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Research Article

Versatile chimeric antigen receptor platform for controllable and combinatorial T cell therapy

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Article: 1785608 | Received 23 Apr 2020, Accepted 15 Jun 2020, Published online: 03 Jul 2020

References

  • Kuwana Y, Asakura Y, Utsunomiya N, Nakanishi M, Arata Y, Itoh S, Nagase F, Kurosawa Y. Expression of chimeric receptor composed of immunoglobulin-derived V resions and T-cell receptor-derived C regions. Biochem Biophys Res Commun. 1987;149(3):960–15. doi:10.1016/0006-291X(87)90502-X.
  • Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity.  Proc Natl Acad Sci U S A. 1989;86(24):10024–10028. doi:10.1073/pnas.86.24.10024.
  • Bachmann M. The UniCAR system: A modular CAR T cell approach to improve the safety of CAR T cells. Immunol Lett. 2019;211:13–22. doi:10.1016/j.imlet.2019.05.003.
  • June CH, O’Connor RS, Kawalekar OU, Ghassemi S, Milone MC. CAR T cell immunotherapy for human cancer. Science. 2018;359(6382):1361–1365. doi:10.1126/science.aar6711.
  • Cartellieri M, Bachmann M, Feldmann A, Bippes C, Stamova S, Wehner R, Temme A, Schmitz M. Chimeric antigen receptor-engineered T cells for immunotherapy of cancer. J Biomed Biotechnol. 2010;2010:956304. doi: 10.1155/2010/956304.
  • Neelapu SS, Locke FL, Bartlett NL, Lekakis LJ, Miklos DB, Jacobson CA, Braunschweig I, Oluwole OO, Siddiqi T, Lin Y, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. New England J Med. 2017;377(26):2531–2544. doi:10.1056/NEJMoa1707447.
  • Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, Bader P, Verneris MR, Stefanski HE, Myers GD, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. New England J Med. 2018;378(5):439–448. doi:10.1056/NEJMoa1709866.
  • Schuster SJ, Bishop MR, Tam CS, Waller EK, Borchmann P, McGuirk JP, Jäger U, Jaglowski S, Andreadis C, Westin JR, et al. Tisagenlecleucel in adult relapsed or refractory diffuse large B-cell lymphoma. New England J Med. 2019;380(1):45–56. doi:10.1056/NEJMoa1804980.
  • Majzner RG, Mackall CL. Clinical lessons learned from the first leg of the CAR T cell journey. Nat Med. 2019;25(9):1341–1355. doi:10.1038/s41591-019-0564-6.
  • Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Molecular Therapy. 2010;18(4):843–851. doi:10.1038/mt.2010.24.
  • Urbanska K, Lanitis E, Poussin M, Lynn RC, Gavin BP, Kelderman S, Yu J, Scholler N, Powell DJ. A universal strategy for adoptive immunotherapy of cancer through use of a novel T-cell antigen receptor. Cancer Res. 2012;72(7):1844–1852. doi:10.1158/0008-5472.CAN-11-3890.
  • Tamada K, Geng D, Sakoda Y, Bansal N, Srivastava R, Li Z, Davila E. Redirecting gene-modified T cells toward various cancer types using tagged antibodies. Clin Cancer Res. 2012;18(23):6436–6445. doi:10.1158/1078-0432.CCR-12-1449.
  • Ma JS, Kim JY, Kazane SA, Choi S-H, Yun HY, Kim MS, Rodgers DT, Pugh HM, Singer O, Sun SB, et al. Versatile strategy for controlling the specificity and activity of engineered T cells. Proc Natl Acad Sci U S A. 2016;113(4):E450–E458. doi:10.1073/pnas.1524193113.
  • Kudo K, Imai C, Lorenzini P, Kamiya T, Kono K, Davidoff AM, Chng WJ, Campana D. T lymphocytes expressing a CD16 signaling receptor exert antibody-dependent cancer cell killing. Cancer Res. 2014;74(1):93–103. doi:10.1158/0008-5472.CAN-13-1365.
  • Urbanska K, Lynn RC, Stashwick C, Thakur A, Lum LG, Powell DJ. Targeted cancer immunotherapy via combination of designer bispecific antibody and novel gene-engineered T cells. J Transl Med. 2014;12(1):347. doi:10.1186/s12967-014-0347-2.
