Targeting CD20+ aggressive B-cell non-hodgkin lymphoma by Anti-CD20 CAR mRNA-modified expanded natural killer cells in vitro and in NSG Mice

Cancer Immunology Research

Volumn 3, Issue 4, 2015, Pages 333-344

  Chu, Yaya ^a   Hochberg, Jessica ^a   Yahr, Ashlin ^a   Ayello, Janet ^a   Van De Ven, Carmella ^a   Barth, Matthew ^b   Czuczman, Myron ^c   Cairo, Mitchell S ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIBODY; CD20 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; RITUXIMAB;

ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B-CELL LYMPHOMA CELL LINE; BURKITT LYMPHOMA; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CANCER SIZE; CELL EXPANSION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DEGRANULATION; EX VIVO STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; JURKAT CELL LINE; LARGE CELL LYMPHOMA; LUCIFERASE ASSAY; MOUSE; NATURAL KILLER T CELL; NOD SCID GAMMA MOUSE; NONHUMAN; PROTEIN EXPRESSION; SURVIVAL TIME; TUMOR XENOGRAFT; ANIMAL; CELL MOTION; DRUG SCREENING; EVALUATION STUDY; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOMA, B-CELL; METABOLISM; NATURAL KILLER CELL; NONOBESE DIABETIC MOUSE; PROCEDURES; SCID MOUSE; TRANSPLANTATION; TUMOR CELL CULTURE;

ANIMALS; ANTIGENS, CD20; BURKITT LYMPHOMA; CELL MOVEMENT; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNOTHERAPY; KILLER CELLS, NATURAL; LYMPHOMA, B-CELL; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MICE, INBRED NOD; MICE, SCID; RNA, MESSENGER; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84934281880     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0114     Document Type: Article

References (50)

