A new class of bispecific antibodies to redirect T cells for cancer immunotherapy

mAbs

Volumn 6, Issue 2, 2014, Pages 381-391

  Rossi, Diane L ^a   Rossi, Edmund A ^a,b   Cardillo, Thomas M ^a   Goldenberg, David M ^a,b,c   Chang, Chien Hsing ^a,b  

^a IMMUNOMEDICS INC   (United States)

^b IBC Pharmaceuticals Inc   (United States)

^c CENTER FOR MOLECULAR MEDICINE AND IMMUNOLOGY   (United States)

Author keywords

Bispecific antibody; Burkitt lymphoma; DOCK AND LOCK; Pancreatic cancer; T cell redirected therapy

Indexed keywords

ANTINEOPLASTIC AGENT; BISPECIFIC ANTIBODY; BISPECIFIC MONOCLONAL ANTIBODY OKT3 SCFV AD2; CD3 ANTIGEN; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BURKITT LYMPHOMA; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CHEMICAL ANALYSIS; CLINICAL STUDY; CONTROLLED STUDY; CYTOTOXICITY; DAUDI CELL; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; IN VITRO STUDY; IN VIVO STUDY; KIDNEY CLEARANCE; LEUKEMIA CELL LINE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PANCREAS CARCINOMA; PLASMA CLEARANCE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TARGET CELL;

BISPECIFIC ANTIBODY; BURKITT LYMPHOMA; DOCK-AND-LOCK; PANCREATIC CANCER; T-CELL REDIRECTED THERAPY;

ANIMALS; ANTIGENS, CD3; ANTIGENS, NEOPLASM; BURKITT LYMPHOMA; CANCER VACCINES; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; IMMUNOLOGICAL SYNAPSES; IMMUNOTHERAPY; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, SCID; PANCREATIC NEOPLASMS; PROTEIN BINDING; PROTEIN ENGINEERING; SINGLE-CHAIN ANTIBODIES; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85047686965     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.4161/mabs.27385     Document Type: Article

References (53)

