Chimeric antigen receptor-redirected T cells return to the bench

Seminars in Immunology

Volumn 28, Issue 1, 2016, Pages 3-9

  Geldres, Claudia ^a   Savoldo, Barbara ^b   Dotti, Gianpietro ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Adoptive immunotherapy; Chimeric antigen receptor

Indexed keywords

CHIMERIC ANTIGEN RECEPTOR; CANCER VACCINE; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; T LYMPHOCYTE RECEPTOR;

CANCER IMMUNOTHERAPY; CANCER PATIENT; CELL SURVIVAL; CYTOKINE RELEASE SYNDROME; HUMAN; REVIEW; SOLID TUMOR; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; ADOPTIVE IMMUNOTHERAPY; CELL CULTURE TECHNIQUE; GENE THERAPY; GENETICS; IMMUNOLOGY; METABOLISM; NEOPLASM; PROCEDURES; TRANSPLANTATION;

CANCER VACCINES; CELL CULTURE TECHNIQUES; GENETIC THERAPY; HUMANS; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES;

EID: 84954304691     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2015.12.001     Document Type: Review

References (74)

1. Ramos C.A., Savoldo B., Dotti G. CD19-CAR trials. Cancer J. 2014, 20(March (2)):112-118.
2. Kochenderfer J.N., Rosenberg S.A. Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat. Rev. Clin. Oncol. 2013, 10(May (5)):267-276.
3. Maude S.L., Teachey D.T., Porter D.L., Grupp S.A. CD19-targeted chimeric antigen receptor T-cell therapy for acute lymphoblastic leukemia. Blood 2015, 125(June (26)):4017-4023.
4. Sadelain M., Brentjens R., Riviere I., Park J. CD19 CAR therapy for acute lymphoblastic leukemia. Am. Soc. Clin. Oncol. Educ. Book 2015, 35:e360-e363.
5. Pule M.A., Savoldo B., Myers G.D., Rossig C., Russell H.V., 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(November (11)):1264-1270.
6. Louis C.U., Savoldo B., Dotti G., Pule M., Yvon E., Myers G.D., et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 2011, 118(December (23)):6050-6056.
7. Eshhar Z., Waks T., Gross G., Schindler D.G. 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. 1993, 90(January (2)):720-724.
8. Sadelain M., Brentjens R., Riviere I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013, 3(April (4)):388-398.
9. Dotti G., Gottschalk S., Savoldo B., Brenner M.K. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol. Rev. 2014, 257(January (1)):107-126.
10. Molhoj M., Degan F.D. Leader sequences are not signal peptides. Nat. Biotechnol. 2004, 22(December (12)):1502.
11. Nicholson I.C., Lenton K.A., Little D.J., Decorso T., Lee F.T., Scott A.M., et al. Construction and characterisation of a functional CD19 specific single chain Fv fragment for immunotherapy of B lineage leukaemia and lymphoma. Mol. Immunol. 1997, 34(November (16-17)):1157-1165.
12. Hombach A., Heuser C., Sircar R., Tillmann T., Diehl V., Pohl C., et al. Characterization of a chimeric T-cell receptor with specificity for the Hodgkin's lymphoma-associated CD30 antigen. J. Immunother. 1999, 22(November (6)):473-480.
13. 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(December (12)):3890-3897.
14. Rossig C., Bollard C.M., Nuchtern J.G., Merchant D.A., Brenner M.K. Targeting of G(D2)-positive tumor cells by human T lymphocytes engineered to express chimeric T-cell receptor genes. Int. J. Cancer 2001, 94(October (2)):228-236.
15. Alonso-Camino V., Sanchez-Martin D., Compte M., Sanz L., Alvarez-Vallina L. Lymphocyte display: a novel antibody selection platform based on T cell activation. PLoS One 2009, 4(9):e7174.
16. Hudecek M., Lupo-Stanghellini M.T., Kosasih P.L., Sommermeyer D., Jensen M.C., 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(June (12)):3153-3164.
