Construction and humanization of a functional bispecific EGFR × - CD16 diabody using a refolding system

FEBS Journal

Volumn 279, Issue 2, 2012, Pages 223-233

  Asano, Ryutaro ^a   Nakayama, Makoto ^a   Kawaguchi, Hiroko ^a   Kubota, Tsuguo ^a   Nakanishi, Takeshi ^a   Umetsu, Mitsuo ^a   Hayashi, Hiroki ^a   Katayose, Yu ^a   Unno, Michiaki ^a   Kudo, Toshio ^a   Kumagai, Izumi ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

bispecific diabody; cancer immunotherapy; CD16; epidermal growth factor receptor; humanization

Indexed keywords

BISPECIFIC ANTIBODY; BISPECIFIC DIABODY EX16; CD16 ANTIGEN; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER INHIBITION; COMPLEMENTARITY DETERMINING REGION; CONTROLLED STUDY; DRUG DESIGN; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VITRO STUDY; MOUSE; MUTANT; NATURAL KILLER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG DESIGN; GPI-LINKED PROTEINS; HUMANS; HYBRIDOMAS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC FACTORS; KILLER CELLS, LYMPHOKINE-ACTIVATED; MICE; MOLECULAR SEQUENCE DATA; MUTANT CHIMERIC PROTEINS; NEOPLASMS; PROTEIN REFOLDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, IGG; SEQUENCE ALIGNMENT;

EID: 84855445995     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08417.x     Document Type: Article

References (45)

