Chimeric antigen receptor t-cells: New approaches to improve their efficacy and reduce toxicity

Cancer Journal (United States)

Volumn 21, Issue 6, 2015, Pages 475-479

  Maus, Marcela V ^a,b   Powell, Daniel J ^b,c  

^a Division of Hematology Oncology   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Adoptive transfer; Chimeric antigen receptor; Genetic engineering; Immunotherapy; T cell; Toxicity

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

CANCER IMMUNOTHERAPY; CELL PROLIFERATION; CELL THERAPY; CONDITIONING; ENGRAFTMENT; GENETIC ENGINEERING; HEALTH CARE ACCESS; HOST; HUMAN; PRIORITY JOURNAL; REVIEW; RISK REDUCTION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; THERAPY EFFECT; ADOPTIVE IMMUNOTHERAPY; IMMUNOLOGY; PROCEDURES;

GENETIC ENGINEERING; HUMANS; IMMUNOTHERAPY, ADOPTIVE; RECEPTORS, ANTIGEN, T-CELL;

EID: 84948404186     PISSN: 15289117     EISSN: 1540336X     Source Type: Journal    
DOI: 10.1097/PPO.0000000000000155     Document Type: Review

References (52)

1. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T-cells for sustained remissions in leukemia. N Engl JMed. 2014; 371: 1507-1517.
2. Lamers CH, Sleijfer S, van Steenbergen S, et al. Treatment ofmetastatic renal cell carcinoma with CAIX CAR-engineered T-cells: clinical evaluation and management of on-target toxicity. Mol Ther. 2013; 21: 904-912.
3. Morgan RA, Yang JC, Kitano M, et al. 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: 843-851.
4. 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. 2004; 173: 7125-7130.
5. Muranski P, Boni A, Wrzesinski C, et al. Increased intensity lymphodepletion and adoptive immunotherapy-how far can we go? Nat Clin Pract Oncol. 2006; 3: 668-681.
6. + T-cells. J Exp Med. 2005; 202: 907-912.
7. +) T-cells after allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2015; 21: 1721-1731.
8. Ries CH, Cannarile MA, Hoves S, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell. 2014; 25: 846-859.
9. Yu J, Du W, Yan F, et al. Myeloid-derived suppressor cells suppress antitumor immune responses through IDO expression and correlate with lymph node metastasis in patients with breast cancer. J Immunol. 2013; 190: 3783-3797.
10. Dubovsky JA, Beckwith KA, Natarajan G, et al. Ibrutinib is an irreversible molecular inhibitor of ITK driving a TH1-selective pressure in T lymphocytes. Blood. 2013; 122: 2539-2549.
11. Ninomiya S, Narala N, Huye L, et al. Tumor indoleamine 2, 3-dioxygenase (IDO) inhibits CD19-CART-cells and is downregulated by lymphodepleting drugs. Blood. 2015; 125: 3905-3916.
12. Song DG, Ye Q, Santoro S, et al. Chimeric NKG2D CAR-expressing Tcell-mediated attack of human ovarian cancer is enhanced by histone deacetylase inhibition. Hum Gene Ther. 2013; 24: 295-305.
13. 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. 2011; 121: 1822-1826.
14. Davila ML, Riviere I, Wang X, et al. Efficacy and toxicity management of 19-28z CAR T-cell therapy in B cell acute lymphoblastic leukemia. Sci Transl Med. 2014; 6: 224ra225.
15. Long AH, Haso WM, Shern JF, et al. 4-1BB costimulation ameliorates T-cell exhaustion induced by tonic signaling of chimeric antigen receptors. Nat Med. 2015; 21: 581-590.
16. Song DG, Ye Q, Poussin M, et al. CD27 costimulation augments the survival and antitumor activity of redirected human T-cells in vivo. Blood. 2012; 119: 696-706.
17. Kalos M, Levine BL, Porter DL, et al. T-cells with chimeric antigen receptors have potent antitumor effects and can establishmemory in patientswith advanced leukemia. Sci Transl Med. 2011; 3: 95ra73.
18. Finney HM, Akbar AN, Lawson AD. Activation of resting human primary T-cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCR zeta chain. J Immunol. 2004; 172: 104-113.
19. Pulè MA, Straathof KC, Dotti G, et al. A chimeric T-cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T-cells. Mol Ther. 2005; 12: 933-941.
20. Paulos CM, Carpenito C, Plesa G, et al. The inducible costimulator (ICOS) is critical for the development of human T(H)17 cells. Sci Transl Med. 2010; 2: 55ra78.
21. Guedan S, Chen X, Madar A, et al. ICOS-based chimeric antigen receptors program bipolar TH17/TH1 cells. Blood. 2014; 124: 1070-1080.
22. + T-cell-mediated tumor eradication. Mol Ther. 2010; 18: 413-420.
23. Hombach AA, Rappl G, Abken H. Arming cytokine-induced killer cells with chimeric antigen receptors: CD28 outperforms combined CD28- OX40 "super-stimulation". Mol Ther. 2013; 21: 2268-2277.
24. Guedan S, McGettigan SE, Posey AD Jr, et al. Enhancing T-cell persistence of CAR-redirected T-cells in solid tumors. J Immunother Cancer. 2014; 2 (suppl 3): P244.