  • Rodgers DT, Mazagova M, Hampton EN, Cao Y, Ramadoss NS, Hardy IR, Schulman A, Du J, Wang F, Singer O, et al. Switch-mediated activation and retargeting of CAR-T cells for B-cell malignancies. Proc Natl Acad Sci U S A 2016;113(4):E459–E468. doi:10.1073/pnas.1524155113.
  • Koristka S, Cartellieri M, Feldmann A, Arndt C, Loff S, Michalk I, Aliperta R, von Bonin M, Bornhäuser M, Ehninger A, et al. Flexible antigen-specific redirection of human regulatory T cells via a novel universal chimeric antigen receptor system. Blood. 2014;124(21):3494. doi: 10.1182/blood.V124.21.3494.3494
  • Cho JH, Collins JJ, Wong WW. Universal chimeric antigen receptors for multiplexed and logical control of T cell responses. Cell. 2018;173(6):1426–1438. e11. doi:10.1016/j.cell.2018.03.038.
  • Karches CH, Benmebarek M-R, Schmidbauer ML, Kurzay M, Klaus R, Geiger M, Rataj F, Cadilha BL, Lesch S, Heise C, et al. Bispecific antibodies enable synthetic agonistic receptor-transduced T cells for tumor immunotherapy. Clin Cancer Res. 2019;25(19):5890–5900. doi:10.1158/1078-0432.CCR-18-3927.
  • Cartellieri M, Feldmann A, Koristka S, Arndt C, Loff S, Ehninger A, von Bonin M, Bejestani EP, Ehninger G, Bachmann MP, et al. Switching CAR T cells on and off: a novel modular platform for retargeting of T cells to AML blasts. Blood Cancer J. 2016;6(8):e458. doi:10.1038/bcj.2016.61.
  • O’Rourke DM, Nasrallah MP, Desai A, Melenhorst JJ, Mansfield K, Morrissette JJD, Martinez-Lage M, Brem S, Maloney E, Shen A, et al. A single dose of peripherally infused EGFRvIII-directed CAR T cells mediates antigen loss and induces adaptive resistance in patients with recurrent glioblastoma. Sci Transl Med. 2017;9(399):eaaa0984. doi:10.1126/scitranslmed.aaa0984.
  • Ebert LM, Yu W, Gargett T, Brown MP. Logic-gated approaches to extend the utility of chimeric antigen receptor T-cell technology. Biochem Soc Trans. 2018;46(2):391–401. doi:10.1042/BST20170178.
  • Kloss CC, Condomines M, Cartellieri M, Bachmann M, Sadelain M. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechnol. 2013;31(1):71–75. doi: 10.1038/nbt.2459
  • Wilkie S, van Schalkwyk MC, Hobbs S, Davies DM, van der Stegen SJC, Pereira ACP, Burbridge SE, Box C, Eccles SA, Maher J, et al. Dual targeting of ErbB2 and MUC1 in breast cancer using chimeric antigen receptors engineered to provide complementary signaling. J Clin Immunol. 2012;32(5):1059–1070. doi:10.1007/s10875-012-9689-9.
  • Lanitis E, Poussin M, Klattenhoff AW, Song D, Sandaltzopoulos R, June CH, Powell DJ. Chimeric antigen receptor T Cells with dissociated signaling domains exhibit focused antitumor activity with reduced potential for toxicity in vivo. Cancer Immunol Res. 2013;1(1):43–53. doi:10.1158/2326-6066.CIR-13-0008.
  • Koristka S, Ziller-Walter P, Bergmann R, Arndt C, Feldmann A, Kegler A, Cartellieri M, Ehninger A, Ehninger G, Bornhäuser M, et al. Anti-CAR-engineered T cells for epitope-based elimination of autologous CAR T cells. Cancer Immunol Immunother. 2019;68(9):1401–1415. doi:10.1007/s00262-019-02376-y.
  • Albert S, Arndt C, Feldmann A, Bergmann R, Bachmann D, Koristka S, Ludwig F, Ziller-Walter P, Kegler A, Gärtner S, et al. A novel nanobody-based target module for retargeting of T lymphocytes to EGFR-expressing cancer cells via the modular UniCAR platform. Oncoimmunology. 2017;6(4):e1287246. doi:10.1080/2162402X.2017.1287246.
  • Feldmann A, Arndt C, Bergmann R, Loff S, Cartellieri M, Bachmann D, Aliperta R, Hetzenecker M, Ludwig F, Albert S, et al. Retargeting of T lymphocytes to PSCA- or PSMA positive prostate cancer cells using the novel modular chimeric antigen receptor platform technology “UniCAR”. Oncotarget. 2017;8(19):31368. doi:10.18632/oncotarget.15572.
