Have a personal or library account? Click to login
CAR-T Cells – Main Steps for Obtaining a Proper “Live Drug” Adoptive Therapy Cover

CAR-T Cells – Main Steps for Obtaining a Proper “Live Drug” Adoptive Therapy

Open Access
|Mar 2024

References

  1. Majzner RG, Mackall CL. Clinical lessons learned from the first leg of the CAR T cell journey. Nat Med. 2019;25(9):1341-55. https://doi.org/10.1038/s41591-019-0564-6 PMid:31501612
  2. Cappell KM, Kochenderfer JN. A comparison of chimeric antigen receptors containing CD28 versus 4-1BB costimulatory domains. Nat Rev Clin Oncol. 2021;18(11):715-27. https://doi.org/10.1038/s41571-021-00530-z PMid:34230645
  3. Brudno JN, Kochenderfer JN. Chimeric antigen receptor T-cell therapies for lymphoma. Nat Rev Clin Oncol. 2018;15(1):31-46. https://doi.org/10.1038/nrclinonc.2017.128 PMid:28857075
  4. 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):10024-8. https://doi.org/10.1073/pnas.86.24.10024 PMid:2513569
  5. Maher J, Brentjens RJ, Gunset G, Rivière I, Sadelain M. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta/CD28 receptor. Nat Biotechnol. 2002;20(1):70-5. https://doi.org/10.1038/nbt0102-70 PMid:11753365
  6. Albinger N, Hartmann J, Ullrich E. Current status and perspective of CAR-T and CAR-NK cell therapy trials in Germany. Gene Ther. 2021;28(9):513-27. https://doi.org/10.1038/s41434-021-00246-w PMid:33753909
  7. Deming D, Wang K, Wei C, Feng D, Liu Y, He Q, et al. The BCMA-targeted fourth-generation CAR-T cells secreting IL-7 and CCL19 for therapy of refractory/recurrent multiple myeloma. Front Immunol. 2021;12:609421. https://doi.org/10.3389/fimmu.2021.609421 PMid:33767695
  8. Tian Y, Li Y, Shao Y, Zhang Y. Gene modification strategies for next-generation CAR T cells against solid cancers. J Hematol Oncol. 2020;13(1):54. https://doi.org/10.1186/s13045-020-00890-6 PMid:32423475
  9. Mikkilineni L, Kochenderfer JN. CAR T cell therapies for patients with multiple myeloma. Nat Rev Clin Oncol. 2021;18(2):71-84. https://doi.org/10.1038/s41571-020-0427-6 PMid:32978608
  10. Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, et al. Tisagenlecleucel in children and young adults with b-cell lymphoblastic leukemia. N Engl J Med. 2018;378(5):439-48. https://doi.org/10.1056/NEJMoa1709866 PMid:29385370
  11. Locke FL, Ghobadi A, Jacobson CA, Miklos DB, Lekakis LJ, Oluwole OO, et al. Long-term safety and activity of axicabtagene ciloleucel in refractory large B-cell lymphoma (ZUMA-1): A single-arm, multicentre, phase 1-2 trial. Lancet Oncol. 2019;20(1):31-42. https://doi.org/10.1016/S1470-2045(18)30864-7 PMid:30518502
  12. Abramson JS, Palomba ML, Gordon LI, Lunning MA, Wang M, Arnason J, et al. Lisocabtagene maraleucel for patients with relapsed or refractory large B-cell lymphomas (TRANSCEND NHL 001): A multicentre seamless design study. Lancet. 2020;396(10254):839-52. https://doi.org/10.1016/S0140-6736(20)31366-0 PMid:32888407
  13. Wang M, Munoz J, Goy A, Locke FL, Jacobson CA, Hill BT, et al. KTE-X19 CAR T-cell therapy in relapsed or refractory mantle-cell lymphoma. N Engl J Med. 2020;382(14):1331-42. https://doi.org/10.1056/NEJMoa1914347 PMid:32242358
  14. Feigal EG, Cosenza ME. Cellular-based therapies. In: Translational Medicine. United States: CRC Press; 2021. p. 359-80.