1. June CH. Adoptive T cell therapy for cancer in the clinic. J Clin Invest 2007; 117:1466-76; PMID:17549249; http://dx.doi.org/10.1172/JCI32446
2. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E, Greenberg PD. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A 2002; 99:16168-73; PMID:12427970; http://dx.doi.org/10.1073/pnas.242600099
3. Rosenberg SA. Cell transfer immunotherapy for metastatic solid cancer - what clinicians need to know. Nat Rev Clin Oncol 2011; 8:577-85; PMID:21808266; http://dx.doi.org/10.1038/nrclinonc.2011.116
4. Gilham DE, Debets R, Pule M, Hawkins RE, Abken H. CAR-T cells and solid tumors: tuning T cells to challenge an inveterate foe. Trends Mol Med 2012; 18:377-84; PMID:22613370; http://dx.doi.org/10.1016/j.molmed.2012.04.009
5. Liu L, Sun M, Wang Z. Adoptive T-cell therapy of B-cell malignancies: conventional and physiological chimeric antigen receptors. Cancer Lett 2012; 316:1-5; PMID:22099879; http://dx.doi.org/10.1016/j.canlet.2011.10.027
6. Perez P, Hoffman RW, Shaw S, Bluestone JA, Segal DM. Specific targeting of cytotoxic T cells by anti-T3 linked to anti-target cell antibody. Nature 1985; 316:354-6; PMID:3160953; http://dx.doi.org/10.1038/316354a0
7. Staerz UD, Kanagawa O, Bevan MJ. Hybrid antibodies can target sites for attack by T cells. Nature 1985; 314:628-31; PMID:2859527; http://dx.doi.org/10. 1038/314628a0
8. Staerz UD, Bevan MJ. Hybrid hybridoma producing a bispecific monoclonal antibody that can focus effector T-cell activity. Proc Natl Acad Sci U S A 1986; 83:1453-7; PMID:2869486; http://dx.doi.org/10.1073/pnas.83.5.1453
9. Choi BD, Cai M, Bigner DD, Mehta AI, Kuan CT, Sampson JH. Bispecific antibodies engage T cells for antitumor immunotherapy. Expert Opin Biol Ther 2011; 11:843-53; PMID:21449821; http://dx.doi.org/10.1517/14712598.2011.572874
10. Koristka S, Cartellieri M, Theil A, Feldmann A, Arndt C, Stamova S, Michalk I, Töpfer K, Temme A, Kretschmer K, et al. Retargeting of human regulatory T cells by single-chain bispecific antibodies. J Immunol 2012; 188:1551-8; PMID:22184723; http://dx.doi.org/10.4049/jimmunol.1101760
11. Lum LG, Thakur A. Targeting T cells with bispecific antibodies for cancer therapy. BioDrugs 2011; 25:365-79; PMID:22050339; http://dx.doi.org/10.2165/ 11595950-000000000-00000
12. Segal DM, Weiner GJ, Weiner LM. Bispecific antibodies in cancer therapy. Curr Opin Immunol 1999; 11:558-62; PMID:10508714; http://dx.doi.org/10.1016/ S0952-7915(99)00015-1
13. 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
14. Nagorsen D, Baeuerle PA. Immunomodulatory therapy of cancer with T cell-engaging BiTE antibody blinatumomab. Exp Cell Res 2011; 317:1255-60; PMID:21419116; http://dx.doi.org/10.1016/j.yexcr.2011.03.010
15. 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
16. Moore PA, Zhang W, Rainey GJ, Burke S, Li H, Huang L, Gorlatov S, Veri MC, Aggarwal S, Yang Y, 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
17. Asano R, Ikoma K, Sone Y, Kawaguchi H, Taki S, Hayashi H, Nakanishi T, Umetsu M, Katayose Y, Unno M, et al. Highly enhanced cytotoxicity of a dimeric bispecific diabody, the hEx3 tetrabody. J Biol Chem 2010; 285:20844-9; PMID:20444691; http://dx.doi.org/10.1074/jbc.M110.120444
18. Bühler P, Wolf P, Gierschner D, Schaber I, Katzenwadel A, Schultze-Seemann W, Wetterauer U, Tacke M, Swamy M, Schamel WW, et al. A bispecific diabody directed against prostate-specific membrane antigen and CD3 induces T-cell mediated lysis of prostate cancer cells. Cancer Immunol Immunother 2008; 57:43-52; PMID:17579857; http://dx.doi.org/10.1007/s00262-007- 0348-6
19. Feldmann A, Stamova S, Bippes CC, Bartsch H, Wehner R, Schmitz M, Temme A, Cartellieri M, Bachmann M. Retargeting of T cells to prostate stem cell antigen expressing tumor cells: comparison of different antibody formats. Prostate 2011; 71:998-1011; PMID:21541976; http://dx.doi.org/10.1002/pros.21315
20. Kipriyanov SM, Moldenhauer G, Strauss G, Little M. Bispecific CD3 x CD19 diabody for T cell-mediated lysis of malignant human B cells. Int J Cancer 1998; 77:763-72; PMID:9688311; http://dx.doi.org/10.1002/(SICI)1097-0215(19980831)77: 5〈763::AID-IJC16〉3.0.CO;2-2
21. Stork R, Müller D, Kontermann RE. A novel trifunctional antibody fusion protein with improved pharmacokinetic properties generated by fusing a bispecific single-chain diabody with an albumin-binding domain from streptococcal protein G. Protein Eng Des Sel 2007; 20:569-76; PMID:17982179; http://dx.doi.org/10.1093/protein/gzm061
