Heterodimeric bispecific antibody-derivatives against CD19 and CD16 induce effective antibody-dependent cellular cytotoxicity against B-lymphoid tumor cells

Cancer Letters

Volumn 303, Issue 2, 2011, Pages 128-139

  Kellner, Christian ^a   Bruenke, Joerg ^a   Horner, Heike ^b   Schubert, Joerg ^c   Schwenkert, Michael ^a   Mentz, Kristin ^a   Barbin, Karin ^a   Stein, Christoph ^a   Peipp, Matthias ^d   Stockmeyer, Bernhard ^b   Fey, Georg H ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

Bispecific antibody derivatives; CD19; Fc receptor; Natural killer cells; Tumor immunotherapy

Indexed keywords

BISPECIFIC ANTIBODY; CD16 ANTIBODY; CD19 ANTIBODY; HETERODIMER; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY COMBINING SITE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ARTICLE; B CELL LEUKEMIA; B CELL LYMPHOMA; BINDING AFFINITY; CANCER PATIENT; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOLYSIS; DRUG CYTOTOXICITY; DRUG SYNTHESIS; HEAVY CHAIN; HUMAN; HUMAN CELL; LEUKEMIA CELL; LIGHT CHAIN; LYMPHOMA CELL; NONHUMAN; PRIORITY JOURNAL;

ANTIBODIES, BISPECIFIC; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD19; CELL LINE, TUMOR; DIMERIZATION; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN FRAGMENTS; IMMUNOTHERAPY; KINETICS; LEUKOCYTES, MONONUCLEAR; LYMPHOMA, B-CELL; PROTEIN BINDING; RECEPTORS, IGG; RECOMBINANT FUSION PROTEINS;

EID: 79952038441     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2011.01.020     Document Type: Article

References (52)