17. Hombach A., Koch D., Sircar R., Heuser C., Diehl V., Kruis W., et al. A chimeric receptor that selectively targets membrane-bound carcinoembryonic antigen (mCEA) in the presence of soluble CEA. Gene Ther. 1999, 6(February (2)):300-304.
18. Hassan R., Bera T., Pastan I. Mesothelin: a new target for immunotherapy. Clin. Cancer Res. 2004, 10(June (12 Pt 1)):3937-3942.
19. Long A.H., Haso W.M., Shern J.F., Wanhainen K.M., Murgai M., Ingaramo M., et al. 4-1BB costimulation ameliorates T cell exhaustion induced by tonic signaling of chimeric antigen receptors. Nat. Med. 2015, 21(June (6)):581-590.
20. Frigault M.J., Lee J., Basil M.C., Carpenito C., Motohashi S., Scholler J., et al. Identification of chimeric antigen receptors that mediate constitutive or inducible proliferation of T cells. Cancer Immunol. Res. 2015, 3(April (4)):356-367.
21. Milone M.C., Fish J.D., Carpenito C., Carroll R.G., Binder G.K., 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(August (8)):1453-1464.
22. Maus M.V., Haas A.R., Beatty G.L., Albelda S.M., Levine B.L., Liu X., et al. T cells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol. Res. 2013, 1(July (1)):26-31.
23. Savoldo B., Ramos C.A., Liu E., Mims M.P., Keating M.J., 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(May (5)):1822-1826.
24. Guest R.D., Hawkins R.E., Kirillova N., Cheadle E.J., Arnold J., O'Neill A., 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. 2005, 28(May (3)):203-211.
25. Haso W., Lee D.W., Shah N.N., Stetler-Stevenson M., Yuan C.M., Pastan I.H., et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood 2013, 121(February (7)):1165-1174.
26. Hombach A., Hombach A.A., 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(October (10)):1206-1213.
27. Hudecek M., Sommermeyer D., Kosasih P.L., Silva-Benedict A., Liu L., Rader C., et al. The nonsignaling extracellular spacer domain of chimeric antigen receptors is decisive for in vivo antitumor activity. Cancer Immunol. Res. 2015, 3(February (2)):125-135.
28. Imai C., Mihara K., Andreansky M., Nicholson I.C., Pui C.H., Geiger T.L., et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004, 18(April (4)):676-684.
29. Maher J., Brentjens R.J., Gunset G., Riviere I., Sadelain M. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRzeta/CD28 receptor. Nat. Biotechnol. 2002, 20(January (1)):70-75.
30. Finney H.M., Akbar A.N., Lawson A.D. 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(January (1)):104-113.
31. Finney H.M., Lawson A.D., Bebbington C.R., Weir A.N. Chimeric receptors providing both primary and costimulatory signaling in T cells from a single gene product. J. Immunol. 1998, 161(September (6)):2791-2797.
32. Pule M.A., Straathof K.C., Dotti G., Heslop H.E., Rooney C.M., Brenner M.K. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol. Ther. 2005, 12(November (5)):933-941.
33. Carpenito C., Milone M.C., Hassan R., Simonet J.C., Lakhal M., Suhoski M.M., 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. 2009, 106(March (9)):3360-3365.
34. Brentjens R.J., Davila M.L., Riviere I., Park J., Wang X., Cowell L.G., et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci. Transl. Med. 2013, 5(March 177):177ra38.
35. Lee D.W., Kochenderfer J.N., Stetler-Stevenson M., Cui Y.K., Delbrook C., Feldman S.A., 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 2015, 385(February (9967)):517-528.
36. Kochenderfer J.N., Dudley M.E., Kassim S.H., Somerville R.P., Carpenter R.O., Stetler-Stevenson M., 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. 2015, 33(February (6)):540-549.
37. Maude S.L., Frey N., Shaw P.A., Aplenc R., Barrett D.M., Bunin N.J., et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N. Engl. J. Med. 2014, 371(October (16)):1507-1517.
