Framework shuffling of antibodies to reduce immunogenicity and manipulate functional and biophysical properties

Molecular Immunology

Volumn 44, Issue 11, 2007, Pages 3049-3060

  Damschroder, Melissa M ^a   Widjaja, Lusiana ^a   Gill, Parkash S ^b   Krasnoperov, Valery ^c   Jiang, Weidong ^c   Dall'Acqua, William F ^a   Wu, Herren ^a  

^a MEDIMMUNE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c Vasgene Therapeutics Inc   (United States)

Author keywords

Affinity; Antibody; Expression; Humanization; Isoelectric point; Thermostability

Indexed keywords

EPHRIN RECEPTOR A2; EPHRIN RECEPTOR B4; IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 47; MONOCLONAL ANTIBODY EA2; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BIOCHEMISTRY; CHIMERA; CONTROLLED STUDY; ELECTRICITY; GENETIC ENGINEERING; HUMAN; HUMAN TISSUE; IMMUNOGENICITY; ISOELECTRIC POINT; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; THERMOSTABILITY;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; ANTIGEN-ANTIBODY REACTIONS; CELL LINE, TUMOR; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; MICE; MOLECULAR SEQUENCE DATA; RECEPTOR, EPHA2; RECEPTOR, EPHB4; SEQUENCE ANALYSIS; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

EID: 33947096424     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2006.12.019     Document Type: Article

References (54)

