Adoptive cell therapy: Past, present and future

Immunotherapy

Volumn 9, Issue 2, 2017, Pages 183-196

  Cohen, Jonathan E ^a   Merims, Sharon ^a   Frank, Stephen ^a   Engelstein, Roni ^a   Peretz, Tamar ^a   Lotem, Michal ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

adoptive cell therapy; cancer immunotherapy; tumor infiltrating lymphocytes

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; CYCLOPHOSPHAMIDE; DACARBAZINE; FLUDARABINE; INTERLEUKIN 2; MESOTHELIN; NY ESO 1 ANTIGEN; PEMBROLIZUMAB; RECOMBINANT RECEPTOR; RECOMBINANT T CELL RECEPTOR; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; TUMOR ANTIGEN;

ADOPTIVE IMMUNOTHERAPY; CANCER IMMUNOTHERAPY; CAPILLARY LEAK SYNDROME; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DNA MODIFICATION; DRUG MEGADOSE; ENGRAFTMENT; GENETIC ENGINEERING; HUMAN; KIDNEY CARCINOMA; KILLER CELL; LIVER METASTASIS; LUNG METASTASIS; LYMPHOCYTE DEPLETION; LYMPHOCYTE TRANSFER; METASTATIC MELANOMA; NONHUMAN; OVERALL SURVIVAL; REVIEW; SINGLE DRUG DOSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR REGRESSION; WHOLE BODY RADIATION; ANIMAL; GENETICS; IMMUNOLOGY; NEOPLASMS; PROCEDURES; TRANSPLANTATION; TRENDS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; COSTIMULATORY AND INHIBITORY T-CELL RECEPTORS; GENETIC ENGINEERING; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL;

EID: 85011019285     PISSN: 1750743X     EISSN: 17507448     Source Type: Journal    
DOI: 10.2217/imt-2016-0112     Document Type: Review

References (101)