1. Tedder T.F., Isaacs C.M. Isolation of cDNAs encoding the CD19 antigen of human and mouse B lymphocytes. A new member of the immunoglobulin superfamily. J. Immunol. 1989, 143:712-717.
2. Nadler L.M., Anderson K.C., Marti G., Bates M., Park E., Daley J.F., Schlossman S.F. B4, a human B lymphocyte-associated antigen expressed on normal, mitogen-activated, and malignant B lymphocytes. J. Immunol. 1983, 131:244-250.
3. Anderson K.C., Bates M.P., Slaughenhoupt B.L., Pinkus G.S., Schlossman S.F., Nadler L.M. Expression of human B cell-associated antigens on leukemias and lymphomas: a model of human B cell differentiation. Blood 1984, 63:1424-1433.
4. Ginaldi L., De Martinis M., Matutes E., Farahat N., Morilla R., Catovsky D. Levels of expression of CD19 and CD20 in chronic B cell leukaemias. J. Clin. Pathol. 1998, 51:364-369.
5. Castor A., Nilsson L., Astrand-Grundstrom I., Buitenhuis M., Ramirez C., Anderson K., Strombeck B., Garwicz S., Bekassy A.N., Schmiegelow K., Lausen B., Hokland P., Lehmann S., Juliusson G., Johansson B., Jacobsen S.E. Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nat. Med. 2005, 11:630-637.
6. Kong Y., Yoshida S., Saito Y., Doi T., Nagatoshi Y., Fukata M., Saito N., Yang S., Iwamoto C., Okamura J., Liu K., Huang X., Lu D., Shultz L., Harada M., Ishikawa F. CD34+CD38+CD19+ as well as CD34+CD38-CD19+ cells are leukemia-initiating cells with self-renewal capacity in human B-precursor ALL. Leukemia 2008, 22:1207-1213.
7. le Viseur C., Hotfilder M., Bomken S., Wilson K., Rottgers S., Schrauder A., Rosemann A., Irving J., Stam R.W., Shultz L.D., Harbott J., Jurgens H., Schrappe M., Pieters R., Vormoor J. In childhood acute lymphoblastic leukemia, blasts at different stages of immunophenotypic maturation have stem cell properties. Cancer Cell 2008, 14:47-58.
8. Grossbard M.L., Press O.W., Appelbaum F.R., Bernstein I.D., Nadler L.M. Monoclonal antibody-based therapies of leukemia and lymphoma. Blood 1992, 80:863-878.
9. Scheuermann R.H., Racila E. CD19 antigen in leukemia and lymphoma diagnosis and immunotherapy. Leuk. Lymphoma 1995, 18:385-397.
10. Horton H.M., Bernett M.J., Pong E., Peipp M., Karki S., Chu S.Y., Richards J.O., Vostiar I., Joyce P.F., Repp R., Desjarlais J.R., Zhukovsky E.A. Potent in vitro and in vivo activity of an Fc-engineered anti-CD19 monoclonal antibody against lymphoma and leukemia. Cancer Res. 2008, 68:8049-8057.
11. Yazawa N., Hamaguchi Y., Poe J.C., Tedder T.F. Immunotherapy using unconjugated CD19 monoclonal antibodies in animal models for B lymphocyte malignancies and autoimmune disease. Proc. Natl. Acad. Sci. USA 2005, 102:15178-15183.
12. Pietersz G.A., Wenjun L., Sutton V.R., Burgess J., McKenzie I.F., Zola H., Trapani J.A. In vitro and in vivo antitumor activity of a chimeric anti-CD19 antibody. Cancer Immunol. Immunother. 1995, 41:53-60.
13. Lang P., Barbin K., Feuchtinger T., Greil J., Peipp M., Zunino S.J., Pfeiffer M., Handgretinger R., Niethammer D., Fey G.H. Chimeric CD19 antibody mediates cytotoxic activity against leukemic blasts with effector cells from pediatric patients who received T-cell-depleted allografts. Blood 2004, 103:3982-3985.
14. Hekman A., Honselaar A., Vuist W.M., Sein J.J., Rodenhuis S., ten Bokkel Huinink W.W., Somers R., Rumke P., Melief C.J. Initial experience with treatment of human B cell lymphoma with anti-CD19 monoclonal antibody. Cancer Immunol. Immunother. 1991, 32:364-372.
15. Schwemmlein M., Stieglmaier J., Kellner C., Peipp M., Saul D., Oduncu F., Emmerich B., Stockmeyer B., Lang P., Beck J.D., Fey G.H. A CD19-specific single-chain immunotoxin mediates potent apoptosis of B-lineage leukemic cells. Leukemia 2007, 21:1405-1412.
16. Flavell D.J., Warnes S.L., Bryson C.J., Field S.A., Noss A.L., Packham G., Flavell S.U. 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, 134:157-170.
17. Clynes R.A., Towers T.L., Presta L.G., Ravetch J.V. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat. Med. 2000, 6:443-446.