1. Cao Y, &, Lam L, (2003) Bispecific antibody conjugates in therapeutics. Adv Drug Del Rev 55, 171-197. (Pubitemid 36135915)
2. Kufer P, Lutterbuse R, &, Baeuerle PA, (2004) A revival of bispecific antibodies. Trends Biotechnol 22, 238-244. (Pubitemid 38515741)
3. Raso V, &, Griffin T, (1981) Hybrid antibodies with dual specificity for the delivery of ricin to immunoglobulin-bearing target cells. Cancer Res 41, 2073-2078. (Pubitemid 11111397)
4. Suresh MR, Cuello AC, &, Milstein C, (1986) Bispecific monoclonal antibodies from hybrid hybridomas. Methods Enzymol 121, 210-228. (Pubitemid 16057895)
5. Kriangkum J, Xu B, Nagata LP, Fulton RE, &, Suresh MR, (2001) Bispecific and bifunctional single chain recombinant antibodies. Biomol Eng 18, 31-40. (Pubitemid 32776592)
6. Perisic O, Webb PA, Holliger P, Winter G, &, Williams RL, (1994) Crystal structure of a diabody, a bivalent antibody fragment. Structure 2, 1217-1226. (Pubitemid 124001320)
7. Arndt MA, Krauss J, Kipriyanov SM, Pfreundschuh M, &, Little M, (1999) A bispecific diabody that mediates natural killer cell cytotoxicity against xenotransplantated human Hodgkin's tumors. Blood 94, 2562-2568. (Pubitemid 29477283)
8. Gao Y, Xiong D, Yang M, Liu H, Peng H, Shao X, Xu Y, Xu C, Fan D, Qin L, et al. (2004) Efficient inhibition of multidrug-resistant human tumors with a recombinant bispecific anti-P-glycoprotein x anti-CD3 diabody. Leukemia 18, 513-520. (Pubitemid 38425866)
9. Kipriyanov SM, Cochlovius B, Schafer HJ, Moldenhauer G, Bahre A, Le Gall F, Knackmuss S, &, Little M, (2002) Synergistic antitumor effect of bispecific CD19 x CD3 and CD19 x CD16 diabodies in a preclinical model of non-Hodgkin's lymphoma. J Immunol 169, 137-144. (Pubitemid 34686129)
10. Xiong D, Xu Y, Liu H, Peng H, Shao X, Lai Z, Fan D, Yang M, Han J, Xie Y, et al. (2002) Efficient inhibition of human B-cell lymphoma xenografts with an anti-CD20 x anti-CD3 bispecific diabody. Cancer Lett 177, 29-39. (Pubitemid 34102396)
11. Asano R, Takemura S, Tsumoto K, Sakurai N, Teramae A, Ebara S, Katayose Y, Shinoda M, Suzuki M, Imai K, et al. (2000) Functional construction of the anti-mucin core protein (MUC1) antibody MUSE11 variable regions in a bacterial expression system. J Biochem (Tokyo) 127, 673-679. (Pubitemid 30238362)
12. Asano R, Kudo T, Nishimura Y, Makabe K, Hayashi H, Suzuki M, Tsumoto K, &, Kumagai I, (2002) Efficient construction of a diabody using a refolding system: anti-carcinoembryonic antigen recombinant antibody fragment. J Biochem (Tokyo) 132, 903-909. (Pubitemid 36090656)
13. Asano R, Sone Y, Makabe K, Tsumoto K, Hayashi H, Katayose Y, Unno M, Kudo T, &, Kumagai I, (2006) Humanization of the bispecific epidermal growth factor receptor x CD3 diabody and its efficacy as a potential clinical reagent. Clin Cancer Res 12, 4036-4042. (Pubitemid 44078091)
14. Asano R, Sone Y, Ikoma K, Hayashi H, Nakanishi T, Umetsu M, Katayose Y, Unno M, Kudo T, &, Kumagai I, (2008) Preferential heterodimerization of a bispecific diabody based on a humanized anti-EGFR antibody 528. Protein Eng Des Sel 21, 597-603.
15. Foote J, &, Winter G, (1992) Antibody framework residues affecting the conformation of the hypervariable loops. J Mol Biol 224, 487-499.
16. Vargas-Madrazo E, &, Paz-Garcia E, (2003) An improved model of association for VH-VL immunoglobulin domains: asymmetries between VH and VL in the packing of some interface residues. J Mol Recognit 16, 113-120. (Pubitemid 36815049)
17. Fischer-Colbrie J, Witt A, Heinzl H, Speiser P, Czerwenka K, Sevelda P, &, Zeillinger R, (1997) EGFR and steroid receptors in ovarian carcinoma: comparison with prognostic parameters and outcome of patients. Anticancer Res 17, 613-619. (Pubitemid 27105536)
18. Ferrini S, Cambiaggi A, Sforzini S, Marciano S, Canevari S, Mezzanzanica D, Colnaghi MI, Grossi CE, &, Moretta L, (1993) Targeting of T lymphocytes against EGF-receptor+ tumor cells by bispecific monoclonal antibodies: requirement of CD3 molecule cross-linking for T-cell activation. Int J Cancer 55, 931-937. (Pubitemid 24005337)
19. Pfosser A, Brandl M, Salih H, Grosse-Hovest L, &, Jung G, (1999) Role of target antigen in bispecific-antibody-mediated killing of human glioblastoma cells: a pre-clinical study. Int J Cancer 80, 612-616. (Pubitemid 29047529)
20. Nagorsen D, &, Baeuerle PA, (2011) Immunomodulatory therapy of cancer with T cell-engaging BiTE antibody blinatumomab. Exp Cell Res 317, 1255-1260.
21. Tsumoto K, Shinoki K, Kondo H, Uchikawa M, Juji T, &, Kumagai I, (1998) Highly efficient recovery of functional single-chain Fv fragments from inclusion bodies overexpressed in Escherichia coli by controlled introduction of oxidizing reagent-application to a human single-chain Fv fragment. J Immunol Methods 219, 119-129. (Pubitemid 28513157)
22. Jones PT, Dear PH, Foote J, Neuberger MS, &, Winter G, (1986) Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321, 522-525. (Pubitemid 16052256)
23. Riechmann L, Clark M, Waldmann H, &, Winter G, (1988) Reshaping human antibodies for therapy. Nature 332, 323-327. (Pubitemid 18091075)