22. Seimetz D, Lindhofer H, Bokemeyer C. Development and approval of the trifunctional antibody catumaxomab (anti-EpCAM x anti-CD3) as a targeted cancer immunotherapy. Cancer Treat Rev 2010; 36:458-67; PMID:20347527; http://dx.doi.org/10.1016/j.ctrv.2010.03.001
23. Sheridan C. Amgen swallows Micromet to BiTE into ALL market. Nat Biotechnol 2012; 30:300-1; PMID:22491268; http://dx.doi.org/10.1038/nbt0412-300c
24. Frankel SR, Baeuerle PA. Targeting T cells to tumor cells using bispecific antibodies. Curr Opin Chem Biol 2013; 17:385-92; PMID:23623807; http://dx.doi.org/10.1016/j.cbpa.2013.03.029
25. Winkler U, Jensen M, Manzke O, Schulz H, Diehl V, Engert A. Cytokine-release syndrome in patients with B-cell chronic lymphocytic leukemia and high lymphocyte counts after treatment with an anti-CD20 monoclonal antibody (rituximab, IDECC2B8). Blood 1999; 94:2217-24; PMID:10498591
26. Wing MG, Moreau T, Greenwood J, Smith RM, Hale G, Isaacs J, Waldmann H, Lachmann PJ, Compston A. Mechanism of first-dose cytokine-release syndrome by CAMPATH 1-H: involvement of CD16 (FcgammaRIII) and CD11a/CD18 (LFA-1) on NK cells. J Clin Invest 1996; 98:2819-26; PMID:8981930; http://dx.doi.org/10.1172/ JCI119110
27. Chatenoud L, Ferran C, Reuter A, Legendre C, Gevaert Y, Kreis H, Franchimont P, Bach JF. Systemic reaction to the anti-T-cell monoclonal antibody OKT3 in relation to serum levels of tumor necrosis factor and interferon-gamma [corrected]. N Engl J Med 1989; 320:1420-1; PMID:2785642; http://dx.doi.org/10. 1056/NEJM198905253202117
28. Suntharalingam G, Perry MR, Ward S, Brett SJ, Castello-Cortes A, Brunner MD, Panoskaltsis N. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med 2006; 355:1018-28; PMID:16908486; http://dx.doi.org/10.1056/NEJMoa063842
29. Klinger M, Brandl C, Zugmaier G, Hijazi Y, Bargou RC, Topp MS, Gökbuget N, Neumann S, Goebeler M, Viardot A, et al. Immunopharmacologic response of patients with B-lineage acute lymphoblastic leukemia to continuous infusion of T cell-engaging CD19/CD3-bispecific BiTE antibody blinatumomab. Blood 2012; 119:6226-33; PMID:22592608; http://dx.doi.org/10.1182/blood-2012-01- 400515
30. Kiewe P, Hasmüller S, Kahlert S, Heinrigs M, Rack B, Marmé A, Korfel A, Jäger M, Lindhofer H, Sommer H, et al. Phase I trial of the trifunctional anti-HER2 x anti-CD3 antibody ertumaxomab in metastatic breast cancer. Clin Cancer Res 2006; 12:3085-91; PMID:16707606; http://dx.doi.org/10. 1158/1078-0432.CCR-05-2436
31. Heiss MM, Ströhlein MA, Jäger M, Kimmig R, Burges A, Schoberth A, Jauch KW, Schildberg FW, Lindhofer H. Immunotherapy of malignant ascites with trifunctional antibodies. Int J Cancer 2005; 117:435-43; PMID:15906359; http://dx.doi.org/10.1002/ijc.21165
32. Chang CH, Rossi EA, Goldenberg DM. The dock and lock method: a novel platform technology for building multivalent, multifunctional structures of defined composition with retained bioactivity. Clin Cancer Res 2007; 13:5586s-91s; PMID:17875793; http://dx.doi.org/10.1158/1078-0432.CCR-07-1217
33. Rossi EA, Goldenberg DM, Chang CH. The dock-and-lock method combines recombinant engineering with site-specific covalent conjugation to generate multifunctional structures. Bioconjug Chem 2012; 23:309-23; PMID:22168393; http://dx.doi.org/10.1021/bc2004999
34. Rossi EA, Goldenberg DM, Cardillo TM, McBride WJ, Sharkey RM, Chang CH. Stably tethered multifunctional structures of defined composition made by the dock and lock method for use in cancer targeting. Proc Natl Acad Sci U S A 2006; 103:6841-6; PMID:16636283; http://dx.doi.org/10.1073/pnas.0600982103
35. Rossi EA, Chang CH, Cardillo TM, Goldenberg DM. Optimization of multivalent bispecific antibodies and immunocytokines with improved in vivo properties. Bioconjug Chem 2013; 24:63-71; PMID:23116517; http://dx.doi.org/10. 1021/bc300488f
36. Rossi DL, Rossi EA, Goldenberg DM, Chang CH. A new mammalian host cell with enhanced survival enables completely serum-free development of high-level protein production cell lines. Biotechnol Prog 2011; 27:766-75; PMID:21473000; http://dx.doi.org/10.1002/btpr.584
37. Hultin LE, Hausner MA, Hultin PM, Giorgi JV. CD20 (pan-B cell) antigen is expressed at a low level on a subpopulation of human T lymphocytes. Cytometry 1993; 14:196-204; PMID:7679964; http://dx.doi.org/10.1002/cyto.990140212