18. Cartron G., Dacheux L., Salles G., Solal-Celigny P., Bardos P., Colombat P., Watier H. Therapeutic activity of humanized anti-CD20 monoclonal antibody and polymorphism in IgG Fc receptor FcgammaRIIIa gene. Blood 2002, 99:754-758.
19. Weng W.K., Levy R. Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J. Clin. Oncol. 2003, 21:3940-3947.
20. Musolino A., Naldi N., Bortesi B., Pezzuolo D., Capelletti M., Missale G., Laccabue D., Zerbini A., Camisa R., Bisagni G., Neri T.M., Ardizzoni A. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J. Clin. Oncol. 2008, 26:1789-1796.
21. Barbin K., Stieglmaier J., Saul D., Stieglmaier K., Stockmeyer B., Pfeiffer M., Lang P., Fey G.H. Influence of variable N-glycosylation on the cytolytic potential of chimeric CD19 antibodies. J. Immunother. 2006, 29:122-133.
22. Peipp M., Valerius T. Bispecific antibodies targeting cancer cells. Biochem. Soc. Trans. 2002, 30:507-511.
23. Otz T., Grosse-Hovest L., Hofmann M., Rammensee H.G., Jung G. A bispecific single-chain antibody that mediates target cell-restricted, supra-agonistic CD28 stimulation and killing of lymphoma cells. Leukemia 2009, 23:71-77.
24. Bruenke J., Fischer B., Barbin K., Schreiter K., Wachter Y., Mahr K., Titgemeyer F., Niederweis M., Peipp M., Zunino S.J., Repp R., Valerius T., Fey G.H. A recombinant bispecific single-chain Fv antibody against HLA class II and FcgammaRIII (CD16) triggers effective lysis of lymphoma cells. Br. J. Haematol. 2004, 125:167-179.
25. Guyre P.M., Graziano R.F., Vance B.A., Morganelli P.M., Fanger M.W. Monoclonal antibodies that bind to distinct epitopes on Fc gamma RI are able to trigger receptor function. J. Immunol. 1989, 143:1650-1655.
26. Muller D., Kontermann E. Bispecific antibodies. Handbook of Therapeutic Antibodies 2007, 345-378. WILEY, VCH Verlag Weinheim. S. Dübel (Ed.).
27. Bruenke J., Barbin K., Kunert S., Lang P., Pfeiffer M., Stieglmaier K., Niethammer D., Stockmeyer B., Peipp M., Repp R., Valerius T., Fey G.H. Effective lysis of lymphoma cells with a stabilised bispecific single-chain Fv antibody against CD19 and FcgammaRIII (CD16). Br. J. Haematol. 2005, 130:218-228.
28. Kipriyanov S.M., Cochlovius B., Schafer H.J., Moldenhauer G., Bahre A., Le Gall F., Knackmuss S., Little M. Synergistic antitumor effect of bispecific CD19×CD3 and CD19×CD16 diabodies in a preclinical model of non-Hodgkin's lymphoma. J. Immunol. 2002, 169:137-144.
29. Bargou R., Leo E., Zugmaier G., Klinger M., Goebeler M., Knop S., Noppeney R., Viardot A., Hess G., Schuler M., Einsele H., Brandl C., Wolf A., Kirchinger P., Klappers P., Schmidt M., Riethmuller G., Reinhardt C., Baeuerle P.A., Kufer P. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008, 321:974-977.
30. d'Argouges S., Wissing S., Brandl C., Prang N., Lutterbuese R., Kozhich A., Suzich J., Locher M., Kiener P., Kufer P., Hofmeister R., Baeuerle P.A., Bargou R.C. 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. 2008.
31. Eyrich M., Lang P., Lal S., Bader P., Handgretinger R., Klingebiel T., Niethammer D., Schlegel P.G. A prospective analysis of the pattern of immune reconstitution in a paediatric cohort following transplantation of positively selected human leucocyte antigen-disparate haematopoietic stem cells from parental donors. Br. J. Haematol. 2001, 114:422-432.
32. McCall A.M., Shahied L., Amoroso A.R., Horak E.M., Simmons H.H., Nielson U., Adams G.P., Schier R., Marks J.D., Weiner L.M. Increasing the affinity for tumor antigen enhances bispecific antibody cytotoxicity. J. Immunol. 2001, 166:6112-6117.
33. Shahied L.S., Tang Y., Alpaugh R.K., Somer R., Greenspon D., Weiner L.M. Bispecific minibodies targeting HER2/neu and CD16 exhibit improved tumor lysis when placed in a divalent tumor antigen binding format. J. Biol. Chem. 2004, 279:53907-53914.
34. Schoonjans R., Willems A., Schoonooghe S., Fiers W., Grooten J., Mertens N. Fab chains as an efficient heterodimerization scaffold for the production of recombinant bispecific and trispecific antibody derivatives. J. Immunol. 2000, 165:7050-7057.
