Ibrutinib enhances chimeric antigen receptor T-cell engraftment and efficacy in leukemia

Blood

Volumn 127, Issue 9, 2016, Pages 1117-1127

  Fraietta, Joseph A ^a,b   Beckwith, Kyle A ^c   Patel, Prachi R ^a,b   Ruella, Marco ^a,b   Zheng, Zhaohui ^a,b   Barrett, David M ^d   Lacey, Simon F ^a,b   Melenhorst, Jan Joseph ^a,b   McGettigan, Shannon E ^a,b   Cook, Danielle R ^a,b   Zhang, Changfeng ^a,b   Xu, Jun ^a,b   Do, Priscilla ^c   Hulitt, Jessica ^d   Kudchodkar, Sagar B ^a,b   Cogdill, Alexandria P ^a,b   Gill, Saar ^a,e   Porter, David L ^a,b,e   Woyach, Jennifer A ^c   Long, Meixiao ^c   Johnson, Amy J ^c   Maddocks, Kami ^c   Muthusamy, Natarajan ^c   Levine, Bruce L ^a,b,f   June, Carl H ^a,b,f   Byrd, John C ^c   Maus, Marcela V ^g   more..

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e Division of Hematology Oncology   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD200 ANTIGEN; CD28 ANTIGEN; CD3 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; GAMMA INTERFERON; IBRUTINIB; IONOMYCIN; PHORBOL 13 ACETATE 12 MYRISTATE; PROGRAMMED DEATH 1 LIGAND 1; TISAGENLECLEUCEL T; ANTIGENS, CD200; CTL019 CHIMERIC ANTIGEN RECEPTOR; LEUKOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; PDCD1 PROTEIN, HUMAN; PROGRAMMED DEATH 1 RECEPTOR; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CANCER SURVIVAL; CELL FUNCTION; CHRONIC LYMPHATIC LEUKEMIA; DISEASE CLEARANCE; DRUG EFFECT; DRUG EFFICACY; ENGRAFTMENT; EVALUATION STUDY; EX VIVO STUDY; FEASIBILITY STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TREATMENT DURATION; TREATMENT RESPONSE; AGED; ANIMAL; CELL PROLIFERATION; CLINICAL TRIAL; CYTOTOXICITY; DEMOGRAPHY; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; GENE TRANSFER; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; K-562 CELL LINE; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; METABOLISM; MIDDLE AGED; MOUSE; ORAL DRUG ADMINISTRATION; PATHOLOGY; TIME FACTOR; TREATMENT OUTCOME; TUMOR CELL LINE;

ADMINISTRATION, ORAL; AGED; ANIMALS; ANTIGENS, CD; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; DEMOGRAPHY; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; GENE TRANSFER TECHNIQUES; HUMANS; IMMUNOSUPPRESSION; K562 CELLS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MICE; MIDDLE AGED; PROGRAMMED CELL DEATH 1 RECEPTOR; PYRAZOLES; PYRIMIDINES; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TIME FACTORS; TREATMENT OUTCOME;

EID: 84960444794     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-11-679134     Document Type: Article

References (50)

