Adoptive T Cell Therapies: A Comparison of T Cell Receptors and Chimeric Antigen Receptors

Trends in Pharmacological Sciences

Volumn 37, Issue 3, 2016, Pages 220-230

  Harris, Daniel T ^a   Kranz, David M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

CAR; cell therapies; gene therapies; immunotherapy; receptors; TCR

Indexed keywords

B7 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; DNA; LYMPHOCYTE ANTIGEN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN; NIMOTUZUMAB; T LYMPHOCYTE RECEPTOR; HYBRID PROTEIN;

ADOPTIVE TRANSFER; ANTIGEN RECOGNITION; ANTINEOPLASTIC ACTIVITY; B CELL LEUKEMIA; B CELL LYMPHOMA; BINDING AFFINITY; CANCER REGRESSION; CLINICAL TRIAL (TOPIC); DNA MODIFICATION; GENE TRANSFER; HEMATOLOGIC MALIGNANCY; HUMAN; LYMPHOCYTE TRANSFER; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING; RECEPTOR DENSITY; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIRAL GENE DELIVERY SYSTEM; ADOPTIVE IMMUNOTHERAPY; ANIMAL; COMPARATIVE STUDY; GENETICS; IMMUNOLOGY; NEOPLASMS; PROCEDURES;

ANIMALS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

EID: 84958744448     PISSN: 01656147     EISSN: 18733735     Source Type: Journal    
DOI: 10.1016/j.tips.2015.11.004     Document Type: Review

References (98)

