The extent of affinity maturation differs between the memory and antibody-forming cell compartments in the primary immune response

EMBO Journal

Volumn 16, Issue 11, 1997, Pages 2996-3006

  Smith, Kenneth G C ^a   Light, Amanda ^c   Nossal, G J V ^b   Tarlinton, David M ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c NONE

Author keywords

(4 hydroxy 3 nitrophenyl)acetyl; Affinity maturation; Bone marrow; Germinal center; Somatic hypermutation

Indexed keywords

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCING CELL; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL MATURATION; CONTROLLED STUDY; LYMPHOCYTE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; MOUSE; NONHUMAN; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; SOMATIC MUTATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODY AFFINITY; B-LYMPHOCYTE SUBSETS; BASE SEQUENCE; BONE MARROW; BONE MARROW CELLS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MUTATION; NITROPHENOLS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPLEEN; VACCINATION;

EID: 0030925491     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.11.2996     Document Type: Article

References (49)

1. Allen, D., Simon, T., Sablitzky, F., Rajewsky, K. and Cumano, A. (1988) Antibody engineering for the analysis of affinity maturation of an anti-hapten response. EMBO J., 7, 1995-2001.
2. Anderson, B. (1972) Studies on antibody affinity at the cellular level. J. Exp. Med., 135, 312-322.
3. Bachmann, M.F., Kündig, T.M., Odermatt, B., Hengartner, H. and Zinkernagel, R.M. (1994) Free recirculation of memory B cells versus antigen-dependent differentiation to antibody-forming cells. J. Immunol., 153, 3386-3397.
4. Benner, R., Hijmans, W. and Haaijman, J.J. (1981) The bone marrow: the major source of serum immunoglobulins, but still a neglected site of antibody formation. Clin. Exp. Immunol., 46, 1-8.
5. Betz, A.G., Rada, C., Pannell, R., Milstein, C. and Neuberger, M.S. (1993) Passenger transgenes reveal intrinsic specificity of the antibody hypermutation mechanism: clustering, polarity, and specific hotspots. Proc. Natl Acad. Sci. USA, 90, 2385-2388.
6. Blier, P.R. and Bothwell, A. (1987) A limited number of B-cell lineages generates the heterogeneity of the secondary immune response. J. Immunol., 139, 3996-4006.
7. Bothwell, A.L.M., Paskind, M., Reth, M., Imanishi-Kari, T., Rajewsky, K. and Baltimore, D. (1981) Heavy chain variable region contribution to the NPb family of antibodies: somatic mutation evident in a gamma 2a variable region. Cell, 24, 625-637.
8. Bruggemann, M., Muller, H.J., Burger, C. and Rajewsky, K. (1986) Idiotypic selection of an antibody mutant with changed hapten binding specificity, resulting from a point mutation in position 50 of the heavy chain. EMBO J., 5, 1561-1566.
9. Celada, F., Schmidt, D. and Strom, R. (1969) Determination of avidity of anti-albumin antibodies in the mouse. Immunology, 17, 189-198.
10. Cumano, A. and Rajewsky, K. (1985) Structure of primary anti-(4-hydroxy-3-nitrophenyl)acetyl (NP) antibodies in normal and idiotypically suppressed C57BL/6 mice. Eur. J. Immunol., 15, 512-520.
11. Cumano, A. and Rajewsky, K. (1986) Clonal recruitment and somatic mutation in the generation of immunological memory to the hapten NP. EMBO J., 5, 2459-2468.
12. Dilosa, R.M., Maeda, K., Masuda, A., Szakal, A.K. and Tew, J.G. (1991) Germinal center B cells and antibody production in the bone marrow. J. Immunol., 146, 4071-4077.
13. Eisen, H.N. and Siskind, G.N. (1964) Variations in affinities of antibodies during the immune response. Biochem., 3, 996-1008.
