Chimeric antigen receptors against CD33/CD123 antigens efficiently target primary acute myeloid leukemia cells in vivo

Leukemia

Volumn 28, Issue 8, 2014, Pages 1596-1605

  Pizzitola, I ^a,b   Anjos Afonso, F ^b   Rouault Pierre, K ^b   Lassailly, F ^b   Tettamanti, S ^a   Spinelli, O ^c   Biondi, A ^a   Biagi, E ^a   Bonnet, D ^b  

^a SAN GERARDO HOSPITAL   (Italy)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c OSPEDALI RIUNITI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CELL LINE, TUMOR; CYTOKINE-INDUCED KILLER CELLS; HUMANS; INTERLEUKIN-3 RECEPTOR ALPHA SUBUNIT; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, SCID; RECEPTORS, ANTIGEN; RECOMBINANT FUSION PROTEINS; SIALIC ACID BINDING IG-LIKE LECTIN 3; T-LYMPHOCYTES;

EID: 84905714921     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2014.62     Document Type: Article

References (34)

1. Majeti R. Monoclonal antibody therapy directly against human acute myeloid leukemia stem cells. Oncogene 2011; 30: 1009-1019.
2. Horton S, Huntly B. Recent advances in acute myeloid leukemia stem cell biology. Haematologica 2012; 97: 966-974.
3. Lu PH, Negrin RS. A novel population of expanded human CD3+CD56+ cells derived from T cells with potent in vivo antitumor activity in mice with severe combined immunodeficiency. J Immunol 1994; 153: 1687-1696.
4. Franceschetti M, Pievani A, Borleri G, Vago L, Fleischhauer K, Golay J et al. Cytokine-induced killer cells are terminally differentiated activated CD8 cytotoxic T-EMRA lymphocytes. Exp Hematol 2009; 37: 616-628, e612.
5. Linn YC, Lau SK, Liu BH, Ng LH, Yong HX, Hui KM. Characterization of the recognition and functional heterogeneity exhibited by cytokine-induced killer cell subsets against acute myeloid leukaemia target cell. Immunology 2009; 126: 423-435.
6. Niam M, Linn YC, Fook Chong S, Lim TJ, Chu S, Choong A et al. Clinical scale expansion of cytokine-induced killer cells is feasible from healthy donors and patients with acute and chronic myeloid leukemia at various stages of therapy. Exp Hematol 2011; 39: 897-903, e891.
7. Baker J, Verneris MR, Ito M, Shizuru JA, Negrin RS. Expansion of cytolytic CD8(+) natural killer T cells with limited capacity for graft-versus-host disease induction due to interferon gamma production. Blood 2001; 97: 2923-2931.
8. Nishimura R, Baker J, Beilhack A, Zeiser R, Olson JA, Sega EI et al. In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood 2008; 112: 2563-2574.
9. Laport GG, Sheehan K, Baker J, Armstrong R, Wong RM, Lowsky R et al. NAdoptive immunotherapy with cytokine-induced killer cells for patients with relapse hematologic malignacies after allogeneic hematopoetic cell transplantation. Biol Blood Marrow Transplant 2011; 17: 1679-1687.
10. Biagi E, Marin V, Attianese GM, Pizzitola I, Tettamanti S, Cribioli E et al. New advances in leukaemia immunotherapy by the use of Chimeric Artificial Antigen Receptors (CARs): state of the art and perspectives for the near future. Ital J Pediatr 2011; 37: 46.
11. Kochenderfer JN, Rosenberg SA. Chimeric antigen receptor-modified T cells in CLL. N Engl J Med 2011; 365: 1937-1938 (author reply 1938).
12. 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: 1509-1518.
13. Casucci M, Nicolis di Robilant B, Falcone L, Camisa B, Norelli M, Genovese P et al. CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood 2013; 122: 3461-3472.
14. Marin V, Pizzitola I, Agostoni V, Attianese GM, Finney H, Lawson A et al. Cytokine-induced killer cells for cell therapy of acute myeloid leukemia: improvement of their immune activity by expression of CD33-specific chimeric receptors. Haematologica 2010; 95: 2144-2152.
15. Tettamanti S, Marin V, Pizzitola I, Magnani CF, Giordano Attianese GM, Cribioli E et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br J Haematol 2013; 161: 389-401.
