Driving CAR-based T-cell therapy to success

Current Hematologic Malignancy Reports

Volumn 9, Issue 1, 2014, Pages 50-56

  Jena, Bipulendu ^a   Moyes, Judy S ^a   Huls, Helen ^a   Cooper, Laurence J N ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

B cell malignancies; Chimeric antigen receptor; Gene therapy; T cell therapy

Indexed keywords

CD137 ANTIGEN; CD19 ANTIGEN; CD28 ANTIGEN; CD8ALPHA ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; FC RECEPTOR; HYBRID PROTEIN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G4; LENTIVIRUS VECTOR; MONOCLONAL ANTIBODY; RETROVIRUS VECTOR; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; T LYMPHOCYTE RECEPTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ACUTE LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; B CELL LEUKEMIA; CELL THERAPY; CHRONIC LEUKEMIA; CLINICAL TRIAL (TOPIC); GENE TARGETING; HUMAN; IMMUNOTHERAPY; LEUKEMIA; NONHUMAN; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSPOSON; VIRAL GENE DELIVERY SYSTEM;

ANTIGENS, CD19; CLINICAL TRIALS AS TOPIC; GENETIC ENGINEERING; HEMATOLOGIC NEOPLASMS; HUMANS; IMMUNOTHERAPY; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

EID: 84896728443     PISSN: 15588211     EISSN: 1558822X     Source Type: Journal    
DOI: 10.1007/s11899-013-0197-7     Document Type: Review

References (53)