1. Rossi D, Sozzi E, Puma A, et al. The prognosis of clinical monoclonal B cell lymphocytosis differs from prognosis of Rai 0 chronic lymphocytic leukaemia and is recapitulated by biological risk factors. Br J Haematol. 2009;146(1):64-75.
2. Moreira J, Rabe KG, Cerhan JR, et al. Infectious complications among individuals with clinical monoclonal B-cell lymphocytosis (MBL): a cohort study of newly diagnosed cases compared to controls. Leukemia. 2013;27(1):136-141.
3. D'Arena G, D'Auria F, Simeon V, et al. A shorter time to the first treatment may be predicted by the absolute number of regulatory T-cells in patients with Rai stage 0 chronic lymphocytic leukemia. Am J Hematol. 2012;87(6):628-631.
4. D'Arena G, Laurenti L, Minervini MM, et al. Regulatory T-cell number is increased in chronic lymphocytic leukemia patients and correlates with progressive disease. Leuk Res. 2011;35(3):363-368.
5. Palmer S, Hanson CA, Zent CS, et al. Prognostic importance of T and NK-cells in a consecutive series of newly diagnosed patients with chronic lymphocytic leukaemia. Br J Haematol. 2008;141(5):607-614.
6. Rozman C, Montserrat E, Vinõlas N. Serum immunoglobulins in B-chronic lymphocytic leukemia. Natural history and prognostic significance. Cancer. 1988;61(2):279-283.
7. 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(8):725-733.
8. Kalos M, Levine BL, Porter DL, 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(95):95ra73.
9. Grupp SA, Kalos M, Barrett D, et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med. 2013;368(16):1509-1518.
10. 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.
11. Porter DL, Hwang WT, Frey NV, et al. Chimeric antigen receptor T cells persist and induce sustained remissions in relapsed refractory chronic lymphocytic leukemia. Sci Transl Med. 2015;7(303):303ra139.
12. Evans AG, Rothberg PG, Burack WR, et al. Evolution to plasmablastic lymphoma evades CD19-directed chimeric antigen receptor T cells [published online ahead of print June 18, 2015]. Br J Haematol.
13. Sotillo E, Barrett DM, Black KL, et al. Convergence of Acquired Mutations and Alternative Splicing of CD19 Enables Resistance to CART-19 Immunotherapy. Cancer Discov. 2015;5(12):1282-1295.
14. Brentjens RJ, Rivière I, Park JH, et al. Safety and persistence of adoptively transferred autologous CD19-targeted T cells in patients with relapsed or chemotherapy refractory B-cell leukemias. Blood. 2011;118(18):4817-4828.
15. Kochenderfer JN, Dudley ME, Feldman SA, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptortransduced T cells. Blood. 2012;119(12):2709-2720.
16. 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.
17. Dubovsky JA, Beckwith KA, Natarajan G, et al. Ibrutinib is an irreversible molecular inhibitor of ITK driving a Th1-selective pressure in T lymphocytes. Blood. 2013;122(15):2539-2549.
18. Sagiv-Barfi I, Kohrt HE, Czerwinski DK, Ng PP, Chang BY, Levy R. Therapeutic antitumor immunity by checkpoint blockade is enhanced by ibrutinib, an inhibitor of both BTK and ITK. Proc Natl Acad Sci USA. 2015;112(9):E966-E972.
19. Hertlein E, Beckwith KA, Lozanski G, et al. Characterization of a new chronic lymphocytic leukemia cell line for mechanistic in vitro and in vivo studies relevant to disease. PLoS One. 2013;8(10):e76607.
20. Milone MC, Fish JD, Carpenito C, 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(8):1453-1464.
21. Parish CR, Glidden MH, Quah BJ, Warren HS. Use of the intracellular fluorescent dye CFSE to monitor lymphocyte migration and proliferation. Curr Protoc Immunol. 2009; Chapter 4:Unit4.9. doi:10.1002/0471142735.im0409s84.
22. Porter DL, Levine BL, Bunin N, et al. A phase 1 trial of donor lymphocyte infusions expanded and activated ex vivo via CD3/CD28 costimulation. Blood. 2006;107(4):1325-1331.
23. Riches JC, Davies JK, McClanahan F, et al. T cells from CLL patients exhibit features of T-cell exhaustion but retain capacity for cytokine production. Blood. 2013;121(9):1612-1621.
24. Bennett F, Luxenberg D, Ling V, et al. Program death-1 engagement upon TCR activation has distinct effects on costimulation and cytokinedriven proliferation: attenuation of ICOS, IL-4, and IL-21, but not CD28, IL-7, and IL-15 responses. J Immunol. 2003;170(2):711-718.
25. Chemnitz JM, Parry RV, Nichols KE, June CH, Riley JL. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J Immunol. 2004;173(2):945-954.
26. Parry RV, Chemnitz JM, Frauwirth KA, et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol. 2005;25(21):9543-9553.
