Critical contribution of VH-VL interaction to reshaping of an antibody: The case of humanization of anti-lysozyme antibody, HyHEL-10

Protein Science

Volumn 17, Issue 2, 2008, Pages 261-270

  Nakanishi, Takeshi ^a   Tsumoto, Kouhei ^a,c   Yokota, Akiko ^a,d   Kondo, Hidemasa ^b   Kumagai, Izumi ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Antibody; CDR grafting; Humanization; Protein protein interaction; Thermodynamics; X ray crystallography

Indexed keywords

LYSOZYME;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENTHALPY; ENTROPY; IMMUNOGLOBULIN VARIABLE REGION; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIBODIES; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIGEN-ANTIBODY COMPLEX; ANTIGEN-ANTIBODY REACTIONS; CRYSTALLOGRAPHY, X-RAY; HUMANS; IMMUNOGLOBULIN FRAGMENTS; IMMUNOGLOBULIN VARIABLE REGION; MICE; MURAMIDASE; MUTANT PROTEINS; THERMODYNAMICS;

MURINAE;

EID: 38649139063     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.073156708     Document Type: Article

References (61)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
2. Asano, R., Sone, Y., Makabe, K., Tsumoto, K., Hayashi, H., Katayose, Y., Unno, M., Kudo, T., and 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.
3. Bhat, T.N., Bentley, G.A., Fischmann, T.O., Boulot, G., and Poljak, R.J. 1990. Small rearrangements in structures of Fv and Fab fragments of antibody D1.3 on antigen binding. Nature 347: 483-485.
4. Braden, B.C. and Poljak, R.J. 1995. Structural features of the reactions between antibodies and protein antigens. FASEB J. 9: 9-16.
5. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
6. Co, M.S., Deschamps, M., Whitley, R.J., and Queen, C. 1991. Humanized antibodies for antiviral therapy. Proc. Natl. Acad. Sci. 88: 2869-2873.
7. Co, M.S., Avdalovic, N.M., Caron, P.C., Avdalovic, M.V., Scheinberg, D.A., and Queen, C. 1992. Chimeric and humanized antibodies with specificity for the CD33 antigen. J. Immunol. 48: 1149-1154.
8. Collaborative Computational Project Number 4. 1994. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr 50: 760-763.
9. Davies, D.R. and Cohen, G.H. 1996. Interactions of protein antigens with antibodies. Proc. Natl. Acad. Sci. 93: 7-12.
10. Dunitz, J.D. 1994. The entropic cost of bound water in crystals and biomolecules. Science 264: 670. doi: 10.1126/science.264.5159.670.
11. Ewert, S., Honegger, A., and Plückthun, A. 2004. Stability improvement of antibodies for extracellular and intracellular applications: CDR grafting to stable frameworks and structure-based framework engineering. Methods 34: 184-199.
12. Foote, J. and Winter, G. 1992. Antibody framework residues affecting the conformation of the hypervariable loops. J. Mol. Biol. 224: 487-499.
13. Furukawa, K., Akasako-Furukawa, A., Shirai, H., Nakamura, H., and Azuma, T. 1999. Junctional amino acids determine the maturation pathway of an antibody. Immunity 11: 329-338.
14. Holmes, M.A., Buss, T.N., and Foote, J. 1998. Conformational correction mechanisms aiding antigen recognition by a humanized antibody. J. Exp. Med. 187: 479-485.
15. Holmes, M.A., Buss, T.N., and Foote, J. 2001. Structural effects of framework mutations on a humanized anti-lysozyme antibody. J. Immunol. 167: 296-301.
16. Hugo, N., Weidenhaupt, M., Beukes, M., Xu, B., Janson, J.C., Vernet, T., and Altschuh, D. 2003. VL position 34 is a key determinant for the engineering of stable antibodies with fast dissociation rates. Protein Eng. 16: 381-386.
17. Imoto, T., Johnson, T.M., North, A.C.T., Phillips, D.C., and Rupley, J.A. 1972. Vertebrate lysozymes. In The enzymes (ed. P. Boyer), Vol. 7, pp. 665-868. Academic Press, San Diego, CA.
18. Jirholt, P., Ohlin, M., Borrebaeck, C.A., and Soderlind, E. 1998. Exploiting sequence space: Shuffling in vivo formed complementarity determining regions into a master framework. Gene 215: 471-476.
19. Jones, P.T., Dear, P.H., Foote, J., Neuberger, M.S., and Winter, G. 1986. Replacing the complementarity-determining regions in a human antibody with those from a mouse. Nature 321: 522-525.
20. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