25. Wilkie S, van Schalkwyk MC, Hobbs S, et al. Dual targeting of ErbB2 and MUC1 in breast cancer using chimeric antigen receptors engineered to provide complementary signaling. J Clin Immunol. 2012; 32: 1059-1070.
26. Lanitis E, Poussin M, Klattenhoff AW, et al. Chimeric antigen receptor T-cells with dissociated signaling domains exhibit focused antitumor activity with reduced potential for toxicity in vivo. Cancer Immunol Res. 2013; 1: 43-53.
27. Kloss CC, Condomines M, Cartellieri M, et al. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T-cells. Nat Biotechnol. 2013; 31: 71-75.
28. Condomines M, Zhao Z, Wang X, et al. 4-1BBL costimulation enables CD4 T-cells expressing a CD28/zeta chimeric antigen receptor to eliminate aggressive leukemia. The J Immunol. 2013; 190.
29. Wang E, Wang LC, Tsai CY, et al. Generation of potent T-cell immunotherapy for cancer using DAP12-based, multichain, chimeric immunoreceptors. Cancer Immunol Res. 2015; 3: 815-826.
30. Condomines M, Arnason J, Benjamin R, et al. Tumor-targeted human T-cells expressing CD28-based chimeric antigen receptors circumvent CTLA-4 inhibition. PLoS One. 2015; 10: e0130518.
31. Adusumilli PS, Cherkassky L, Villena-Vargas J, et al. Regional delivery of mesothelin-targeted CAR T-cell therapy generates potent and longlasting CD4-dependent tumor immunity. Sci Transl Med. 2014; 6: 261ra151.
32. Moon EK, Carpenito C, Sun J, et al. Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T-cells expressing a mesothelin-specific chimeric antibody receptor. Clin Cancer Res. 2011; 17: 4719-4730.
33. Caruana I, Savoldo B, Hoyos V, et al. Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes. Nat Med. 2015; 21: 524-529.
34. Lo A, Wang LC, Scholler J, et al. Tumor-promoting desmoplasia is disrupted by depleting FAP-expressing stromal cells. Cancer Res. 2015; 75: 2800-2810.
35. Santoro SP, KimS, Motz GT, et al. T-cells bearing a chimeric antigen receptor against prostate-specific membrane antigen mediate vascular disruption and result in tumor regression. Cancer Immunol Res. 2015; 3: 68-84.
36. Chinnasamy D, Tran E, Yu Z, et al. Simultaneous targeting of tumor antigens and the tumor vasculature using T lymphocyte transfer synergize to induce regression of established tumors in mice. Cancer Res. 2013; 73: 3371-3380.
37. Sallusto F, Langenkamp A, Geginat J, et al. Functional subsets of memory T-cells identified by CCR7 expression. Curr TopMicrobiol Immunol. 2000; 251: 167-171.
38. + T-cells derived from centralmemory cells establishes persistent T-cell memory in primates. J Clin Invest. 2008; 118: 294-305.
39. Gattinoni L, Lugli E, Ji Y, et al. A human memory T-cell subset with stem cell-like properties. Nat Med. 2011; 17: 1290-1297.
40. MausMV, Grupp SA, Porter DL, et al. Antibody-modified T-cells: CARs take the front seat for hematologic malignancies. Blood. 2014; 123: 2625-2635.
41. Dotti G, Gottschalk S, Savoldo B, et al. Design and development of therapies using chimeric antigen receptor-expressing T-cells. Immunol Rev. 2014; 257: 107-126.
42. + T-cells. J Immunol. 2015; 194: 911-920.
43. Song DG, Ye Q, Poussin M, et al. A fully human chimeric antigen receptor with potent activity against cancer cells but reduced risk for offtumor toxicity. In: Oncotarget. 2015; 6: 21533-21546.
44. Cameron BJ, Gerry AB, Dukes J, 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.
45. Lee DW, Gardner R, Porter DL, et al. Current concepts in the diagnosis and management of cytokine release syndrome. Blood. 2014; 124: 188-195.
46. Munshi NC, Govindarajan R, Drake R, et al. Thymidine kinase (TK) gene-transduced human lymphocytes can be highly purified, remain fully functional, and are killed efficiently with ganciclovir. Blood. 1997; 89: 1334-1340.
47. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl JMed. 2011; 365: 1673-1683.
48. Philip B, Kokalaki E, Mekkaoui L, et al. A highly compact epitope-based marker/suicide gene for easier and safer T-cell therapy. Blood. 2014; 124: 1277-1287.
49. Wang X, Chang WC, Wong CW, et al. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood. 2011; 118: 1255-1263.
50. 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.
51. Poirot L, Philip B, Schiffer-Mannioui C, et al. Multiplex genome-edited T-cell manufacturing platform for "off-the-shelf " adoptive T-cell immunotherapies. Cancer Res. 2015; 75: 3853-3864.
52. Urbanska K, Lanitis E, Poussin M, et al. A universal strategy for adoptive immunotherapy of cancer through use of a novel T-cell antigen receptor. In: Cancer Res. 2012; 72: 1844-1852.