Development of CAR-T cell therapy for B-ALL using a point-of-care approach

References

• Park JH, Rivière I, Gonen M, Wang X, Sénéchal B, Curran KJ, Sauter C, Wang Y, Santomasso B, Mead E, et al. Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia. N Engl J Med. 2018;378(5):449–10. doi:10.1056/NEJMoa1709919.
   PubMed Web of Science ®Google Scholar
• 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. N Engl J Med. 2018;378(5):439–448. doi:10.1056/NEJMoa1709866.
   PubMed Web of Science ®Google Scholar
• 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. N Engl J Med. 2017;377(26):2531–2544. doi:10.1056/NEJMoa1707447.
   PubMed Web of Science ®Google Scholar
• 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. N Engl J Med. 2019;380(1):45–56. doi:10.1056/NEJMoa1804980.
   PubMed Web of Science ®Google Scholar
• June CH, Sadelain M. Chimeric antigen receptor therapy. N Engl J Med. 2018;379(1):64–73. doi:10.1056/NEJMra1706169.
   PubMed Web of Science ®Google Scholar
• Fry TJ, Shah NN, Orentas RJ, Stetler-Stevenson M, Yuan CM, Ramakrishna S, Wolters P, Martin S, Delbrook C, Yates B, et al. CD22-targeted CAR T cells induce remission in B-ALL that is naive or resistant to CD19-targeted CAR immunotherapy. Nat Med. 2018;24(1):20–28. doi:10.1038/nm.4441.
   PubMed Web of Science ®Google Scholar
• Pan J, Niu Q, Deng B, Liu S, Wu T, Gao Z, Liu Z, Zhang Y, Qu X, Zhang Y, et al. CD22 CAR T-cell therapy in refractory or relapsed B acute lymphoblastic leukemia. Leukemia. 2019;33(12):2854–2866. doi:10.1038/s41375-019-0488-7.
   Google Scholar
• Xu J, Chen L-J, Yang -S-S, Sun Y, Wu W, Liu Y-F, Xu J, Zhuang Y, Zhang W, Weng X-Q, et al. Exploratory trial of a biepitopic CAR T-targeting B cell maturation antigen in relapsed/refractory multiple myeloma. Proc Natl Acad Sci. 2019;116(19):9543–9551. doi:10.1073/pnas.1819745116.
   PubMed Web of Science ®Google Scholar
• Cohen AD, Garfall AL, Stadtmauer EA, Melenhorst JJ, Lacey SF, Lancaster E, Vogl DT, Weiss BM, Dengel K, Nelson A, et al. B cell maturation antigen–specific CAR T cells are clinically active in multiple myeloma. J Clin Invest. 2019;129(6):2210–2221. doi:10.1172/JCI126397.
   PubMed Web of Science ®Google Scholar
• Brudno JN, Maric I, Hartman SD, Rose JJ, Wang M, Lam N, Stetler-Stevenson M, Salem D, Yuan C, Pavletic S, et al. T cells genetically modified to express an anti–B-cell maturation antigen chimeric antigen receptor cause remissions of poor-prognosis relapsed multiple myeloma. J Clin Oncol. 2018;36(22):2267–2280. doi:10.1200/JCO.2018.77.8084.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Wang X, Rivière I. Clinical manufacturing of CAR T cells: foundation of a promising therapy. Mol Ther Oncolytics. 2016;3:16015. doi:10.1038/mto.2016.15.
   PubMed Web of Science ®Google Scholar
• Poorebrahim M, Sadeghi S, Fakhr E, Abazari MF, Poortahmasebi V, Kheirollahi A, Askari H, Rajabzadeh A, Rastegarpanah M, Line A, et al. Production of CAR T-cells by GMP-grade lentiviral vectors: latest advances and future prospects. Crit Rev Clin Lab Sci. 2019;56(6):393–419.
