CD19 as an attractive target for antibody-based therapy

mAbs

Volumn 4, Issue 5, 2012, Pages 571-577

  Hammer, Ohad ^a  

^a Pontifax Venture   (Israel)

Author keywords

Antibody drug conjugates; Bispecific antibodies; CD19 immunotherapy; Chimeric antigen receptors; Fc engineered antibodies

Indexed keywords

AFM 11; ANTI CD19 CHIMERIC-ANTIGEN RECEPTOR; ANTINEOPLASTIC AGENT; BENDAMUSTINE; BETA1A INTERFERON; BISPECIFIC ANTIBODY; BLINATUMOMAB; CART 19; CD19 ANTIBODY; CD19 TARGETED CHIMERIC ANTIGEN RECEPTOR; CD19XCD3 DUAL AFFINITY RETARGETING ANTIBODY; COMBOTOX; CYCLOPHOSPHAMIDE; DT 2219ARL; FLUDARABINE; GAMMA INTERFERON; GBR 401; IMMUNOTOXIN; MDX 1342; MEDI 551; MONOCLONAL ANTIBODY; MOR 208; RITUXIMAB; SAR 3419; SGN CD19A; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; XMAB 5574; XMAB 5871;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; B CELL LEUKEMIA; B LYMPHOCYTE ACTIVATION; BLOOD; BLURRED VISION; CANCER CHEMOTHERAPY; CAPILLARY LEAK SYNDROME; CARCINOGENESIS; CENTRAL NERVOUS SYSTEM DISEASE; CHILL; CHRONIC LYMPHATIC LEUKEMIA; CORTICOSTEROID THERAPY; CROSS REACTION; DRUG WITHDRAWAL; EYE TOXICITY; FEVER; FLU LIKE SYNDROME; FOLLOW UP; HAPLORHINI; HUMAN; HUMORAL IMMUNE DEFICIENCY; HYPOTENSION; IMMUNOGLOBULIN DEFICIENCY; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; INFUSION RELATED REACTION; INTRACELLULAR SIGNALING; KIDNEY FAILURE; LARGE CELL LYMPHOMA; LYMPHOCYTOPENIA; MONONUCLEAR CELL; MONOTHERAPY; MULTIPLE MYELOMA; NAUSEA; NONHODGKIN LYMPHOMA; NONHUMAN; PANCREATITIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; RHEUMATOID ARTHRITIS; RIGOR; SCLERODERMA; SIDE EFFECT; T LYMPHOCYTE; TARGET CELL; TUMOR LYSIS SYNDROME; XENOGRAFT;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; ANTIGENS, CD19; CLINICAL TRIALS AS TOPIC; HUMANS; IMMUNOTHERAPY; LEUKEMIA, B-CELL; LYMPHOMA, B-CELL; MICE;

EID: 84866559756     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.21338     Document Type: Review

References (61)