1. Arndt M.A., Krauss J., Schwarzenbacher R., Vu B.K., Greene S., and Rybak S.M. Generation of a highly stable, internalizing anti-CD22 single-chain Fv fragment for targeting non-Hodgkin's lymphoma. Int. J. Cancer 107 (2003) 822-829
2. Benhar I., Padlan E.A., Jung S.H., Lee B., and Pastan I. Rapid humanization of the Fv of monoclonal antibody B3 by using framework exchange of the recombinant immunotoxin B3(Fv)-PE38. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 12051-12055
3. Boshart M., Weber F., Jahn G., Dorsch-Hasler K., Fleckenstein B., and Schaffner W. A very strong enhancer is located upstream of an immediate early gene of human cytomegalovirus. Cell 41 (1985) 521-530
4. Carles-Kinch K., Kilpatrick K.E., Stewart J.C., and Kinch M.S. Antibody targeting of the EphA2 tyrosine kinase inhibits malignant cell behavior. Cancer Res. 62 (2002) 2840-2847
5. Cleland J.L., Powell M.F., and Shire S.J. The development of stable protein formulations: a close look at protein aggregation, deamidation, and oxidation. Crit. Rev. Therapeut. Drug Carr. Syst. 10 (1993) 307-377
6. Coffman K.T., Hu M., Carles-Kinch K., Tice D., Donacki N., Munyon K., Kifle G., Woods R., Langermann S., Kiener P.A., and Kinch M.S. Differential EphA2 epitope display on normal versus malignant cells. Cancer Res. 63 (2003) 7907-7912
7. Dall'Acqua W.F., Damschroder M.M., Zhang J., Woods R.M., Widjaja L., Yu J., and Wu H. Antibody humanization by framework shuffling. Methods 36 (2005) 43-60
8. Delagrave S., Catalan J., Sweet C., Drabik G., Henry A., Rees A., Monath T.P., and Guirakhoo F. Effects of humanization by variable domain resurfacing on the antiviral activity of a single-chain antibody against respiratory syncytial virus. Protein Eng. 12 (1999) 357-362
9. Demarest S.J., Chen G., Kimmel B.E., Gustafson D., Wu J., Salbato J., Poland J., Elia M., Tan X., Wong K., Short J., and Hansen G. Engineering stability into Escherichia coli secreted Fabs leads to increased functional expression. Protein Eng. Des. Sel. 19 (2006) 325-336
10. Ewert S., Honegger A., and Pluckthun A. Stability improvement of antibodies for extracellular and intracellular applications: CDR grafting to stable frameworks and structure-based framework engineering. Methods 34 (2004) 184-199
11. Gonzales N.R., De Pascalis R., Schlom J., and Kashmiri S.V. Minimizing the immunogenicity of antibodies for clinical application. Tumour Biol. 26 (2005) 31-43
12. Hasholzner U., Stieber P., Meier W., and Lamerz R. Value of HAMA--determination in clinical practice--an overview. Anticancer Res. 17 (1997) 3055-3058
13. Hemmer B., Kondo T., Gran B., Pinilla C., Cortese I., Pascal J., Tzou A., McFarland H.F., Houghten R., and Martin R. Minimal peptide length requirements for CD4(+) T cell clones--implications for molecular mimicry and T cell survival. Int. Immunol. 12 (2000) 375-383
14. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., and Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77 (1989) 51-59
15. Johnson S., Oliver C., Prince G.A., Hemming V.G., Pfarr D.S., Wang S.C., Dormitzer M., O'Grady J., Koenig S., Tamura J.K., Woods R., Bansal G., Couchenour D., Tsao E., Hall W.C., and Young J.F. Development of a humanized monoclonal antibody (MEDI-493) with potent in vitro and in vivo activity against respiratory syncytial virus. J. Infect. Dis. 176 (1997) 1215-1224
16. Johnsson B., Lofas S., and Lindquist G. Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal. Biochem. 198 (1991) 268-277
17. Jones P.T., Dear P.H., Foote J., Neuberger M.S., and Winter G. Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321 (1986) 522-525
18. Jung S., Honegger A., and Pluckthun A. Selection for improved protein stability by phage display. J. Mol. Biol. 294 (1999) 163-180
19. Jung S., and Pluckthun A. Improving in vivo folding and stability of a single-chain Fv antibody fragment by loop grafting. Protein Eng. 10 (1997) 959-966
20. Kabat E.A., Wu T.T., Perry H.M., Gottesman K.S., and Foeller. Sequences of Proteins of Immunological Interest (1991), U.S. Public Health Service, National Institutes of Health, Washington, DC
21. Kim I., Kobayashi H., Yoo T.M., Kim M.K., Le N., Han E.S., Wang Q.C., Pastan I., Carrasquillo J.A., and Paik C.H. Lowering of pI by acylation improves the renal uptake of 99mTc-labeled anti-Tac dsFv: effect of different acylating reagents. Nucl. Med. Biol. 29 (2002) 795-801
22. Kim S.J., Park Y., and Hong H.J. Antibody engineering for the development of therapeutic antibodies. Mol. Cells 20 (2005) 17-29
23. Klee G.G. Human anti-mouse antibodies. Arch. Pathol. Lab. Med. 124 (2000) 921-923
24. Knappik A., and Pluckthun A. Engineered turns of a recombinant antibody improve its in vivo folding. Protein Eng. 8 (1995) 81-89
25. Krauss J., Arndt M.A., Martin A.C., Liu H., and Rybak S.M. Specificity grafting of human antibody frameworks selected from a phage display library: generation of a highly stable humanized anti-CD22 single-chain Fv fragment. Protein Eng. 16 (2003) 753-759
26. Kumar S.R., Singh J., Xia G., Krasnoperov V., Hassanieh L., Ley E.J., Scehnet J., Kumar N.G., Hawes D., Press M.F., Weaver F.A., and Gill P.S. Receptor tyrosine kinase EphB4 is a survival factor in breast cancer. Am. J. Pathol. 169 (2006) 279-293
27. Kuus-Reichel K., Grauer L.S., Karavodin L.M., Knott C., Krusemeier M., and Kay N.E. Will immunogenicity limit the use, efficacy, and future development of therapeutic monoclonal antibodies?. Clin. Diagn. Lab. Immunol. 1 (1994) 365-372
28. Manning M.C., Patel K., and Borchardt R.T. Stability of protein pharmaceuticals. Pharm. Res. 6 (1989) 903-918