1. C.H. June, and et al. Adoptive cellular therapy: a race to the finish line Sci. Transl. Med. 7 2015 280ps287
2. I.M. Stromnes, and et al. Re-adapting T cells for cancer therapy: from mouse models to clinical trials Immunol. Rev. 257 2014 145 164
3. K.J. Curran, and R.J. Brentjens Chimeric antigen receptor T cells for cancer immunotherapy J. Clin. Oncol. 33 2015 1703 1706
4. M. Sadelain, and et al. CD19 CAR therapy for acute lymphoblastic leukemia Am. Soc. Clin. Oncol. Educ. Book 35 2015 e360 e363
5. M.C. Jensen, and S.R. Riddell Designing chimeric antigen receptors to effectively and safely target tumors Curr. Opin. Immunol. 33 2015 9 15
6. J. Zikherman, and B. Au-Yeung The role of T cell receptor signaling thresholds in guiding T cell fate decisions Curr. Opin. Immunol. 33 2015 43 48
7. M.G. Rudolph, and et al. How TCRs bind MHCs, peptides, and coreceptors Annu. Rev. Immunol. 24 2006 419 466
8. M.M. Davis, and et al. Dynamics of cell surface molecules during T cell recognition Annu. Rev. Biochem. 72 2003 717 742
9. M.E. Birnbaum, and et al. Molecular architecture of the alphabeta T cell receptor-CD3 complex Proc. Natl. Acad. Sci. U.S.A. 111 2014 17576 17581
10. E.N. Kersh, and et al. Fidelity of T cell activation through multistep T cell receptor zeta phosphorylation Science 281 1998 572 575
11. D.J. Irvine, and et al. Direct observation of ligand recognition by T cells Nature 419 2002 845 849
12. M.A. Purbhoo, and et al. T cell killing does not require the formation of a stable mature immunological synapse Nat. Immunol. 5 2004 524 530
13. Y. Sykulev, and et al. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response Immunity 4 1996 565 571
14. J. Huang, and et al. A single peptide-major histocompatibility complex ligand triggers digital cytokine secretion in CD4(+) T cells Immunity 39 2013 846 857
15. M.N. Artyomov, and et al. CD4 and CD8 binding to MHC molecules primarily acts to enhance Lck delivery Proc. Natl. Acad. Sci. U.S.A. 107 2010 16916 16921
16. Q.J. Li, and et al. CD4 enhances T cell sensitivity to antigen by coordinating Lck accumulation at the immunological synapse Nat. Immunol. 5 2004 791 799
17. L.I. Ehrlich, and et al. Dynamics of p56lck translocation to the T cell immunological synapse following agonist and antagonist stimulation Immunity 17 2002 809 822
18. P.W. Kim, and et al. A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8 Science 301 2003 1725 1728
19. J. Casas, and et al. Ligand-engaged TCR is triggered by Lck not associated with CD8 coreceptor Nat. Commun. 5 2014 5624
20. P.A. van der Merwe, and O. Dushek Mechanisms for T cell receptor triggering Nat. Rev. Immunol. 11 2011 47 55
21. P.P. Yachi, and et al. Nonstimulatory peptides contribute to antigen-induced CD8-T cell receptor interaction at the immunological synapse Nat. Immunol. 6 2005 785 792
22. M. Krogsgaard, and et al. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity Nature 434 2005 238 243
23. N. Anikeeva, and et al. Quantum dot/peptide-MHC biosensors reveal strong CD8-dependent cooperation between self and viral antigens that augment the T cell response Proc. Natl. Acad. Sci. U.S.A. 103 2006 16846 16851
24. C. Xu, and et al. Regulation of T cell receptor activation by dynamic membrane binding of the CD3epsilon cytoplasmic tyrosine-based motif Cell 135 2008 702 713
25. D. Gil, and et al. Recruitment of Nck by CD3 epsilon reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation Cell 109 2002 901 912
26. L. Kjer-Nielsen, and et al. Crystal structure of the human T cell receptor CD3 epsilon gamma heterodimer complexed to the therapeutic mAb OKT3 Proc. Natl. Acad. Sci. U.S.A. 101 2004 7675 7680
27. T. Beddoe, and et al. Antigen ligation triggers a conformational change within the constant domain of the alphabeta T cell receptor Immunity 30 2009 777 788
28. S.T. Kim, and et al. The alphabeta T cell receptor is an anisotropic mechanosensor J. Biol. Chem. 284 2009 31028 31037
29. Y.C. Li, and et al. Cutting Edge: mechanical forces acting on T cells immobilized via the TCR complex can trigger TCR signaling J. Immunol. 184 2010 5959 5963
30. S.J. Davis, and P.A. van der Merwe The kinetic-segregation model: TCR triggering and beyond Nat. Immunol. 7 2006 803 809
31. J.R. James, and R.D. Vale Biophysical mechanism of T-cell receptor triggering in a reconstituted system Nature 487 2012 64 69
32. D.L. Mueller, and et al. Clonal expansion versus functional clonal inactivation: a costimulatory signalling pathway determines the outcome of T cell antigen receptor occupancy Annu. Rev. Immunol. 7 1989 445 480
33. R.J. Greenwald, and et al. The B7 family revisited Annu. Rev. Immunol. 23 2005 515 548
34. J.S. Boomer, and J.M. Green An enigmatic tail of CD28 signaling Cold Spring Harb. Perspect. Biol. 2 2010 a002436