21. Kam-Morgan, L.N., Smith-Gill, S.J., Taylor, M.G., Zhang, L., Wilson, A.C., and Kirsch, J.F. 1993. High-resolution mapping of the HyHEL-10 epitope of chicken lysozyme by site-directed mutagenesis. Proc. Natl. Acad. Sci. 90: 3958-3962.
22. Khalifa, M.B., Weidenhaupt, M., Choulier, L., Chatellier, J., Rauffer-Bruyere, N., Altschuh, D., and Vernet, T. 2000. Effects on interaction kinetics of mutations at the VH-VL interface of Fabs depend on the structural context. J. Mol. Recognit. 13: 127-139.
23. Kondo, H., Shiroishi, M., Matsushima, M., Tsumoto, K., and Kumagai, I. 1999. Crystal structure of anti-Hen egg white lysozyme antibody (HyHEL-10) Fv-antigen complex. Local structural changes in the protein antigen and water-mediated interactions of Fv-antigen and light chain-heavy chain interfaces. J. Biol. Chem. 274: 27623-27631.
24. Kumagai, I., Nishimiya, Y., Kondo, H., and Tsumoto, K. 2003. Structural consequences of target epitope-directed functional alteration of an antibody. The case of anti-hen lysozyme antibody, HyHEL-10. J. Biol. Chem. 278: 24929-24936.
25. Lawrence, M.C. and Colman, P.M. 1993. Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234: 946-950.
26. Lemmon, M.A. and Ladbury, J.E. 1994. Thermodynamic studies of tyrosylphosphopeptide binding to the SH2 domain of p56lck. Biochemistry 33: 5070-5076.
27. Mariuzza, R.A. and Pojak, R.J. 1993. The basics of binding: Mechanisms of antigen recognition and mimicry by antibodies. Curr. Opin. Immunol. 5: 50-55.
28. Masuda, K., Sakamoto, K., Kojima, M., Aburatani, T., Ueda, T., and Ueda, H. 2006. The role of interface framework residues in determining antibody V(H)/V(L) interaction strength and antigen-binding affinity. FEBS J. 273: 2184-2194.
29. Mehta, D.V., DiGate, R.J., Banville, D.L., and Guiles, R.D. 1997. Optimized gene synthesis, high level expression, isotopic enrichment, and refolding of human interleukin-5. Protein Expr. Purif. 11: 86-94.
30. Merk, H., Stiege, W., Tsumoto, K., Kumagai, I., and Erdmann, V.A. 1999. Cell-free expression of two single-chain monoclonal antibodies against lysozyme: Effect of domain arrangement on the expression. J. Biochem. 125: 328-333.
31. Morton, C.J. and Ladbury, J.E. 1996. Water-mediated protein-DNA interactions: The relationship of thermodynamics to structural detail. Protein Sci. 5: 2115-2118.
32. Myszka, D.G., Sweet, R.W., Hensley, P., Brigham-Burke, M., Kwong, P.D., Hendrickson, W.A., Wyatt, R., Sodroski, J., and Doyle, M.L. 2000. Energetics of the HIV gp120-CD4 binding reaction. Proc. Natl. Acad. Sci. 97: 9026-9031.
33. Nishibori, N., Horiuchi, H., Furusawa, S., and Matsuda, H. 2006. Humanization of chicken monoclonal antibody using phage-display system. Mol. Immunol. 43: 634-642.
34. Ohtomo, T., Tsuchiya, M., Sato, K., Shimizu, K., Moriuchi, S., Miyao, Y., Akimoto, T., Akamatsu, K., Hayakawa, T., and Ohsugi, Y. 1995. Humanization of mouse ONS-M21 antibody with the aid of hybrid variable regions. Mol. Immunol. 32: 407-416.
35. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
36. Padlan, E.A. 1996. X-ray crystallography of antibodies. Adv. Protein Chem. 49: 57-133.
37. Padlan, E.A., Silverton, E.W., Sheriff, S., Cohen, G.H., Smith-Gill, S.J., and Davies, D.R. 1989. Structure of an antibody-antigen complex: Crystal structure of the HyHEL-10 Fab-lysozyme complex. Proc. Natl. Acad. Sci. 86: 5938-5942.
38. Pons, J., Rajpal, A., and Kirsch, J.F. 1999. Energetic analysis of an antigen/antibody interface: Alanine scanning mutagenesis and double mutant cycles on the HyHEL-10/lysozyme interaction. Protein Sci. 8: 958-968.
39. 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. 1989. A humanized antibody that binds to the interleukin 2 receptor. Proc. Natl. Acad. Sci. 86: 10029-10033.
40. Riechmann, L., Clark, M., Waldmann, H., and Winter, G. 1988. Reshaping human antibodies for therapy. Nature 332: 323-327.
41. Sato, K., Tsuchiya, M., Saldanha, J., Koishihara, Y., Ohsugi, Y., Kishimoto, T., and Bendig, M.M. 1994. Humanization of a mouse anti-human interleukin-6 receptor antibody comparing two methods for selecting human framework regions. Mol. Immunol. 31: 371-381.