1. Hagemeister F. Rituximab for the treatment of non-Hodgkin's lymphoma and chronic lymphocytic leukaemia. Drugs 2010; 70:261-72; PMID:20166765; http://dx.doi.org/10.2165/11532180-000000000-00000.
2. Polson AG, Calemine-Fenaux J, Chan P, Chang W, Christensen E, Clark S, et al. Antibody-drug conjugates for the treatment of non-Hodgkin's lymphoma: target and linker-drug selection. Cancer Res 2009; 69:2358-64; PMID:19258515; http://dx.doi.org/10.1158/0008-5472.CAN-08-2250.
3. Krause G, Patz M, Isaeva P, Wigger M, Baki I, Vondey V, et al. Action of novel CD37 antibodies on chronic lymphocytic leukemia cells. Leukemia 2012; 26:546-9; PMID:21886169; http://dx.doi.org/10.1038/leu.2011.233.
4. Kantarjian H, Thomas D, Jorgensen J, Jabbour E, Kebriaei P, Rytting M, et al. Inotuzumab ozogamicin, an anti-CD22-calecheamicin conjugate, for refractory and relapsed acute lymphocytic leukaemia: a phase 2 study. Lancet Oncol 2012; 13:403-11; PMID:22357140; http://dx.doi.org/10.1016/S1470-2045(11)70386-2.
5. Gerber HP, Kung-Sutherland M, Stone I, Morris-Tilden C, Miyamoto J, McCormick R, et al. Potent antitumor activity of the anti-CD19 auristatin antibody drug conjugate hBU12-vcMMAE against rituximab-sensitive and -resistant lymphomas. Blood 2009; 113:4352-61; PMID:19147785; http://dx.doi.org/10.1182/ blood-2008-09-179143.
6. Davis TA, Czerwinski DK, Levy R. Therapy of B-cell lymphoma with anti-CD20 antibodies can result in the loss of CD20 antigen expression. Clin Cancer Res 1999; 5:611-5; PMID:10100713.
7. Ingle GS, Chan P, Elliott JM, Chang WS, Koeppen H, Stephan JP, et al. High CD21 expression inhibits internalization of anti-CD19 antibodies and cytotoxicity of an anti-CD19-drug conjugate. Br J Haematol 2008; 140:46-58; PMID:17991300.
8. Flavell DJ, Warnes SL, Bryson CJ, Field SA, Noss AL, Packham G, et al. The anti-CD20 antibody rituximab augments the immunospecific therapeutic effectiveness of an anti-CD19 immunotoxin directed against human B-cell lymphoma. Br J Haematol 2006; 134:157-70; PMID:16771848; http://dx.doi.org/10. 1111/j.1365-2141.2006.06155.x.
9. Wolf E, Hofmeister R, Kufer P, Schlereth B, Baeuerle PA. BiTEs: bispecific antibody constructs with unique anti-tumor activity. Drug Discov Today 2005; 10:1237-44; PMID:16213416; http://dx.doi.org/10.1016/ S1359-6446(05)03554-3.
10. Baeuerle PA, Reinhardt C. Bispecific T-cell engaging antibodies for cancer therapy. Cancer Res 2009; 69:4941-4; PMID:19509221; http://dx.doi.org/10. 1158/0008-5472.CAN-09-0547.
11. Amann M, Brischwein K, Lutterbuese P, Parr L, Petersen L, Lorenczewski G, et al. Therapeutic window of MuS110, a single-chain antibody construct bispecific for murine EpCAM and murine CD3. Cancer Res 2008; 68:143-51; PMID:18172306; http://dx.doi.org/10.1158/0008-5472.CAN-07-2182.
12. d'Argouges S, Wissing S, Brandl C, Prang N, Lutterbuese R, Kozhich A, et al. Combination of rituximab with blinatumomab (MT103/MEDI-538), a T cell-engaging CD19-/CD3-bispecific antibody, for highly efficient lysis of human B lymphoma cells. Leuk Res 2009; 33:465-73; PMID:18835037; http://dx.doi.org/ 10.1016/j.leukres.2008.08.025.
13. Dreier T, Baeuerle PA, Fichtner I, Grün M, Schlereth B, Lorenczewski G, et al. T cell costimulus-independent and very efficacious inhibition of tumor growth in mice bearing subcutaneous or leukemic human B cell lymphoma xenografts by a CD19-/CD3- bispecific single-chain antibody construct. J Immunol 2003; 170:4397-402; PMID:12682277.
14. Viardot A, Goebeler M, Scheele JS, Zugmaier G, Noppeney R, Knop S, et al. Treatment of Patients with Non-Hodgkin Lymphoma (NHL) with CD19/ CD3 Bispecific Antibody Blinatumomab (MT103): Double-Step Dose Increase to Continuous Infusion of 60 {micro}g/m2/d Is Tolerable and Highly Effective. ASH Annual Meeting Abstracts 2010; 116:2880.
