The structural basis of repertoire shift in an immune response to phosphocholine

Journal of Experimental Medicine

Volumn 191, Issue 12, 2000, Pages 2101-2111

  Brown, McKay ^a   Schumacher, Maria A ^a   Wiens, Gregory D ^a   Brennan, Richard G ^b   Rittenberg, Marvin B ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Affinity maturation; Antibody affinity; Immunoglobulin; Somatic mutation; X ray crystallography

Indexed keywords

IMMUNOGLOBULIN LIGHT CHAIN; PHOSPHORYLCHOLINE;

AMINO ACID SEQUENCE; ANTIBODY AFFINITY; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; IMMUNE RESPONSE; PRIORITY JOURNAL; PROTEIN STRUCTURE; SOMATIC MUTATION; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANTIBODY AFFINITY; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; GENE REARRANGEMENT; HAPTENS; HEMOCYANIN; HYBRIDOMAS; IMMUNOGLOBULINS; IMMUNOLOGIC MEMORY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORYLCHOLINE; SURFACE PROPERTIES;

EID: 0034686496     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.191.12.2101     Document Type: Article

References (80)

1. Eisen, H.N., and G.W. Siskind. 1964. Variations in affinities of antibodies during the immune response. Biochemistry. 3:996-1008.
2. Cumano, A., and K. Rajewsky. 1986. Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO (Eur. Mol. Biol. Organ.) J. 5:2459-2468.
3. Foote, J., and C. Milstein. 1991. Kinetic maturation of an immune response. Nature. 352:530-532.
4. Wysocki, L., T. Manser, and M.L. Gefter. 1986. Somatic evolution of variable region structures during an immune response. Proc. Natl. Acad. Sci. USA. 83:1847-1851.
5. Weigert, M.G., I.M. Cesari, S.J. Yonkovich, and M. Cohn. 1970. Variability in the lambda light chain sequences of mouse antibody. Nature. 228:1045-1047.
6. Berek, C., and C. Milstein. 1987. Mutation drift and repertoire shift in the maturation of the immune response. Immunol. Rev. 96:23-41.
7. Stenzel-Poore, M.P., U. Bruderer, and M.B. Rittenberg. 1988. The adaptive potential of the memory response: clonal recruitment and epitope recognition. Immunol. Rev. 105: 113-136.
8. Manser, T., L.J. Wysocki, T. Gridley, R.I. Near, and M.L. Gefter. 1985. The molecular evolution of the immune response. Immunol. Today. 6:94-100.
9. Bennett, L., and C.T. Bishop. 1977. Structure of the type XXVII Streptococcus pneumoniae (pneumococcal) capsular polysaccharide. Can. J. Chem. 55:8-16.
10. Lim, P.L., D.T.M. Leung, Y.L. Chui, and C.H. Ma. 1994. Structural analysis of a phosphorylcholine-binding antibody which exhibits a unique carrier specificity for Trichinella spiralis. Mol. Immunol. 31:1109-1116.
11. McWilliam, A.S., G.A. Stewart, and W. Allen. 1986. Phosphorylcholine bearing components of some helminthic parasites: localization to parasite lipoproteins. Comp. Biochem. Physiol. B. 85:627-633.
12. Chang, S.P., M. Brown, and M.B. Rittenberg. 1982. Immunologic memory to phosphocholine. II. PC-KLH induces two antibody populations that dominate different isotypes. J. Immunol. 128:702-706.
13. Rodwell, J., P.J. Gearhart, and F. Karush. 1983. Restriction in IgM expression. IV. Affinity analysis of monoclonal antiphosphorylcholine antibodies. J. Immunol. 130:313-316.
14. Wicker, L.S., G. Guelde, I. Scher, and J.J. Kenny. 1982. Antibodies from the Lyb5-B cell subset predominate in the secondary IgG response to phosphocholine. J. Immunol. 129: 950-953.