42. Schwarz, F.P., Tello, D., Goldbaum, F.A., Mariuzza, R.A., and Poljak, R.J. 1995. Thermodynamics of antigen-antibody binding using specific anti-lysozyme antibodies. Eur. J. Biochem. 228: 388-394.
43. Shiroishi, M., Yokota, A., Tsumoto, K., Kondo, H., Nishimiya, Y., Horii, K., Matsushima, M., Ogasahara, K., Yutani, K., and Kumagai, I. 2001. Structural evidence for entropic contribution of salt bridge formation to a protein antigen-antibody interaction: The case of hen lysozyme-HyHEL-10 Fv complex. J. Biol. Chem. 276: 23042-23050.
44. Soderlind, E., Strandberg, L., Jirholt, P., Kobayashi, N., Alexeiva, V., Aberg, A.M., Nilsson, A., Jansson, B., Ohlin, M., Wingren, C., et al. 2000. Recombining germline-derived CDR sequences for creating diverse single-framework antibody libraries. Nat. Biotechnol. 18: 852-856.
45. Spolar, R.S. and Record, M.T. 1994. Coupling of local folding to site-specific binding of proteins to DNA. Science 263: 777-784.
46. Stern, M. and Herrmann, R. 2005. Overview of monoclonal antibodies in cancer therapy: Present and promise. Crit. Rev. Oncol. Hematol. 54: 11-29.
47. Stochwin, L.H. and Holmes, S. 2003. The role of therapeutic antibodies in drug discovery. Biochem. Soc. Trans. 31: 433-436.
48. Sturtevant, J.M. 1994. The thermodynamic effects of protein mutations. Curr. Opin. Struct. Biol. 4: 69-78.
49. 15N shift correlation NMR spectroscopy of the Fv and Fab fragments of anti-dansyl mouse monoclonal antibody. J. Mol. Biol. 243: 494-503.
50. Torigoe, H., Nakayama, T., Imazato, M., Shimada, I., Arata, Y., and Sarai, A. 1995. The affinity maturation of anti-4-hydroxy-3-nitrophenylacetyl mouse monoclonal antibody. A calorimetric study of the antigen-antibody interaction. J. Biol. Chem. 270: 22218-22222.
51. Tsumoto, K., Nakaoki, Y., Ueda, Y., Ogasahara, K., Yutani, K., Watanabe, K., and Kumagai, I. 1994a. Effect of the order of antibody variable regions on the expression of the single-chain HyHEL10 Fv fragment in E. coli and the thermodynamic analysis of its antigen-binding properties. Biochem. Biophys. Res. Commun. 201: 546-551.
52. Tsumoto, K., Ueda, Y., Maenaka, K., Watanabe, K., Ogasahara, K., Yutani, K., and Kumagai, I. 1994b. Contribution to antibody-antigen interaction of structurally perturbed antigenic residues upon antibody binding. J. Biol. Chem. 269: 28777-28782.
53. Tsumoto, K., Ogasahara, K., Ueda, Y., Watanabe, K., Yutani, K., and Kumagai, I. 1995. Role of Tyr residues in the contact region of anti-lysozyme monoclonal antibody HyHEL10 for antigen binding. J. Biol. Chem. 270: 18551-18557.
54. Tsumoto, K., Ogasahara, K., Ueda, Y., Watanabe, K., Yutani, K., and Kumagai, I. 1996. Role of salt bridge formation in antigen-antibody interaction. Entropic contribution to the complex between hen egg white lysozyme and its monoclonal antibody HyHEL10. J. Biol. Chem. 271: 32612-32616.
55. Ueda, Y., Tsumoto, K., Watanabe, K., and Kumagai, I. 1993. Synthesis and expression of a DNA encoding the Fv domain of an anti-lysozyme monoclonal antibody, HyHEL10, in Streptomyces lividans. Gene 129: 129-134.
56. Ueda, H., Tsumoto, K., Kubota, K., Suzuki, E., Nagamune, T., Nishimura, H., Schueler, P.A., Winter, G., Kumagai, I., and Mohoney, W.C. 1996. Open sandwich ELISA: A novel immunoassay based on the interchain interaction of antibody variable region. Nat. Biotechnol. 14: 1714-1718.
57. Vagin, A. and Teplyakov, A. 2000. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56: 1622-1624.
58. Vargas-Madrazo, E. and 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.
59. Verhoeyen, M., Milstein, C., and Winter, G. 1988. Reshaping human antibodies: Grafting an antilysozyme activity. Science 239: 1534-1536.
60. Xavier, K.A., Shick, K.A., Smith-Gil, S.J., and Willson, R.C. 1997. Involvement of water molecules in the association of monoclonal antibody HyHEL-5 with bobwhite quail lysozyme. Biophys. J. 73: 2116-2125.
61. Yokota, A., Tsumoto, K., Shiroishi, M., Kondo, H., and 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.