Chimeric antigen receptor T-cell therapy to target hematologic malignancies

Cancer Research

Volumn 74, Issue 22, 2014, Pages 6383-6389

  Kenderian, Saad Sirop ^a,b   Ruella, Marco ^a   Gill, Saar ^a,c   Kalos, Michael ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MAYO CLINIC   (United States)

^c HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^d ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; HYBRID PROTEIN;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; B LYMPHOCYTE; CELLULAR IMMUNITY; GENETIC ENGINEERING; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOTHERAPY; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR IMMUNITY; CLINICAL TRIAL (TOPIC); HEMATOLOGIC NEOPLASMS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PROCEDURES;

CLINICAL TRIALS AS TOPIC; GENETIC ENGINEERING; HEMATOLOGIC NEOPLASMS; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

EID: 84918558415     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1530     Document Type: Review

References (52)

1. Kalos M, June CH. Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 2013;39:49-60.
2. Thomas E, Buckner C, Clift R, Fefer A, Johnson F, Neiman P, et al. Marrow transplantation for acute nonlymphoblastic leukemia in first remission. N Engl J Med 1979;301:597-9.
3. Heslop HE, Slobod KS, Pule MA, Hale GA, Rousseau A, Smith CA, et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 2010;115:925-35.
4. Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol 2005;23:2346-57.
5. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013;369:122-33.
6. Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan D-AN, Feldman SA, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther 2011;19:620-6.
7. Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood 2013;122:863-71.
8. Cameron BJ, Gerry AB, Dukes J, Harper JV, Kannan V, Bianchi FC, et al. Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med 2013;5:197ra103.
9. Kahlon KS, Brown C, Cooper LJN, Raubitschek A, Forman SJ, Jensen MC. Specific recognition and killing of glioblastoma multiforme by interleukin 13-zetakine redirected cytolytic T cells specific recognition and killing of glioblastoma multiforme by interleukin 13- zetakine redirected cytolytic T cells. Cancer Res 2004;64:9160-6.
10. 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;86:10024-8.
11. Till BG, Jensen MC, Wang J, Chen EY, Wood BL, Greisman HA, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 2008;112:2261-71.
12. 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;20:70-5.
13. Milone MC, Fish JD, Carpenito C, Carroll RG, Binder GK, Teachey D, et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 2009;17:1453-64.
14. Till BG, Jensen MC, Wang J, Qian X, Gopal AK, Maloney DG, et al. CD20-specific adoptive immunotherapy for lymphoma using a chimeric antigen receptor with both CD28 and 4-1BB domains: pilot clinical trial results. Blood 2012;119:3940-50.
15. Zhong X-S, Matsushita M, Plotkin J, Riviere I, Sadelain M. Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3kinase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol Ther 2010;18:413-20.
16. Haso W, Lee DW, Shah NN, Stetler-Stevenson M, Yuan CM, Pastan IH, et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood 2013;121:1165-74.
17. Pulè M a, Straathof KC, Dotti G, Heslop HE, Rooney CM, Brenner MK. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther 2005;12:933-41.
18. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 2013;5:177ra38.
19. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, Maric I, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood 2012;119:2709-20.
20. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011;365:725-33.
21. Savoldo B, Ramos CA, Liu E, Mims MP, Keating MJ, Carrum G, et al. Brief report CD28 costimulation improves expansion and persistence of chimeric antigen receptor - modified T cells in lymphoma patients. J Clin Invest 2011;121:1822-6.
22. Cruz CRY, 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;122:2965-73.
23. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric Antigen Receptor-Modified T Cells for Acute Lymphoid Leukemia. N Engl J Med 2013;368:1509-18.
24. Scholler J, Brady TL, Binder-Scholl G, Hwang W-T, Plesa G, Hege KM, et al. Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells. Sci Transl Med 2012;4:132ra53.
25. Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996;272:263-7.
