10.1038/s41591-019-0472-9.
   PubMed Web of Science ®Google Scholar
• Autologous T cells with or without cyclophosphamide and fludarabine in treating patients with recurrent or persistent advanced ovarian epithelial cancer, primary peritoneal cavity cancer, or fallopian tube cancer (fludarabine treatment closed as of 12/01/2009). Accessed on 03/06/2019. https://ClinicalTrials.gov/show/NCT00562640
   Google Scholar
• Genetically modified T cells in treating patients with stage III-IV non-small cell lung cancer or mesothelioma. Accessed on 03/06/2019. https://ClinicalTrials.gov/show/NCT02408016
   Google Scholar
• A phase I/II study of gene-modified WT1 TCR therapy in MDS & AML patients. Accessed on 12/06/2018. Available from: https://ClinicalTrials.gov/show/NCT02550535.
   Google Scholar
• Bendle GM, Linnemann C, Hooijkaas AI, Bies L, de Witte MA, Jorritsma A, Kaiser ADM, Pouw N, Debets R, Kieback E, et al. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med. 2010;16(5):565–U98. doi:10.1038/nm.2128.
   PubMed Web of Science ®Google Scholar
• van Loenen MM, de Boer R, Amir AL, Hagedoorn RS, Volbeda GL, Willemze R, van Rood JJ, Falkenburg JHF, Heemskerk MHM. Mixed T cell receptor dimers harbor potentially harmful neoreactivity. Proc Natl Acad Sci. 2010;107(24):10972–10977. doi:10.1073/pnas.1005802107.
   PubMed Web of Science ®Google Scholar
• Janelle V, Carli C, Taillefer J, Orio J, Delisle JS. Defining novel parameters for the optimal priming and expansion of minor histocompatibility antigen-specific T cells in culture. J Transl Med. 2015;13:13. doi:10.1186/s12967-015-0495-z.
   PubMed Web of Science ®Google Scholar
• Kagoya Y, Nakatsugawa M, Ochi T, Cen YC, Guo TX, Anczurowski M, Saso K, Butler MO, Hirano N. Transient stimulation expands superior antitumor T cells for adoptive therapy. JCI Insight. 2017;2(2):13. doi:10.1172/jci.insight.89580.
   Web of Science ®Google Scholar
• Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu ZY, 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(6):1616–1626. doi:10.1172/JCI24480.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, Almeida JR, Gostick E, Yu Z, Carpenito C, et al. A human memory T cell subset with stem cell-like properties. Nat Med. 2011;17(10):1290–U325. doi:10.1038/nm.2446.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer. 2012;12(10):671–684. doi:10.1038/nrc3322.
   PubMed Web of Science ®Google Scholar
• Minagawa A, Yoshikawa T, Yasukawa M, Hotta A, Kunitomo M, Iriguchi S, Takiguchi M, Kassai Y, Imai E, Yasui Y, et al. Enhancing T Cell Receptor Stability in Rejuvenated iPSC-Derived T Cells Improves Their Use in Cancer Immunotherapy. Cell Stem Cell. 2018;23(6):850-+. doi:10.1016/j.stem.2018.10.005.
   PubMed Web of Science ®Google Scholar
• Snauwaert S, Verstichel G, Bonte S, Goetgeluk G, Vanhee S, Van Caeneghem Y, De Mulder K, Heirman C, Stauss H, Heemskerk MHM, et al. In vitro generation of mature, naive antigen-specific CD8 (+) T cells with a single T-cell receptor by agonist selection. Leukemia. 2014;28(4):830–841. doi:10.1038/leu.2013.285.
   PubMed Web of Science ®Google Scholar
• Van Caeneghem Y, De Munter S, Tieppo P, Goetgeluk G, Weening K, Verstichel G, Bonte S, Taghon T, Leclercq G, Kerre T, et al. Antigen receptor-redirected T cells derived from hematopoietic precursor cells lack expression of the endogenous TCR/CD3 receptor and exhibit specific antitumor capacities. OncoImmunology. 2017;6(3):14. doi:10.1080/2162402X.2017.1283460.
   Web of Science ®Google Scholar
• Van Coppernolle S, Verstichel G, Timmermans F, Velghe I, Vermijlen D, De Smedt M, Leclercq G, Plum J, Taghon T, Vandekerckhove B, et al. Functionally mature CD4 and CD8 TCRαβ cells are generated in OP9-DL1 cultures from human CD34+ hematopoietic cells. J Immunol. 2009;183(8):4859–4870. doi:10.4049/jimmunol.0900714.
   PubMed Web of Science ®Google Scholar
• Scala S, Basso-Ricci L, Dionisio F, Pellin D, Giannelli S, Salerio FA, Leonardelli L, Cicalese MP, Ferrua F, Aiuti A, et al. Dynamics of genetically engineered hematopoietic stem and progenitor cells after autologous transplantation in humans. Nat Med. 2018;24(11):1683-+. doi:10.1038/s41591-018-0195-3.