15. Heusser, C.H., J.P.A. Bews, R. Abersold, and K. Blaser. 1984. Anti-phosphocholine antibodies with a preferred reactivity for either PC or PC phenyl represent independent expressions. Ann. Immunol. 135C:123-129.
16. Brown, M., M.P. Stenzel-Poore, S. Stevens, S.K. Kondoleon, J. Ng, H.P. Bachinger, and M.B. Rittenberg. 1992. Immunologic memory to phospocholine keyhole limpet hemocyanin: recurrent mutations in the λ1 light chain increase affinity for antigen. J. Immunol. 148:339-346.
17. Stenzel-Poore, M.P., and M.B. Rittenberg. 1991. Unequal distribution of replacement mutations in κ and λ light chains and their associated H chains: the group II antibody response to phosphocholine-KLH. In Somatic Hypermutation. E.J. Steele, editor. CRC Press, Boca Raton, FL. 95-104.
18. Wilson, I.A., and R.L. Stanfield. 1993. Antibody-antigen interactions. Curr. Opin. Struct. Biol. 3:113-118.
19. Boss, M.A., J.H. Kenten, C.R. Wood, and J.S. Emtage. 1984. Assembly of functional antibodies from immunoglobulin heavy and light chains synthesized in E. Coli. Nucleic Acids Res. 12:3791-3806.
20. Barbar, E., T.M. Martin, M. Brown, M.B. Rittenberg, and D.H. Peyton. 1996. Binding of phenylphosphocholine-carrier conjugates to the combining site of antibodies maintains a conformation of the hapten. Biochemistry. 35:2958-2967.
21. Moulton, H.M. 1996. Structure and specificity of the binding site of the anti-phenylphosphocholine antibody M3C65: interactions with haptens and hapten-carrier conjugates. Ph.D. thesis. Portland State University, Portland, OR. 197 pp.
22. Chang, S.P., and M.B. Rittenberg. 1981. Immunologic memory to phosphorylcholine in vitro. I. Asymmetric expression of clonal dominance. J. Immunol. 126:975-980.
23. Bizebard, T., Y. Mauguen, J.J. Skehel, and M. Knossow. 1991. Use of molecular replacement in the solution of an immunoglobulin Fab fragment structure. Acta Crystallogr. B47: 549-555.
24. Kissinger, C.R., D.K. Gehlaer, and D.B. Fogel. 1999. Rapid automated molecular replacement by evolutionary search. Acta. Crystallogr. D55:484-491.
25. Tronrud, D.E., L.F. TenEyck, and B.W. Matthews. 1985. An efficient general purpose least-squares refinement program for macromolecular structures. Acta. Crystallogr. A43: 489-501.
26. Bhat, T.N., G.A. Bently, G. Boulot, M.I. Greene, D. Tello, W. Dall'Acqua, H. Souchon, F.P. Schwarz, R.A. Mariuzza, and R.J. Poljak. 1994. Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc. Natl. Acad. Aci. USA. 91:1089-1093.
27. Laskowski, R.A., M.W. MacArthur, and J.M. Thornton. 1993. PROCHECK: a program to check the sterochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
28. Gelewitz, E.W., W.L. Riedeman, and I.M. Klotz. 1954. Some quantitative aspects of the reaction of diazonium compounds with serum albumin. Arch. Biochem. Biophys. 53:411-423.
29. Swerdlow, R.D., R.F. Ebert, P. Lee, C. Bonaventura, and K.I. Miller. 1996. Keyhole limpet hemocyanin: structural and functional characterization of two different subunits and multimers. Comp. Biochem. Physiol. 113B:537-548.
30. von Holt, C., W.F. Brandt, H.J. Greyling, G.G. Lindsey, J.D. Retief, J.A. Rodrigues, S. Schwager, and B.T. Sewell. 1989. Isolation and characterization of histones. Methods Enzymol. 170:503-522.