35. Schoonjans R., Willems A., Schoonooghe S., Leoen J., Grooten J., Mertens N. A new model for intermediate molecular weight recombinant bispecific and trispecific antibodies by efficient heterodimerization of single chain variable domains through fusion to a Fab-chain. Biomol. Eng. 2001, 17:193-202.
36. Lu H., Shi M., Wang M., Xie Z., Hu M., Yu M., Shen B., Ma Y., Guo N. In vitro and in vivo antitumor effect of a trivalent bispecific antibody targeting ErbB2 and CD16. Cancer Biol. Ther. 2008, 7.
37. Kontermann R.E. Recombinant bispecific antibodies for cancer therapy. Acta Pharmacol. Sin. 2005, 26:1-9.
38. Bird R.E., Walker B.W. Single chain antibody variable regions. Trends Biotechnol. 1991, 9:132-137.
39. Quintero-Hernandez V., Juarez-Gonzalez V.R., Ortiz-Leon M., Sanchez R., Possani L.D., Becerril B. The change of the scFv into the Fab format improves the stability and in vivo toxin neutralization capacity of recombinant antibodies. Mol. Immunol. 2007, 44:1307-1315.
40. Meeker T.C., Miller R.A., Link M.P., Bindl J., Warnke R., Levy R. A unique human B lymphocyte antigen defined by a monoclonal antibody. Hybridoma 1984, 3:305-320.
41. Fleit H.B., Wright S.D., Unkeless J.C. Human neutrophil Fc gamma receptor distribution and structure. Proc. Natl. Acad. Sci. USA 1982, 79:3275-3279.
42. Greil J., Gramatzki M., Burger R., Marschalek R., Peltner M., Trautmann U., Hansen-Hagge T.E., Bartram C.R., Fey G.H., Stehr K., et al. The acute lymphoblastic leukaemia cell line SEM with t(4;11) chromosomal rearrangement is biphenotypic and responsive to interleukin-7. Br. J. Haematol. 1994, 86:275-283.
43. Peipp M., Kupers H., Saul D., Schlierf B., Greil J., Zunino S.J., Gramatzki M., Fey G.H. A recombinant CD7-specific single-chain immunotoxin is a potent inducer of apoptosis in acute leukemic T cells. Cancer Res. 2002, 62:2848-2855.
44. J. Sambrook, D.W. Russel, Molecular Cloning: A Laboratory Manual, Cold Spring Harbour, NY, 2001.
45. Kellner C., Bruenke J., Stieglmaier J., Schwemmlein M., Schwenkert M., Singer H., Mentz K., Peipp M., Lang P., Oduncu F., Stockmeyer B., Fey G.H. A novel CD19-directed recombinant bispecific antibody derivative with enhanced immune effector functions for human leukemic cells. J. Immunother. 2008, 31:871-884.
46. Benedict C.A., MacKrell A.J., Anderson W.F. Determination of the binding affinity of an anti-CD34 single-chain antibody using a novel, flow cytometry based assay. J. Immunol. Methods 1997, 201:223-231.
47. Adams G.P., Schier R., McCall A.M., Crawford R.S., Wolf E.J., Weiner L.M., Marks J.D. Prolonged in vivo tumour retention of a human diabody targeting the extracellular domain of human HER2/neu. Br. J. Cancer 1998, 77:1405-1412.
48. Elsasser D., Valerius T., Repp R., Weiner G.J., Deo Y., Kalden J.R., van de Winkel J.G., Stevenson G.T., Glennie M.J., Gramatzki M. HLA class II as potential target antigen on malignant B cells for therapy with bispecific antibodies in combination with granulocyte colony-stimulating factor. Blood 1996, 87:3803-3812.
49. Zola H., MacArdle P.J., Bradford T., Weedon H., Yasui H., Kurosawa Y. Preparation and characterization of a chimeric CD19 monoclonal antibody. Immunol. Cell Biol. 1991, 69(Pt 6):411-422.
50. C. Rao-Naik, D.J. King, J. Liu, H. Huang, D.B. Passmore, A.F. Bell, J. Cardarelli, C. Pan, T.U. Thi Do, S. Chen, CD19 antibodies and their uses, WO 2007/002223, 2007.
51. Kipriyanov S.M., Moldenhauer G., Schuhmacher J., Cochlovius B., Von der Lieth C.W., Matys E.R., Little M. Bispecific tandem diabody for tumor therapy with improved antigen binding and pharmacokinetics. J. Mol. Biol. 1999, 293:41-56.
52. P.A. Thompson, J.A. Ledbetter, M.S. Hayden-Ledbetter, L.S. Grosmaire, R. Bader, W. Brady, L. Tchistiakova, M.T. Follettie, V. Calabro, Single-chain multivalent binding proteins with effector function, WO 2007/146968, 2007.