1. .•• Savoldo B, Ramos CA, Liu E, Mims MP, Keating MJ, Carrum G, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest. 2011;121:1822-6. Clinical trial showed that second generation CAR performed better in terms of in vivo expansion and persistence than first generation CAR in a competitive repopulation experiment.
2. Jena B, Dotti G, Cooper LJ. Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. Blood. 2010;116:1035-44.
3. Suhoski MM, Golovina TN, Aqui NA, Tai VC, Varela-Rohena A, Milone MC, et al. Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol Ther. 2007;15:981-8. (Pubitemid 46621657)
4. 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.
5. Hombach A, Wieczarkowiecz A, Marquardt T, Heuser C, Usai L, Pohl C, 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. 2001;167:6123-31. (Pubitemid 33081538)
6. Hudecek M, Lupo-Stanghellini M-T, Kosasih PL, Sommermeyer D, Jensen MC, Rader C, et al. Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clin Cancer Res. 2013;19: 3153 -64.
7. Grada Z, Hegde M, Byrd T, Shaffer DR, Ghazi A, Brawley VS, et al. TanCAR: a novel bispecific Chimeric antigen receptor for cancer immunotherapy. Mol Ther Nucl Acids. 2013;2:e105-e.
8. Choi BD, Gedeon PC, Kuan C-T, Sanchez-Perez L, Archer GE, Bigner DD, et al. Rational design and generation of recombinant control reagents for bispecific antibodies through CDR mutagenesis. J Immunol Methods. 2013;395:14-20.
9. .• 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. First clinical report to describe antigen escape and emergence of CD19neg variants in response to CAR-mediated T-cell therapy.
10. 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.
11. .• 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. Case report of a serious adverse event attributed to the use of a third generation CAR that resulted in the death of a patient.
12. Lamers CHJ, 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.
13. Di Stasi A, Tey S-K, Dotti G, Fujita Y, Kennedy-Nasser A, Martinez C, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med. 2011;365:1673-83.
14. Barrett DM, Zhao Y, Liu X, Jiang S, Carpenito C, Kalos M, et al. Treatment of advanced leukemia in mice with mRNA engineered T cells. Hum Gene Ther. 2011;22:1575-86.
15. .•• 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-+. A report that showed CARs could combine signaling to target tumors positive for two different antigens.
16. Lanitis E, Poussin M, Klattenhoff AW, Song D, Sandaltzopoulos R, June CH, 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.
17. + CLL due to their persistence and functioning as serial killers.
18. Brentjens R, Yeh R, Bernal Y, Riviere I, Sadelain M. Treatment of chronic lymphocytic leukemia with genetically targeted autologous T cells: case report of an unforeseen adverse event in a phase I clinical trial. Mol Ther. 2010;18:666-8.
19. Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood. 2010;116: 4099-102.
20. Vera J, Savoldo B, Vigouroux S, Biagi E, Pule M, Rossig C, et al. T lymphocytes redirected against the kappa light chain of human immunoglobulin efficiently kill mature B lymphocyte-derived malignant cells. Blood. 2006;108:3890-7. (Pubitemid 44864573)
21. Cooper LJ, Topp MS, Serrano LM, Gonzalez S, Chang WC, Naranjo A, et al. T-cell clones can be rendered specific for CD19: toward the selective augmentation of the graft-versus-B-lineage leukemia effect. Blood. 2003;101:1637-44. (Pubitemid 36182545)
22. Jensen MC, Popplewell L, Cooper LJ, DiGiusto D, Kalos M, Ostberg JR, et al. Antitransgene rejection responses contribute to attenuated persistence of adoptively transferred CD20/CD19-specific chimeric antigen receptor redirected T cells in humans. Biol Blood Marrow Transplant. 2010;16:1245-56.
23. Hombach A, Hombach AA, Abken H. 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. 2010;17:1206-13.
24. Armour KL, Clark MR, Hadley AG, Williamson LM. Recombinant human IgG molecules lacking Fc gamma receptor I binding and monocyte triggering activities. Eur J Immunol. 1999;29:2613-24. (Pubitemid 29378132)
25. Reddy MP, Kinney CAS, Chaikin MA, Payne A, Fishman-Lobell J, Tsui P, et al. Elimination of Fc receptor-dependent effector functions of a modified IgG4 monoclonal antibody to human CD4. J Immunol. 2000;164:1925-33. (Pubitemid 30108747)
26. Jefferis R. Glycosylation as a strategy to improve antibody-based therapeutics. Nat Rev Drug Discov. 2009;8:226-34.
27. Davila ML, Brentjens R, Wang X, Riviere I, Sadelain M. How do CARs work? Early insights from recent clinical studies targeting CD19. Oncoimmunology. 2012;1:1577-83.
28. Kalos M, June CH. Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity. 2013;39:49-60.
29. Kochenderfer JN, Rosenberg SA. Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat Rev Clin Oncol. 2013;10:267-76.
30. Maiti SN, Huls H, Singh H, Dawson M, Figliola M, Olivares S, et al. Sleeping beauty systemto redirect T-cell specificity for human applications. J Immunother. 2013;36:112-23.
31. Jena B, Maiti S, Huls H, Singh H, Lee DA, Champlin RE, et al. Chimeric antigen receptor (CAR)-specific monoclonal antibody to detect CD19-specific Tcells in clinical trials. Plos One. 2013;8:e57838.
32. Kochenderfer JN, Dudley ME, Carpentor RO, Kassim SH. Donor-derived CD19-targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood. 2013;122(25):4129-39.
33. Davila ML, Kloss CC, Gunset G, Sadelain M. CD19 CAR-targeted T cells induce long-term remission and B cell aplasia in an immunocompetent mouse model of B cell acute lymphoblastic leukemia. Plos One. 2013;8:e61338.
34. Restifo NP, Gattinoni L. Lineage relationship of effector and memory T cells. Curr Opin Immunol. 2013;25:556-63.
35. Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat Rev Cancer. 2012;12:671-84.
36. .• Cieri N, Camisa B, Cocchiarella F, Forcato M, Oliveira G, Provasi E, et al. IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood. 2013;121:573-84. This study showed that a memory stem-cell like CD8+ Tcell population could be generated from naïve precursor cells in vitro and this has translational appeal.
37. Gattinoni L, Restifo NP. Moving T memory stem cells to the clinic. Blood. 2013;121:567-8.
38. Izhak L, Ambrosino E, Kato S, Parish ST, O'Konek JJ, Weber H, et al. Delicate balance among three types of T cells in concurrent regulation of tumor immunity. Cancer Res. 2013;73:1514-23.
39. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480:480-9.
40. Shin JH, Park HB, Oh YM, Lim DP, Lee JE, Seo HH, et al. Positive conversion of negative signaling of CTLA4 potentiates antitumor efficacy of adoptive T-cell therapy in murine tumor models. Blood. 2012;119:5678-87.
41. Prosser ME, Brown CE, Shami AF, Forman SJ, Jensen MC. Tumor PD-L1 co-stimulates primary human CD8(+) cytotoxic T cells modified to express a PD1:CD28 chimeric receptor. Mol Immunol. 2012;51:263-72.
42. Ankri C, Shamalov K, Horovitz-Fried M, Mauer S, Cohen CJ. Human T cells engineered to express a programmed death 1/28 costimulatory retargeting molecule display enhanced antitumor activity. J Immunol. 2013;191:4121-9.
43. 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.
44. Hackett PB, Largaespada DA, Cooper LJ. A transposon and transposase system for human application. Mol Ther. 2010;18: 674-83.
45. .• Singh H, Manuri PR, Olivares S, Dara N, Dawson MJ, Huls H, et al. Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res. 2008;68:2961-71. Non-viral vectors such as the transposon based Sleeping Beauty system were shown as alternatives to commonly used viral vectors such as gammaretrovirus or lentivirus for genetic modification of T cells. (Pubitemid 351556297)
46. Fukuda T, Chen L, Endo T, Tang L, Lu D, Castro JE, et al. Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal, antigen and receptor for Wnt5a. Proc Natl Acad Sci U S A. 2008;105:3047-52. (Pubitemid 351723665)
47. Zhang S, Chen L, Wang-Rodriguez J, Zhang L, Cui B, Frankel W, et al. The onco-embryonic antigen ROR1 is expressed by a variety of human cancers. Am J Pathol. 2012;181:1903-10.
48. Hinrichs CS, Restifo NP. Reassessing target antigens for adoptive T-cell therapy. Nat Biotechnol. 2013;31:999-1008.
49. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008;14:1264-70.
50. O'Connor CM, Sheppard S, Hartline CA, Huls H, Johnson M, Palla SL, et al. Adoptive T-cell therapy improves treatment of canine non-Hodgkin lymphoma post chemotherapy. Sci Rep. 2012;2:249.
51. Liadi I, Roszik J, Romain G, Cooper LJN, Varadarajan N. Quantitative high-throughput single-cell cytotoxicity assay for T cells. J Vis Exp: JoVE. 2013:e50058-e.
52. Varadarajan N, Kwon DS, Law KM, Ogunniyi AO, Anahtar MN, Richter JM, et al. Rapid, efficient functional characterization and recovery of HIV-specific human CD8(+) T cells using microengraving. Proc Natl Acad Sci U S A. 2012;109: 3885-90.
53. Dominguez MH, Chattopadhyay PK, Ma S, Lamoreaux L, McDavid A, Finak G, et al. Highly multiplexed quantitation of gene expression on single cells. J Immunol Methods. 2013;391: 133-45.