Strategy for affinity maturation of an antibody with high evolvability to (4-hydroxy-3-nitrophenyl) acetyl hapten

Molecular Immunology

Volumn 44, Issue 9, 2007, Pages 2436-2445

  Furukawa, Koji ^a   Shimizu, Takeyuki ^b   Murakami, Akikazu ^b   Kono, Ryo ^b   Nakagawa, Masatoshi ^b   Sagawa, Takuma ^c   Yamato, Ichiro ^b   Azuma, Takachika ^b  

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

^b TOKYO UNIVERSITY OF SCIENCE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Affinity maturation; Antigen antibody interaction; Binding thermodynamics; Clonally related antibodies

Indexed keywords

(4 HYDROXY 3 NITROPHENYL)ACETYL HAPTEN; ACETIC ACID DERIVATIVE; AMINO ACID; ANTIBODY; HAPTEN; HAPTEN ANTIBODY; HYDROXYL GROUP; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIBODY AFFINITY; ANTIBODY STRUCTURE; ANTIGEN ANTIBODY REACTION; ANTIGEN BINDING; ARTICLE; ENTHALPY; ENTROPY; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROCESSING; SITE DIRECTED MUTAGENESIS; SOMATIC HYPERMUTATION; STRUCTURAL PROTEOMICS; THERMODYNAMICS;

6-AMINOCAPROIC ACID; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIBODIES, MONOCLONAL; ANTIBODY AFFINITY; ANTIBODY FORMATION; CALORIMETRY; CIRCULAR DICHROISM; CLONE CELLS; HAPTENS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN LIGHT CHAINS; IMMUNOGLOBULIN VARIABLE REGION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NITROPHENOLS; PROTEIN CONFORMATION; THERMODYNAMICS;

EID: 33846204395     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2006.10.023     Document Type: Article

References (47)

