Preclinical targeting of human T-cell malignancies using CD4-specific chimeric antigen receptor (CAR)-engineered T cells

Leukemia

Volumn 30, Issue 3, 2016, Pages 701-707

  Pinz, K ^a   Liu, H ^b   Golightly, M ^b   Jares, A ^b   Lan, F ^c   Zieve, G W ^a   Hagag, N ^c   Schuster, M ^c   Firor, A E ^a   Jiang, X ^a   Ma, Y ^a,b,d  

^a Long Island High Technology Incubator   (United States)

^b Stony Brook Medicine   (United States)

^c STONY BROOK UNIVERSITY MEDICAL CENTER   (United States)

^d MACAU UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Macao)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD45RO ANTIGEN; CD8 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; L SELECTIN; ARTIFICIAL RECEPTOR; CHIMERIC PROTEIN;

ADOPTIVE TRANSFER; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MEMORY T LYMPHOCYTE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PERIPHERAL T CELL LYMPHOMA; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; UMBILICAL CORD BLOOD; ANIMAL; CANCER TRANSPLANTATION; CD4+ T LYMPHOCYTE; CELL ENGINEERING; COCULTURE; CYTOLOGY; CYTOTOXICITY; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LEUKEMIA; LYMPHOMA, T-CELL, PERIPHERAL; MALE; MORTALITY; NONOBESE DIABETIC MOUSE; PATHOLOGY; PRIMARY CELL CULTURE; SURVIVAL ANALYSIS; TRANSPLANTATION; TUMOR CELL LINE;

ADOPTIVE TRANSFER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL ENGINEERING; CELL LINE, TUMOR; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; GENE EXPRESSION; HUMANS; LEUKEMIA; LYMPHOMA, T-CELL, PERIPHERAL; MALE; MICE; MICE, INBRED NOD; MUTANT CHIMERIC PROTEINS; NEOPLASM TRANSPLANTATION; PRIMARY CELL CULTURE; RECEPTORS, ARTIFICIAL; SURVIVAL ANALYSIS;

EID: 84959357452     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2015.311     Document Type: Article

References (51)