15. Topp MS, Kufer P, Gökbuget N, Goebeler M, Klinger M, Neumann S, et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy- refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol 2011; 29:2493-8; PMID:21576633; http://dx.doi.org/10.1200/JCO.2010.32.7270.
16. Kikuchi M, Tanaka J, Kondo T, Hashino S, Kasai M, Kurosawa M, et al. Clinical significance of minimal residual disease in adult acute lymphoblastic leukemia. Int J Hematol 2010; 92:481-9; PMID:20830615; http://dx.doi.org/10. 1007/s12185-010-0670-1.
17. Cazzaniga G, Valsecchi MG, Gaipa G, Conter V, Biondi A. Defining the correct role of minimal residual disease tests in the management of acute lymphoblastic leukaemia. Br J Haematol 2011; 155:45-52; PMID:21812769; http://dx.doi.org/10.1111/j.1365-2141.2011.08795.x.
18. Topp MS, Goekbuget N, Zugmaier G, Viardot A, Stelljes M, Neumann S, et al. Anti-CD19 BiTE Blinatumomab Induces High Complete Remission Rate In Adult Patients with Relapsed B-Precursor ALL: Updated Results of An Ongoing Phase II Trial. ASH Annual Meeting Abstracts 2011; 118:252.
19. Blanc V, Bousseau A, Caron A, Carrez C, Lutz RJ, Lambert JM. SAR3419: an anti-CD19-Maytansinoid Immunoconjugate for the treatment of B-cell malignancies. Clin Cancer Res 2011; 17:6448-58; PMID:22003072; http://dx.doi.org/10.1158/ 1078-0432.CCR-11-0485.
20. Al-Katib AM, Aboukameel A, Mohammad R, Bissery MC, Zuany-Amorim C. Superior antitumor activity of SAR3419 to rituximab in xenograft models for non-Hodgkin's lymphoma. Clin Cancer Res 2009; 15:4038-45; PMID:19509168; http://dx.doi.org/10.1158/1078-0432.CCR-08-2808.
21. Younes A, Gordon L, Kim S, Romaguera J, Copeland AR, de Castro Farial S, et al. Phase I Multi-Dose Escalation Study of the Anti-CD19 Maytansinoid Immunoconjugate SAR3419 Administered by Intravenous (IV) Infusion Every 3 Weeks to Patients with Relapsed/ Refractory B-Cell Non-Hodgkin's Lymphoma (NHL). ASH Annual Meeting Abstracts 2009; 114:585.
22. Coiffier B, Ribrag V, Dupuis J, Tilly H, Haioun C, Morschhauseret F, et al. Phase I/II study of the anti-CD19 maytansinoid immunoconjugate SAR3419 administered weekly to patients with relapsed/refractory B-cell non-Hodgkin's lymphoma (NHL). J Clin Oncol 2011; 29(suppl):8017.
23. Coiffier B, Morschhauser F, Dupuis J, Haioun C, Laine F, Houot R, et al. Phase I study cohort evaluating an optimized administration schedule of SAR3419, an anti-CD19 DM4-loaded antibody drug conjugate (ADC), in patients (pts) with CD19 positive relapsed/ refractory b-cell non-Hodgkin's lymphoma. J Clin Oncol 2012; 30(suppl):8057.
24. Herbst R, Wang Y, Gallagher S, Mittereder N, Kuta E, Damschroder M, et al. B-cell depletion in vitro and in vivo with an afucosylated anti-CD19 antibody. J Pharmacol Exp Ther 2010; 335:213-22; PMID:20605905; http://dx.doi.org/10.1124/jpet.110.168062.
25. Ward E, Mittereder N, Kuta E, Sims GP, Bowen MA, Dall'Acqua W, et al. A glycoengineered anti-CD19 antibody with potent antibody-dependent cellular cytotoxicity activity in vitro and lymphoma growth inhibition in vivo. Br J Haematol 2011; 155:426-37; PMID:21902688; http://dx.doi.org/10.1111/j.1365-2141. 2011.08857.x.
26. Goswami T, Forero A, Hamadani M, Sonet A, Verhoef G, Fanale MA, et al. Phase I/II study of MEDI-551, a humanized monoclonal antibody targeting CD19, in subjects with relapsed or refractory advanced B-cell malignancies. J Clin Oncol 2012; 30(suppl):8065.
27. Herrera L, Farah RA, Pellegrini VA, Aquino DB, Sandler ES, Buchanan GR, et al. Immunotoxins against CD19 and CD22 are effective in killing precursor-B acute lymphoblastic leukemia cells in vitro. Leukemia 2000; 14:853-8; PMID:10803517; http://dx.doi.org/10.1038/sj.leu.2401779.