  • Loureiro L, Feldmann A, Bergmann R, Koristka S, Berndt N, Arndt C, Pietzsch J, Novo C, Videira P, Bachmann M, et al. Development of a novel target module redirecting UniCAR T cells to Sialyl Tn-expressing tumor cells. Blood Cancer J. 2018;8(9):81. doi:10.1038/s41408-018-0113-4.
  • Mitwasi N, Feldmann A, Bergmann R, Berndt N, Arndt C, Koristka S, Kegler A, Jureczek J, Hoffmann A, Ehninger A, et al. Development of novel target modules for retargeting of UniCAR T cells to GD2 positive tumor cells. Oncotarget. 2017;8(65):108584. doi:10.18632/oncotarget.21017.
  • Arndt C, Feldmann A, Koristka S, Schäfer M, Bergmann R, Mitwasi N, Berndt N, Bachmann D, Kegler A, Schmitz M, et al. A theranostic PSMA ligand for PET imaging and retargeting of T cells expressing the universal chimeric antigen receptor UniCAR. OncoImmunology. 2019;8(11):1659095. doi:10.1080/2162402X.2019.1659095.
  • Albert S, Arndt C, Koristka S, Berndt N, Bergmann R, Feldmann A, Schmitz M, Pietzsch J, Steinbach J, Bachmann M et al. From mono- to bivalent: improving theranostic properties of target modules for redirection of UniCAR T cells against EGFR-expressing tumor cells in vitro and in vivo. Oncotarget. 2018 May 22;9(39):25597–25616. doi:10.18632/oncotarget.25390.
  • Fasslrinner F, Arndt C, Koristka S, Feldmann A, Altmann H, von Bonin M, Schmitz M, Bornhäuser M, Bachmann M. Midostaurin abrogates CD33-directed UniCAR and CD33-CD3 bispecific antibody therapy in acute myeloid leukaemia. Br J Haematol. 2019 Sep;186(5):735–740. doi:10.1111/bjh.15975.
  • Mitwasi N, Feldmann A, Arndt C, Koristka S, Berndt N, Jureczek J, Loureiro LR, Bergmann R, Máthé D, Hegedüs N, et al. “UniCAR”-modified off-the-shelf NK-92 cells for targeting of GD2-expressing tumour cells. Sci Rep. 2020 Feb 7;10(1):2141. doi:10.1038/s41598-020-59082-4.
  • Bachmann D, Aliperta R, Bergmann R, Feldmann A, Koristka S, Arndt C, Loff S, Welzel P, Albert S, Kegler A et al. Retargeting of UniCAR T cells with an in vivo synthesized target module directed against CD19 positive tumor cells. Oncotarget. 2018 Jan 26;9(7):7487–7500. doi:10.18632/oncotarget.23556.
  • Cartellieri M, Koristka S, Arndt C, Feldmann A, Stamova S, von Bonin M, Töpfer K, Krüger T, Geib M, Michalk I, et al. A novel ex vivo isolation and expansion procedure for chimeric antigen receptor engrafted human T cells. PLoS One. 2014;9(4):e93745. doi:10.1371/journal.pone.0093745.
  • Feldmann A, Arndt C, Topfer K  Stamova S, Krone F, Cartellieri M, Koristka S, Michalk I, Lindemann D, Schmitz M, et al. Novel humanized and highly efficient bispecific antibodies mediate killing of prostate stem cell antigen-expressing tumor cells by CD8+ and CD4+ T cells. J Immunol. 2012 Sep 15;189(6):3249–3259. doi:10.4049/jimmunol.1200341.
  • Arndt C, Feldmann A, Koristka S, Cartellieri M, Dimmel M, Ehninger A, Ehninger G, Bachmann M. Simultaneous targeting of prostate stem cell antigen and prostate-specific membrane antigen improves the killing of prostate cancer cells using a novel modular T cell-retargeting system. Prostate. 2014 Sep;74(13):1335–1346. doi:10.1002/pros.22850.
  • Feldmann A, Stamova S, Bippes CC, Bartsch H, Wehner R, Schmitz M, Temme A, Cartellieri M, Bachmann M. Retargeting of T cells to prostate stem cell antigen expressing tumor cells: comparison of different antibody formats. Prostate. 2011 Jun 15;71(9):998–1011. doi:10.1002/pros.21315.