  15. Munshi NC, Anderson LD Jr., Shah N, Madduri D, Berdeja J, Lonial S, et al. Idecabtagene vicleucel in relapsed and refractory multiple myeloma. N Engl J Med. 2021;384(8):705-16. https://doi.org/10.1056/NEJMoa2024850 PMid:33626253
  16. Martin T, Usmani SZ, Berdeja JG, Agha M, Cohen AD, Hari P, et al. Ciltacabtagene autoleucel, an anti-B-cell maturation antigen chimeric antigen receptor T-Cell therapy, for relapsed/refractory multiple myeloma: CARTITUDE-1 2-Year follow-up. J Clin Oncol. 2023;41(6):1265-74. https://doi.org/10.1200/JCO.22.00842 PMid:35658469
  17. Fowler NH, Dickinson M, Dreyling M, Martinez-Lopez J, Kolstad A, Butler J, et al. Tisagenlecleucel in adult relapsed or refractory follicular lymphoma: The phase 2 ELARA trial. Nat Med. 2022;28(2):325-32. https://doi.org/10.1038/s41591-021-01622-0 PMid:34921238
  18. Cappell KM, Kochenderfer JN. Long-term outcomes following CAR T cell therapy: What we know so far. Nat Rev Clin Oncol. 2023;20:359-71. https://doi.org/10.1038/s41571-023-00754-1 PMid:37055515
  19. Jacobson CA, Chavez JC, Sehgal AR, William BM, Munoz J, Salles G, et al. Axicabtagene ciloleucel in relapsed or refractory indolent non-Hodgkin lymphoma (ZUMA-5): A single-arm, multicentre, phase 2 trial. Lancet Oncol. 2022;23(1):91-103. https://doi.org/10.1016/S1470-2045(21)00591-X PMid:34895487
  20. Crump M, Neelapu SS, Farooq U, Van Den Neste E, Kuruvilla J, Westin J, et al. Outcomes in refractory difuse large B-cell lymphoma: Results from the international SCHOLAR-1 study. Blood. 2017;130(16):1800-8. https://doi.org/10.1182/blood-2017-03-769620 PMid:28774879
  21. Shah BD, Ghobadi A, Oluwole OO, Logan AC, Boissel N, Cassaday RD, et al. KTE-X19 for relapsed or refractory adult B-cell acute lymphoblastic leukaemia: Phase 2 results of the single-arm, open-label, multicentre ZUMA-3 study. Lancet. 2021;398(10299):491-502. https://doi.org/10.1016/S0140-6736(21)01222-8 PMid:34097852
  22. Brudno JN, Kochenderfer JN. Recent advances in CAR T-cell toxicity: Mechanisms, manifestations and management. Blood Rev. 2019;34:45-55. https://doi.org/10.1016/j.blre.2018.11.002 PMid:30528964
  23. Amini L, Silbert SK, Maude SL, Nastoupil LJ, Ramos CA, Brentjens RJ, et al. Preparing for CAR T cell therapy: Patient selection, bridging therapies and lymphodepletion. Nat Rev Clin Oncol. 2022;19(5):342-55. https://doi.org/10.1038/s41571-022-00607-3 PMid:35318469
  24. Yip A, Webster RM. The market for chimeric antigen receptor T cell therapies. Nat Rev Drug Discov. 2018;17(3):161-2. https://doi.org/10.1038/nrd.2017.266 PMid:29375140
  25. Albelda SM. CAR T cell therapy for patients with solid tumours: Key lessons to learn and unlearn. Nat Rev Clin Oncol. 2024;21:47-66. https://doi.org/10.1038/s41571-023-00832-4 PMid:37904019
  26. Abou-el-Enein M, Elsallab M, Feldman SA, Andrew D. Fesnak AD, Heslop HE, et al. Scalable manufacturing of CAR T cells for cancer immunotherapy. Blood Cancer Discov. 2021;2(5):408-22. https://doi.org/10.1158/2643-3230.BCD-21-0084 PMid:34568831
  27. Lin JK, Muffly LS, Spinner MA, Barnes JI, Owens DK, Goldhaber-Fiebert JD. Cost effectiveness of chimeric antigen receptor T-cell therapy in multiply relapsed or refractory adult large B-cell lymphoma. J Clin Oncol. 2019;37(24):2105-19. https://doi.org/10.1200/JCO.18.02079 PMid:31157579
  28. Engstad CS, Gutteberg TJ, Osterud B. Modulation of blood cell activation by four commonly used anticoagulants. Thromb Haemost. 1997;77(4):690-6. PMid:9134644
  29. McFarland DC, Zhang C, Thomas HC, Ratliff TL. Confounding effects of platelets on flow cytometric analysis and cellsorting experiments using blood-derived cells. Cytometry A. 2006;69:86-94. https://doi.org/10.1002/cyto.a.20207 PMid:16419063
  30. Fesnak A, Lin C, Siegel DL, Maus MV. CAR-T cell therapies from the transfusion medicine perspective. Transfus Med Rev. 2016;30(3):139-45. https://doi.org/10.1016/j.tmrv.2016.03.001 PMid:27067907
  31. Atanackovic D, Radhakrishnan SV, Bhardwaj N, Luetkens T. Chimeric antigen receptor (CAR) therapy for multiple myeloma. Br J Haematol. 2016;172(5):685-98. https://doi.org/10.1111/bjh.13889 PMid:26791002
