Affinity Maturation of a Humanized Rat Antibody for Anti-RAGE Therapy: Comprehensive Mutagenesis Reveals a High Level of Mutational Plasticity Both Inside and Outside the Complementarity-Determining Regions

Journal of Molecular Biology

Volumn 388, Issue 3, 2009, Pages 541-558

  Finlay, William J ^a   Cunningham, Orla ^a   Lambert, Matthew A ^a   Darmanin Sheehan, Alfredo ^a   Liu, Xuemei ^a   Fennell, Brian J ^a   Mahon, Ciara M ^a   Cummins, Emma ^a   Wade, Jason M ^a   O'Sullivan, Cliona M ^a   Tan, Xiang Yang ^b   Piche, Nicole ^b   Pittman, Debra D ^b   Paulsen, Janet ^b   Tchistiakova, Lioudmila ^b   Kodangattil, Sreekumar ^b   Gill, Davinder ^b   Hufton, Simon E ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b PFIZER INC   (United States)

Author keywords

affinity maturation; antibody humanization; phage display; RAGE; ribosome display

Indexed keywords

IMMUNOGLOBULIN G; MONOCLONAL ANTIBODY; RECEPTOR FOR ADVANCED GLYCATION END PRODUCT ANTIBODY; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG; XT M4;

ARTICLE; BINDING AFFINITY; CELL SURFACE; CONTROLLED STUDY; DRUG EFFICACY; EXPERIMENTAL MODEL; FLUORESCENCE ANALYSIS; GENETIC VARIABILITY; HEAVY CHAIN; HUMAN; IN VIVO STUDY; KINETICS; MUTAGENESIS; MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; RAT; RIBOSOME; SEPSIS;

RATTUS;

EID: 64649099284     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.03.019     Document Type: Article

References (57)