1. Firor AE, Jares A, Ma Y. From humble beginnings to success in the clinic: chimeric antigen receptor-modified T-cells and implications for immunotherapy. Exp Biol Med 2015; 240: 1087-1098
2. Gill S, June CH. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol Rev 2015; 263: 68-89
3. Skarbnik AP, Burki M, Pro B. Peripheral T-cell lymphomas: a review of current approaches and hopes for the future. Front Oncol 2013; 3: 138
4. Foss FM, Zinzani PL, Vose JM, Gascoyne RD, Rosen ST, Tobinai K. Peripheral T-cell lymphoma. Blood 2011; 117: 6756-6767
5. Jonker M, Slingerland W, Treacy G, van Eerd P, Pak KY, Wilson E, et al. In vivo treatment with a monoclonal chimeric anti-CD4 antibody results in prolonged depletion of circulating CD4+ cells in chimpanzees. Clin Exp Immunol 1993; 93: 301-307
6. Scheerens H, Su Z, Irving B, Townsend MJ, Zheng Y, Stefanich E, et al. MTRX1011A, a humanized anti-CD4 monoclonal antibody, in the treatment of patients with rheumatoid arthritis: a phase I randomized, double-blind, placebo-controlled study incorporating pharmacodynamic biomarker assessments. Arthritis Res Ther 2011; 13: R177
7. Moreland LW, Pratt PW, Bucy RP, Jackson BS, Feldman JW, Koopman WJ. Treatment of refractory rheumatoid arthritis with a chimeric anti-CD4 monoclonal antibody. Long-Term followup of CD4+ T cell counts. Arthritis Rheum 1994; 37: 834-838
8. Wendling D, Racadot E, Morel-Fourrier B, Wijdenes J. Treatment of rheumatoid arthritis with anti CD4 monoclonal antibody. Open study of 25 patients with the B-F5 clone. Clin Rheumatol 1992; 11: 542-547
9. Choy EH, Chikanza IC, Kingsley GH, Corrigall V, Panayi GS. Treatment of rheumatoid arthritis with single dose or weekly pulses of chimaeric anti-CD4 monoclonal antibody. Scand J Immunol 1992; 36: 291-298
10. Horneff G, Burmester GR, Emmrich F, Kalden JR. Treatment of rheumatoid arthritis with an anti-CD4 monoclonal antibody. Arthritis Rheum 1991; 34: 129-140
11. Lindsey JW, Hodgkinson S, Mehta R, Mitchell D, Enzmann D, Steinman L. Repeated treatment with chimeric anti-CD4 antibody in multiple sclerosis. Ann Neurol 1994; 36: 183-189
12. Lindsey JW, Hodgkinson S, Mehta R, Siegel RC, Mitchell DJ, Lim M, et al. Phase 1 clinical trial of chimeric monoclonal anti-CD4 antibody in multiple sclerosis. Neurology 1994; 44 (Pt 1): 413-419
13. Racadot E, Rumbach L, Bataillard M, Galmiche J, Henlin JL, Truttmann M, et al. Treatment of multiple sclerosis with anti-CD4 monoclonal antibody A preliminary report on B-F5 in 21 patients. J Autoimmun 1993; 6: 771-786
14. Prinz JC, Meurer M, Reiter C, Rieber EP, Plewig G, Riethmuller G. Treatment of severe cutaneous lupus erythematosus with a chimeric CD4 monoclonal antibody, cM-T412. J Am Acad Dermatol 1996; 34 (Pt 1): 244-252
15. Nicolas JF, Chamchick N, Thivolet J, Wijdenes J, Morel P, Revillard JP. CD4 antibody treatment of severe psoriasis. Lancet 1991; 338: 321
16. Gottlieb AB, Lebwohl M, Shirin S, Sherr A, Gilleaudeau P, Singer G, et al. Anti-CD4 monoclonal antibody treatment of moderate to severe psoriasis vulgaris: results of a pilot, multicenter, multiple-dose, placebo-controlled study. J Am Acad Dermatol 2000; 43: 595-604
17. Skov L, Kragballe K, Zachariae C, Obitz ER, Holm EA, Jemec GB, et al. HuMax-CD4: a fully human monoclonal anti-CD4 antibody for the treatment of psoriasis vulgaris. Arch Dermatol 2003; 139: 1433-1439
18. Knox S, Hoppe RT, Maloney D, Gibbs I, Fowler S, Marquez C, et al. Treatment of cutaneous T-cell lymphoma with chimeric anti-CD4 monoclonal antibody. Blood 1996; 87: 893-899
19. Kim YH, Duvic M, Obitz E, Gniadecki R, Iversen L, Osterborg A, et al. Clinical efficacy of zanolimumab (HuMax-CD4): two phase 2 studies in refractory cutaneous T-cell lymphoma. Blood 2007; 109: 4655-4662
20. d'Amore F, Radford J, Relander T, Jerkeman M, Tilly H, Osterborg A, et al. Phase II trial of zanolimumab (HuMax-CD4) in relapsed or refractory non-cutaneous peripheral T cell lymphoma. Br J Haematol 2010; 150: 565-573
21. Hagberg H, Pettersson M, Bjerner T, Enblad G. Treatment of a patient with a nodal peripheral T-cell lymphoma (angioimmunoblastic T-Cell lymphoma) with a human monoclonal antibody against the CD4 antigen (HuMax-CD4). Med Oncol 2005; 22: 191-194
22. Rider DA, Havenith CE, de Ridder R, Schuurman J, Favre C, Cooper JC, et al A human CD4 monoclonal antibody for the treatment of T-cell lymphoma combines inhibition of T-cell signaling by a dual mechanism with potent Fc-dependent effector activity. Cancer Res 2007; 67: 9945-9953
23. Maus MV, Fraietta JA, Levine BL, Kalos M, Zhao Y, June CH. Adoptive immunotherapy for cancer or viruses. Annu Rev Immunol 2014; 32: 189-225
24. Marzo AL, Vezys V, Klonowski KD, Lee SJ, Muralimohan G, Moore M, et al. Fully functional memory CD8 T cells in the absence of CD4 T cells. J Immunol 2004; 173: 969-975
25. Davila ML, Kloss CC, Gunset G, Sadelain M. CD19 CAR-Targeted T cells induce longterm remission and B Cell aplasia in an immunocompetent mouse model of B cell acute lymphoblastic leukemia. PLoS One 2013; 8: e61338