  32. Wang Z, Chen C, Wang L, Jia Y, Qin Y. Chimeric antigen receptor T-cell therapy for multiple myeloma. Front Immunol. 2022;13:1050522. https://doi.org/10.3389/fimmu.2022.1050522 PMid:36618390
  33. Wang QS, Wang Y, Lv HY, Han QW, Fan H, Guo B, et al. Treatment of CD33-directed chimeric antigen receptor-modified T cells in one patient with relapsed and refractory acute myeloid leukemia. Mol Ther. 2015;23(1):184-91. https://doi.org/10.1038/mt.2014.164 PMid:25174587
  34. Ali SA, Shi V, Maric I, Wang M, Stroncek DF, Rose JJ, et al. T cells expressing an anti-B-cell maturation antigen chimeric antigen receptor cause remissions of multiple myeloma. Blood. 2016;128(13):1688-700. https://doi.org/10.1182/blood-2016-04-711903 PMid:27412889
  35. Hollyman D, Stefanski J, Przybylowski M, Bartido S, Borquez-Ojeda O, Taylor C, et al. Manufacturing validation of biologically functional T cells targeted to CD19 antigen for autologous adoptive cell therapy. J Immunother. 2009;32(2):169-80. https://doi.org/10.1097/CJI.0b013e318194a6e8 PMid:19238016
  36. Turtle CJ, Hanafi LA, Berger C, Gooley TA, Cherian S, Hudecek M, et al. CD19 CAR-T cells of defined CD4+:CD8+ composition in adult B cell ALL patients. J Clin Invest. 2016;126(6):2123-38. https://doi.org/10.1172/JCI85309 PMid:27111235
  37. El Marabti E, Abdel-Wahab O. Enhancing CD19 chimeric antigen receptor T cells through memory-enriched T cells. Clin Cancer Res. 2023;29(4):694-6. https://doi.org/10.1158/1078-0432.CCR-22-3232 PMid:36507801
  38. Arcangeli S, Bove C, Mezzanotte C, Camisa B, Falcone L, Manfredi F, et al. CAR T cell manufacturing from naive/stem memory T lymphocytes enhances antitumor responses while curtailing cytokine release syndrome. J Clin Invest. 2022;132(12):e150807. https://doi.org/10.1172/JCI150807 PMid:35503659
  39. Singh H, Figliola MJ, Dawson MJ, Olivares S, Zhang L, Yang G, et al. Manufacture of clinical-grade CD19-specific T cells stably expressing chimeric antigen receptor using sleeping beauty system and artificial antigen presenting cells. PLoS One. 2013;8(5):e64138. https://doi.org/10.1371/journal.pone.0064138 PMid:23741305
  40. Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013;13(4):227-42. https://doi.org/10.1038/nri3405 PMid:23470321
  41. Levine BL. Performance-enhancing drugs: Design and production of redirected chimeric antigen receptor (CAR) T cells. Cancer Gene Ther. 2015;22(2):79-84. https://doi.org/10.1038/cgt.2015.5 PMid:25675873
  42. Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12(6):492-499. https://doi.org/10.1038/ni.2035 PMid:21739672
  43. Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, et al. A human memory T cell subset with stem cell-like properties. Nat Med. 2011;17(10):1290-7. https://doi.org/10.1038/nm.2446 PMid:21926977
  44. Barrett DM, Singh N, Liu X, Jiang S, June CH, Grupp SA, et al. Relation of clinical culture method to T-cell memory status and efficacy in xenograft models of adoptive immunotherapy. Cytotherapy. 2014;16(5):619-30. https://doi.org/10.1016/j.jcyt.2013.10.013 PMid:24439255
  45. Ghassemi S, Bedoya F, Nunez-Cruz S, June C, Melenhorst J, Milone M. Shortened T cell culture with IL-7 and IL-15 provides the most potent chimeric antigen receptor (CAR)-modified T cells for adoptive immunotherapy. Cancer Immunother Cancer Vaccines. 2016;24(Suppl 1):S79. https://doi.org/10.1016/S1525-0016(16)33012-X
  46. Ukrainskaya VM, Rubtsov YP, Pershin DS, Podoplelova NA, Terekhov SS, Yaroshevich I, et al. Antigen-specific stimulation and expansion of CAR-T cells using membrane vesicles as target cell surrogates. Small. 2021;17(45):2102643. https://doi.org/10.1002/smll.202102643 PMid:34605165
  47. Ghassemi S, Durgin JS, Nunez-Cruz S, Patel J, Leferovich J, Pinzone M, et al. Rapid manufacturing of non-activated potent CAR T cells. Nat Biomed Eng. 2022;6(2):118-28. https://doi.org/10.1038/s41551-021-00842-6 PMid:35190680
  48. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med. 2011;3(95):95ra73. https://doi.org/10.1126/scitranslmed.3002842 PMid:21832238