16. Mardiros A, Dos Santos C, McDonald T, Brown CE, Wang X, Budde LE et al. T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and anti-tumor effects against human acute myeloid leukemia. Blood 2013; 122: 3138-3148.
17. Jordan CT, Upchurch D, Szilvassy SJ, Guzman ML, Howard DS, Pettigrew AL et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000; 14: 1777-1784.
18. Taussig DC, Pearce DJ, Simpson C, Rohatiner AZ, Lister TA, Kelly G et al. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood 2005; 106: 4086-4092.
19. Jin L, Lee EM, Ramshaw HS, Busfield SJ, Peoppl AG, Wilkinson L et al. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 2009; 5: 31-42.
20. Sun Q, Woodcock JM, Rapoport A, Stromski FC, Korpelainen EJ, Bagley CJ et al. Monoclonal antibody 7G3 recognizes the N-terminal domain of the human interleukin-3 (IL-3) receptor alpha-chain and functions as a specific IL-3 receptor antagonist. Blood 1996; 87: 83-92.
21. 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: 3890-3897.
22. Aigner M, Feulner J, Schaffer S, Kischel R, Kufer P, Schneider K et al. T lymphocytes can be effectively recruited for ex vivo and in vivo lysis of AML blasts by a novel CD33/CD3-bispecific BiTE((R)) antibody construct. Leukemia 2013; 7: 1107-1115.
23. Walter RB, Appelbaum FR, Estey EH, Bernstein ID. Acute myeloid leukemia stem cells and CD33-targeted immunotherapy. Blood 2012; 119: 6198-6208.
24. Testa U, Riccioni R, Militi S, Coccia E, Stellacci E, Samoggia P et al. Elevated expression of IL3Ralpha in acute myeloid leukemia associated with enhanced blast proliferation, increased cellularity, and poor prognosis. Blood 2002; 100: 2980-2988.
25. Hernández-Caselles T, Martí nez-Esparza M, Pérez-Oliva AB, Quintanilla-Cecconi AM, Garcí a-Alonso A, Alvarez-López DM et al. A study of CD33 (SIGLEC-3) antigen expression and function on activated human T and NK cells: two isoforms of CD33 are generated by alternative splicing. J Leukoc Biol 2006; 79: 46-58.
26. Sievers EL, Larson RA, Stadtmauer EA, Estey E, Löwenberg B, Dombret H et al. Mylotarg Study Group. Efficacy and safety of gemtuzumab ozogamicin in patients with CD33-positive acute myeloid leukemia in first relapse. J Clin Oncol 2001; 19: 3244-3254.
27. Roberts AW, He S, Bradstock KF, Hertzberg MS, Durrant STS, Ritchie D et al. A phase 1 and correlative biological study of CSL360 (anti-CD123 mAb) in AML. Blood 2008; 112: (2956a).
28. Kugler M, Stein C, Kellner C, Mentz K, Saul D, Schwenkert M et al. A recombinant trispecific single chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukemia cells by dual targeting. Br J Haematol 2010; 150: 574-586.
29. Stein C, Kellner C, Kugler M, Reiff N, Mentz K, Schwenkert M et al. Novel conjugates of single-chain Fv antibody fragments specific for stem cell antigen CD1233 mediates a potent death of acute myeloid leukemia. Br J Haematol 2010; 148: 879-889.
30. Cartellieri M, Bachmann M, Feldmann A, Bippes C, Stamova S, Wehner R et al. Chimeric antigen receptor-engineered T cells for immunotherapy of cancer. J Biomed Biotechnol 2010; 2010: 956304.
31. Huang X, Guo H, Kang J, Choi S, Zhou TC, Tammana S et al. Sleeping beauty transposon-mediated engineering of human primary T cells for therapy of CD19+ lymphoid malignancies. Mol Ther 2008; 16: 580-589.
32. Barrett DM, Liu X, Jiang S, June CH, Grupp SA, Zhao Y. Regimen-specific effects of RNA-modified chimeric antigen receptor T cells in mice with advance leukemia. Hum Gene Ther 2013; 24: 717-727.
33. Kebriaei HHP, Singh H, Olivares S, Figliola M, Dawson M, Jena B, Jackson DBR, Rondon G, McNiece I, Hackett P, Shpall E, Champlin RE. First clinical trials employing Sleeping Beauty system and artificial chimeric antigen presenting cells to generate T cells expressing CD-19 specific chimeric antigen receptor. 18th Congress of the European Hematology Association. Stockholm, Sweden, 2013.
34. Di Stasi A, Tey SK, 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: 1673-1683.