   PubMed Web of Science ®Google Scholar
• Vormittag P, Gunn R, Ghorashian S, Veraitch FS. A guide to manufacturing CAR T cell therapies. Curr Opin Biotechnol. 2018;53:164–181. doi:10.1016/j.copbio.2018.01.025.
   PubMed Web of Science ®Google Scholar
• Chicaybam L, Abdo L, Carneiro M, Peixoto B, Viegas M, de Sousa P, Fornazin MC, Spago MC, Albertoni Laranjeira AB, de Campos-lima PO, et al. CAR T cells generated using sleeping beauty transposon vectors and expanded with an EBV-transformed lymphoblastoid cell line display antitumor activity in vitro and in vivo. Hum Gene Ther. 2019;30(4):511–522. doi:10.1089/hum.2018.218.
   PubMed Web of Science ®Google Scholar
• Magnani CF, Mezzanotte C, Cappuzzello C, Bardini M, Tettamanti S, Fazio G, Cooper LJN, Dastoli G, Cazzaniga G, Biondi A, et al. Preclinical efficacy and safety of CD19CAR cytokine-induced killer cells transfected with sleeping beauty transposon for the treatment of acute lymphoblastic leukemia. Hum Gene Ther. 2018;29(5):602–613. doi:10.1089/hum.2017.207.
   PubMed Web of Science ®Google Scholar
• Monjezi R, Miskey C, Gogishvili T, Schleef M, Schmeer M, Einsele H, Ivics Z, Hudecek M. Enhanced CAR T-cell engineering using non-viral Sleeping Beauty transposition from minicircle vectors. Leukemia. 2017;31(1):186–194. doi:10.1038/leu.2016.180.
   PubMed Web of Science ®Google Scholar
• Kebriaei P, Izsvák Z, Narayanavari SA, Singh H, Ivics Z. Gene therapy with the sleeping beauty transposon system. Trends Genet. 2017;33(11):852–870. doi:10.1016/j.tig.2017.08.008.
   PubMed Web of Science ®Google Scholar
• Huang X, Guo H, Tammana S, Jung Y-C, Mellgren E, Bassi P, Cao Q, Tu ZJ, Kim YC, Ekker SC, et al. Gene transfer efficiency and genome-wide integration profiling of sleeping beauty, Tol2, and piggybac transposons in human primary T cells. Mol Ther. 2010;18(10):1803–1813. doi:10.1038/mt.2010.141.
   PubMed Web of Science ®Google Scholar
• Yant SR, Wu X, Huang Y, Garrison B, Burgess SM, Kay MA. High-resolution genome-wide mapping of transposon integration in mammals. Mol Cell Biol. 2005;25(6):2085–2094. doi:10.1128/MCB.25.6.2085-2094.2005.
   PubMed Web of Science ®Google Scholar
• de Jong J, Akhtar W, Badhai J, Rust AG, Rad R, Hilkens J, Berns A, van Lohuizen M, Wessels LFA, de Ridder J, et al. Chromatin landscapes of retroviral and transposon integration profiles. PLoS Genetics. 2014;10(4):e1004250. doi:10.1371/journal.pgen.1004250.
   PubMed Web of Science ®Google Scholar
• Field A-C, Vink C, Gabriel R, Al-Subki R, Schmidt M, Goulden N, Stauss H, Thrasher A, Morris E, Qasim W, et al. Comparison of lentiviral and sleeping beauty mediated αβ T cell receptor gene transfer. PLoS One. 2013;8(6):e68201. doi:10.1371/journal.pone.0068201.
   PubMed Web of Science ®Google Scholar
• Wu X. Transcription start regions in the human genome are favored targets for MLV Integration. Science. 2003;300(5626):1749–1751. doi:10.1126/science.1083413.
   PubMed Web of Science ®Google Scholar
• Qin D-Y, Huang Y, Li D, Wang Y-S, Wang W, Wei Y-Q. Paralleled comparison of vectors for the generation of CAR-T cells. Anticancer Drugs. 2016;27(8):711–722. doi:10.1097/CAD.0000000000000387.