1. Pinkerton R CM. Childhood non-Hodgkin lymphoma. In: Mitchell S, Cairo SLP, editors. Hematological malignancies in children, adolescents and young adults. Singapore: World Scientific; 2012. p. 299-328.
2. Cairo MS, Gerrard M, Sposto R, Auperin A, Pinkerton CR, Michon J, et al. Results of a randomized international study of high-risk central nervous system Bnon-Hodgkin lymphoma and B acute lymphoblastic leukemia in children and adolescents. Blood 2007;109:2736-43.
3. Gerrard M, Cairo MS, Weston C, Auperin A, Pinkerton R, Lambilliote A, et al. Excellent survival following two courses of COPAD chemotherapy in children and adolescents with resected localized B-cell non-Hodgkin's lymphoma: results of the FAB/LMB 96 international study. Br J Haematol 2008;141:840-7.
4. Cairo MS, Sposto R, Gerrard M, Auperin A, Goldman SC, Harrison L, et al. Advanced stage, increased lactate dehydrogenase, and primary site, but not adolescent age (>/= 15 years), are associated with an increased risk of treatment failure in children and adolescents with mature B-cell non-Hodgkin's lymphoma: results of the FAB LMB 96 study. J Clin Oncol 2012;30:387-93.
5. Miles RR, Arnold S, Cairo MS. Risk factors and treatment of childhood and adolescentBurkitt lymphoma/leukaemia. Br J Haematol 2012;156:730-43.
6. Blum KA, Lozanski G, Byrd JC. Adult Burkitt leukemia and lymphoma. Blood 2004;104:3009-20.
7. LeBien TW, Tedder TF. B lymphocytes: how they develop and function. Blood 2008;112:1570-80.
8. Perkins SL, Lones MA, Davenport V, Cairo MS. B-Cell non-Hodgkin's lymphoma in children and adolescents: surface antigen expression and clinical implications for future targeted bioimmune therapy: a children's cancer group report. Clin Adv Hematol Oncol 2003;1:314-7.
9. Coiffier B, Lepage E, Briere J, Herbrecht R, Tilly H, Bouabdallah R, et al. CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 2002;346:235-42.
10. Goldman S, Smith L, Anderson JR, Perkins S, Harrison L, Geyer MB, et al. Rituximab and FAB/LMB 96 chemotherapy in children with Stage III/IV B-cell non-Hodgkin lymphoma: a Children's Oncology Group report. Leukemia 2013;27:1174-7.
11. Dunleavy K, Pittaluga S, Shovlin M, Steinberg SM, Cole D, Grant C, et al. Low-intensity therapy in adults with Burkitt's lymphoma. N Engl J Med 2013;369:1915-25.
12. Paust S, von Andrian UH Natural killer cell memory. Nat Immunol 2011;12:500-8.
13. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011;331:44-9.
14. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol 2008;9:503-10.
15. Raulet DH, Vance RE. Self-tolerance of natural killer cells. Nat Rev Immunol 2006;6:520-31.
16. Shereck E, Satwani P, Morris E, Cairo MS. Human natural killer cells in health and disease. Pediatr Blood Cancer 2007;49:615-23.
17. 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;106:376-83.
18. Berg M, Lundqvist A, McCoy P Jr, Samsel L, Fan Y, Tawab A, et al. Clinicalgrade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy 2009;11:341-55.
19. Robinson KL, Ayello J, Hughes R, van de Ven C, Issitt L, Kurtzberg J, et al. Ex vivo expansion, maturation, and activation ofumbilical cord blood-derived T lymphocytes with IL-2, IL-12, anti-CD3, and IL-7. Potential for adoptive cellular immunotherapy post-umbilical cord blood transplantation. Exp Hematol 2002;30:245-51.
20. Ayello J, van de Ven C, Cairo E, Hochberg J, Baxi L, Satwani P, et al. Characterization of natural killer and natural killer-like T cells derived from ex vivo expanded and activated cord blood mononuclear cells: implications for adoptive cellular immunotherapy. Exp Hematol 2009;37:1216-29.
21. Imai C, Mihara K, Andreansky M, Nicholson IC, Pui CH, Geiger TL, et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004;18:676-84.
22. Kohn DB, Dotti G, Brentjens R, Savoldo B, Jensen M, Cooper LJ, et al. CARs on track in the clinic. Mol Ther 2011;19:432-8.
23. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor modified T cells in chronic lymphoid leukemia. N Engl J Med 2011;365: 725-33.
24. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, et al. Chimeric antigenreceptor-modifiedTcellsfor acutelymphoidleukemia. N Engl J Med 2013;368:1509-18.
25. Brentjens RJ, Davila ML, Riviere I, Park J, Wang X, Cowell LG, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med 2013;5:177ra38.
26. 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-recep-tor-transduced T cells. Blood 2012;119:2709-20.
27. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002;295:2097-100.
28. Czuczman MS, Olejniczak S, Gowda A, Kotowski A, Binder A, Kaur H, et al. Acquirement of rituximab resistance in lymphoma cell lines is associated with both global CD20 gene and protein down-regulation regulated at the pretranscriptional and posttranscriptional levels. Clin Cancer Res 2008;14: 1561-70.
29. Shimasaki N, Fujisaki H, Cho D, Masselli M, Lockey T, Eldridge P, et al. A clinically adaptable method to enhance the cytotoxicity of natural killer cells against B-cell malignancies. Cytotherapy 2012;14:830-40.
30. Nishimura R, Baker J, Beilhack A, Zeiser R, Olson JA, Sega EI, et al. In vivo trafficking and survival of cytokine-induced killer cells resultinginminimal GVHD with retention of antitumor activity. Blood 2008;112:2563-74.
31. Zheng J, Xu L, Zhou H, Zhang W, Chen Z. Quantitative analysis of cell tracing by in vivo imaging system. J Huazhong Univ Sci Technolog Med Sci 2010;30:541-5.
32. Tomayko MM, Reynolds CP. Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 1989;24: 148-54.
33. Zhao Y, Moon E, Carpenito C, Paulos CM, Liu X, Brennan AL, et al. Multiple injections of electroporated autologous T cells expressing a chimeric antigenreceptor mediate regressionofhuman disseminatedtumor. Cancer Res 2010;70:9053-61.
34. North J, Bakhsh I, Marden C, Pittman H, Addison E, Navarrete C, et al. Tumor-primed human natural killer cells lyse NK-resistant tumor targets: evidence of a two-stage process in resting NK cell activation. J Immunol 2007;178:85-94.
35. Hasenkamp J, Borgerding A, Wulf G, Uhrberg M, Jung W, Dingeldein S, et al. Resistance against natural killer cell cytotoxicity: analysis of mechanisms. Scand J Immunol 2006;64:444-9.
36. de Preval C, Mach B. The absence of beta 2-microglobulin in Daudi cells: active gene but inactive messenger RNA. Immunogenetics 1983;17: 133-40.
37. Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004;294:15-22.
38. Hacein-Bey-Abina S, von Kalle C, Schmidt M, Le Deist F, Wulffraat N, McIntyre E, et al. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N Engl J Med 2003;348: 255-6.
39. Barrett DM, Zhao Y, Liu X, Jiang S, Carpenito C, Kalos M, et al. Treatment of advanced leukemiain mice with mRNA engineered Tcells. Hum Gene Ther 2011;22:1575-86.
40. Somanchi SS, Somanchi A, Cooper LJ, Lee DA. Engineering lymph node homing of ex vivo-expanded human natural killer cells via trogocytosis of the chemokine receptor CCR7. Blood 2012;119:5164-72.
41. Guimaraes F, Guven H, Donati D, Christensson B, Ljunggren HG, Bejarano MT, et al. Evaluation of ex vivo expanded human NK cells on antileukemia activity in SCID-beige mice. Leukemia 2006;20:833-9.
42. Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res 2011;17:6287-97.
43. Singh N, Liu X, Hulitt J, Jiang S, June CH, Grupp SA, 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;2:1059-70.
44. Pietra G, Manzini C, Rivara S, Vitale M, Cantoni C, Petretto A, et al. Melanoma cells inhibit natural killer cell function by modulating the expression of activating receptors and cytolytic activity. Cancer Res 2012; 72:1407-15.
45. Garcia-Iglesias T, Del Toro-Arreola A, Albarran-Somoza B, Del Toro-Arreola S, Sanchez-Hernandez PE, Ramirez-Dueñas MG, et al. Low NKp30, NKp46 and NKG2D expression and reduced cytotoxic activity on NK cells in cervical cancer and precursor lesions. BMC Cancer 2009;9:186.
46. Ciccone E, Pende D, Viale O, Than A, Di Donato C, Orengo AM, et al. Involvement of HLA class I alleles in natural killer (NK) cell-specific functions: expression of HLA-Cw3 confers selective protection from lysis by alloreactive NK clones displaying a defined specificity (specificity 2). J Exp Med 1992;176:963-71.
47. Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res 2008;68:6368-76.
48. Chu Y, Yahr A, Ayello J, Lo L, Katz J, Cairo M. Effectively targeting sensitive and resistant Burkitt lymphoma by anti-CD20 chimeric antigen receptor (CAR) modified expanded natural killer (NK) cells combined with a histone deacetylase inhibitor, romidepsin. Bone Marrow Transpl 2013; 48:S15-S.
49. Scott SD Rituximab: a new therapeutic monoclonal antibody for non-Hodgkin's lymphoma. Cancer Pract 1998;6:195-7.
50. Davis TA, Grillo-Lopez AJ, White CA, McLaughlin P, Czuczman MS, Link BK, et al. Rituximab anti-CD20 monoclonal antibody therapy in non-Hodgkin's lymphoma: safety and efficacy of re-treatment. J Clin Oncol 2000;18:3135-43.