1. Pages F, Galon J, Dieu-Nosjean MC, Tartour E, Sautes- Fridman C, Fridman WH. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 29(8), 1093-1102 (2009).
2. Mitchison NA. Passive transfer of transplantation immunity. Nature 171(4345), 267-268 (1953).
3. Fefer A, Einstein AB, Cheever MA. Adoptive chemoimmunotherapy of cancer in animals: a review of results, principles, and problems. Ann. NY Acad. Sci. 277(1), 492-504 (1976).
4. Robb RJ, Kutny RM, Chowdhry V. Purification and partial sequence analysis of human T-cell growth factor. Proc. Natl Acad. Sci. USA 80(19), 5990-5994 (1983).
5. Rosenberg SA, Barry JM. The Transformed Cell: Unlocking the Mysteries of Cancer. Putnam Adult, NY, USA (1992).
6. Aldesleukin Product Approval Information - Licensing Action. www.fda.gov/Drugs/DevelopmentApprovalProcess/.HowDrugsareDevelopedandApproved/.ApprovalApplications/TherapeuticBiologicApplications/.ucm080733.htm
7. Rosenberg SA, Spiess P, Lafreniere R. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 233(4770), 1318-1321 (1986).
8. Brandes L, Galton DaG, Wiltshaw E. Originally published as Volume 2, Issue 7719 New approach to immunotherapy of melanoma. Lancet 298(7719), 293-295 (1971).
9. McPeak CJ. Intralymphatic therapy with immune lymphocytes. Cancer 28(5), 1126-1128 (1971).
10. Atkins MB, Lotze MT, Dutcher JP, et al. High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J. Clin. Oncol. 17(7), 2105 (1999).
11. Atkins MB, Kunkel L, Sznol M, Rosenberg SA. High-dose recombinant interleukin-2 therapy in patients with metastatic melanoma: long-Term survival update. Cancer J. Sci. Am. 6 (Suppl. 1), S11-S14 (2000).
12. Topalian SL, Solomon D, Avis FP, et al. Immunotherapy of patients with advanced cancer using tumor-infiltrating lymphocytes and recombinant interleukin-2: a pilot study. J. Clin. Oncol. 6(5), 839-853 (1988).
13. Rosenberg SA, Packard BS, Aebersold PM, et al. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N. Engl. J. Med. 319(25), 1676-1680 (1988).
14. Rosenberg SA, Yannelli JR, Yang JC, et al. Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J. Natl Cancer Inst. 86(15), 1159-1166 (1994).
15. Slavin S, Nagler A, Naparstek E, et al. Nonmyeloablative stem cell transplantation and cell therapy as an alternative to conventional bone marrow transplantation with lethal cytoreduction for the treatment of malignant and nonmalignant hematologic diseases. Blood 91(3), 756-763 (1998).
16. Dudley ME, Wunderlich JR, Yang JC, et al. A Phase I study of nonmyeloablative chemotherapy and adoptive transfer of autologous tumor antigen-specific T lymphocytes in patients with metastatic melanoma. J. Immunother. 25(3), 243-251 (2002).
17. Dudley ME, Wunderlich JR, Robbins PF, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298(5594), 850-854 (2002).
18. Dudley ME, Wunderlich JR, Yang JC, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J. Clin. Oncol. 23(10), 2346-2357 (2005).
19. Zaretsky JM, Garcia-Diaz A, Shin DS, et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N. Engl. J. Med. doi:10.1056/NEJMoa1604958 (2016) (Epub ahead of print).
20. Dudley ME, Yang JC, Sherry R, et al. Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 26(32), 5233-5239 (2008).
21. Gattinoni L, Finkelstein SE, Klebanoff CA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J. Exp. Med. 202(7), 907-912 (2005).
22. Goff SL, Dudley ME, Citrin DE, et al. Randomized, prospective evaluation comparing intensity of lymphodepletion before adoptive transfer of tumor-infiltrating lymphocytes for patients with metastatic melanoma. J. Clin. Oncol. 34(20), 2389-2397 (2016).
23. Antony PA, Piccirillo CA, Akpinarli A, et al. CD8+ T cell immunity against a tumor/self-Antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J. Immunol. 174(5), 2591-2601 (2005).
24. Paulos CM, Wrzesinski C, Kaiser A, et al. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J. Clin. Invest. 117(8), 2197-2204 (2007).
25. Sivan A, Corrales L, Hubert N, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350(6264), 1084- 1089 (2015).
26. Vetizou M, Pitt JM, Daillere R, et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350(6264), 1079-1084 (2015).
27. Fisher RI, Rosenberg SA, Fyfe G. Long-Term survival update for high-dose recombinant interleukin-2 in patients with renal cell carcinoma. Cancer J. Sci. Am. 6(Suppl. 1) S55-57 (2000).
28. Nishikawa H, Sakaguchi S. Regulatory T cells in cancer immunotherapy. Curr. Opin. Immunol. 27, 1-7 (2014).
29. Hirakawa M, Matos T, Liu H, et al. Low-dose IL-2 selectively activates subsets of CD4+ Tregs and NK cells. JCI Insight 1(18), e89278 (2016).