   PubMed Web of Science ®Google Scholar
• Ghassemi S, Nunez-Cruz S, O’Connor RS, Fraietta JA, Patel PR, Scholler J, Barrett DM, Lundh SM, Davis MM, Bedoya F, et al. Reducing ex vivo culture improves the antileukemic activity of chimeric antigen receptor (CAR) T cells. Cancer Immunol Res. 2018;6(9):1100–1109. doi:10.1158/2326-6066.CIR-17-0405.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, 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(6);115:1616–1626. doi:10.1172/JCI24480.
   PubMed Web of Science ®Google Scholar
• Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE, Palmer DC, Antony PA, Hwang ST, Rosenberg SA, et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci. 2005;102(27):9571–9576. doi:10.1073/pnas.0503726102.
   PubMed Web of Science ®Google Scholar
• Alizadeh D, Wong RA, Yang X, Wang D, Pecoraro JR, Kuo C-F, Aguilar B, Qi Y, Ann DK, Starr R, et al. IL15 enhances CAR-T cell antitumor activity by reducing mTORC1 activity and preserving their stem cell memory phenotype. Cancer Immunol Res. 2019;7(5):759–772. doi:10.1158/2326-6066.CIR-18-0466.
   PubMed Web of Science ®Google Scholar
• Fraietta JA, Lacey SF, Orlando EJ, Pruteanu-Malinici I, Gohil M, Lundh S, Boesteanu AC, Wang Y, O’Connor RS, Hwang W-T, et al. Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia. Nat Med. 2018;24(5):563–571. doi:10.1038/s41591-018-0010-1.
   PubMed Web of Science ®Google Scholar
• Brentjens RJ, Santos E, Nikhamin Y, Yeh R, Matsushita M, La Perle K, Quintas-Cardama A, Larson SM, Sadelain M. Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin Cancer Res Off J Am Assoc Cancer Res. 2007;13(18):5426–5435. doi:10.1158/1078-0432.CCR-07-0674.
   PubMed Web of Science ®Google Scholar
• Castella M, Boronat A, Martín-Ibáñez R, Rodríguez V, Suñé G, Caballero M, Marzal B, Pérez-Amill L, Martín-Antonio B, Castaño J, et al. Development of a novel anti-CD19 chimeric antigen receptor: a paradigm for an affordable CAR T cell production at academic institutions. Mol Ther Methods Clin Dev. 2019;12:134–144. doi:10.1016/j.omtm.2018.11.010.
   PubMed Web of Science ®Google Scholar
• Feucht J, Sun J, Eyquem J, Ho Y-J, Zhao Z, Leibold J, Dobrin A, Cabriolu A, Hamieh M, Sadelain M, et al. Calibration of CAR activation potential directs alternative T cell fates and therapeutic potency. Nat Med. 2019;25(1):82–88. doi:10.1038/s41591-018-0290-5.
   PubMed Web of Science ®Google Scholar
• Chicaybam L, Sodré AL, Bonamino M. Chimeric antigen receptors in cancer immuno-gene therapy: current status and future directions. Int Rev Immunol. 2011;30(5–6):294–311. doi:10.3109/08830185.2011.595855.
   PubMed Web of Science ®Google Scholar
• Chicaybam L, Bonamino MH. Moving receptor redirected adoptive cell therapy toward fine tuning of antitumor responses. Int Rev Immunol. 2014;33(5):402–416. doi:10.3109/08830185.2014.917412.
   PubMed Web of Science ®Google Scholar
• Highfill SL, Stroncek DF. Overcoming challenges in process development of cellular therapies. Curr Hematol Malig Rep. 2019;14(4):269–277. doi:10.1007/s11899-019-00529-5.
   PubMed Web of Science ®Google Scholar
• Draaisma D. Lithium: the gripping history of a psychiatric success story. Nature. 2019;572(7771):584–585. doi:10.1038/d41586-019-02480-0.