  • Kegler A, Koristka S, Bergmann R, Berndt N, Arndt C, Feldmann A, Hoffmann A, Bornhäuser M, Schmitz M, Bachmann MP, et al. T cells engrafted with a UniCAR 28/z outperform UniCAR BB/z-transduced T cells in the face of regulatory T cell-mediated immunosuppression. Oncoimmunology. 2019;8(9):e1621676. doi:10.1080/2162402X.2019.1621676.
  • Albert S, Koristka S, Gerbaulet A, Cartellieri M, Arndt C, Feldmann A, Berndt N, Loureiro LR, von Bonin M, Ehninger G, et al. Tonic signaling and its effects on lymphopoiesis of CAR-armed hematopoietic stem and progenitor cells. J Immunol. 2019;202(6):1735–1746. doi:10.4049/jimmunol.1801004.
  • Heninger A-K, Eugster A, Kuehn D, Buettner F, Kuhn M, Lindner A, Dietz S, Jergens S, Wilhelm C, Beyerlein A et al. A divergent population of autoantigen-responsive CD4 + T cells in infants prior to β cell autoimmunity. Sci Transl Med. 2017 Feb 22;9(378):378. doi:10.1126/scitranslmed.aaf8848.
  • Koristka S, Kegler A, Bergmann R, Arndt C, Feldmann A, Albert S, Cartellieri M, Ehninger A, Ehninger G, Middeke JM, et al. Engrafting human regulatory T cells with a flexible modular chimeric antigen receptor technology. J Autoimmun. 2018;90:116–131. doi:10.1016/j.jaut.2018.02.006.
  • Aliperta R, Welzel PB, Bergmann R, Freudenberg U, Berndt N, Feldmann A, Arndt C, Koristka S, Stanzione M, Cartellieri M, et al. Cryogel-supported stem cell factory for customized sustained release of bispecific antibodies for cancer immunotherapy. Sci Rep. 2017 Feb;7(1):42855. doi:10.1038/srep42855.
  • Geyer MB. First CAR to pass the road test: tisagenlecleucel’s drive to FDA approval. Clin Cancer Res. 2019;25(4):1133–1135. doi:10.1158/1078-0432.CCR-18-3328.
  • Bouchkouj N, Kasamon YL, de Claro RA, George B, Lin X, Lee S, Blumenthal GM, Bryan W, McKee AE, Pazdur R et al. FDA approval summary: axicabtagene ciloleucel for relapsed or refractory large B-cell Lymphoma. Clin Cancer Res. 2019 Mar 15;25(6):1702–1708. doi:10.1158/1078-0432.CCR-18-2743.
  • Zhu M, Wu B, Brandl C, Johnson J, Wolf A, Chow A, Doshi S. Blinatumomab, a bispecific T-cell engager (BiTE®) for CD-19 targeted cancer immunotherapy: clinical pharmacology and its implications. Clin Pharmacokinet. 2016;55(10):1271–1288. doi:10.1007/s40262-016-0405-4.
  • Slaney CY, Wang P, Darcy PK, Kershaw MH. CARs versus BiTEs: a comparison between T cell–redirection strategies for cancer treatment. Cancer Discov. 2018;8(8):924–934. doi:10.1158/2159-8290.CD-18-0297.
  • Jureczek J, Bergmann R, Berndt N, Koristka S, Kegler A, Puentes-Cala E, Soto JA, Arndt C, Bachmann M, Feldmann A, et al. An oligo-His-tag of a targeting module does not influence its biodistribution and the retargeting capabilities of UniCAR T cells. Sci Rep. 2019;9(1):1–15. doi:10.1038/s41598-019-47044-4.
  • Benmebarek M-R, Karches CH, Cadilha BL, Lesch S, Endres S, Kobold S. Killing mechanisms of chimeric antigen receptor (CAR) T cells. Int J Mol Sci. 2019 March 14;20(6):6. doi:10.3390/ijms20061283.
  • Feldmann A, Arndt C, Koristka S, Berndt N, Bergmann R, Bachmann MP. Conventional CARs versus modular CARs. Cancer Immunol Immunother. 2019;68(10):1713–1719. doi:10.1007/s00262-019-02399-5.
  • Arndt C, Bachmann M, Bergmann R Berndt N, Feldmann A, Koristka S. Theranostic CAR T cell targeting: A brief review. J Labelled Comp Radiopharm. 2019 Jun 30;62(8):533–540. doi:10.1002/jlcr.3727.