35. S.V. Janardhan, and et al. Evidence implicating the Ras pathway in multiple CD28 costimulatory functions in CD4+ T cells PLoS ONE 6 2011 e24931
36. M. Croft The role of TNF superfamily members in T-cell function and diseases Nat. Rev. Immunol. 9 2009 271 285
37. D.M. Pardoll The blockade of immune checkpoints in cancer immunotherapy Nat. Rev. Cancer 12 2012 252 264
38. T. Blankenstein, and et al. Targeting cancer-specific mutations by T cell receptor gene therapy Curr. Opin. Immunol. 33 2015 112 119
39. Z. Eshhar, and et al. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors Proc. Natl. Acad. Sci. U.S.A. 90 1993 720 724
40. M.J. Frigault, and et al. Identification of chimeric antigen receptors that mediate constitutive or inducible proliferation of T cells Cancer Immunol. Res. 3 2015 356 367
41. A.H. Long, and et al. 4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors Nat. Med. 21 2015 581 590
42. A. Hombach, and et al. Adoptive immunotherapy with genetically engineered T cells: modification of the IgG1 Fc 'spacer' domain in the extracellular moiety of chimeric antigen receptors avoids 'off-target' activation and unintended initiation of an innate immune response Gene Ther. 17 2010 1206 1213
43. M. Hudecek, and et al. The nonsignaling extracellular spacer domain of chimeric antigen receptors is decisive for in vivo antitumor activity Cancer Immunol. Res. 3 2015 125 135
44. M. Hudecek, and et al. Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells Clin. Cancer Res. 19 2013 3153 3164
45. R.D. Guest, and et al. The role of extracellular spacer regions in the optimal design of chimeric immune receptors: evaluation of four different scFvs and antigens J. Immunother. 28 2005 203 211
46. H. Shi, and et al. Improving the efficacy and safety of engineered T cell therapy for cancer Cancer Lett. 328 2013 191 197
47. T. Zhang, and et al. An NKp30-based chimeric antigen receptor promotes T cell effector functions and antitumor efficacy in vivo J. Immunol. 189 2012 2290 2299
48. M.A. Pule, and et al. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells Mol. Ther. 12 2005 933 941
49. J.S. Bridgeman, and et al. The optimal antigen response of chimeric antigen receptors harboring the CD3zeta transmembrane domain is dependent upon incorporation of the receptor into the endogenous TCR/CD3 complex J. Immunol. 184 2010 6938 6949
50. B.G. Till, and et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells Blood 112 2008 2261 2271
51. A. Hombach, and et al. Tumor-specific T cell activation by recombinant immunoreceptors: CD3 zeta signaling and CD28 costimulation are simultaneously required for efficient IL-2 secretion and can be integrated into one combined CD28/CD3 zeta signaling receptor molecule J. Immunol. 167 2001 6123 6131
52. S. Tammana, and et al. 4-1BB and CD28 signaling plays a synergistic role in redirecting umbilical cord blood T cells against B-cell malignancies Hum. Gene Ther. 21 2010 75 86
53. C. Imai, and et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia Leukemia 18 2004 676 684
54. J. Maher, and et al. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta/CD28 receptor Nat. Biotechnol. 20 2002 70 75
55. C.M. Kowolik, and et al. CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells Cancer Res. 66 2006 10995 11004
56. D.G. Song, and et al. In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4-1BB) Cancer Res. 71 2011 4617 4627
57. M.C. Milone, and et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo Mol. Ther. 17 2009 1453 1464
58. C. Carpenito, and et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains Proc. Natl. Acad. Sci. U.S.A. 106 2009 3360 3365
59. X.S. Zhong, and et al. 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. 18 2010 413 420
60. C.C. Kloss, and et al. Combinatorial antigen recognition with balanced signaling promotes selective tumor eradication by engineered T cells Nat. Biotechnol. 31 2013 71 75
61. V.D. Fedorov, and et al. Novel approaches to enhance the specificity and safety of engineered T cells Cancer J. 20 2014 160 165
62. V.D. Fedorov, and et al. PD-1- and CTLA-4-based inhibitory chimeric antigen receptors (iCARs) divert off-target immunotherapy responses Sci. Transl. Med. 5 2013 215ra172
63. S. Valitutti, and et al. Serial triggering of many T-cell receptors by a few peptide-MHC complexes Nature 375 1995 148 151
64. P.D. Holler, and et al. TCRs with high affinity for foreign pMHC show self-reactivity Nat. Immunol. 4 2003 55 62
65. N.A. Bowerman, and et al. Engineering the binding properties of the T cell receptor:peptide:MHC ternary complex that governs T cell activity Mol. Immunol. 46 2009 3000 3008