27. Okazaki T, Maeda A, Nishimura H, Kurosaki T, Honjo T. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc Natl Acad Sci USA. 2001;98(24):13866-13871.
28. Patsoukis N, Brown J, Petkova V, Liu F, Li L, Boussiotis VA. Selective effects of PD-1 on Akt and Ras pathways regulate molecular components of the cell cycle and inhibit T cell proliferation. Sci Signal. 2012;5(230):ra46.
29. Patsoukis N, Sari D, Boussiotis VA. PD-1 inhibits T cell proliferation by upregulating p27 and p15 and suppressing Cdc25A. Cell Cycle. 2012;11(23):4305-4309.
30. McClanahan F, Hanna B, Miller S, et al. PD-L1 checkpoint blockade prevents immune dysfunction and leukemia development in a mouse model of chronic lymphocytic leukemia. Blood. 2015;126(2):203-211.
31. Wong KK, Brenneman F, Chesney A, Spaner DE, Gorczynski RM. Soluble CD200 is critical to engraft chronic lymphocytic leukemia cells in immunocompromised mice. Cancer Res. 2012;72(19):4931-4943.
32. Coles SJ, Wang ECY, Man S, et al. CD200 expression suppresses natural killer cell function and directly inhibits patient anti-tumor response in acute myeloid leukemia. Leukemia. 2011;25(5):792-799.
33. Kretz-Rommel A, Qin F, Dakappagari N, et al. CD200 expression on tumor cells suppresses antitumor immunity: new approaches to cancer immunotherapy. J Immunol. 2007;178(9):5595-5605.
34. Wong KK, Khatri I, Shaha S, Spaner DE, Gorczynski RM. The role of CD200 in immunity to B cell lymphoma. J Leukoc Biol. 2010;88(2):361-372.
35. Kohrt HE, Sagiv-Barfi I, Rafiq S, et al. Ibrutinib antagonizes rituximab-dependent NK cell-mediated cytotoxicity. Blood. 2014;123(12):1957-1960.
36. Woyach JA, Furman RR, Liu TM, et al. Resistance mechanisms for the Bruton's tyrosine kinase inhibitor ibrutinib. N Engl J Med. 2014;370(24):2286-2294.
37. Cheung KJ, Johnson NA, Affleck JG, et al. Acquired TNFRSF14 mutations in follicular lymphoma are associated with worse prognosis. Cancer Res. 2010;70(22):9166-9174.
38. Steidl C, Shah SP, Woolcock BW, et al. MHC class II transactivator CIITA is a recurrent gene fusion partner in lymphoid cancers. Nature. 2011;471(7338):377-381.
39. Peretz Y, He Z, Shi Y, et al. CD160 and PD-1 co-expression on HIV-specific CD8 T cells defines a subset with advanced dysfunction. PLoS Pathog. 2012;8(8):e1002840.
40. Alapat D, Coviello-Malle J, Owens R, et al. Diagnostic usefulness and prognostic impact of CD200 expression in lymphoid malignancies and plasma cell myeloma. Am J Clin Pathol. 2012;137(1):93-100.
41. Dorfman DM, Shahsafaei A. CD200 (OX-2 membrane glycoprotein) expression in b cellderived neoplasms. Am J Clin Pathol. 2010;134(5):726-733.
42. Gorczynski L, Chen Z, Hu J, et al. Evidence that an OX-2-positive cell can inhibit the stimulation of type 1 cytokine production by bone marrowderived B7-1 (and B7-2)-positive dendritic cells. J Immunol. 1999;162(2):774-781.
43. Shiratori I, Yamaguchi M, Suzukawa M, et al. Down-regulation of basophil function by human CD200 and human herpesvirus-8 CD200. J Immunol. 2005;175(7):4441-4449.
44. Gorczynski RM. Transplant tolerance modifying antibody to CD200 receptor, but not CD200, alters cytokine production profile from stimulated macrophages. Eur J Immunol. 2001;31(8):2331-2337.
45. Jenmalm MC, Cherwinski H, Bowman EP, Phillips JH, Sedgwick JD. Regulation of myeloid cell function through the CD200 receptor. J Immunol. 2006;176(1):191-199.
46. Pallasch CP, Ulbrich S, Brinker R, Hallek M, Uger RA, Wendtner CM. Disruption of T cell suppression in chronic lymphocytic leukemia by CD200 blockade. Leuk Res. 2009;33(3):460-464.
47. Ramsay AG, Clear AJ, Fatah R, Gribben JG. Multiple inhibitory ligands induce impaired T-cell immunologic synapse function in chronic lymphocytic leukemia that can be blocked with lenalidomide: establishing a reversible immune evasion mechanism in human cancer. Blood. 2012;120(7):1412-1421.
48. Maddocks KJ, Ruppert AS, Lozanski G, et al. Etiology of Ibrutinib Therapy Discontinuation and Outcomes in Patients With Chronic Lymphocytic Leukemia. JAMA Oncol. 2015;1(1):80-87.
49. de Rooij MF, Kuil A, Geest CR, et al. The clinically active BTK inhibitor PCI-32765 targets B-cell receptor- and chemokine-controlled adhesion and migration in chronic lymphocytic leukemia. Blood. 2012;119(11):2590-2594.
50. Sagiv-Barfi I, Kohrt HE, Burckhardt L, Czerwinski DK, Levy R. Ibrutinib enhances the antitumor immune response induced by intratumoral injection of a TLR9 ligand in mouse lymphoma. Blood. 2015;125(13):2079-2086.