1. Neeper M., Schmidt A.M., Brett J., Yan S.D., Wang F., Pan Y.C., et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J. Biol. Chem. 267 (1992) 14998-15004
2. Schmidt A.M., and Stern D.M. Receptor for age (RAGE) is a gene within the major histocompatibility class III region: implications for host response mechanisms in homeostasis and chronic disease. Front. Biosci. 6 (2001) D1151-D1160
3. Schmidt A.M., Yan S.D., Yan S.F., and Stern D.M. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J. Clin. Invest. 108 (2001) 949-955
4. Hofmann M.A., Drury S., Hudson B.I., Gleason M.R., Qu W., Lu Y., et al. RAGE and arthritis: the G82S polymorphism amplifies the inflammatory response. Genes Immun. 3 (2002) 123-135
5. Basta G., Lazzerini G., Massaro M., Simoncini T., Tanganelli P., Fu C., et al. Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation 105 (2002) 816-822
6. Tanji N., Markowitz G.S., Fu C., Kislinger T., Taguchi A., Pischetsrieder M., et al. Expression of advanced glycation end products and their cellular receptor RAGE in diabetic nephropathy and nondiabetic renal disease. J. Am. Soc. Nephrol. 11 (2000) 1656-1666
7. Hori O., Brett J., Slattery T., Cao R., Zhang J., Chen J.X., et al. The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of RAGE and amphoterin in the developing nervous system. J. Biol. Chem. 270 (1995) 25752-25761
8. Hofmann M.A., Drury S., Fu C., Qu W., Taguchi A., Lu Y., et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97 (1999) 889-901
9. Yan S.D., Zhu H., Zhu A., Golabek A., Du H., Roher A., et al. Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat. Med. 6 (2000) 643-651
10. Chavakis T., Bierhaus A., Al-Fakhri N., Schneider D., Witte S., Linn T., et al. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: a novel pathway for inflammatory cell recruitment. J. Exp. Med. 198 (2003) 1507-1515
11. Park J.S., Svetkauskaite D., He Q., Kim J.Y., Strassheim D., Ishizaka A., and Abraham E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279 (2004) 7370-7377
12. Yang H., Ochani M., Li J., Qiang X., Tanovic M., Harris H.E., et al. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl Acad. Sci. USA 101 (2004) 296-301
13. Lutterloh E.C., Opal S.M., Pittman D.D., Keith Jr. J.C., Tan X.Y., Clancy B.M., et al. Inhibition of the RAGE products increases survival in experimental models of severe sepsis and systemic infection. Crit. Care 11 (2007) R122
14. Hoogenboom H.R. Selecting and screening recombinant antibody libraries. Nat. Biotechnol. 23 (2005) 1105-1116
15. Dufner P., Jermutus L., and Minter R.R. Harnessing phage and ribosome display for antibody optimisation. Trends Biotechnol. 24 (2006) 523-529
16. Wark K.L., and Hudson P.J. Latest technologies for the enhancement of antibody affinity. Adv. Drug Delivery Rev. 58 (2006) 657-670
17. 3-specific humanized mAb. Proc. Natl Acad. Sci. USA 95 (1998) 6037-6042
18. Wu H., Pfarr D.S., Johnson S., Brewah Y.A., Woods R.M., Patel N.K., et al. Development of motavizumab, an ultra-potent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J. Mol. Biol. 368 (2007) 652-665
19. Yang G.H., Yoon S.O., Jang M.H., and Hong H.J. Affinity maturation of an anti-hepatitis B virus PreS1 humanized antibody by phage display. J. Microbiol. 45 (2007) 528-533
20. Yoon S.O., Lee T.S., Kim S.J., Jang M.H., Kang Y.J., Park J.H., et al. Construction, affinity maturation, and biological characterization of an anti-tumor-associated glycoprotein-72 humanized antibody. J. Biol. Chem. 281 (2006) 6985-6992
21. Schlapschy M., Gruber H., Gresch O., Schafer C., Renner C., Pfreundschuh M., and Skerra A. Functional humanization of an anti-CD30 Fab fragment for the immunotherapy of Hodgkin's lymphoma using an in vitro evolution approach. Protein Eng. Des. Sel. 17 (2004) 847-860
22. Razai A., Garcia-Rodriguez C., Lou J., Geren I.N., Forsyth C.M., Robles Y., et al. Molecular evolution of antibody affinity for sensitive detection of botulinum neurotoxin type A. J. Mol. Biol. 351 (2005) 158-169
23. L genes, minigenes, and complementarity-determining regions to binding of antibody-combining sites. J. Immunol. 147 (1991) 1709-1719
24. Shirai H., Kidera A., and Nakamura H. Structural classification of CDR-H3 in antibodies. FEBS Lett. 399 (1996) 1-8
25. Shirai H., Nakajima N., Higo J., Kidera A., and Nakamura H. Conformational sampling of CDR-H3 in antibodies by multicanonical molecular dynamics simulation. J. Mol. Biol. 278 (1998) 481-496
26. Thom G., Cockroft A.C., Buchanan A.G., Candotti C.J., Cohen E.S., Lowne D., et al. Probing a protein-protein interaction by in vitro evolution. Proc. Natl Acad. Sci. USA 103 (2006) 7619-7624
27. Ignatovich O., Tomlinson I.M., Jones P.T., and Winter G. The creation of diversity in the human immunoglobulin V(lambda) repertoire. J. Mol. Biol. 268 (1997) 69-77
28. Tomlinson I.M., Walter G., Jones P.T., Dear P.H., Sonnhammer E.L., and Winter G. The imprint of somatic hypermutation on the repertoire of human germline V genes. J. Mol. Biol. 256 (1996) 813-817
29. Chothia C., Lesk A.M., Tramontano A., Levitt M., Smith-Gill S.J., Air G., et al. Conformations of immunoglobulin hypervariable regions. Nature 342 (1989) 877-883
30. Chothia C., Novotny J., Bruccoleri R., and Karplus M. Domain association in immunoglobulin molecules. The packing of variable domains. J. Mol. Biol. 186 (1985) 651-663
31. Miller R.A., Oseroff A.R., Stratte P.T., and Levy R. Monoclonal antibody therapeutic trials in seven patients with T-cell lymphoma. Blood 62 (1983) 988-995