   PubMed Web of Science ®Google Scholar
• Barber DL, Wherry EJ, Masopust D, Zhu BG, Allison JP, Sharpe AH, Freeman GJ, Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006;439(7077):682–687. doi:10.1038/nature04444.
   PubMed Web of Science ®Google Scholar
• Wirth TC, Xue -H-H, Rai D, Sabel JT, Bair T, Harty JT, Badovinac VP. Repetitive antigen stimulation induces stepwise transcriptome diversification but preserves a core signature of memory CD8+ T cell differentiation. Immunity. 2010;33(1):128–140. doi:10.1016/j.immuni.2010.06.014.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Speiser DE, Lichterfeld M, Bonini C. T memory stem cells in health and disease. Nat Med. 2017;23:18. doi:10.1038/nm.4241.
   PubMed Web of Science ®Google Scholar
• Yang S, Liu F, Wang QJ, Rosenberg SA, Morgan RA, Teague RM. The shedding of CD62L (L-selectin) regulates the acquisition of lytic activity in human tumor reactive T lymphocytes. PLoS One. 2011;6(7):e22560. doi:10.1371/journal.pone.0022560.
   PubMed Web of Science ®Google Scholar
• Kelly-Rogers J, Madrigal-Estebas L, O’Connor T, Doherty DG. Activation-induced expression of CD56 by T cells is associated with a reprogramming of cytolytic activity and cytokine secretion profile in vitro. Hum Immunol. 2006;67(11):863–873. doi:10.1016/j.humimm.2006.08.292.
   PubMed Web of Science ®Google Scholar
• Verneris MR, Karimi M, Baker J, Jayaswal A, Negrin RS. Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells. Blood. 2004;103(8):3065–3072. doi:10.1182/blood-2003-06-2125.
   PubMed Web of Science ®Google Scholar
• Chikuma S, Terawaki S, Hayashi T, Nabeshima R, Yoshida T, Shibayama S, Okazaki T, Honjo T. PD-1-mediated suppression of IL-2 production induces CD8+ T cell anergy in vivo. The Journal of Immunology. 2009;182(11):6682–6689. doi:10.4049/jimmunol.0900080.
   PubMed Web of Science ®Google Scholar
• Bucks CM, Norton JA, Boesteanu AC, Mueller YM, Katsikis PD. Chronic antigen stimulation alone is sufficient to drive CD8(+) T cell exhaustion. J Immunol. 2009;182(11):6697–6708. doi:10.4049/jimmunol.0800997.
   PubMed Web of Science ®Google Scholar
• Lang KS, Recher M, Navarini AA, Harris NL, Lohning M, Junt T, Probst H, Hengartner H, Zinkernagel R. Inverse correlation between IL-7 receptor expression and CD8 T cell exhaustion during persistent antigen stimulation. Eur J Immunol. 2005;35(3):738–745. doi:10.1002/eji.200425828.
   PubMed Web of Science ®Google Scholar
• Offner F, Kerre T, De Smedt M, Plum J. Bone marrow CD34 cells generate fewer T cells in vitro with increasing age and following chemotherapy. Br J Haematol. 1999;104(4):801–808. doi:10.1046/j.1365-2141.1999.01265.x.
   PubMed Web of Science ®Google Scholar
• Huang XJ, Liu DH, Liu KY, Xu LP, Chen H, Han W. Donor lymphocyte infusion for the treatment of leukemia relapse after HLA-mismatched/haploidentical T-cell-replete hematopoietic stem cell transplantation. Haematol-Hematol J. 2007;92(3):414–417. doi:10.3324/haematol.10570.
   PubMed Web of Science ®Google Scholar
• Mackall CL, Fleisher TA, Brown MR, Andrich MP, Chen CC, Feuerstein IM, Magrath IT, Wexler LH, Dimitrov DS, Gress RE, et al. Distinctions between CD8(+) and CD4(+) T-cell regenerative pathways result in prolonged T-cell subset imbalance after intensive chemotherapy. Blood. 1997;89(10):3700–3707. doi:10.1182/blood.V89.10.3700.
   PubMed Web of Science ®Google Scholar
• Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor–modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365(8):725–733. doi:10.1056/NEJMoa1103849.
   PubMed Web of Science ®Google Scholar
• Dombret H, Gardin C. An update of current treatments for adult acute myeloid leukemia. Blood. 2016;127(1):53–61. doi:10.1182/blood-2015-08-604520.
   PubMed Web of Science ®Google Scholar
• Brentjens RJ, Riviere I, Park JH, Davila ML, Wang X, Stefanski J, Taylor C, Yeh R, Bartido S, Borquez-Ojeda O, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118(18):4817–4828. doi:10.1182/blood-2011-04-348540.
   PubMed Web of Science ®Google Scholar
• Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645. doi:10.1038/367645a0.
   PubMed Web of Science ®Google Scholar
• Ishikawa F, Yoshida S, Saito Y, Hijikata A, Kitamura H, Tanaka S, Nakamura R, Tanaka T, Tomiyama H, Saito N, et al. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol. 2007;25:1315. doi:10.1038/nbt1350.