26. Terakura S, Yamamoto TN, Gardner RA, Turtle CJ, Jensen MC, Riddell SR. Generation of CD19-chimeric antigen receptor modified CD8+ T cells derived from virus-specific central memory T cells. Blood 2012; 119: 72-82
27. Wang X, Naranjo A, Brown CE, Bautista C, Wong CW, Chang WC, et al. Phenotypic and functional attributes of lentivirus-modified CD19-specific human CD8+ central memory T cells manufactured at clinical scale. J Immunother 2012; 35: 689-701
28. Kuritzkes DR, Jacobson J, Powderly WG, Godofsky E, DeJesus E, Haas F, et al. Antiretroviral activity of the anti-CD4 monoclonal antibody TNX-355 in patients infected with HIV type 1. J Infect Dis 2004; 189: 286-291
29. Boon L, Holland B, Gordon W, Liu P, Shiau F, Shanahan W, et al. Development of anti-CD4 MAb hu5A8 for treatment of HIV-1 infection: preclinical assessment in non-human primates. Toxicology 2002; 172: 191-203
30. Reimann KA, Lin W, Bixler S, Browning B, Ehrenfels BN, Lucci J, et al A humanized form of a CD4-specific monoclonal antibody exhibits decreased antigenicity and prolonged plasma half-life in rhesus monkeys while retaining its unique biological and antiviral properties. AIDS Res Hum Retroviruses 1997; 13: 933-943
31. Meng X, Su RJ, Baylink DJ, Neises A, Kiroyan JB, Lee WY, et al. Rapid and efficient reprogramming of human fetal and adult blood CD34+ cells into mesenchymal stem cells with a single factor. Cell Res 2013; 23: 658-672
32. Nikitin AG, Kochkin IT, June CM, Willis CM, McBain I, Videiko MY. Mitochondrial DNA sequence variation in the Boyko, Hutsul, and Lemko populations of the Carpathian highlands. Hum Biol 2009; 81: 43-58
33. Kitchen SG, Korin YD, Roth MD, Landay A, Zack JA. Costimulation of naive CD8(+) lymphocytes induces CD4 expression and allows human immunodeficiency virus type 1 infection. J Virol 1998; 72: 9054-9060
34. Yang LP, Riley JL, Carroll RG, June CH, Hoxie J, Patterson BK, et al. Productive infection of neonatal CD8+ T lymphocytes by HIV-1. J Exp Med 1998; 187: 1139-1144
35. Budde LE, Berger C, Lin Y, Wang J, Lin X, Frayo SE, et al. Combining a CD20 chimeric antigen receptor and an inducible caspase 9 suicide switch to improve the efficacy and safety of T cell adoptive immunotherapy for lymphoma. PLoS One 2013; 8: e82742
36. Ambrosini V, Quarta C, Zinzani PL, Fini M, Giavaresi G, Torricelli P, et al. 18F-FDG small animal PET for early detection of human anaplastic large cells lymphoma xenograft in immunocompromised mice. Anticancer Res 2008; 28: 981-987
37. Kochenderfer JN, Feldman SA, Zhao Y, Xu H, Black MA, Morgan RA, et al. Construction and preclinical evaluation of an anti-CD19 chimeric antigen receptor. J Immunother 2009; 32: 689-702
38. Pitzalis C, Kingsley G, Murphy J, Panayi G. Abnormal distribution of the helperinducer and suppressor-inducer T-lymphocyte subsets in the rheumatoid joint. Clin Immunol Immunopathol 1987; 45: 252-258
39. Schulze-Koops H, Lipsky PE. Anti-CD4 monoclonal antibody therapy in human autoimmune diseases. Curr Dir Autoimmun 2000; 2: 24-49
40. Pohlers D, Nissler K, Frey O, Simon J, Petrow PK, Kinne RW, et al. Anti-CD4 monoclonal antibody treatment in acute and early chronic antigen-induced arthritis: influence on T helper cell activation. Clin Exp Immunol 2004; 135: 409-415
41. van Oosten BW, Lai M, Hodgkinson S, Barkhof F, Miller DH, Moseley IF, et al. Treatment of multiple sclerosis with the monoclonal anti-CD4 antibody cM-T412: results of a randomized, double-blind, placebo-controlled, MR-monitored phase II trial. Neurology 1997; 49: 351-357
42. Lee DW, Kochenderfer JN, Stetler-Stevenson M, Cui YK, Delbrook C, Feldman SA, 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 2014; 385: 517-528
43. 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
44. Wofsy D. Treatment of murine lupus with anti-CD4 monoclonal antibodies. Immunol Ser 1993; 59: 221-236
45. Connolly K, Roubinian JR, Wofsy D. Development of murine lupus in CD4-depleted NZB/NZW mice. Sustained inhibition of residual CD4+ T cells is required to suppress autoimmunity. J Immunol 1992; 149: 3083-3088
46. Yu H, Tawab-Amiri A, Dzutsev A, Sabatino M, Aleman K, Yarchoan R, et al. IL-15 ex vivo overcomes CD4+ T cell deficiency for the induction of human antigenspecific CD8+ T cell responses. J Leukoc Biol 2011; 90: 205-214
47. Maus MV, Grupp SA, Porter DL, June CH. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood 2014; 123: 2625-2635
48. Barao I. The TNF receptor-ligands 4-1BB-4-1BBL and GITR-GITRL in NK cell responses. Front Immunol 2012; 3: 402
49. Sun A, Wei H, Sun R, Xiao W, Yang Y, Tian Z. Human interleukin-15 improves engraftment of human T cells in NOD-SCID mice. Clin Vaccine Immunol 2006; 13: 227-234
50. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 2011; 3: 95ra73
51. Globerson-Levin A, Waks T, Eshhar Z. Elimination of progressive mammary cancer by repeated administrations of chimeric antigen receptor-modified T cells. Mol Ther 2014; 22: 1029-1038