Structural design of disialoganglioside GD2 and CD3-bispecific antibodies to redirect T cells for tumor therapy

International Journal of Cancer

Volumn 136, Issue 2, 2015, Pages 476-486

  Cheng, Ming ^a   Ahmed, Mahiuddin ^a   Xu, Hong ^a   Cheung, Nai Kong V ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

bispecificity; disialoganglioside; immunotherapy; neuroblastoma; structure

Indexed keywords

ANTINEOPLASTIC AGENT; GD2 CD3 SCFV ANTIBODY; UNCLASSIFIED DRUG; BISPECIFIC ANTIBODY; CD3 ANTIGEN; GANGLIOSIDE; GANGLIOSIDE, GD2; MONOCLONAL ANTIBODY; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY STRUCTURE; ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL MEDIATED CYTOTOXICITY; COMPUTER MODEL; CONTROLLED STUDY; CYTOKINE RELEASE; DISULFIDE BOND; DRUG DESIGN; DRUG EFFICACY; DRUG STRUCTURE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MOLECULAR MODEL; MOUSE; NEUROBLASTOMA; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SMALL CELL LUNG CANCER; T LYMPHOCYTE; THERMOSTABILITY; TUMOR CELL DESTRUCTION; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; NUDE MOUSE; TRANSPLANTATION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; BLOTTING, WESTERN; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GANGLIOSIDES; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MELANOMA; MICE; MICE, INBRED BALB C; MICE, NUDE; MODELS, MOLECULAR; NEUROBLASTOMA; SINGLE-CHAIN ANTIBODIES; T-LYMPHOCYTES; TUMOR CELLS, CULTURED;

EID: 84921332022     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29007     Document Type: Article

References (35)