32. Shawler D.L., Bartholomew R.M., Smith L.M., and Dillman R.O. Human immune response to multiple injections of murine monoclonal IgG. J. Immunol. 135 (1985) 1530-1535
33. 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
34. Schier R., Balint R.F., McCall A., Apell G., Larrick J.W., and Marks J.D. Identification of functional and structural amino-acid residues by parsimonious mutagenesis. Gene 169 (1996) 147-155
35. Luginbuhl B., Kanyo Z., Jones R.M., Fletterick R.J., Prusiner S.B., Cohen F.E., et al. Directed evolution of an anti-prion protein scFv fragment to an affinity of 1 pM and its structural interpretation. J. Mol. Biol. 363 (2006) 75-97
36. Graff C.P., Chester K., Begent R., and Wittrup K.D. Directed evolution of an anti-carcinoembryonic antigen scFv with a 4-day monovalent dissociation half-time at 37 °C. Protein Eng. Des. Sel. 17 (2004) 293-304
37. Wu H., Pfarr D.S., Tang Y., An L.L., Patel N.K., Watkins J.D., et al. Ultra-potent antibodies against respiratory syncytial virus: effects of binding kinetics and binding valence on viral neutralization. J. Mol. Biol. 350 (2005) 126-144
38. Lu D., Shen J., Vil M.D., Zhang H., Jimenez X., Bohlen P., et al. Tailoring in vitro selection for a picomolar affinity human antibody directed against vascular endothelial growth factor receptor 2 for enhanced neutralizing activity. J. Biol. Chem. 278 (2003) 43496-43507
39. Adams G.P., Schier R., McCall A.M., Simmons H.H., Horak E.M., Alpaugh R.K., et al. High affinity restricts the localization and tumor penetration of single-chain Fv antibody molecules. Cancer Res. 61 (2001) 4750-4755
40. Lacy S.E., DeVries P.J., Xie N., Fung E., Lesniewski R.R., and Reilly E.B. The potency of erythropoietin-mimic antibodies correlates inversely with affinity. J. Immunol. 181 (2008) 1282-1287
41. Barbas III C.F., Bain J.D., Hoekstra D.M., and Lerner R.A. Semisynthetic combinatorial antibody libraries: a chemical solution to the diversity problem. Proc. Natl Acad. Sci. USA 89 (1992) 4457-4461
42. Balint R.F., and Larrick J.W. Antibody engineering by parsimonious mutagenesis. Gene 137 (1993) 109-118
43. Sharkey R.M., Juweid M., Shevitz J., Behr T., Dunn R., Swayne L.C., et al. Evaluation of a complementarity-determining region-grafted (humanized) anti-carcinoembryonic antigen monoclonal antibody in preclinical and clinical studies. Cancer Res. 55 (1995) 5935s-5945s
44. Singer I.I., Kawka D.W., DeMartino J.A., Daugherty B.L., Elliston K.O., Alves K., et al. Optimal humanization of 1B4, an anti-CD18 murine monoclonal antibody, is achieved by correct choice of human V-region framework sequences. J. Immunol. 150 (1993) 2844-2857
45. Stephens S., Emtage S., Vetterlein O., Chaplin L., Bebbington C., Nesbitt A., et al. Comprehensive pharmacokinetics of a humanized antibody and analysis of residual anti-idiotypic responses. Immunology 85 (1995) 668-674
46. Gonzales N.R., Padlan E.A., De Pascalis R., Schuck P., Schlom J., and Kashmiri S.V. Minimizing immunogenicity of the SDR-grafted humanized antibody CC49 by genetic manipulation of the framework residues. Mol. Immunol. 40 (2003) 337-349
47. Kashmiri S.V., De Pascalis R., Gonzales N.R., and Schlom J. SDR grafting-a new approach to antibody humanization. Methods 36 (2005) 25-34
48. Hanes J., Schaffitzel C., Knappik A., and Pluckthun A. Picomolar affinity antibodies from a fully synthetic naive library selected and evolved by ribosome display. Nat. Biotechnol. 18 (2000) 1287-1292
49. Desplancq D., King D.J., Lawson A.D., and Mountain A. Multimerization behaviour of single chain Fv variants for the tumour-binding antibody B72.3. Protein Eng. 7 (1994) 1027-1033
50. Pantoliano M.W., Bird R.E., Johnson S., Asel E.D., Dodd S.W., Wood J.F., and Hardman K.D. Conformational stability, folding, and ligand-binding affinity of single-chain Fv immunoglobulin fragments expressed in Escherichia coli. Biochemistry 30 (1991) 10117-10125
51. Stemmer W.P., Morris S.K., and Wilson B.S. Selection of an active single chain Fv antibody from a protein linker library prepared by enzymatic inverse PCR. BioTechniques 14 (1993) 256-265
52. Whitlow M., Bell B.A., Feng S.L., Filpula D., Hardman K.D., Hubert S.L., et al. An improved linker for single-chain Fv with reduced aggregation and enhanced proteolytic stability. Protein Eng. 6 (1993) 989-995
53. Andris-Widhopf J., Rader C., Steinberger P., Fuller R., and Barbas III C.F. Methods for the generation of chicken monoclonal antibody fragments by phage display. J. Immunol. Methods 242 (2000) 159-181
54. Hawkins R.E., Russell S.J., Baier M., and Winter G. The contribution of contact and non-contact residues of antibody in the affinity of binding to antigen. The interaction of mutant D1.3 antibodies with lysozyme. J. Mol. Biol. 234 (1993) 958-964
55. Hanes J., Jermutus L., and Pluckthun A. Selecting and evolving functional proteins in vitro by ribosome display. Methods Enzymol. 328 (2000) 404-430
56. Vaughan T.J., Williams A.J., Pritchard K., Osbourn J.K., Pope A.R., Earnshaw J.C., et al. Human antibodies with sub-nanomolar affinities isolated from a large non-immunized phage display library. Nat. Biotechnol. 14 (1996) 309-314
57. Cummins E., Luxenberg D.P., McAleese F., Widom A., Fennell B.J., Darmanin-Sheehan A., et al. A simple high-throughput purification method for hit identification in protein screening. J. Immunol. Methods 339 (2008) 38-46