24. Queen C, Schneider WP, Selick HE, Payne PW, Landolfi NF, Duncan JF, Avdalovic NM, Levitt M, Junghans RP, &, Waldmann TA, (1989) A humanized antibody that binds to the interleukin 2 receptor. Proc Natl Acad Sci U S A 86, 10029-10033. (Pubitemid 20030769)
25. Co MS, Deschamps M, Whitley RJ, &, Queen C, (1991) Humanized antibodies for antiviral therapy. Proc Natl Acad Sci U S A 88, 2869-2873. (Pubitemid 21916521)
26. Ohtomo T, Tsuchiya M, Sato K, Shimizu K, Moriuchi S, Miyao Y, Akimoto T, Akamatsu K, Hayakawa T, &, Ohsugi Y, (1995) Humanization of mouse ONS-M21 antibody with the aid of hybrid variable regions. Mol Immunol 32, 407-416.
27. Nakanishi T, Tsumoto K, Yokota A, Kondo H, &, Kumagai I, (2008) Critical contribution of VH-VL interaction to reshaping of an antibody: the case of humanization of anti-lysozyme antibody, HyHEL-10. Protein Sci 17, 261-270. (Pubitemid 351171838)
28. Lu D, Jimenez X, Witte L, &, Zhu Z, (2004) The effect of variable domain orientation and arrangement on the antigen-binding activity of a recombinant human bispecific diabody. Biochem Biophys Res Commun 318, 507-513. (Pubitemid 38553809)
29. Loffler A, Kufer P, Lutterbuse R, Zettl F, Daniel PT, Schwenkenbecher JM, Riethmuller G, Dorken B, &, Bargou RC, (2000) A recombinant bispecific single-chain antibody, CD19 × CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood 95, 2098-2103. (Pubitemid 30151651)
30. Bruenke J, Barbin K, Kunert S, Lang P, Pfeiffer M, Stieglmaier K, Niethammer D, Stockmeyer B, Peipp M, Repp R, et al. (2005) Effective lysis of lymphoma cells with a stabilised bispecific single-chain Fv antibody against CD19 and FcgammaRIII (CD16). Br J Haematol 130, 218-228. (Pubitemid 41602522)
31. Kellner C, Bruenke J, Stieglmaier J, Schwemmlein M, Schwenkert M, Singer H, Mentz K, Peipp M, Lang P, Oduncu F, et al. (2008) A novel CD19-directed recombinant bispecific antibody derivative with enhanced immune effector functions for human leukemic cells. J Immunother 31, 871-884.
32. Singer H, Kellner C, Lanig H, Aigner M, Stockmeyer B, Oduncu F, Schwemmlein M, Stein C, Mentz K, Mackensen A, et al. (2010) Effective elimination of acute myeloid leukemic cells by recombinant bispecific antibody derivatives directed against CD33 and CD16. J Immunother 33, 599-608.
33. Bruenke J, Fischer B, Barbin K, Schreiter K, Wachter Y, Mahr K, Titgemeyer F, Niederweis M, Peipp M, Zunino SJ, et al. (2004) A recombinant bispecific single-chain Fv antibody against HLA class II and FcgammaRIII (CD16) triggers effective lysis of lymphoma cells. Br J Haematol 125, 167-179. (Pubitemid 38534968)
34. Asano R, Ikoma K, Kawaguchi H, Ishiyama Y, Nakanishi T, Umetsu M, Hayashi H, Katayose Y, Unno M, Kudo T, et al. (2010) Application of the Fc fusion format to generate tag-free bi-specific diabodies. FEBS J 277, 477-487.
35. Asano R, Kawaguchi H, Watanabe Y, Nakanishi T, Umetsu M, Hayashi H, Katayose Y, Unno M, Kudo T, &, Kumagai I, (2008) Diabody-based recombinant formats of humanized IgG-like bispecific antibody with effective retargeting of lymphocytes to tumor cells. J Immunother 31, 752-761.
36. Asano R, Ikoma K, Sone Y, Kawaguchi H, Taki S, Hayashi H, Nakanishi T, Umetsu M, Katayose Y, Unno M, et al. (2010) Highly enhanced cytotoxicity of a dimeric bispecific diabody, the hEx3 tetrabody. J Biol Chem 285, 20844-20849.
37. Ono K, Ohtomo T, Yoshida K, Yoshimura Y, Kawai S, Koishihara Y, Ozaki S, Kosaka M, &, Tsuchiya M, (1999) The humanized anti-HM1.24 antibody effectively kills multiple myeloma cells by human effector cell-mediated cytotoxicity. Mol Immunol 36, 387-395. (Pubitemid 29331647)
38. Sato K, Tsuchiya M, Saldanha J, Koishihara Y, Ohsugi Y, Kishimoto T, &, Bendig MM, (1993) Reshaping a human antibody to inhibit the interleukin 6-dependent tumor cell growth. Cancer Res 53, 851-856. (Pubitemid 23077873)
39. Sato K, Tsuchiya M, Saldanha J, Koishihara Y, Ohsugi Y, Kishimoto T, &, Bendig MM, (1994) Humanization of a mouse anti-human interleukin-6 receptor antibody comparing two methods for selecting human framework regions. Mol Immunol 31, 371-381. (Pubitemid 24118607)
40. Wang X, &, Stollar BD, (1999) Immunoglobulin VH gene expression in human aging. Clin Immunol 93, 132-142. (Pubitemid 29523389)
41. Ramsland PA, Brock CR, Moses J, Robinson BG, Edmundson AB, &, Raison RL, (1999) Structural aspects of human IgM antibodies expressed in chronic B lymphocytic leukemia. Immunotechnology 4, 217-229. (Pubitemid 29170030)
42. Yokota A, Tsumoto K, Shiroishi M, Kondo H, &, Kumagai I, (2003) The role of hydrogen bonding via interfacial water molecules in antigen-antibody complexation. The HyHEL-10-HEL interaction. J Biol Chem 278, 5410-5418. (Pubitemid 36801057)
43. Sondermann P, &, Jacob U, (1999) Human Fcgamma receptor IIb expressed in Escherichia coli reveals IgG binding capability. Biol Chem 380, 717-721. (Pubitemid 29322364)
44. Asano R, Ikoma K, Shimomura I, Taki S, Nakanishi T, Umetsu M, &, Kumagai I, (2011) Cytotoxic enhancement of a bispecific diabody by format conversion to tandem single-chain variable fragment (taFv): the case of the hEx3 diabody. J Biol Chem 286, 1812-1818.
45. Kabat EA, Wu TT, Perry HM, Gottesman KS, &, Foeller C, (1991) Sequences of Proteins of Immunological Interest, 5th edn. National Institutes of Health, Bethesda, MD.