38. Singh H., Manuri P.R., Olivares S., Dara N., Dawson M.J., Huls H., et al. Redirecting specificity of T-cell populations for CD19 using the Sleeping Beauty system. Cancer Res. 2008, 68(April (8)):2961-2971.
39. Schumann K., Lin S., Boyer E., Simeonov D.R., Subramaniam M., Gate R.E., et al. Generation of knock-in primary human T cells using Cas9 ribonucleoproteins. Proc. Natl. Acad. Sci. U. S. A. 2015, 112(August (33)):10437-10442.
40. Powell D.J., Dudley M.E., Robbins P.F., Rosenberg S.A. Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 2005, 105(January (1)):241-250.
41. Jin J., Sabatino M., Somerville R., Wilson J.R., Dudley M.E., Stroncek D.F., et al. Simplified method of the growth of human tumor infiltrating lymphocytes in gas-permeable flasks to numbers needed for patient treatment. J. Immunother. 2012, 35(April (3)):283-292.
42. Gattinoni L., Klebanoff C.A., Palmer D.C., Wrzesinski C., Kerstann K., Yu Z., et al. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J. Clin. Invest. 2005, 115(June (6)):1616-1626.
43. Gattinoni L., Zhong X.S., Palmer D.C., Ji Y., Hinrichs C.S., Yu Z., et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 2009, 15(July (7)):808-813.
44. Xu Y., Zhang M., Ramos C.A., Durett A., Liu E., Dakhova O., et al. Closely related T-memory stem cells correlate with in vivo expansion of CAR.CD19-T cells and are preserved by IL-7 and IL-15. Blood 2014, 123(June (24)):3750-3759.
45. 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(January (4)):573-584.
46. Wang X., Berger C., Wong C.W., Forman S.J., Riddell S.R., Jensen M.C. Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. Blood 2011, 117(February (6)):1888-1898.
47. Cruz C.R., Micklethwaite K.P., Savoldo B., Ramos C.A., 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(October (17)):2965-2973.
48. Imai C., Iwamoto S., Campana D. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood 2005, 106(July (1)):376-383.
49. Rischer M., Pscherer S., Duwe S., Vormoor J., Jurgens H., Rossig C. Human gammadelta T cells as mediators of chimaeric-receptor redirected anti-tumour immunity. Br. J. Haematol. 2004, 126(August (4)):583-592.
50. Heczey A., Liu D., Tian G., Courtney A.N., Wei J., Marinova E., et al. Invariant NKT cells with chimeric antigen receptor provide a novel platform for safe and effective cancer immunotherapy. Blood 2014, 124(October (18)):2824-2833.
51. Geldres C., Savoldo B., Hoyos V., Caruana I., Zhang M., Yvon E., et al. T lymphocytes redirected against the chondroitin sulfate proteoglycan-4 control the growth of multiple solid tumors both in vitro and in vivo. Clin. Cancer Res. 2014, 20(February (4)):962-971.
52. Ahmed N., Brawley V.S., Hegde M., Robertson C., Ghazi A., Gerken C., et al. Human epidermal growth factor receptor 2 (HER2)-specific chimeric antigen receptor-modified T cells for the immunotherapy of HER2-positive sarcoma. J. Clin. Oncol. 2015, 33(May (15)):1688-1696.
53. Di Stasi A., De Angelis B., Rooney C.M., Zhang L., Mahendravada A., Foster A.E., et al. T lymphocytes coexpressing CCR4 and a chimeric antigen receptor targeting CD30 have improved homing and antitumor activity in a Hodgkin tumor model. Blood 2009, 113(June (25)):6392-6402.
54. Craddock J.A., Lu A., Bear A., Pule M., Brenner M.K., Rooney C.M., et al. Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J. Immunother. 2010, 33(October (8)):780-788.
55. Caruana I., Savoldo B., Hoyos V., Weber G., Liu H., Kim E.S., et al. Heparanase promotes tumor infiltration and antitumor activity of CAR-redirected T lymphocytes. Nat. Med. 2015, 21(May (5)):524-529.