66. A.S. Chervin, and et al. The impact of TCR-binding properties and antigen presentation format on T cell responsiveness J. Immunol. 183 2009 1166 1178
67. K. Watanabe, and et al. Target antigen density governs the efficacy of anti-CD20-CD28-CD3 zeta chimeric antigen receptor-modified effector CD8+ T cells J. Immunol. 194 2015 911 920
68. J.D. Stone, and et al. A sensitivity scale for targeting T cells with chimeric antigen receptors (CARs) and bispecific T-cell Engagers (BiTEs) Oncoimmunology 1 2012 863 873
69. M. Chmielewski, and et al. T cell activation by antibody-like immunoreceptors: increase in affinity of the single-chain fragment domain above threshold does not increase T cell activation against antigen-positive target cells but decreases selectivity J. Immunol. 173 2004 7647 7653
70. X. Liu, and et al. Affinity-tuned ErbB2 or EGFR chimeric antigen receptor T cells exhibit an increased therapeutic index against tumors in mice Cancer Res. 75 2015 3596 3607
71. H.G. Caruso, and et al. Tuning sensitivity of CAR to EGFR density limits recognition of normal tissue while maintaining potent antitumor activity Cancer Res. 75 2015 3505 3518
72. L.A. Johnson, and et al. Rational development and characterization of humanized anti-EGFR variant III chimeric antigen receptor T cells for glioblastoma Sci. Transl. Med. 7 2015 275ra222
73. B. Engels, and et al. Long-term persistence of CD4(+) but rapid disappearance of CD8(+) T cells expressing an MHC class I-restricted TCR of nanomolar affinity Mol. Ther. 20 2012 652 660
74. P.S. Adusumilli, and et al. Regional delivery of mesothelin-targeted CAR T cell therapy generates potent and long-lasting CD4-dependent tumor immunity Sci. Transl. Med. 6 2014 261ra151
75. R. Roychoudhuri, and et al. The interplay of effector and regulatory T cells in cancer Curr. Opin. Immunol. 33 2015 101 111
76. D.H. Aggen, and et al. Single-chain ValphaVbeta T-cell receptors function without mispairing with endogenous TCR chains Gene Ther. 19 2012 365 374
77. J.D. Stone, and et al. A novel T cell receptor single-chain signaling complex mediates antigen-specific T cell activity and tumor control Cancer Immunol. Immunother. 63 2014 1163 1176
78. D.L. Porter, and et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia N. Engl. J. Med. 365 2011 725 733
79. R.J. Brentjens, and et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia Sci. Transl. Med. 5 2013 177ra138
80. S.A. Grupp, and et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia N. Engl. J. Med. 368 2013 1509 1518
81. D.W. Lee, and 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 2015 517 528
82. S. Kakarla, and S. Gottschalk CAR T cells for solid tumors: armed and ready to go? Cancer J. 20 2014 151 155
83. C.H. Lamers, and et al. Treatment of metastatic renal cell carcinoma with CAIX CAR-engineered T cells: clinical evaluation and management of on-target toxicity Mol. Ther. 21 2013 904 912
84. J.R. Park, and et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma Mol. Ther. 15 2007 825 833
85. G.A. Rabinovich, and et al. Immunosuppressive strategies that are mediated by tumor cells Annu. Rev. Immunol. 25 2007 267 296
86. R.A. Morgan, and 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. 18 2010 843 851
87. R.A. Morgan, and et al. Cancer regression in patients after transfer of genetically engineered lymphocytes Science 314 2006 126 129
88. L.A. Johnson, and et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen Blood 114 2009 535 546
89. A.G. Chapuis, and et al. Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients Sci. Transl. Med. 5 2013 174ra127
90. P.F. Robbins, and 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 2015 1019 1027
91. P.F. Robbins, and et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1 J. Clin. Oncol. 29 2011 917 924
92. M. Aleksic, and et al. Different affinity windows for virus and cancer-specific T-cell receptors: implications for therapeutic strategies Eur. J. Immunol. 42 2012 3174 3179
93. P.D. Holler, and et al. In vitro evolution of a T cell receptor with high affinity for peptide/MHC Proc. Natl. Acad. Sci. U.S.A. 97 2000 5387 5392
94. Y. Li, and et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display Nat. Biotechnol. 23 2005 349 354
95. G.P. Linette, and et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma Blood 122 2013 863 871
96. R.A. Morgan, and et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy J. Immunother. 36 2013 133 151
97. J.D. Stone, and et al. TCR affinity for p/MHC formed by tumor antigens that are self-proteins: impact on efficacy and toxicity Curr. Opin. Immunol. 33 2015 16 22
98. K. Kudo, and et al. T lymphocytes expressing a CD16 signaling receptor exert antibody-dependent cancer cell killing Cancer Res. 74 2014 93 103