  49. Casati A, Varghaei-Nahvi A, Feldman SA, Assenmacher M, Rosenberg SA, Dudley ME, et al. Clinical-scale selection and viral transduction of human naïve and central memory CD8+ T cells for adoptive cell therapy of cancer patients. Cancer Immunol Immunother. 2013;62(10):1563-73. https://doi.org/10.1007/s00262-013-1459-x PMid:23903715
  50. Deeks SG, Wagner B, Anton PA, Mitsuyasu RT, Scadden DT, Huang C, et al. A phase II randomized study of HIV-specific T-cell gene therapy in subjects with undetectable plasma viremia on combination antiretroviral therapy. Mol Ther. 2002;5(6):788-97. https://doi.org/10.1006/mthe.2002.0611 PMid:12027564
  51. Kebriaei P, Huls H, Singh H, Olivares S, Figliola M, Maiti S, et al. Adoptive therapy using sleeping beauty gene transfer system and artificial antigen presenting cells to manufacture T cells expressing CD19-specific chimeric antigen receptor. Blood. 2014;124:311. https://doi.org/10.1371/journal.pone.0064138
  52. Cruz CR, Micklethwaite KP, Savoldo B, Ramos CA, Lam S, Ku S, et al. Infusion of donor-derived CD19-redirected virus-specific T cells for B-cell malignancies relapsed after allogeneic stem cell transplant: A phase 1 study. Blood. 2013;122(17):2965-73. https://doi.org/10.1182/blood-2013-06-506741 PMid:24030379
  53. Lana MG, Strauss BE. Production of lentivirus for the establishment of CAR-T cells. Methods Mol Biol. 2020;2086:61-7. https://doi.org/10.1007/978-1-0716-0146-4_4 PMid:31707667
  54. Brentjens RJ, Riviere I, Park JH, Davila ML, Wang X, Stefanski J, 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):4817-28. https://doi.org/10.1182/blood-2011-04-348540 PMid:21849486
  55. Ghorashian S, Pule M, Amrolia P. CD19 chimeric antigen receptor T cell therapy for haematological malignancies. Br J Haematol. 2015;169(4):463-78. https://doi.org/10.1111/bjh.13340 PMid:25753571
  56. Hamada M, Nishio N, Okuno Y, Suzuki S, Kawashima N, Muramatsu H, et al. Integration mapping of piggyBac-Mediated CD19 chimeric antigen receptor T cells analyzed by novel tagmentation-assisted PCR. EBioMedicine. 2018;34:18-26. https://doi.org/10.1016/j.ebiom.2018.07.008 PMid:30082227
  57. Ramanayake S, Bilmon I, Bishop D, Dubosq MC, Blyth E, Clancy L, et al. Low-cost generation of Good Manufacturing Practice-grade CD19-specific chimeric antigen receptor-expressing T cells using piggyBac gene transfer and patient-derived materials. Cytotherapy. 2015;17(9):1251-67. https://doi.org/10.1016/j.jcyt.2015.05.013 PMid:26212611
  58. Merten OW, Hebben M, Bovolenta C. Production of lentiviral vectors. Mol Ther Methods Clin Dev. 2016;3:16017. https://doi.org/10.1038/mtm.2016.17 PMid:27110581
  59. Sanber KS, Knight SB, Stephen SL, Bailey R, Escors D, Minshull J, et al. Construction of stable packaging cell lines for clinical lentiviral vector production. Sci Rep. 2015;5:9021. https://doi.org/10.1038/srep09021 PMid:25762005
  60. Wang X, Rivière I. Manufacture of tumor- and virus-specific T lymphocytes for adoptive cell therapies. Cancer Gene Ther. 2015;22(2):85-94. https://doi.org/10.1038/cgt.2014.81 PMid:25721207
  61. Ivics Z, Hackett PB, Plasterk RH, Izsvák Z. Molecular reconstruction of sleeping beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell. 1997;91(4):501-10. https://doi.org/10.1016/s0092-8674(00)80436-5 PMid:9390559
  62. Moretti A, Ponzo M, Nicolette CA, Tcherepanova IY, Biondi A, Magnani CF. The past, present, and future of non-viral CAR T cells. Front Immunol. 2022;13:867013. https://doi.org/10.3389/fimmu.2022.867013 PMid:35757746
  63. Singh H, Figliola MJ, Dawson MJ, Huls H, Olivares S, Switzer K, et al. Reprogramming CD19-specific T cells with IL-21 signaling can improve adoptive immunotherapy of B-lineage malignancies. Cancer Res. 2011;71(10):3516-27. https://doi.org/10.1158/0008-5472.CAN-10-3843 PMid:21558388
  64. Kebriaei P, Ciurea SO, Huls MH, Singh H, Olivares S, Su S, et al. Pre-emptive donor lymphocyte infusion with CD19-directed, CAR-modified T cells infused after allogeneic hematopoietic cell transplantation for patients with advanced CD19+ malignancies. Blood. 2015;126:862.