28. Herrera L, Yarbrough S, Ghetie V, Aquino DB, Vitetta ES. Treatment of SCID/human B cell precursor ALL with anti-CD19 and anti-CD22 immunotoxins. Leukemia 2003; 17:334-8; PMID:12592332; http://dx.doi.org/10.1038/sj.leu. 2402790.
29. Herrera L, Bostrom B, Gore L, Sandler E, Lew G, Schlegel PG, et al. A phase 1 study of Combotox in pediatric patients with refractory B-lineage acute lymphoblastic leukemia. J Pediatr Hematol Oncol 2009; 31:936-41; PMID:19875969; http://dx.doi.org/10.1097/MPH.0b013e3181bdf211.
30. Schindler J, Gajavelli S, Ravandi F, Shen Y, Parekh S, Braunchweig I, et al. A phase I study of a combination of anti-CD19 and anti-CD22 immunotoxins (Combotox) in adult patients with refractory B-lineage acute lymphoblastic leukaemia. Br J Haematol 2011; 154:471-6; PMID:21732928; http://dx.doi.org/10. 1111/j.1365-2141.2011.08762.x.
31. Vallera DA, Chen H, Sicheneder AR, Panoskaltsis-Mortari A, Taras EP. Genetic alteration of a bispecific ligand-directed toxin targeting human CD19 and CD22 receptors resulting in improved efficacy against systemic B cell malignancy. Leuk Res 2009; 33:1233-42; PMID:19327829; http://dx.doi.org/10.1016/ j.leukres. 2009.02.006.
32. Horton HM, Bernett MJ, Pong E, Peipp M, Karki S, Chu SY, et al. Potent in vitro and in vivo activity of an Fc-engineered anti-CD19 monoclonal antibody against lymphoma and leukemia. Cancer Res 2008; 68:8049-57; PMID:18829563; http://dx.doi.org/10.1158/0008-5472.CAN-08-2268.
33. Awan FT, Lapalombella R, Trotta R, Butchar JP, Yu B, Benson DM Jr., et al. CD19 targeting of chronic lymphocytic leukemia with a novel Fc-domain-engineered monoclonal antibody. Blood 2010; 115:1204-13; PMID:19965644; http://dx.doi.org/10.1182/blood-2009-06-229039.
34. Rafiq S, Cheney C, Mo X, Jarjoura D, Muthusamy N, Byrd JC. XmAb-5574 antibody demonstrates superior antibody-dependent cellular cytotoxicity as compared with CD52- and CD20-targeted antibodies in adult acute lymphoblastic leukemia cells. Leukemia 2012; PMID:22333878; http://dx.doi.org/10.1038/leu. 2012.40.
35. Zalevsky J, Leung IW, Karki S, Chu SY, Zhukovsky EA, Desjarlais JR, et al. The impact of Fc engineering on an anti-CD19 antibody: increased Fcgamma receptor affinity enhances B-cell clearing in nonhuman primates. Blood 2009; 113:3735-43; PMID:19109559; http://dx.doi.org/10.1182/blood-2008-10-182048.
36. http://www.morphosys.com/pressrelease/morphosys-and-xencor-complete- enrollment-mor208-xmab5574-phase-1-trial-cll.
37. Chu SY, Vostiar I, Karki S, Moore GL, Lazar GA, Pong E, et al. Inhibition of B cell receptor-mediated activation of primary human B cells by coengagement of CD19 and FcgammaRIIb with Fc-engineered antibodies. Mol Immunol 2008; 45:3926-33; PMID:18691763; http://dx.doi.org/10.1016/j.molimm.2008.06.027.
38. Horton HM, Chu SY, Ortiz EC, Pong E, Cemerski S, Leung IW, et al. Antibody-mediated coengagement of FcγRIIb and B cell receptor complex suppresses humoral immunity in systemic lupus erythematosus. J Immunol 2011; 186:4223-33; PMID:21357255; http://dx.doi.org/10.4049/jimmunol.1003412.
39. Cardarelli PM, Rao-Naik C, Chen S, Huang H, Pham A, Moldovan-Loomis MC, et al. A nonfucosylated human antibody to CD19 with potent B-cell depletive activity for therapy of B-cell malignancies. Cancer Immunol Immunother 2010; 59:257-65; PMID:19657637; http://dx.doi.org/10.1007/s00262-009-0746-z.
40. Camacho LH, Joyce R, Brown JR, Chanan-Khan A, Amrein PC, Assad A, et al. A Phase 1, open-label, multi-center, multiple-dose, dose-escalation study of MDX-1342 in patients with CD19-positive refractory/ relapsed chronic lymphocytic leukemia. American Society of Hematology 51st annual meeting abstracts 2009; 114:3425.