   PubMed Web of Science ®Google Scholar
• Eppert K, Takenaka K, Lechman ER, Waldron L, Nilsson B, van Galen P, Metzeler KH, Poeppl A, Ling V, Beyene J, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med. 2011;17:1086. doi:10.1038/nm.2415.
   PubMed Web of Science ®Google Scholar
• Ruella M, Xu J, Barrett DM, Fraietta JA, Reich TJ, Ambrose DE, Klichinsky M, Shestova O, Patel PR, Kulikovskaya I, et al. Induction of resistance to chimeric antigen receptor T cell therapy by transduction of a single leukemic B cell. Nat Med. 2018;24(10):1499–1503. doi:10.1038/s41591-018-0201-9.
   PubMed Web of Science ®Google Scholar
• Broxmeyer HE, Srour EF, Hangoc G, Cooper S, Anderson SA, Bodine DM. High-efficiency recovery of functional hematopoietic progenitor and stem cells from human cord blood cryopreserved for 15 years. Proc Natl Acad Sci U S A. 2003;100(2):645–650. doi:10.1073/pnas.0237086100.
   PubMed Web of Science ®Google Scholar
• Donnenberg AD, Koch EK, Griffin DL, Stanczak HM, Kiss JE, Carlos TM, BuchBarker DM, Yeager AM. Viability of cryopreserved BM progenitor cells stored for more than a decade. Cytotherapy. 2002;4(2):157–163. doi:10.1080/146532402317381866.
   PubMed Web of Science ®Google Scholar
• Broxmeyer HE, Lee MR, Hangoc G, Cooper S, Prasain N, Kim YJ, Mallett C, Ye Z, Witting S, Cornetta K, et al. Hematopoietic stem/progenitor cells, generation of induced pluripotent stem cells, and isolation of endothelial progenitors from 21- to 23.5-year cryopreserved cord blood. Blood. 2011;117(18):4773–4777. doi:10.1182/blood-2011-01-330514.
   PubMed Web of Science ®Google Scholar
• Stockschlader M, Hassan HT, Krog C, Kruger W, Loliger C, Horstman M, ALTNODER M, CLAUSEN J, GRIMM J, KABISCH H, et al. Long-term follow-up of leukaemia patients after related cryopreserved allogeneic bone marrow transplantation. Br J Haematol. 1997;96(2):382–386. doi:10.1046/j.1365-2141.1997.d01-2032.x.
   PubMed Web of Science ®Google Scholar
• Kim DH, Jamal N, Saragosa R, Loach D, Wright J, Gupta V, Kuruvilla J, Lipton JH, Minden M, Messner HA, et al. Similar outcomes of cryopreserved allogeneic peripheral stem cell transplants (PBSCT) compared to fresh allografts. Biol Blood Marrow Transplant. 2007;13(10):1233–1243. doi:10.1016/j.bbmt.2007.07.003.
   PubMed Web of Science ®Google Scholar
• Gao L, Bellantuono I, Elsasser A, Marley SB, Gordon MY, Goldman JM, Stauss HJ. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood. 2000;95(7):2198–2203. doi:10.1182/blood.V95.7.2198.
   PubMed Web of Science ®Google Scholar
• Li Y, Moysey R, Molloy PE, Vuidepot AL, Mahon T, Baston E, Dunn S, Liddy N, Jacob J, Jakobsen BK, et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat Biotechnol. 2005;23(3):349–354. doi:10.1038/nbt1070.
   PubMed Web of Science ®Google Scholar
• Holler PD, Holman PO, Shusta EV, O’Herrin S, Wittrup KD, Kranz DM. In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc Natl Acad Sci U S A. 2000;97(10):5387–5392. doi:10.1073/pnas.080078297.
   PubMed Web of Science ®Google Scholar
• Harris DT, Hager MV, Smith SN, Cai Q, Stone JD, Kruger P, Lever M, Dushek O, Schmitt TM, Greenberg PD, et al. Comparison of T cell activities mediated by human TCRs and CARs that use the same recognition domains. The Journal of Immunology. 2018;200(3):1088–1100. doi:10.4049/jimmunol.1700236.
   PubMed Web of Science ®Google Scholar
• Stone JD, Harris DT, Soto CM, Chervin AS, Aggen DH, Roy EJ, Kranz DM. A novel T cell receptor single-chain signaling complex mediates antigen-specific T cell activity and tumor control. Cancer Immunol Immunother. 2014;63(11):1163–1176. doi:10.1007/s00262-014-1586-z.
   PubMed Web of Science ®Google Scholar
• Legut M, Dolton G, Mian AA, Ottmann OG, Sewell AK. CRISPR-mediated TCR replacement generates superior anticancer transgenic T cells. Blood. 2018;131(3):311–322. doi:10.1182/blood-2017-05-787598.
   PubMed Web of Science ®Google Scholar