31. Kocks, C., and K. Rajewsky. 1988. Stepwise intraclonal maturation of antibody affinity through somatic hypermutation. Proc. Natl. Acad. Sci. USA. 85:8206-8210.
32. Sharon, J. 1990. Structural correlates of high antibody affinity: Three engineered amino acid substitutions can increase the affinity of an anti-p-azophenylarsonate antibody 200-fold. Proc. Natl. Acad Sci. USA. 87:4814-4817.
33. Chen, C., V.A. Roberts, S. Stevens, M. Brown, M.P. Stenzel-Poore, and M.B. Rittenberg. 1995. Enhancement and destruction of antibody function by somatic mutation: unequal occurrence is controlled by V gene combinatorial associations. EMBO (Eur. Mol. Biol. Organ.) J. 14:2784-2794.
34. Giusti, A.M., N.C. Chien, D.J. Zack, S.-U. Shin, and M.D. Scharff. 1987. Somatic diversification of S107 from an antiphosphocholine to an anti-DNA autoantibody is due to a single base change in its heavy chain variable region. Proc. Natl. Acad. Sci. USA. 84:2926-2930.
35. Hande, S., and T. Manser. 1997. Single amino acid substitutions in V(H) CDR2 are sufficient to generate or enhance the specificity of two forms of an anti-arsonate antibody variable region for DNA. Mol. Immunol. 34:1281-1290.
36. Kussie, P.H., B. Parhami-Seren, L.J. Wysocki, and M.N. Margolies. 1994. A single engineered amino acid substitution changes antibody fine specificity. J. Immunol. 152:146-152.
37. Brünger, A.T., D.J. Leahy, T.R. Hynes, and R.O. Fox. 1991. 2.9 Å resolution structure of an anti-dinitrophenyl-spin-label monoclonal antibody Fab fragment with bound hapten. J. Mol. Biol. 221:239-256.
38. Nicholls, A., K. Sharp, and B.H. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 11:281-296.
39. Doughtery, D.A. 1996. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science. 271:163-168.
40. Padlan, E.A., C. Abergel, and J.P. Tipper. 1995. Identification of specificity-determining residues in antibodies. FASEB J. 9:133-139.
41. Shapiro, G.S., K. Aviszus, D. Ikle, and L.J. Wysocki. 1999. Predicting regional mutability in antibody V genes based solely on di- and trinucleotide sequence composition. J. Immunol. 163:259-268.
42. Jeffrey, P.D., R.K. Strong, L.C. Sieker, C.Y. Chang, R.L. Campbell, G.A. Petsko, E. Haber, M.N. Margolies, and S. Sheriff. 1993. 26-10 Fab-digoxin complex: affinity and specificity due to surface complementarity. Proc. Natl. Acad. Sci. USA. 90:10310-10314.
43. Chien, N.C., V.A. Roberts, A.M. Giusti, M.D. Scharff, and E.D. Getzoff. 1989. Significant structural and functional change of an antigen-binding site by a distant amino acid substitution: proposal of a structural mechanism. Proc. Natl. Acad. Sci. USA. 86:5532-5536.
44. Strong, R.K., G.A. Petsko, J. Sharon, and M.N. Margolies. 1991. Three-dimensional structure of murine anti-p-azophenylarsonate Fab 36-71. 2. Structural basis of hapten binding and idiotypy. Biochemistry. 30:3749-3757.
45. Padlan, E. A. 1994. Anatomy of the antibody molecule. Mol. Immunol. 31:169-217.
46. Patten, P.A., N.S. Gray, P.L. Yang, C.B. Marks, G.J. Wedemayer, J.J. Boniface, R.C. Stevens, and P.G. Schultz. 1996. The immunological evolution of catalysis. Science. 271:1086-1091.
47. Derewenda, Z.S., L. Lee, and U. Derewenda. 1995. The occurrence of CH...O hydrogen bonds in proteins. J. Mol. Biol. 252:248-262.
48. Milstein, C., and M.S. Neuberger. 1996. Maturation of the immune response. Adv. Protein Chem. 49:451-485.