56. Nishio N., Diaconu I., Liu H., Cerullo V., Caruana I., Hoyos V., et al. Armed oncolytic virus enhances immune functions of chimeric antigen receptor-modified T cells in solid tumors. Cancer Res. 2014, 74(September (18)):5195-5205.
57. Hoyos V., Savoldo B., Quintarelli C., Mahendravada A., Zhang M., Vera J., et al. Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 2010, 24(June (6)):1160-1170.
58. Markley J.C., Sadelain M. IL-7 and IL-21 are superior to IL-2 and IL-15 in promoting human T cell-mediated rejection of systemic lymphoma in immunodeficient mice. Blood 2010, 115(April (17)):3508-3519.
59. Perna S.K., De A.B., Pagliara D., Hasan S.T., Zhang L., Mahendravada A., et al. Interleukin 15 provides relief to CTLs from regulatory T cell-mediated inhibition: implications for adoptive t cell-based therapies for lymphoma. Clin. Cancer Res. 2013, 19(January (1)):106-117.
60. Perna S.K., Pagliara D., Mahendravada A., Liu H., Brenner M.K., Savoldo B., et al. Interleukin-7 mediates selective expansion of tumor-redirected cytotoxic T lymphocytes (CTLs) without enhancement of regulatory T-cell inhibition. Clin. Cancer Res. 2014, 20(January (1)):131-139.
61. Chmielewski M., Kopecky C., Hombach A.A., Abken H. IL-12 release by engineered T cells expressing chimeric antigen receptors can effectively Muster an antigen-independent macrophage response on tumor cells that have shut down tumor antigen expression. Cancer Res. 2011, 71(September (17)):5697-5706.
62. Koneru M., Purdon T.J., Spriggs D., Koneru S., Brentjens R.J. IL-12 secreting tumor-targeted chimeric antigen receptor T cells eradicate ovarian tumors. Oncoimmunology 2015, 4(March (3)):e994446.
63. Chinnasamy D., Yu Z., Kerkar S.P., Zhang L., Morgan R.A., Restifo N.P., et al. Local delivery of interleukin-12 using T cells targeting VEGF receptor-2 eradicates multiple vascularized tumors in mice. Clin. Cancer Res. 2012, 18(March (6)):1672-1683.
64. Prosser M.E., Brown C.E., Shami A.F., Forman S.J., Jensen M.C. Tumor PD-L1 co-stimulates primary human CD8(+) cytotoxic T cells modified to express a PD1:CD28 chimeric receptor. Mol. Immunol. 2012, 51(July (3-4)):263-272.
65. Morgan R.A., Yang J.C., Kitano M., Dudley M.E., Laurencot C.M., Rosenberg S.A. 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(April (4)):843-851.
66. Beatty G.L., Haas A.R., Maus M.V., Torigian D.A., Soulen M.C., 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(February (2)):112-120.
67. 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(November (18)):1673-1683.
68. Wang X., Chang W.C., Wong C.W., Colcher D., Sherman M., Ostberg J.R., et al. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood 2011, 118(August (5)):1255-1263.
69. Kloss C.C., 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(January (1)):71-75.
70. Fedorov V.D., 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(December (215)). 215ra172.
71. Davila M.L., 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(February (224)). 224ra25.
72. Zhou X., Dotti G., Krance R.A., Martinez C.A., Naik S., Kamble R.T., et al. Inducible caspase-9 suicide gene controls adverse effects from alloreplete T cells after haploidentical stem cell transplantation. Blood 2015, 125(June (26)):4103-4113.
73. Straathof K.C., Pule M.A., Yotnda P., Dotti G., Vanin E.F., Brenner M.K., et al. An inducible caspase 9 safety switch for T-cell therapy. Blood 2005, 105(June (11)):4247-4254.
74. Wu C.Y., Roybal K.T., Puchner E.M., Onuffer J., Lim W.A. Remote control of therapeutic T cells through a small molecule-gated chimeric receptor. Science 2015, 350(October (6258)). aab4077.