Murine allogeneic CD19 CAR T cells harbor potent antileukemic activity but have the potential to mediate lethal GVHD

Blood

Volumn 127, Issue 10, 2016, Pages 1361-1370

  Jacoby, Elad ^a   Yang, Yinmeng ^a   Qin, Haiying ^a   Chien, Christopher D ^a   Kochenderfer, James N ^b   Fry, Terry J ^a  

^a Oncology Branch   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; INTERLEUKIN 6; CASR PROTEIN, MOUSE; G PROTEIN COUPLED RECEPTOR; HYBRID PROTEIN;

ACUTE GRAFT VERSUS HOST DISEASE; ACUTE LYMPHOBLASTIC LEUKEMIA; ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CELL EXPANSION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DONOR LYMPHOCYTE INFUSION; EFFECTOR CELL; GRAFT VERSUS HOST REACTION; IMMUNOCOMPETENCE; LEUKEMIA RELAPSE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; ALLOGRAFT; ANIMAL; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE TRANSFUSION; PATHOLOGY; TRANSPLANTATION;

ALLOGRAFTS; ANIMALS; ANTIGENS, CD19; GRAFT VS HOST DISEASE; INTERLEUKIN-6; LYMPHOCYTE TRANSFUSION; MICE; MICE, KNOCKOUT; NEOPLASMS, EXPERIMENTAL; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECEPTORS, G-PROTEIN-COUPLED; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

EID: 84960517214     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-08-664250     Document Type: Article

References (44)