49. Linton, P.J., D. Lo, L. Lai, G.J. Thornbecke, and N.R. Klinman. 1992. Among naive precursor cell subpopulations only progenitors of memory B cells originate germinal centers. Eur. J. Immunol. 22:1293-1297.
50. Gearhart, P.J., N.D. Johnson, R. Douglas, and L. Hood. 1981. IgG antibodies to phosphorylcholine exhibit more diversity than their IgM counterparts. Nature. 291:29-34.
51. Andres, C.M., A. Maddalena, S. Hudak, N.M. Young, and J.L. Claflin. 1981. Anti-phosphocholine hybridoma antibodies II. Functional analysis of binding sites within three antibody families. J. Exp. Med. 154:1584-1598.
52. Claflin, J.L., J. George, C. Dell, and J. Berry. 1989. Patterns of mutations and selection in antibodies to the phosphocholine-specific determinant in Proteus morganii. J. Immunol. 143: 3054-3063.
53. Chen, C., V.A. Roberts, and M.B. Rittenberg. 1992. Generation and analysis of random point mutations in an antibody CDR2 sequence: many mutated antibodies lose their ability to bind antigen. J. Exp. Med. 176:855-866.
54. Claflin, J.L., and J. Berry. 1988. Genetics of the phosphocholine-specific antibody response to Streptococcus pneumoniae. J. Immunol. 141:4012-4019.
55. Kalinke, U., E.M. Bucher, B. Ernst, A. Oxenius, H.-P. Roost, S. Geley, R. Kofler, R.M. Zinkernagel, and H. Hengartner. 1996. The role of somatic mutation in the generation of the protective humoral immune response against vesicular stomatitis virus. Immunity. 5:639-652.
56. Wiens, G.D., K.A. Heldwein, M.P. Stenzel-Poore, and M.B. Rittenberg. 1997. Somatic mutation in VH complementarity-determining region 2 and framework region 2: differential effects on antigen binding and immunoglobulin secretion. J. Immunol. 159:1293-1302.
57. Wiens, G.D., V.A. Roberts, E.A. Whitcomb, T. O'Hare, M.P. Stenzel-Poore, and M.B. Rittenberg. 1998. Harmful somatic mutations: lessons from the dark side. Immunol. Rev. 162:197-209.
58. Karush, F. 1962. Immunologic specificity and molecular structure. Adv. Immunol. 2:1-40.
59. Källberg, E., D. Gray, and T. Leanderson. 1995. The effect of carrier and carrier priming on the kinetics and pattern of somatic mutation in the VκOx1 gene. Eur. J. Immunol. 25: 2349-2354.
60. Bruderer, U., M.P. Stenzel-Poore, H.P. Bachinger, J.H. Fellman, and M.B. Rittenberg. 1989. Antibody combining site heterogeneity within the response to phosphocholine-keyhole limpet hemocyanin. Mol. Immunol. 26:63-71.
61. O'Hare, T., and M.B. Rittenberg. 1998. A simple method for determining KAs of both low and high affinity IgG antibodies. J. Immunol. Methods. 218:161-167.
62. Brown, M., M.B. Rittenberg, C. Chen, and V.A. Roberts. 1996. Tolerance to single, but not multiple, amino acid replacements in antibody VH CDR2: a means of minimizing B cell wastage from somatic hypermutation? J. Immunol. 156: 3285-3291.
63. Segal, D.M., E.A. Padlan, G.H. Cohen, S. Rudikoff, M. Potter, and D.R. Davies. 1974. The three dimensional structure of a phosphorylcholine-binding mouse immunoglobulin Fab and the nature of the antigen binding site. Proc. Natl. Acad. Sci. USA. 71:4298-4302.
64. Satow, Y., G.H. Cohen, E.A. Padlan, and D.R. Davies. 1986. Phosphocholine binding immunoglobulin Fab McPC.603: an X-ray diffraction study at 2.7 Å. J. Mol. Biol. 190:593-604.