38. Chang CH, Wang Y, Trisal P, Li R, Rossi DL, Nair A, Gupta P, Losman M, Cardillo TM, Rossi EA, et al. Evaluation of a novel hexavalent humanized anti-IGF-1R antibody and its bivalent parental IgG in diverse cancer cell lines. PLoS One 2012; 7:e44235; PMID:22952934; http://dx.doi.org/10.1371/journal.pone. 0044235
39. Gupta P, Goldenberg DM, Rossi EA, Cardillo TM, Byrd JC, Muthusamy N, Furman RR, Chang CH. Dual-targeting immunotherapy of lymphoma: potent cytotoxicity of anti-CD20/CD74 bispecific antibodies in mantle cell and other lymphomas. Blood 2012; 119:3767-78; PMID:22271448; http://dx.doi.org/10.1182/ blood-2011-09-381988
40. Rossi EA, Goldenberg DM, Cardillo TM, Stein R, Wang Y, Chang CH. Novel designs of multivalent anti-CD20 humanized antibodies as improved lymphoma therapeutics. Cancer Res 2008; 68:8384-92; PMID:18922911; http://dx.doi.org/10. 1158/0008-5472.CAN-08-2033
41. Rossi EA, Goldenberg DM, Cardillo TM, Stein R, Chang CH. Hexavalent bispecific antibodies represent a new class of anticancer therapeutics: 1. Properties of anti-CD20/CD22 antibodies in lymphoma. Blood 2009; 113:6161-71; PMID:19372261; http://dx.doi.org/10.1182/blood-2008-10-187138
42. Gold DV, Goldenberg DM, Karacay H, Rossi EA, Chang CH, Cardillo TM, McBride WJ, Sharkey RM. A novel bispecific, trivalent antibody construct for targeting pancreatic carcinoma. Cancer Res 2008; 68:4819-26; PMID:18559529; http://dx.doi.org/10.1158/0008-5472.CAN-08-0232
43. Sharkey RM, van Rij CM, Karacay H, Rossi EA, Frielink C, Regino C, Cardillo TM, McBride WJ, Chang CH, Boerman OC, et al. A new Tri-Fab bispecific antibody for pretargeting Trop-2-expressing epithelial cancers. J Nucl Med 2012; 53:1625-32; PMID:22952342; http://dx.doi.org/10.2967/jnumed.112.104364
44. Rossi EA, Goldenberg DM, Cardillo TM, Stein R, Chang CH. CD20-targeted tetrameric interferon-alpha, a novel and potent immunocytokine for the therapy of B-cell lymphomas. Blood 2009; 114:3864-71; PMID:19710501; http://dx.doi.org/10.1182/blood-2009-06-228890
45. Rossi EA, Rossi DL, Stein R, Goldenberg DM, Chang CH. A bispecific antibody-IFNalpha2b immunocytokine targeting CD20 and HLA-DR is highly toxic to human lymphoma and multiple myeloma cells. Cancer Res 2010; 70:7600-9; PMID:20876805; http://dx.doi.org/10.1158/0008-5472.CAN-10-2126
46. Rossi EA, Rossi DL, Cardillo TM, Stein R, Goldenberg DM, Chang CH. Preclinical studies on targeted delivery of multiple IFNα 2b to HLA-DR in diverse hematologic cancers. Blood 2011; 118:1877-84; PMID:21680794; http://dx.doi.org/10.1182/blood-2011-03-343145
47. Chang CH, Rossi EA, Cardillo TM, Nordstrom DL, McBride WJ, Goldenberg DM. A new method to produce monoPEGylated dimeric cytokines shown with human interferon-α 2b. Bioconjug Chem 2009; 20:1899-907; PMID:19736932; http://dx.doi.org/10.1021/bc9001773
48. Chang CH, Hinkula J, Loo M, Falkeborn T, Li R, Cardillo TM, Rossi EA, Goldenberg DM, Wahren B. A novel class of anti-HIV agents with multiple copies of enfuvirtide enhances inhibition of viral replication and cellular transmission in vitro. PLoS One 2012; 7:e41235; PMID:22844444; http://dx.doi.org/10.1371/journal.pone.0041235
49. Bargou R, Leo E, Zugmaier G, Klinger M, Goebeler M, Knop S, Noppeney R, Viardot A, Hess G, Schuler M, et al. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008; 321:974-7; PMID:18703743; http://dx.doi.org/10.1126/science.1158545
50. Topp MS, Kufer P, Gökbuget N, Goebeler M, Klinger M, Neumann S, Horst HA, Raff T, Viardot A, Schmid M, et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapyrefractory 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
51. Bluemel C, Hausmann S, Fluhr P, Sriskandarajah M, Stallcup WB, Baeuerle PA, Kufer P. Epitope distance to the target cell membrane and antigen size determine the potency of T cell-mediated lysis by BiTE antibodies specific for a large melanoma surface antigen. Cancer Immunol Immunother 2010; 59:1197-209; PMID:20309546; http://dx.doi.org/10.1007/s00262-010-0844-y
52. Dreier T, Baeuerle PA, Fichtner I, Grün M, Schlereth B, Lorenczewski G, Kufer P, Lutterbüse R, Riethmüller G, Gjorstrup P, 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
53. Schlereth B, Fichtner I, Lorenczewski G, Kleindienst P, Brischwein K, da Silva A, Kufer P, Lutterbuese R, Junghahn I, Kasimir-Bauer S, et al. Eradication of tumors from a human colon cancer cell line and from ovarian cancer metastases in immunodeficient mice by a single-chain Ep-CAM-/CD3-bispecific antibody construct. Cancer Res 2005; 65:2882-9; PMID:15805290; http://dx.doi.org/10.1158/0008-5472.CAN-04-2637