Novel T cells with improved in vivo anti-tumor activity generated by RNA electroporation

Protein and Cell

Volumn 8, Issue 7, 2017, Pages 514-526

  Liu, Xiaojun ^a,b   Jiang, Shuguang ^b   Fang, Chongyun ^b   Li, Hua ^b   Zhang, Xuhua ^b   Zhang, Fuqin ^b   June, Carl H ^b   Zhao, Yangbing ^b  

^a SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CAR; gene transfer; manufacture; RNA electroporation; T lymphocytes

Indexed keywords

CD137 LIGAND; CD28 ANTIGEN; CD3 ANTIBODY; CD3 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 2; L SELECTIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; OKT 3; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; CD137 ANTIGEN; MESSENGER RNA;

ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLUMINESCENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY ASSAY; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; LEUKEMIA; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; T LYMPHOCYTE; ANIMAL; CELLULAR IMMUNITY; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGY; K-562 CELL LINE; PATHOLOGY;

ANIMALS; ANTIGENS, CD137; ANTIGENS, CD28; ELECTROPORATION; HUMANS; IMMUNITY, CELLULAR; INTERLEUKIN-2; K562 CELLS; MICE; MUROMONAB-CD3; NEOPLASMS, EXPERIMENTAL; RNA, MESSENGER; T-LYMPHOCYTES;

EID: 85019642198     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-017-0422-6     Document Type: Article

References (33)