1. Allen D., Simon T., Sablitzky E., Rajewsky K., and Cumano A. Antibody engineering for the analysis of affinity maturation of an anti-hapten response. EMBO J. 7 (1988) 1995-2001
2. Azuma T., Sakato N., and Fujio H. Maturation of the immune response to (4-hydroxy-3-nitrophenyl)-acetyl (NP) haptens in C57BL/6 mice. Mol. Immunol. 24 (1987) 287-296
3. Berek C., Griffiths G.M., and Milstein C. Molecular events during maturation of the immune response to oxazolone. Nature 316 (1985) 412-418
4. Berek C., Berger A., and Apel M. Maturation of the immune response in germinal centers. Cell 67 (1991) 1121-1129
5. Bothwell A.L., Paskind M., Reth M., Imanishi-Kari T., Rajewsky K., and Baltimore D. Heavy chain variable region contribution to the NPb family of antibodies: somatic mutation evident in a gamma 2a variable region. Cell 24 (1981) 625-637
6. Brownstone A., Mitchison N.A., and Pitt-Rivers R. Chemical and serological studies with an iodine-containing synthetic immunological determinant 4-hydroxy-3-iodo-5-nitrophenylacetic acid (NIP) and related compounds. Immunology 10 (1966) 465-479
7. Carter P.J., Winter G., Wilkinson A.J., and Fersht A.R. The use of double mutants to detect structural changes in the active site of the tyrosyl-tRNA synthetase (Bacillus stearothermophilus). Cell 38 (1984) 835-840
8. Chen C., Martin T.M., Stevens S., and Rittenberg M.B. Defective secretion of an immunoglobulin caused by mutations in the heavy chain complementarity determining region 2. J. Exp. Med. 180 (1994) 577-586
9. Chen C., Roberts V.A., Stevens S., Brown M., Stenzel-Poore M.P., and Rittenberg M.B. Enhancement and destruction of antibody function by somatic mutation: unequal occurrence is controlled by V gene combinatorial associations. EMBO J. 14 (1995) 2784-2794
10. Cumano A., and Rajewsky K. Structure of primary anti-(4-hydroxy-3-nitrophenyl)acetyl (NP) antibodies in normal and idiotypically suppressed C57BL/6 mice. Eur. J. Immunol. 15 (1985) 512-520
11. Cumano A., and Rajewsky K. Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J. 5 (1986) 2459-2468
12. Desiderio S.V., Yancopoulos G.D., Paskind M., Thomas E., Boss M.A., Landau N., Alt F.W., and Baltimore D. Insertion of N regions into heavy-chain genes is correlated with expression of terminal deoxytransferase in B cells. Nature 311 (1984) 752-755
13. French D.L., Laskov R., and Scharff M.D. The role of somatic hypermutation in the generation of antibody diversity. Science 244 (1989) 1152-1157
14. Furukawa K., Akasako-Furukawa A., Shirai H., Nakamura H., and Azuma T. Junctional amino acids determine the maturation pathway of an antibody. Immunity 11 (1999) 329-338
15. Furukawa K., Shirai H., Azuma T., and Nakamura H. A role of the third complementarity-determining region in the affinity maturation of an antibody. J. Biol. Chem. 276 (2001) 27622-27628
16. Furukawa K., Manabe A., Furukawa A., Kuba H., Okajima T., and Azuma T. Initial repertoire of anti-(4-hydroxy-3-nitrophenylacetyl) antibodies as potential donors for effective affinity maturation. Mol. Immunol. 43 (2006) 1751-1760
17. Griffiths G.M., Berek C., Kaartinen M., and Milstein C. Somatic mutation and the maturation of immune response to 2-phenyl oxazolone. Nature 312 (1984) 271-275
18. Gurney R.W. Ionic Process in Solution (1953), McGraw-Hill, New York
19. Hibbits K.A., Gill D.S., and Willson R.C. Isothermal titration calorimetric study of the association of hen egg lysozyme and the anti-lysozyme antibody HyHEL-5. Biochemistry 33 (1994) 3584-3590
20. Ito W., Iba Y., and Kurosawa Y. Effects of substitutions of closely related amino acids at the contact surface in an antigen-antibody complex on thermodynamic parameters. J. Biol. Chem. 268 (1993) 16639-16647
21. Jacob J., Kassir R., and Kelsoe G. In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J. Exp. Med. 173 (1991) 1165-1175
22. Joyce G.F. Evolutionary chemistry: getting there from here. Science 276 (1997) 1658-1659
23. Kabat, E.A., Wu, T.T., Perry, H., Gottesman, K., Foeller, C, 1991. Sequences of Proteins of Immunological Interest. 5th Edition. NIH Publication No. 91-3242. Bethesda, MD
24. Kelsoe G. Life and death in germinal centers (redux). Immunity 4 (1996) 107-111
25. Kim S.T., Shirai H., Nakajima N., Higo J., and Nakamura H. Enhanced conformational diversity search of CDR-H3 in antibodies: role of the first CDR-H3 residue. Proteins 37 (1999) 683-696
26. Koradi R., Billeter M., and Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 51-55 (1996) 29-32
27. Lefranc M.P., Pommie C., Ruiz M., Giudicelli V., Foulquier E., Truong L., Thouvenin-Contet V., and Lefranc G. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev. Comp. Immunol. 27 (2003) 55-77
28. Liu Y.J., Johnson G.D., Gordon J., and MacLennan I.C. Germinal centres in T-cell-dependent antibody responses. Immunol. Today 13 (1992) 17-21
29. MacLennan I.C., Liu Y.J., and Johnson G.D. Maturation and dispersal of B-cell clones during T cell-dependent antibody responses. Immunol. Rev. 126 (1992) 143-161
30. McHeyzer-Williams M.G., McLean M.J., Lalor P.A., and Nossal G.J. Antigen-driven B cell differentiation in vivo. J. Exp. Med. 178 (1993) 295-307
31. Milstein C., and Rada C. The maturation of the antibody response. In: Honjo T., and Alt F.W. (Eds). Immunoglobulin Genes. second ed. (1995), Academic Press, London 57-81
32. Mizutani R., Miura K., Nakayama T., Shimada I., Arata Y., and Satow Y. Three-dimensional structures of the Fab fragment of murine N1G9 antibody from the primary immune response and of its complex with (4-hydroxy-3-nitrophenyl)acetate. J. Mol. Biol. 254 (1995) 208-222
33. Motoyama N., Okada H., and Azuma T. Somatic mutation in constant regions of mouse lambda 1 light chains. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 7933-7937
34. Motoyama N., Miwa T., Suzuki Y., Okada H., and Azuma T. Comparison of somatic mutation frequency among immunoglobulin genes. J. Exp. Med. 179 (1994) 395-403
35. Painter R.G., Sage H.J., and Tanford C. Contributions of heavy and light chains of rabbit immunoglobulin G to antibody activity. I. Binding studies on isolated heavy and light chains. Biochemistry 11 (1972) 1327-1337
36. Painter R.G., Sage H.J., and Tanford C. Contributions of heavy and light chains of rabbit immunoglobulin G to antibody activity. II. Binding activities of reconstituted immunoglobulins. Biochemistry 11 (1972) 1338-1345
37. Rajewsky K., Forster I., and Cumano A. Evolutionary and somatic selection of the antibody repertoire in the mouse. Science 238 (1987) 1088-1094
38. Rothenfluh H.S., Taylor L., Bothwell A.L., Both G.W., and Steele E.J. Somatic hypermutation in 5' flanking regions of heavy chain antibody variable regions. Eur. J. Immunol. 23 (1993) 2152-2159
39. Sagawa T., Oda M., Ishimura M., Furukawa K., and Azuma T. Thermodynamic and kinetic aspects of antibody evolution during the immune response to hapten. Mol. Immunol. 39 22 (2003) 801-808
40. Storb U. Progress in understanding the mechanism and consequences of somatic hypermutation. Immunol. Rev. 162 (1998) 5-11
41. Taketani M., Naitoh A., Motoyama N., and Azuma T. Role of conserved amino acid residues in the complementarity determining regions on hapten-antibody interaction of anti-(4-hydroxy-3-nitrophenyl) acetyl antibodies. Mol. Immunol. 32 (1995) 983-990
42. Tao W., and Bothwell A.L. Development of B cell lineages during a primary anti-hapten immune response. J. Immunol. 145 (1990) 3216-3222
43. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
44. Torigoe H., Nakayama T., Imazato M., Shimada I., Arata Y., and Sarai A. The affinity maturation of anti-4-hydroxy-3-nitrophenylacetyl mouse monoclonal antibody. A calorimetric study of the antigen-antibody interaction. J. Biol. Chem. 270 (1995) 22218-22222
45. Tsumoto K., Ogasahara K., Ueda Y., Watanabe K., Yutani K., and Kumagai I. Role of Tyr residues in the contact region of anti-lysozyme monoclonal antibody HyHEL10 for antigen binding. J. Biol. Chem. 270 (1995) 18551-18557
46. Wedemayer G.J., Patten P.A., Wang L.H., Schultz P.G., and Stevens R.C. Structural insights into the evolution of an antibody combining site. Science 276 (1997) 1665-1669
47. Wysocki L., Manser T., and Gefter M.L. Somatic evolution of variable region structures during an immune response. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 1847-1851