1. Bhojwani D, Pui C-H. Relapsed childhood acute lymphoblastic leukaemia. Lancet Oncol. 2013; 14(6):e205-e217.
2. Satwani P, Sather H, Ozkaynak F, et al. Allogeneic bone marrow transplantation in first remission for children with ultra-high-risk features of acute lymphoblastic leukemia: A children's oncology group study report. Biol Blood Marrow Transplant. 2007;13(2): 218-227.
3. Pulsipher MA, Peters C, Pui CH. High-risk pediatric acute lymphoblastic leukemia: To transplant or not to transplant? Biol Blood Marrow Transplant. 2011;17(suppl 1): S137-S148.
4. Raetz EA, Bhatla T. Where do we stand in the treatment of relapsed acute lymphoblastic leukemia? Hematology Am Soc Hematol Educ Program. 2012;2012:129-136.
5. Fry TJ, Willasch A, Bader P. The graft-versustumor effect in pediatric malignancy. Pediatr Clin North Am. 2010;57(1):67-81.
6. Pulsipher MA, Langholz B, Wall DA, et al. The addition of sirolimus to tacrolimus/methotrexate GVHD prophylaxis in children with ALL: A phase 3 Children's Oncology Group/Pediatric Blood and Marrow Transplant Consortium trial. Blood. 2014; 123(13):2017-2025.
7. Horowitz MM, Gale RP, Sondel PM, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75(3): 555-562.
8. Collins RH Jr, Shpilberg O, Drobyski WR, et al. Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. J Clin Oncol. 1997; 15(2):433-444.
9. Schmid C, Labopin M, Nagler A, et al; EBMT Acute Leukemia Working Party. Donor lymphocyte infusion in the treatment of first hematological relapse after allogeneic stem-cell transplantation in adults with acute myeloid leukemia: A retrospective risk factors analysis and comparison with other strategies by the EBMT Acute Leukemia Working Party. J Clin Oncol. 2007;25(31):4938-4945.
10. Levine JE, Barrett AJ, Zhang M-J, et al. Donor leukocyte infusions to treat hematologic malignancy relapse following allo-SCT in a pediatric population. Bone Marrow Transplant. 2008;42(3):201-205.
11. Kochenderfer JN, Rosenberg SA. Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors. Nat Rev Clin Oncol. 2013; 10(5):267-276.
12. Sadelain M, Brentjens R, Riviere I. The basic principles of chimeric antigen receptor design. Cancer Discov. 2013;3(4):388-398.
13. Maus MV, Grupp SA, Porter DL, June CH. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood. 2014; 123(17):2625-2635.
14. Mackall CL, Merchant MS, Fry TJ. Immune-based therapies for childhood cancer. Nat Rev Clin Oncol. 2014;11(12):693-703.
15. Lee DW, Kochenderfer JN, Stetler-Stevenson M, 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(9967): 517-528.
16. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med. 2014;371(16): 1507-1517.
17. 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(224): 224ra25.
18. Cruz CRY, Micklethwaite KP, Savoldo B, 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(17): 2965-2973.
19. Kochenderfer JN, Dudley ME, Carpenter RO, et al. Donor-derived CD19-Targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood. 2013;122(25): 4129-4139.
20. Capitini CM, Herby S, Milliron M, Anver MR, Mackall CL, Fry TJ. Bone marrow deficient in IFN-gamma signaling selectively reverses GVHD-Associated immunosuppression and enhances a tumor-specific GVT effect. Blood. 2009;113(20):5002-5009.
21. Capitini CM, Nasholm NM, Duncan BB, Guimond M, Fry TJ. Graft-versus-host disease impairs vaccine responses through decreased CD41 and CD81 T cell proliferation and increased perforinmediated CD81 T cell apoptosis. J Immunol. 2013;190(3):1351-1359.
22. Capitini CM, Nasholm NM, Chien CD, et al. Absence of STAT1 in donor-derived plasmacytoid dendritic cells results in increased STAT3 and attenuates murine GVHD. Blood. 2014;124(12):1976-1986.
23. Shand JC, Qin H, Nasholm N, Capitini CM, Fry TJ. Minor antigen distribution predicts sitespecific graft-versus-Tumor activity of adoptively transferred, minor antigen-specific CD8 T Cells. Biol Blood Marrow Transplant. 2014;20(1): 26-36.
24. Bijl J, Sauvageau M, Thompson A, Sauvageau G. High incidence of proviral integrations in the Hoxa locus in a new model of E2a-PBX1-induced B-cell leukemia. Genes Dev. 2005; 19(2):224-233.
25. Kochenderfer JN, Yu Z, Frasheri D, Restifo NP, Rosenberg SA. Adoptive transfer of syngeneic T cells transduced with a chimeric antigen receptor that recognizes murine CD19 can eradicate lymphoma and normal B cells. Blood. 2010;116(19):3875-3886.
26. Cooke KR, Kobzik L, Martin TR, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-3239.
27. Gattinoni L, Finkelstein SE, Klebanoff CA, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD81 T cells. J Exp Med. 2005;202(7):907-912.
28. Wrzesinski C, Paulos CM, Kaiser A, et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells. J Immunother. 2010;33(1):1-7.
29. Brochu S, Rioux-Mass̈e B, Roy J, Roy DC, Perreault C. Massive activation-induced cell death of alloreactive T cells with apoptosis of bystander postthymic T cells prevents immune reconstitution in mice with graft-versus-host disease. Blood. 1999;94(2):390-400.
30. Dey B, Yang Y-G, Preffer F, et al. The fate of donor T-cell receptor transgenic T cells with known host antigen specificity in a graft-versushost disease model. Transplantation. 1999; 68(1):141-149.
31. Meunier MC, Roy-Proulx G, Labrecque N, Perreault C. Tissue distribution of target antigen has a decisive influence on the outcome of adoptive cancer immunotherapy. Blood. 2003; 101(2):766-770.
32. Alpdogan SÖ , Lu SX, Patel N, et al. Rapidly proliferating CD44hi peripheral T cells undergo apoptosis and delay posttransplantation T-cell reconstitution after allogeneic bone marrow transplantation. Blood. 2008;112(12): 4755-4764.
33. Capitini CM, Davis JPE, Larabee SM, Herby S, Nasholm NM, Fry TJ. Extracorporeal photopheresis attenuates murine graft-versushost disease via bone marrow-derived interleukin-10 and preserves responses to dendritic cell vaccination. Biol Blood Marrow Transplant. 2011; 17(6):790-799.
34. Tawara I, Koyama M, Liu C, et al. Interleukin-6 modulates graft-versus-host responses after experimental allogeneic bone marrow transplantation. Clin Cancer Res. 2011;17(1): 77-88.
35. Baker MB, Riley RL, Podack ER, Levy RB. Graft-versus-host-disease-Associated lymphoid hypoplasia and B cell dysfunction is dependent upon donor T cell-mediated Fas-ligand function, but not perforin function. Proc Natl Acad Sci USA. 1997;94(4):1366-1371.
36. Lee DW, Gardner R, Porter DL, et al. Current concepts in the diagnosis and management of cytokine release syndrome [published correction appears in Blood. 2015;126(8):1048]. Blood. 2014;124(2):188-195.
37. Cooke KR, Gerbitz A, Crawford JM, et al. LPS antagonism reduces graft-versus-host disease and preserves graft-versus-leukemia activity after experimental bone marrow transplantation. J Clin Invest. 2001;107(12):1581-1589.
38. Gartlan KH, Markey KA, Varelias A, et al. Tc17 cells are a proinflammatory, plastic lineage of pathogenic CD81 T cells that induce GVHD without antileukemic effects. Blood. 2015;126(13): 1609-1620.
39. Brentjens RJ, Santos E, Nikhamin Y, et al. Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin Cancer Res. 2007;13(18 pt 1): 5426-5435.
40. Haso W, Lee DW, Shah NN, et al. Anti-CD22-chimeric antigen receptors targeting B-cell precursor acute lymphoblastic leukemia. Blood. 2013;121(7):1165-1174.
41. Singh N, Liu X, Hulitt J, et al. Nature of tumor control by permanently and transiently modified GD2 chimeric antigen receptor T cells in xenograft models of neuroblastoma. Cancer Immunol Res. 2014;2(11):1059-1070.
42. Chan WK, Suwannasaen D, Throm RE, et al. Chimeric antigen receptor-redirected CD45RAnegative T cells have potent antileukemia and pathogen memory response without graft-versushost activity. Leukemia. 2015;29(2):387-395.
43. Kennedy GA, Varelias A, Vuckovic S, et al. Addition of interleukin-6 inhibition with tocilizumab to standard graft-versus-host disease prophylaxis after allogeneic stem-cell transplantation: A phase 1/2 trial. Lancet Oncol. 2014;15(13):1451-1459.
44. Fisher DT, Appenheimer MM, Evans SS. The two faces of IL-6 in the tumor microenvironment. Semin Immunol. 2014;26(1):38-47.