1. Barrett DM, Zhao Y, Liu X, Jiang S, Carpenito C, Kalos M, Carroll RG, June CH, Grupp SA (2011) Treatment of advanced leukemia in mice with mRNA engineered T cells. Human Gene Ther 22:1575–1586
2. Barrett DM, Singh N, Liu X, Jiang S, June CH, Grupp SA, Zhao Y (2014) Relation of clinical culture method to T-cell memory status and efficacy in xenograft models of adoptive immunotherapy. Cytotherapy 16:619–630
3. Besser MJ, Shapira-Frommer R, Treves AJ, Zippel D, Itzhaki O, Hershkovitz L, Levy D, Kubi A, Hovav E, Chermoshniuk N et al (2010) Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin Cancer Res 16:2646–2655
4. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, Bartido S, Stefanski J, Taylor C, Olszewska M et al (2013) CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 5:177ra138
5. Butler MO, Imataki O, Yamashita Y, Tanaka M, Ansen S, Berezovskaya A, Metzler G, Milstein MI, Mooney MM, Murray AP et al (2012) Ex vivo expansion of human CD8+ T cells using autologous CD4+ T cell help. PloS ONE 7:e30229
6. Campagnolo C, Meyers KJ, Ryan T, Atkinson RC, Chen YT, Scanlan MJ, Ritter G, Old LJ, Batt CA (2004) Real-Time, label-free monitoring of tumor antigen and serum antibody interactions. J Biochem Biophys Methods 61:283–298
7. Carpenito C, Milone MC, Hassan R, Simonet JC, Lakhal M, Suhoski MM, Varela-Rohena A, Haines KM, Heitjan DF, Albelda SM et al (2009) Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci USA 106:3360–3365
8. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, Finkelstein SE, Theoret MR, Rosenberg SA, Restifo NP (2005) Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Investig 115:1616–1626
9. Gattinoni L, Lugli E, Ji Y, Pos Z, Paulos CM, Quigley MF, Almeida JR, Gostick E, Yu Z, Carpenito C et al (2011) A human memory T cell subset with stem cell-like properties. Nature medicine 17:1290–1297
10. Gattinoni L, Speiser DE, Lichterfeld M, Bonini C (2017) T memory stem cells in health and disease. Nat Med 23:18–27
11. Hermans IF, Silk JD, Yang J, Palmowski MJ, Gileadi U, McCarthy C, Salio M, Ronchese F, Cerundolo V (2004) The VITAL assay: a versatile fluorometric technique for assessing CTL- and NKT-mediated cytotoxicity against multiple targets in vitro and in vivo. J Immunol Methods 285:25–40
12. Kloss CC, Condomines M, Cartellieri M, Bachmann M, Sadelain M (2013) Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells. Nat Biotechnol 31:71–75
13. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, Fry TJ, Orentas R, Sabatino M, Shah NN et al (2015) T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet 385:517–528
14. Levine BL, Bernstein WB, Connors M, Craighead N, Lindsten T, Thompson CB, June CH (1997) Effects of CD28 costimulation on long-term proliferation of CD4+ T cells in the absence of exogenous feeder cells. J Immunol 159:5921–5930
15. Liu X, Jiang S, Fang C, Yang S, Olalere D, Pequignot EC, Cogdill AP, Li N, Ramones M, Granda B et al (2015) Affinity-tuned ErbB2 or EGFR chimeric antigen receptor T cells exhibit an increased therapeutic index against tumors in mice. Cancer Res 75:3596–3607
16. Maus MV, Fraietta JA, Levine BL, Kalos M, Zhao Y, June CH (2014) Adoptive immunotherapy for cancer or viruses. Ann Rev Immunol 32:189–225
17. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP et al (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314:126–129
18. Porter DL, Levine BL, Kalos M, Bagg A, June CH (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365:725–733
19. Powell DJ Jr, Dudley ME, Robbins PF, Rosenberg SA (2005) Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105:241–250
20. Ren J, Liu X, Fang C, Jiang S, June CH, Zhao Y (2016) Multiplex genome editing to generate universal CAR T cells resistant to PD1 inhibition. Clin Cancer Res 23(9):2255–2266
21. Riddell SR, Greenberg PD (1990) The use of anti-CD3 and anti-CD28 monoclonal antibodies to clone and expand human antigen-specific T cells. J Immunol Methods 128:189–201
22. Rosenberg SA (2008) Overcoming obstacles to the effective immunotherapy of human cancer. Proc Natl Acad Sci USA 105:12643–12644
23. Sabatino M, Hu J, Sommariva M, Gautam S, Fellowes V, Hocker JD, Dougherty S, Qin H, Klebanoff CA, Fry TJ et al (2016) Generation of clinical-grade CD19-specific CAR-modified CD8+ memory stem cells for the treatment of human B-cell malignancies. Blood 128:519–528
24. Stephan MT, Ponomarev V, Brentjens RJ, Chang AH, Dobrenkov KV, Heller G, Sadelain M (2007) T cell-encoded CD80 and 4-1BBL induce auto- and transcostimulation, resulting in potent tumor rejection. Nat Med 13:1440–1449
25. Suhoski MM, Golovina TN, Aqui NA, Tai VC, Varela-Rohena A, Milone MC, Carroll RG, Riley JL, June CH (2007) Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol Ther 15:981–988
26. Watts TH (2005) TNF/TNFR family members in costimulation of T cell responses. Ann Rev Immunol 23:23–68
27. Yang S, Dudley ME, Rosenberg SA, Morgan RA (2010) A simplified method for the clinical-scale generation of central memory-like CD8+ T cells after transduction with lentiviral vectors encoding antitumor antigen T-cell receptors. J Immunother 33:648–658
28. Yang S, Ji Y, Gattinoni L, Zhang L, Yu Z, Restifo NP, Rosenberg SA, Morgan RA (2013) Modulating the differentiation status of ex vivo-cultured anti-tumor T cells using cytokine cocktails. Cancer Immunol Immunother 62:727–736
29. Zhao Y, Boczkowski D, Nair SK, Gilboa E (2003) Inhibition of invariant chain expression in dendritic cells presenting endogenous antigens stimulates CD4+ T-cell responses and tumor immunity. Blood 102:4137–4142
30. Zhao Y, Zheng Z, Cohen CJ, Gattinoni L, Palmer DC, Restifo NP, Rosenberg SA, Morgan RA (2006) High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol Ther 13:151–159
31. Zhao Y, Moon E, Carpenito C, Paulos CM, Liu X, Brennan AL, Chew A, Carroll RG, Scholler J, Levine BL et al (2010) Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res 70:9053–9061
32. Zhou J, Dudley ME, Rosenberg SA, Robbins PF (2005a) Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J Immunother 28:53–62
33. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF (2005b) Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol 175:7046–7052