41. http://www.seagen.com/product-pipeline-sgn19a.shtml.
42. Reusch U BC, Knackmuss SH, Fucek I, Eser M, McAleese F, et al. High affinity CD3 RECRUIT-TandAbs for T cell-mediated lysis of malignant CD19+ B cells. Cancer Res 2012; 72(Suppl):4624.
43. Zhukovsky E RU, Burkhardt C, Knackmuss S, Fucek I, Eser M, et al. High affinity CD3 RECRUIT TandAb for T cell-mediated lysis of CD19+ tumor B cells. J Clin Oncol 2012; 30(suppl):8059.
44. Hou SBS, Skegro D, Macoin J, Lissilaa R, Back J. Preclinical pharmacological characterization of GBR 401, a new monoclonal antibody directed against human CD19. Mol Cancer Ther 2011; 10(Suppl):C164; http://dx.doi.org/10. 1158/1535-7163.TARG-11-C164.
45. http://glenmarkpharma.com/GLN-NWS/PDF/Glenmark-GBR-401-final.pdf.
46. Johnson S, Burke S, Huang L, Gorlatov S, Li H, Wang W, et al. Effector cell recruitment with novel Fv-based dual-affinity re-targeting protein leads to potent tumor cytolysis and in vivo B-cell depletion. J Mol Biol 2010; 399:436-49; PMID:20382161; http://dx.doi.org/10.1016/j.jmb.2010.04.001.
47. http://www.macrogenics.com/Platforms-DART.html.
48. Moore PA, Zhang W, Rainey GJ, Burke S, Li H, Huang L, et al. Application of dual affinity retargeting molecules to achieve optimal redirected T-cell killing of B-cell lymphoma. Blood 2011; 117:4542-51; PMID:21300981; http://dx.doi.org/10.1182/blood-2010-09-306449.
49. Chicaybam L, Sodré AL, Bonamino M. Chimeric antigen receptors in cancer immuno-gene therapy: current status and future directions. Int Rev Immunol 2011; 30:294-311; PMID:22053970; http://dx.doi.org/10.3109/08830185. 2011.595855.
50. Kalos M. Muscle CARs and TcRs: turbo-charged technologies for the (T cell) masses. Cancer Immunol Immunother 2012; 61:127-35; PMID:22131062; http://dx.doi.org/10.1007/s00262-011-1173-5.
51. Kershaw MH, Westwood JA, Parker LL, Wang G, Eshhar Z, Mavroukakis SA, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 2006; 12:6106-15; PMID:17062687; http://dx.doi.org/10.1158/1078-0432.CCR-06-1183.
52. Till BG, Jensen MC, Wang J, Chen EY, Wood BL, Greisman HA, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood 2008; 112:2261-71; PMID:18509084; http://dx.doi.org/10.1182/blood-2007-12- 128843.
53. Park JR, Digiusto DL, Slovak M, Wright C, Naranjo A, Wagner J, et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther 2007; 15:825-33; PMID:17299405.
54. Chimeric Antigen Receptor-Modified T Cells in CLL. N Engl J Med 2011; 365:1937-9; http://dx.doi.org/10.1056/NEJMc1111004.
55. 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; 116:3875-86; PMID:20631379; http://dx.doi.org/10.1182/blood-2010-01-265041.
56. 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-receptor-transduced T cells. Blood 2012; 119:2709-20; PMID:22160384; http://dx.doi.org/10.1182/blood-2011-10-384388.
57. Kochenderfer JN, Wilson WH, Janik JE, Dudley ME, Stetler-Stevenson M, Feldman SA, et al. Eradication of B-lineage cells and regression of lymphoma in a patient treated with autologous T cells genetically engineered to recognize CD19. Blood 2010; 116:4099-102; PMID:20668228; http://dx.doi.org/10.1182/blood- 2010-04-281931.
58. Milone MC, Fish JD, Carpenito C, Carroll RG, Binder GK, Teachey D, et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 2009; 17:1453-64; PMID:19384291; http://dx.doi.org/10.1038/mt.2009.83.
59. 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; PMID:21832238; http://dx.doi.org/10.1126/scitranslmed.3002842.
60. 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; PMID:21830940; http://dx.doi.org/10.1056/ NEJMoa1103849.
61. Reichert JM, Dhimolea E. The future of antibodies as cancer drugs. Drug Discov Today 2012; In press. PMID:22561895; http://dx.doi.org/10.1016/j.drudis. 2012.04.006.