30. Goedegebuure PS, Douville LM, Li H, et al. Adoptive immunotherapy with tumor-infiltrating lymphocytes and interleukin-2 in patients with metastatic malignant melanoma and renal cell carcinoma: a pilot study. J. Clin. Oncol. 13(8), 1939-1949 (1995).
31. Ellebaek E, Iversen TZ, Junker N, et al. Adoptive cell therapy with autologous tumor infiltrating lymphocytes and low-dose Interleukin-2 in metastatic melanoma patients. J. Transl. Med. 10, 169 (2012).
32. Yee C, Thompson JA, Byrd D, et al. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc. Natl Acad. Sci. USA 99(25), 16168-16173 (2002).
33. Besser MJ, Shapira-Frommer R, Itzhaki O, et al. Adoptive transfer of tumor-infiltrating lymphocytes in patients with metastatic melanoma: intent-To-Treat analysis and efficacy after failure to prior immunotherapies. Clin. Cancer Res. 19(17), 4792-4800 (2013).
34. Joseph RW, Peddareddigari VR, Liu P, et al. Impact of clinical and pathologic features on tumor-infiltrating lymphocyte expansion from surgically excised melanoma metastases for adoptive T-cell therapy. Clin. Cancer Res. 17(14), 4882-4891 (2011).
35. Ben-Avi R, Itzhaki O, Simansky D, et al. Metastatic lung lesions as a preferred resection site for immunotherapy with tumor infiltrating lymphocytes. J. Immunother. 39(5), 218-222 (2016).
36. Goff SL, Smith FO, Klapper JA, et al. Tumor infiltrating lymphocyte therapy for metastatic melanoma: analysis of tumors resected for TIL. J. Immunother. 33(8), (2010).
37. Chacon JA, Pilon-Thomas S, Sarnaik AA, Radvanyi LG. Continuous 4-1BB co-stimulatory signals for the optimal expansion of tumor-infiltrating lymphocytes for adoptive T-cell therapy. Oncoimmunology 2(9), e25581 (2013).
38. Hernandez-Chacon JA, Li Y, Wu RC, et al. Costimulation through the CD137/4-1BB pathway protects human melanoma tumor-infiltrating lymphocytes from activation-induced cell death and enhances antitumor effector function. J. Immunother. 34(3), 236-250 (2011).
39. Liu S, Etto T, Rodriguez-Cruz T, et al. TGF-beta1 induces preferential rapid expansion and persistence of tumor antigen-specific CD8+ T cells for adoptive immunotherapy. J. Immunother. 33(4), 371-381 (2010).
40. Robbins PF, Dudley ME, Wunderlich J, et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J. Immunol. 173(12), 7125-7130 (2004).
41. Fisher B, Packard BS, Read EJ, et al. Tumor localization of adoptively transferred indium-111 labeled tumor infiltrating lymphocytes in patients with metastatic melanoma. J. Clin. Oncol. 7(2), 250-261 (1989).
42. Cole DJ, Taubenberger JK, Pockaj BA, et al. Histopathological analysis of metastatic melanoma deposits in patients receiving adoptive immunotherapy with tumor-infiltrating lymphocytes. Cancer Immunol. Immunother. 38(5), 299-303 (1994).
43. Pockaj BA, Sherry RM, Wei JP, et al. Localization of 111indium-labeled tumor infiltrating lymphocytes to tumor in patients receiving adoptive immunotherapy. Augmentation with cyclophosphamide and correlation with response. Cancer 73(6), 1731-1737 (1994).
44. Shen X, Zhou J, Hathcock KS, et al. Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J. Immunother. 30(1), 123-129 (2007).
45. Radvanyi LG, Bernatchez C, Zhang M, et al. Specific lymphocyte subsets predict response to adoptive cell therapy using expanded autologous tumor-infiltrating lymphocytes in metastatic melanoma patients. Clin. Cancer Res. 18(24), 6758-6770 (2012).
46. Heemskerk B, Liu K, Dudley ME, et al. Adoptive cell therapy for patients with melanoma, using tumor-infiltrating lymphocytes genetically engineered to secrete interleukin-2. Hum. Gene Ther. 19(5), 496-510 (2008).
47. Robbins PF, Kassim SH, Tran TL, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1- reactive T-cell receptor: long-Term follow-up and correlates with response. Clin. Cancer Res. 21(5), 1019-1027 (2014).
48. Dudley ME, Gross CA, Langhan MM, et al. CD8+ enriched "young" tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Clin. Cancer Res. 16(24), 6122-6131 (2010).
49. Donia M, Junker N, Ellebaek E, Andersen MH, Straten PT, Svane IM. Characterization and comparison of standard and young tumour-infiltrating lymphocytes for adoptive cell therapy at a Danish translational research institution. Scand. J. Immunol. 75(2), 157-167 (2012).
50. Dudley ME, Gross CA, Somerville RP, et al. Randomized selection design trial evaluating CD8+-enriched versus unselected tumor-infiltrating lymphocytes for adoptive cell therapy for patients with melanoma. J. Clin. Oncol. 31(17), 2152-2159 (2013).