1. Cheung NK, Dyer MA,. Neuroblastoma: developmental biology, cancer genomics, and immunotherapy. Nat Rev Cancer 2013; 13: 397-411.
2. Wisloff F, Froland SS, Michaelsen TE,. Antibody-dependent cytotoxicity mediated by human Fc-receptor-bearing cells lacking markers for B- and T-lymphocytes. Int Arch Allergy Appl Immunol 1974; 47: 139-54.
3. Wolf E, Hofmeister R, Kufer P, et al., BiTEs: bispecific antibody constructs with unique anti-tumor activity. Drug Discov Today 2005; 10: 1237-44.
4. Offner S, Hofmeister R, Romaniuk A, et al., Induction of regular cytolytic T cell synapses by bispecific single-chain antibody constructs on MHC class I-negative tumor cells. Mol Immunol 2006; 43: 763-71.
5. Thiery J, Keefe D, Boulant S, et al., Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol 2011; 12: 770-7.
6. Dreier T, Baeuerle PA, Fichtner I, 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.
7. Choi BD, Kuan CT, Cai M, et al., Systemic administration of a bispecific antibody targeting EGFRvIII successfully treats intracerebral glioma. Proc Natl Acad Sci USA 2013; 110: 270-5.
8. Bargou R, Leo E, Zugmaier G, et al., Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008; 321: 974-7.
9. Topp MS, Kufer P, Gokbuget N, 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.
10. Schlereth B, Fichtner I, Lorenczewski G, 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.
11. Lutterbuese R, Raum T, Kischel R, et al., T cell-engaging BiTE antibodies specific for EGFR potently eliminate KRAS- and BRAF-mutated colorectal cancer cells. Proc Natl Acad Sci USA 2010; 107: 12605-10.
12. Wu ZL, Schwartz E, Seeger R, et al., Expression of GD2 ganglioside by untreated primary human neuroblastomas. Cancer Res 1986; 46: 440-3.
13. Hersey P, Jamal O, Henderson C, et al., Expression of the gangliosides GM3, GD3 and GD2 in tissue sections of normal skin, naevi, primary and metastatic melanoma. Int J Cancer 1988; 41: 336-43.
14. Yu AL, Gilman AL, Ozkaynak MF, et al., Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 2010; 363: 1324-34.
15. Albertini MR, Hank JA, Gadbaw B, et al., Phase II trial of hu14.18-IL2 for patients with metastatic melanoma. Cancer Immunol Immunother 2012; 61: 2261-71.
16. Delgado DC, Hank JA, Kolesar J, et al., Genotypes of NK cell KIR receptors, their ligands, and Fcgamma receptors in the response of neuroblastoma patients to Hu14.18-IL2 immunotherapy. Cancer Res 2010; 70: 9554-61.
17. Cheung NK, Cheung IY, Kushner BH, et al., Murine anti-GD2 monoclonal antibody 3F8 combined with granulocyte-macrophage colony-stimulating factor and 13-cis-retinoic acid in high-risk patients with stage 4 neuroblastoma in first remission. J Clin Oncol 2012; 30: 3264-70.
18. Cheung NK, Guo H, Hu J, et al., Humanizing murine IgG3 anti-GD2 antibody m3F8 substantially improves antibody-dependent cell-mediated cytotoxicity while retaining targeting in vivo. Oncoimmunology 2012; 1: 477-86.
19. Yu AL, Gilman AL, Ozkaynak MF, et al., Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 2010; 363: 1324-34.
20. Cheung NK, Modak S, Lin Y, et al., Single-chain Fv-streptavidin substantially improved therapeutic index in multistep targeting directed at disialoganglioside GD2. J Nucl Med 2004; 45: 867-77.
21. Hu J, Huang X, Ling CC, et al., Reducing epitope spread during affinity maturation of an anti-ganglioside GD2 antibody. J Immunol 2009; 183: 5748-55.
22. Chatenoud L,. Anti-CD3 antibodies: towards clinical antigen-specific immunomodulation. Curr Opin Pharmacol 2004; 4: 403-7.
23. Adair JR, Athwal DS, Bodmer MW, et al., Humanization of the murine anti-human CD3 monoclonal antibody OKT3. Hum Antibodies Hybridomas 1994; 5: 41-7.
24. Jung SH, Pastan I, Lee B,. Design of interchain disulfide bonds in the framework region of the Fv fragment of the monoclonal antibody B3. Proteins 1994; 19: 35-47.
25. Reiter Y, Brinkmann U, Lee B, et al., Engineering antibody Fv fragments for cancer detection and therapy: disulfide-stabilized Fv fragments. Nat Biotechnol 1996; 14: 1239-45.
26. Wu G, Robertson DH, Brooks CL 3rd, Vieth M,. Detailed analysis of grid-based molecular docking: a case study of CDOCKER-A CHARMm-based MD docking algorithm. J Comput Chem 2003; 24: 1549-62.
27. Ahmed M, Goldgur Y, Hu J, et al., In silico driven redesign of a clinically relevant antibody for the treatment of GD2 positive tumors. PloS One 2013; 8: e63359.
28. Momany FA, Rone R,. Validation of the general purpose QUANTA 3.2/CHARMm force field. J Comput Chem 1992; 13: 888-900.
29. Weatherill EE, Cain KL, Heywood SP, et al., Towards a universal disulphide stabilised single chain Fv format: importance of interchain disulphide bond location and vL-vH orientation. Protein Eng Des Sel 2012; 25: 321-9.
30. Michaelson JS, Demarest SJ, Miller B, et al., Anti-tumor activity of stability-engineered IgG-like bispecific antibodies targeting TRAIL-R2 and LTbetaR. MAbs 2009; 1: 128-41.
31. Molhoj M, Crommer S, Brischwein K, et al., CD19-/CD3-bispecific antibody of the BiTE class is far superior to tandem diabody with respect to redirected tumor cell lysis. Mol Immunol 2007; 44: 1935-43.
32. Brischwein K, Schlereth B, Guller B, et al., MT110: a novel bispecific single-chain antibody construct with high efficacy in eradicating established tumors. Mol Immunol 2006; 43: 1129-43.
33. Klinger M, Brandl C, Zugmaier G, 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.
34. Ruf P, Schafer B, Eissler N, et al., Ganglioside GD2-specific trifunctional surrogate antibody Surek demonstrates therapeutic activity in a mouse melanoma model. J Transl Med 2012; 10: 219.
35. Eissler N, Ruf P, Mysliwietz J, et al., Trifunctional bispecific antibodies induce tumor-specific T cells and elicit a vaccination effect. Cancer Res 2012; 72: 3958-66.