   Google Scholar
• Zhu F, Shah N, Xu H, Schneider D, Orentas R, Dropulic B, Hari P, Keever-Taylor CA. Closed-system manufacturing of CD19 and dual-targeted CD20/19 chimeric antigen receptor T cells using the CliniMACS Prodigy device at an academic medical center. Cytotherapy. 2018;20(3):394–406. doi:10.1016/j.jcyt.2017.09.005.
   PubMed Web of Science ®Google Scholar
• Zhang W, Jordan KR, Schulte B, Purev E. Characterization of clinical grade CD19 chimeric antigen receptor T cells produced using automated clinimacs prodigy system. Drug Des Devel Ther. 2018;12:3343–3356. doi:10.2147/DDDT.S175113.
   PubMed Web of Science ®Google Scholar
• Gattinoni L, Zhong X-S, Palmer DC, Ji Y, Hinrichs CS, Yu Z, Wrzesinski C, Boni A, Cassard L, Garvin LM, et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat Med. 2009;15(7):808–813. doi:10.1038/nm.1982.
   PubMed Web of Science ®Google Scholar
• Klebanoff CA, Scott CD, Leonardi AJ, Yamamoto TN, Cruz AC, Ouyang C, Ramaswamy M, Roychoudhuri R, Ji Y, Eil RL, et al. Memory T cell–driven differentiation of naive cells impairs adoptive immunotherapy. J Clin Invest. 2016;126(1):318–334. doi:10.1172/JCI81217.
   PubMed Web of Science ®Google Scholar
• Busch DH, Fräßle SP, Sommermeyer D, Buchholz VR, Riddell SR. Role of memory T cell subsets for adoptive immunotherapy. Semin Immunol. 2016;28(1):28–34. doi:10.1016/j.smim.2016.02.001.
   PubMed Web of Science ®Google Scholar
• Kaartinen T, Luostarinen A, Maliniemi P, Keto J, Arvas M, Belt H, Koponen J, Loskog A, Mustjoki S, Porkka K, et al. Low interleukin-2 concentration favors generation of early memory T cells over effector phenotypes during chimeric antigen receptor T-cell expansion. Cytotherapy. 2017;19(6):689–702. doi:10.1016/j.jcyt.2017.03.067.
   PubMed Web of Science ®Google Scholar
• Raeber ME, Zurbuchen Y, Impellizzieri D, Boyman O. The role of cytokines in T-cell memory in health and disease. Immunol Rev. 2018;283(1):176–193. doi:10.1111/imr.12644.
   PubMed Web of Science ®Google Scholar
• Bollino D, Webb TJ. Chimeric antigen receptor–engineered natural killer and natural killer T cells for cancer immunotherapy. Transl Res. 2017;187:32–43. doi:10.1016/j.trsl.2017.06.003.
   PubMed Web of Science ®Google Scholar
• Hung C-F, Xu X, Li L, Ma Y, Jin Q, Viley A, Allen C, Natarajan P, Shivakumar R, Peshwa MV, et al. Development of anti-human mesothelin-targeted chimeric antigen receptor messenger RNA–transfected peripheral blood lymphocytes for ovarian cancer therapy. Hum Gene Ther. 2018;29(5):614–625. doi:10.1089/hum.2017.080.
   PubMed Web of Science ®Google Scholar
• Ceppi F, Rivers J, Annesley C, Pinto N, Park JR, Lindgren C, Mgebroff S, Linn N, Delaney M, Gardner RA, et al. Lymphocyte apheresis for chimeric antigen receptor T-cell manufacturing in children and young adults with leukemia and neuroblastoma. Transfusion (Paris). 2018;58(6):1414–1420. doi:10.1111/trf.14569.