29. Mateo C., Moreno E., Amour K., Lombardero J., Harris W., and Perez R. Humanization of a mouse monoclonal antibody that blocks the epidermal growth factor receptor: recovery of antagonistic activity. Immunotechnology 3 (1997) 71-81
30. Onda M., Kreitman R.J., Vasmatzis G., Lee B., and Pastan I. Reduction of the nonspecific animal toxicity of anti-Tac(Fv)-PE38 by mutations in the framework regions of the Fv which lower the isoelectric point. J. Immunol. 163 (1999) 6072-6077
31. Onda M., Nagata S., Tsutsumi Y., Vincent J.J., Wang Q., Kreitman R.J., Lee B., and Pastan I. Lowering the isoelectric point of the Fv portion of recombinant immunotoxins leads to decreased nonspecific animal toxicity without affecting antitumor activity. Cancer Res. 61 (2001) 5070-5077
32. Padlan E.A. A possible procedure for reducing the immunogenicity of antibody variable domains while preserving their ligand-binding properties. Mol. Immunol. 28 (1991) 489-498
33. Pardridge W.M., Buciak J., Yang J., and Wu D. Enhanced endocytosis in cultured human breast carcinoma cells and in vivo biodistribution in rats of a humanized monoclonal antibody after cationization of the protein. J. Pharmacol. Exp. Ther. 286 (1998) 548-554
34. Pichla S.L., Murali R., and Burnett R.M. The crystal structure of a Fab fragment to the melanoma-associated GD2 ganglioside. J. Struct. Biol. 119 (1997) 6-16
35. Queen C., Schneider W.P., Selick H.E., Payne P.W., Landolfi N.F., Duncan J.F., Avdalovic N.M., Levitt M., Junghans R.P., and Waldmann T.A. A humanized antibody that binds to the interleukin 2 receptor. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 10029-10033
36. Saldanha J.W., Martin A.C., and Leger O.J. A single backmutation in the human kIV framework of a previously unsuccessfully humanized antibody restores the binding activity and increases the secretion in cos cells. Mol. Immunol. 36 (1999) 709-719
37. Sanger F., Nicklen S., and Coulson A.R. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 5463-5467
38. Shearman C.W., Pollock D., White G., Hehir K., Moore G.P., Kanzy E.J., and Kurrle R. Construction, expression and characterization of humanized antibodies directed against the human alpha/beta T cell receptor. J. Immunol. 147 (1991) 4366-4373
39. Shimba N., Torigoe H., Takahashi H., Masuda K., Shimada I., Arata Y., and Sarai A. Comparative thermodynamic analyses of the Fv. Fab* and Fab fragments of anti-dansyl mouse monoclonal antibody. FEBS Lett. 360 (1995) 247-250
40. Tan P., Mitchell D.A., Buss T.N., Holmes M.A., Anasetti C., and Foote J. Superhumanized" antibodies: reduction of immunogenic potential by complementarity-determining region grafting with human germline sequences: application to an anti-CD28. J. Immunol. 169 (2002) 1119-1125
41. Tangri S., LiCalsi C., Sidney J., and Sette A. Rationally engineered proteins or antibodies with absent or reduced immunogenicity. Curr. Med. Chem. 9 (2002) 2191-2199
42. Tischenko V.M., Zav'yalov V.P., Medgyesi G.A., Potekhin S.A., and Privalov P.L. A thermodynamic study of cooperative structures in rabbit immunoglobulin G. Eur. J. Biochem. 126 (1982) 517-521
43. Triguero D., Buciak J.B., Yang J., and Pardridge W.M. Blood-brain barrier transport of cationized immunoglobulin G: enhanced delivery compared to native protein. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 4761-4765
44. Tsai P.K., Bruner M.W., Irwin J.I., Ip C.C., Oliver C.N., Nelson R.W., Volkin D.B., and Middaugh C.R. Origin of the isoelectric heterogeneity of monoclonal immunoglobulin h1B4. Pharm. Res. 10 (1993) 1580-1586
45. Vaisitti T., Deaglio S., and Malavasi F. Cationization of monoclonal antibodies: another step towards the "magic bullet"?. J. Biol. Regul. Homeost. Agents 19 (2005) 105-112
46. Valnickova Z., Christensen T., Skottrup P., Thogersen I.B., Hojrup P., and Enghild J.J. Post-translational modifications of human thrombin-activatable fibrinolysis inhibitor (TAFI): evidence for a large shift in the isoelectric point and reduced solubility upon activation. Biochemistry 45 (2006) 1525-1535
47. Verhoeyen M., Milstein C., and Winter G. Reshaping human antibodies: grafting an antilysozyme activity. Science 239 (1988) 1534-1536
48. Vermeer A.W., and Norde W. The thermal stability of immunoglobulin: unfolding and aggregation of a multi-domain protein. Biophys. J. 78 (2000) 394-404
49. Vermeer A.W., Norde W., and van Amerongen A. The unfolding/denaturation of immunogammaglobulin of isotype 2b and its F(ab) and F(c) fragments. Biophys. J. 79 (2000) 2150-2154
50. Wenisch E., Reiter S., Hinger S., Steindl F., Tauer C., Jungbauer A., Katinger H., and Righetti P.G. Shifts of isoelectric points between cellular and secreted antibodies as revealed by isoelectric focusing and immobilized pH gradients. Electrophoresis 11 (1990) 966-969
51. Willuda J., Honegger A., Waibel R., Schubiger P.A., Stahel R., Zangemeister-Wittke U., and Pluckthun A. High thermal stability is essential for tumor targeting of antibody fragments: engineering of a humanized anti-epithelial glycoprotein-2 (epithelial cell adhesion molecule) single-chain Fv fragment. Cancer Res. 59 (1999) 5758-5767
52. Worn A., and Pluckthun A. Different equilibrium stability behavior of ScFv fragments: identification, classification, and improvement by protein engineering. Biochemistry 38 (1999) 8739-8750
53. Wu H. Simultaneous humanization and affinity optimization of monoclonal antibodies. Meth. Mol. Biol. 207 (2003) 197-212
54. 3-specific humanized mAb. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 6037-6042