26. Ellis J. Silencing and variegation of gammaretrovirus and lentivirus vectors. Hum Gene Ther 2005;16:1241-6.
27. Kebriaei P, Huls H, Jena B, Munsell M, Jackson R, Lee DA, et al. Infusing CD19-directed T cells to augment disease control in patients undergoing autologous hematopoietic stem-cell transplantation for advanced B-lymphoid malignancies. Hum Gene Ther 2012;23:444-50.
28. Zhao Y, Moon E, Carpenito C, Paulos CM, Liu X. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res 2010;70:9053-61.
29. Beatty GL, Haas AR, Maus MV, Torigian DA, Soulen MC, Plesa G, et al. Mesothelin-specific chimeric antigen receptor mRNA-engineered T cells induce anti-tumor activity in solid malignancies. Cancer Immunol Res 2014;2:112-20.
30. Berger C, Jensen MC, Lansdorp PM, Gough M, Elliott C, Riddell SR. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J Clin Invest 2008;118:294-305.
31. Riddell SR, Sommermeyer D, Berger C, Liu LS, Balakrishnan A, Salter A, et al. Adoptive therapy with chimeric antigen. Cancer J 2014;20:141-4.
32. Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012;12:269-81.
33. 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;17:1290-7.
34. Davila ML, Riviere I, Wang X, Bartido S, Park J, Curran K, et al. Efficacy and toxicity management of 19-28z CAR T cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med 2014;6:224ra25.
35. 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;3:95ra73-95ra73.
36. Milone MC, Fish JD, Carpenito C, Carroll RG, Binder GK, Teachey D, et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 2009;17:1453-64.
37. Giordano Attianese GMP, Marin V, Hoyos V, Savoldo B, Pizzitola I, Tettamanti S, et al. In vitro and in vivo model of a novel immunotherapy approach for chronic lymphocytic leukemia by anti-CD23 chimeric antigen receptor. Blood 2011;117:4736-45.
38. Mihara K, Yanagihara K, Takigahira M, Kitanaka M, Imai C. Synergistic and persistent effect of T-cell immunotherapy with anti-CD19 or anti-CD38 chimeric receptor in conjunction with rituximab on B-cell non-Hodgkin lymphoma. Br J Haematol 2010;151:37-46.
39. Hudecek M, Schmitt TM, Baskar S, Lupo-stanghellini MT, Nishida T, Yamamoto TN, et al. The B-cell tumor - associated antigen ROR1 can be targeted with T cells modified to express a ROR1-specific chimeric antigen receptor. Blood 2010;116:4532-41.
40. Ramos CA, Savoldo B, Liu E, Gee A, Mei Z, Grilley BJ, et al. Clinical responses in patients infused with T lymphocytes redirected to target kappa-light immunoglobulin chain. Am Soc Hematol Annu Meet Proc 2013;20:S26.
41. Lamers CH, Sleijfer S, van Steenbergen S, van Elzakker P, van Krimpen B, Groot C, et al. Treatment of metastatic renal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity. Mol Ther 2013;21:904-12.
42. 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. Mol Ther 2010;18:843-51.
43. Carpenter RO, Evbuomwan MO, Pittaluga S, Rose JJ, Raffeld M, Yang S, et al. B-cell maturation antigen is a promising target for adoptive T-cell therapy of multiple myeloma. Clin Cancer Res 2013;19:2048-60.
44. Imai C, Mihara K, Andreansky M, Nicholson IC, Pui C-H, Geiger TL, et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004;18:676-84.
45. Chu J, He S, Deng Y, Zhang J, Peng Y, Hughes T, et al. Genetic modification of T cells redirected towards CS1 enhances eradication of myeloma cells. Clin Cancer Res 2014;20:3989-4000
46. Savoldo B, Rooney CM, Di Stasi A, Abken H, Hombach A, Foster AE, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 2007;110:2620-30.
47. Ritchie DS, Neeson PJ, Khot A, Peinert S, Tai T, Tainton K, et al. Persistence and efficacy of second generation CAR T Cell against the LeY antigen in acute myeloid leukemia. Mol Ther 2013;21:2122-9.
48. Casucci M, Nicolis B, Falcone L, Camisa B, Norelli M, Genovese P, et al. myeloid leukemia and multiple myeloma CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood 2013;122:3461-72.
49. Gill S, Tasian SK, Ruella M, Shestova O, Li Y, Porter DL, et al. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 2014;123:2343-54.
50. Mardiros A, Dos Santos C, McDonald T, Brown CE, Wang X, Budde LE, et al. T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and anti-tumor effects against human acute myeloid leukemia. Blood 2013;122:3138-48.
51. 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;31:71-5.
52. Fedorov VD, Themeli M, Sadelain M. PD-1 - and CTLA-4 - based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses. Sci Transl Med 2013;5:215ra172.