   PubMed Web of Science ®Google Scholar
• Tuazon SA, Li A, Gooley T, Eunson TW, Maloney DG, Turtle CJ, Linenberger ML, Connelly‐Smith LS. Factors affecting lymphocyte collection efficiency for the manufacture of chimeric antigen receptor T cells in adults with B-cell malignancies. Transfusion (Paris). 2019;59(5):1773–1780. doi:10.1111/trf.15178.
   Web of Science ®Google Scholar
• Chicaybam L, Abdo L, Viegas M, Marques LVC, de Sousa P, Batista-Silva LR, Alves-Monteiro V, Bonecker S, Monte-Mór B, Bonamino MH, et al. Transposon-mediated generation of CAR-T cells shows efficient anti B-cell leukemia response after ex vivo expansion. Gene Therapy. 2020;27(1–2):85–95. doi:10.1038/s41434-020-0121-4.
   PubMed Web of Science ®Google Scholar
• Kebriaei P, Singh H, Huls MH, Figliola MJ, Bassett R, Olivares S, Jena B, Dawson MJ, Kumaresan PR, Su S, et al. Phase I trials using Sleeping Beauty to generate CD19-specific CAR T cells. J Clin Invest. 2016;126(9):3363–3376. doi:10.1172/JCI86721.
   PubMed Web of Science ®Google Scholar
• Oh SA, Seki A, Rutz S. Ribonucleoprotein transfection for CRISPR/Cas9-mediated gene knockout in primary T cells. Curr Protoc Immunol. 2019;124(1):e69. doi:10.1002/cpim.69.
   PubMedGoogle Scholar
• Miskey C, Amberger M, Reiser M, Prommersberger S, Beckmann J, Machwirth M, Einsele H, Hudecek M, Bonig H, Ivics Z. Genomic analyses of SLAMF7 CAR-T cells manufactured by sleeping beauty transposon gene transfer for immunotherapy of multiple myeloma. bioRxiv. 2019;675009. doi:10.1101/675009.
   Google Scholar
• Qasim W, Zhan H, Samarasinghe S, Adams S, Amrolia P, Stafford S, Butler K, Rivat C, Wright G, Somana K, et al. Molecular remission of infant B-ALL after infusion of universal TALEN gene-edited CAR T cells. Sci Transl Med. 2017;9(374):eaaj2013. doi:10.1126/scitranslmed.aaj2013.
   Web of Science ®Google Scholar
• Querques I, Mades A, Zuliani C, Miskey C, Alb M, Grueso E, Machwirth M, Rausch T, Einsele H, Ivics Z, et al. A highly soluble Sleeping Beauty transposase improves control of gene insertion. Nat Biotechnol. 2019;37(12):1502–1512. doi:10.1038/s41587-019-0291-z.
   PubMed Web of Science ®Google Scholar
• Chan T, Gallagher J, Cheng N-L, Carvajal-Borda F, Plummer J, Govekung A, Barrett JA, Khare PD, Cooper LJN,  Shah RR. CD19-specific chimeric antigen receptor-modified T cells with safety switch produced under “point-of-care” using the sleeping beauty system for the very rapid manufacture and treatment of b-cell malignancies. Blood. 2017;130(Suppl 1):1324-1324. doi:10.1182/blood.V130.Suppl_1.1324.1324.
   Google Scholar
• Chicaybam L, Sodre AL, Curzio BA, Bonamino MH, Fang D. An efficient low cost method for gene transfer to T lymphocytes. PLoS One. 2013;8(3):e60298. doi:10.1371/journal.pone.0060298.
   PubMed Web of Science ®Google Scholar
• Neri S, Mariani E, Meneghetti A, Cattini L, Facchini A. Calcein- acetyoxymethyl cytotoxicity assay: standardization of a method allowing additional analyses on recovered effector cells and supernatants. Clin Diagn Lab Immunol. 2001;8(6):1131–1135. doi:10.1128/CDLI.8.6.1131-1135.2001.
   PubMedGoogle Scholar