  65. Narayanavari SA, Chilkunda SS, Ivics Z, Izsvák Z. Sleeping Beauty transposition: From biology to applications. Crit Rev Biochem Mol Biol. 2017;52(1):18-44. https://doi.org/10.1080/10409238.2016.1237935 PMid:27696897
  66. Zhang C, Liu J, Zhong JF, Zhang X. Engineering CAR-T cells. Biomark Res. 2017;5:22. https://doi.org/10.1186/s40364-017-0102-y PMid:28652918
  67. Gogol-Doring A, Ammar I, Gupta S, Bunse M, Miskey C, Chen W, et al. Genome-wide profiling reveals remarkable parallels between insertion site selection properties of the MLV retrovirus and the piggyBac transposon in primary human CD4(+) T cells. Mol Ther. 2016;24(3):592-606. https://doi.org/10.1038/mt.2016.11 PMid:26755332
  68. Park JR, Digiusto DL, Slovak M, Wright C, Naranjo A, Wagner J, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther. 2007;15(4):825-33. https://doi.org/10.1038/sj.mt.6300104 PMid:17299405
  69. Jensen MC, Popplewell L, Cooper LJ, DiGiusto D, Kalos M, Ostberg JR, et al. Antitransgene rejection responses contribute to attenuated persistence of adoptively transferred CD20/CD19-specific chimeric antigen receptor redirected T cells in humans. Biol Blood Marrow Transpl. 2010;16(9):1245-56. https://doi.org/10.1016/j.bbmt.2010.03.014 PMid:20304086
  70. Kaiser AD, Assenmacher M, Schroder B, Meyer M, Orentas R, Bethke U, et al. Towards a commercial process for the manufacture of genetically modified T cells for therapy. Cancer Gene Ther. 2015;22(2):72-8. https://doi.org/10.1038/cgt.2014.78 PMid:25613483
  71. Tumaini B, Lee DW, Lin T, Castiello L, Stroncek DF, Mackall C, et al. Simplified process for the production of anti-CD19-CAR-engineered T cells. Cytotherapy. 2013;15(11):1406-15. https://doi.org/10.1016/j.jcyt.2013.06.003 PMid:23992830
  72. Hanley PJ. Fresh versus frozen: Effects of cryopreservation on CAR T cells. Mol Ther. 2019;27(7):1213-4. https://doi.org/10.1016/j.ymthe.2019.06.001 PMid:31202635
  73. Panch SR, Srivastava SK, Elavia N, McManus A, Liu S, Jin P, et al. Effect of cryopreservation on autologous chimeric antigen receptor T cell characteristics. Mol Ther. 2019;27(7):1275-85. https://doi.org/10.1016/j.ymthe.2019.05.015 PMid:31178392
  74. Vormittag P, Gunn R, Ghorashian S, Veraitch FS. A guide to manufacturing CAR T cell therapies. Curr Opin Biotechnol. 2018;53:164-81. https://doi.org/10.1016/j.copbio.2018.01.025 PMid:29462761
Language: English
Page range: 13 - 20
Submitted on: Dec 9, 2023
|
Accepted on: Jan 10, 2024
|
Published on: Mar 12, 2024
Published by: Sciendo
In partnership with: Paradigm Publishing Services
Publication frequency: 1 issue per year

© 2024 Monica Neagu, Carolina Constantin, published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial 4.0 License.