51. Friedman KM, Prieto PA, Devillier LE, et al. Tumor-specific CD4+ melanoma tumor-infiltrating lymphocytes. J. Immunother. 35(5), 400-408 (2012).
52. Hunder NN, Wallen H, Cao J, et al. Treatment of metastatic melanoma with autologous CD4+ T Cells against NY-ESO-1. N. Engl. J. Med. 358(25), 2698-2703 (2008).
53. Chandran SS, Paria BC, Srivastava AK, Rothermel LD, Stephens DJ, Kammula US. Tumor-specific effector CD8+ T cells that can establish immunological memory in humans after adoptive transfer are marked by expression of IL7 receptor and c-myc. Cancer Res. 75(16), 3216-3226 (2015).
54. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4(12), 1191-1198 (2003).
55. Ilyas S, Yang JC. Landscape of tumor antigens in t cell immunotherapy. J. Immunol. 195(11), 5117-5122 (2015).
56. Morgan RA, Dudley ME, Wunderlich JR, et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314(5796), 126 (2006).
57. Johnson LA, Morgan RA, Dudley ME, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114(3), 535 (2009).
58. Morgan RA, Chinnasamy N, Abate-Daga DD, et al. Cancer regression and neurologic toxicity following anti-MAGE-A3 TCR gene therapy. J. Immunother. (Hagerstown, Md: 1997) 36(2), 133-151 (2013).
59. Robbins PF, Kassim SH, Tran TL, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1- reactive T-cell receptor: long-Term follow-up and correlates with response. Clin. Cancer Res. 21(5), 1019-1027 (2015).
60. Parkhurst MR, Yang JC, Langan RC, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther. 19(3), 620-626 (2011).
61. Linette GP, Stadtmauer EA, Maus MV, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 122(6), 863-871 (2013).
62. Robbins PF, Lu Y-C, El-Gamil M, et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 19(6), 747-752 (2013).
63. Tran E, Turcotte S, Gros A, et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science 344(6184), 641 (2014).
64. Shao H, Zhang W, Hu Q, Wu F, Shen H, Huang S. TCR mispairing in genetically modified T cells was detected by fluorescence resonance energy transfer. Mol. Biol. Rep. 37(8), 3951-3956 (2010).
65. Reuß S, Sebestyén Z, Heinz N, et al. TCR-engineered T cells: a model of inducible TCR expression to dissect the interrelationship between two TCRs. Eur. J. Immunol. 44(1), 265-274 (2014).
66. Bunse M, Bendle GM, Linnemann C, et al. RNAi-mediated TCR knockdown prevents autoimmunity in mice caused by mixed TCR dimers following TCR gene transfer. Mol. Ther. 22(11), 1983-1991 (2014).
67. Govers C, Sebestyã NZ, Roszik JN, et al. TCRs genetically linked to CD28 and CD3Îμ do not mispair with endogenous TCR chains and mediate enhanced T cell persistence and anti-melanoma activity. J. Immunol. 193(10), 5315-5326 (2014).
68. Peng W, Ye Y, Rabinovich BA, et al. Transduction of tumor-specific T cells with CXCR2 chemokine receptor improves migration to tumor and antitumor immune responses. Clin. Cancer Res. 16(22), 5458-5468 (2010).
69. Sapoznik S, Ortenberg R, Galore-Haskel G, et al. CXCR1 as a novel target for directing reactive T cells toward melanoma: implications for adoptive cell transfer immunotherapy. Cancer Immunol. Immunother. 61(10), 1833-1847 (2012).
70. Zhang L, Morgan RA, Beane JD, et al. Tumor-infiltrating lymphocytes genetically engineered with an inducible gene encoding interleukin-12 for the immunotherapy of metastatic melanoma. Clin. Cancer Res. 21(10), 2278-2288 (2015).
71. Pato A, Eisenberg G, Machlenkin A, et al. Messenger RNA encoding constitutively active Toll-like receptor 4 enhances effector functions of human T cells. Clin. Exp. Immunol. 182(2), 220-229 (2015).
72. Amos SM, Pegram HJ, Westwood JA, et al. Adoptive immunotherapy combined with intratumoral TLR agonist delivery eradicates established melanoma in mice. Cancer Immunol. Immunother. 60(5), 671-683 (2011).
73. 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. USA 86(24), 10024-10028 (1989).
74. Stancovski I, Schindler DG, Waks T, Yarden Y, Sela M, Eshhar Z. Targeting of T lymphocytes to Neu/HER2- expressing cells using chimeric single chain Fv receptors. J. Immunol. 151(11), 6577-6582 (1993).
75. Lee DW, Kochenderfer JN, Stetler-Stevenson M, et al. T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a Phase 1 dose-escalation trial. Lancet 385(9967), 517-528 (2015).
76. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 371(16), 1507-1517 (2014).
77. Brentjens RJ, Davila ML, Riviere I, et al. CD19-Targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 5(177), 177ra138 (2013).