65. Brown, M., G.D. Wiens, T. O'Hare, M.P. Stenzel-Poore, and M.B. Rittenberg. 1999. Replacements in the exposed loop of the T15 antibody VH CDR2 affect carrier recognition of PC-containing pathogens. Mol. Immunol. 36:205-211.
66. Amit, A.G., R.A. Mariuzza, S.E.V. Phillips, and R.J. Poljak. 1986. Three-dimensional structure of an antigen-antibody complex at 2.8 Å resolution. Science. 233:747-753.
67. Alzari, P.M., S. Spinelli, R.A. Mariuzza, G. Boulot, R.J. Poljak, J.M. Jarvis, and C. Milstein. 1990. Three-dimensional structure determination of an anti-2-phenyloxalone antibody: the role of somatic mutation and heavy/light chain pairing in the maturation of an immune response. EMBO (Eur. Mol. Biol. Organ.) J. 9:3807-3814.
68. Berek, C., G.M. Griffiths, and C. Milstein. 1985. Molecular events during maturation of the immune response to oxazolone. Nature. 316:412-418.
69. Manser, T., L.J. Wysocki, M.N. Margolies, and M.L. Gefter. 1987. Evolution of antibody variable region structure during the immune response. Immunol. Rev. 96:141-162.
70. Newman, M.A., C.R. Mainhart, C.P. Mallett, T.B. Lavoire, and S.J. Smith-Gill. 1992. Patterns of antibody specificity during the BALB/c immune response to hen eggwhite lysozyme. J. Immunol. 149:3260-3272.
71. Clarke, S.H., L.M. Staudt, J. Kavaler, D. Schwartz, W.U. Gerhard, and M.G. Weigert. 1990. V region gene usage and somatic mutation in the primary and secondary responses to influenza virus hemagglutinin. J. Immunol. 144:2795-2801.
72. Goldbaum, F.A., A. Cauerhff, A. Velikovsky, A. Llera, M.-M. Riottot, and R.J. Poljak. 1999. Lack of significant differences in association rates and affinities of antibodies from short-term and long-term responses to hen egg lysozyme. J. Immunol. 162:6040-6045.
73. Roost, H.P., M.F. Bachmann, A. Haag, U. Kalinke, V. Pliska, H. Hengartner, and R.M. Zinkernagel. 1995. Early high-affinity neutralizing anti-viral IgG responses without further overall improvements of affinity. Proc. Natl. Acad. Sci. USA. 92:1257-1261.
74. Foote, J., and H.N. Eisen. 1995. Kinetic and affinity limits on antibodies produced during immune responses. Proc. Natl. Acad. Sci. USA. 92:1254-1256.
75. Batista, F.D., and M.S. Neuberger. 1998. Affinity dependence of the B cell response to antigen: a threshold, a ceiling, and the importance of off-rate. Immunity. 8:751-759.
76. England, P., R. Nageotte, M. Renard, A.-L. Page, and H. Bedouelle. 1999. Functional characterization of the somatic hypermutation process leading to antibody D1.3, a high affinity antibody directed against lysozyme. J. Immunol. 162: 2129-2136.
77. McManus, S., and L. Riechmann. 1991. Use of 2D NMR, protein engineering, and molecular modeling to study the hapten-binding site of an antibody Fv fragment against 2-phenyloxazolone. Biochemistry. 30:5851-5857.
78. Lascombe, M.-B., P.M. Alzari, R.J. Poljak, and A. Nisonoff. 1992. Three-dimensional structure of two crystal forms of Fab R19.9 from a monoclonal anti-arsonate antibody. Proc. Natl. Acad. Sci. USA. 89:9429-9433.
79. Wedemayer, G.J., P.A. Patten, L.H. Wang, P.G. Schultz, and R.C. Stevens. 1997. Structural insights into the evolution of an antibody combining site. Science. 276:1665-1669.
80. Kabat, E.A., T.T. Wu, H.M. Perry, R.S. Gottesman, and C. Foeller. 1991. Sequences of Proteins of Immunological Interest. 5th edition. U.S. Department of Health and Human Services, Bethesda, MD. 2,597 pp.