78. Kochenderfer JN, Dudley ME, Kassim SH, et al. Chemotherapy-refractory diffuse large B-cell lymphoma and indolent B-cell malignancies can be effectively treated with autologous T cells expressing an anti-CD19 chimeric antigen receptor. J. Clin. Oncol. 33(6), 540-549 (2015).
79. Brudno JN, Somerville RPT, Shi V, et al. Allogeneic T cells that express an anti-CD19 chimeric antigen receptor induce remissions of B-cell malignancies that progress after allogeneic hematopoietic stem-cell transplantation without causing graft-versus-host disease. J. Clin. Oncol. 34(10), 1112-1121 (2016).
80. Yvon E, Del Vecchio M, Savoldo B, et al. Immunotherapy of metastatic melanoma using genetically engineered GD2- specific T cells. Clin. Cancer Res. 15(18), 5852-5860 (2009).
81. Prapa M, Caldrer S, Spano C, et al. A novel anti-GD2/4-1BB chimeric antigen receptor triggers neuroblastoma cell killing. Oncotarget 6(28), 24884-24894 (2015).
82. Lo AS, Ma Q, Liu DL, Junghans RP. Anti-GD3 chimeric sFv-CD28/T-cell receptor zeta designer T cells for treatment of metastatic melanoma and other neuroectodermal tumors. Clin. Cancer Res. 16(10), 2769-2780 (2010).
83. Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-Term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118(23), 6050-6056 (2011).
84. Morello A, Sadelain M, Adusumilli PS. Mesothelin-Targeted CARs: driving T cells to solid tumors. Cancer Discov. 6(2), 133-146 (2016).
85. Beatty GL, Haas AR, Maus MV, et al. Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce anti-Tumor activity in solid malignancies. Cancer Immunol. Res. 2(2), 112-120 (2014).
86. Janos Laszlo Tanyi, Andrew R Haas, Gregory Lawrence Beatty, et al. Anti-mesothelin chimeric antigen receptor T cells in patients with epithelial ovarian cancer. Presented at: 2016 ASCO Annual Meeting. J. Clin. Oncol. 34(Suppl. Abstract 5511) (2016).
87. Di Stasi A, Tey S-K, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365(18), 1673-1683 (2011).
88. Adusumilli PS, Cherkassky L, Villena-Vargas J, et al. Regional delivery of mesothelin-Targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity. Sci. Transl. Med. 6(261), 261ra151 (2014).
89. Katz SC, Burga RA, Mccormack E, et al. Phase I hepatic immunotherapy for metastases study of intra-Arterial chimeric antigen receptor-modified T-cell therapy for CEA+ liver metastases. Clin. Cancer Res. 21(14), 3149-3159 (2015).
90. Katz SC, Point GR, Cunetta M, et al. Regional CAR-T cell infusions for peritoneal carcinomatosis are superior to systemic delivery. Cancer Gene Ther. 23(5), 142-148 (2016).
91. Ma Q, Gomes EM, Lo AS, Junghans RP. Advanced generation anti-prostate specific membrane antigen designer T cells for prostate cancer immunotherapy. Prostate 74(3), 286-296 (2014).
92. Zuccolotto G, Fracasso G, Merlo A, et al. PSMA-specific CAR-engineered T cells eradicate disseminated prostate cancer in preclinical models. PLoS ONE 9(10), e109427 (2014).
93. Rafiq S, Dao T, Liu C, Scheinberg DA, Brentjens RJ. Engineered T cell receptor-mimic antibody, (TCRm) chimeric antigen receptor (CAR) T cells against the intracellular protein Wilms tumor-1 (WT1) for treatment of hematologic and solid cancers. Blood 124(21), 2155-2155 (2014).
94. Sommermeyer D, Hudecek M, Kosasih PL, et al. Chimeric antigen receptor-modified T cells derived from defined CD8+ and CD4+ subsets confer superior antitumor reactivity in vivo. Leukemia 30(2), 492-500 (2016).
95. Turtle CJ, Hanafi LL-AC, Berger C, et al. CD19 CAR-T cells of defined CD4+: CD8+ composition in adult B cell ALL patients. J. Clin. Invest. 126(6), 2123-2138 (2016).
96. Sabatino M, Hu J, Sommariva M, et al. Generation of clinical-grade CD19-specific CAR-modified CD8+ memory stem cells for the treatment of human B-cell malignancies. Blood 128(4), 519-528 (2016).
97. Savoldo B, Ramos CA, Liu E, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor modified T cells in lymphoma patients. J. Clin. Invest. 121(5), 1822-1826 (2011).
98. Imai C, Mihara K, Andreansky M, et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 18(4), 676-684 (2004).
99. Cherkassky L, Morello A, Villena-Vargas J, et al. Human CAR T cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated inhibition. J. Clin. Invest. 126(8), 3130-3144 (2016).
100. Bendle GM, Linnemann C, Bies L, Song JY, Schumacher TN. Blockade of TGF-beta signaling greatly enhances the efficacy of TCR gene therapy of cancer. J. Immunol. 191(6), 3232-3239 (2013).
101. Rosenberg SA, Yang JC, Sherry RM, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res. 17(13), 4550-4557 (2011).