14. Elliott, L.H. and Roszman, T.L. (1975) Antigenic selection of IgG precursor subpopulations. J. Immunol., 115, 495-501.
15. Gray, D. (1994) Regulation of immunological memory. Curr. Opin. Immunol., 6, 425-430.
16. Gray, D. and Skarvall, H. (1988) B-cell memory is short lived in the absence of antigen. Nature, 336, 70-73.
17. Goidl, E.A., Paul, W.E., Siskind, G.W. and Benacerraf, B. (1968) The effect of antigen dose and time after immunization on the amount and afinity of anti-hapten antibody. J. Immunol., 100, 371-375.
18. Herzenberg, L.A., Black, S.J., Tokuhisa, T. and Herzenberg, L.A. (1980) Memory B cells at successive stages of differentiation. Affinity maturation and the role of IgD receptors. J. Exp. Med., 151, 1071-1087.
19. Heyman, B. (1990) The immune complex: possible ways of regulating the antibody response. Immunol. Today, 11, 310-313.
20. Ho, F. Lortan, J.E., MacLennan, I.C.M. and Kahn, M. (1986) Distinct short-lived antibody producing cell populations. Eur. J. Immunol., 16, 1297-1301.
21. Hyland, L., Sangster, M., Sealy, R. and Coleclough, C. (1994) Respiratory virus infection of mice provokes a permanent humoral immune response. J. Virol., 68, 6083-6086.
22. Jacob, J., Kassir, R. and Kelsoe, G. (1991) 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, 1165-1175.
23. Jacob, J., Przylepa, J., Miller, C. and Kelsoe, G. (1993) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. III. The kinetics of V region mutation and selection in germinal center B cells. J. Exp. Med., 178, 1293-1307.
24. Kabat, E.A., Wu, T.T., Perry, H.M., Gottesman, K.S. and Foeller, C. (1991) Sequences of Proteins of Immunological Interest. US National Institutes of Health, Bethesda, MD, p. 1394.
25. Karasuyama, H. and Melchers, F. (1988) Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4, or 5, using modified cDNA expression vectors. Eur. J. Immunol., 18, 97-104.
26. Kelsoe, G. (1996) Life and death in germinal centers (redux). Immunity, 4, 107-111.
27. + B cells from antibody secreting and memory B cell pathways in the C57BL/6 immune response to NP. Eur. J. Immunol., 22, 3001-3011.
28. Liu, A.H., Jena, P.K., and Wysocki, L.J. (1996) Tracing the development of single memory-lineage B cells in a highly defined immune response. J. Exp. Med., 183, 2053-2063.
29. MacLennan, I.C.M. (1994) Germinal centers. Annu. Rev. Immunol., 12, 117-139.
30. McHeyzer-Williams, M.G., Nossal, G.J.V. and Lalor, P.A. (1991) Molecular characterisation of single memory B cells. Nature, 350, 501-505.
31. McHeyzer-Williams, M.G, McLean, M.J., Lalor, P.A. and Nossal, G.J.V. (1993) Antigen-driven B cell differentiation in vivo. J. Exp. Med., 178, 295-307.
32. Nossal, G.J.V. (1992) The molecular and cellular basis of affinity maturation in the antibody response. Cell, 68, 1-2.
33. Nossal, G.J.V. and Reidel, C. (1989) Sudden appearance of anti-protein IgG1-forming cell precursors early during primary immunization. Proc. Natl Acad. Sci. USA, 86, 4679-4683.
34. Rajewsky, K. (1996) Clonal selection and learning in the antibody system. Nature 381, 751-758.
35. Ridderstad, A., Nossal, G.J.V. and Tarlinton, D.M. (1996) The xid mutation diminishes memory B cell generation but does not affect somatic hypermutation and selection. J. Immunol., 157, 3357-3365.
36. Schittek, B. and Rajewsky, K. (1990) Maintenance of B cell memory by long-lived cells generated from proliferating precursors. Nature, 346, 749-751.
37. Siskind, G.D. and Benaceraff, B. (1969) Cell selection by antigen in the immune response, Adv. Immunol., 10, 1-50.
38. Siskind, G.W., Dunn, P. and Walker, J.G. (1968) Studies on the control of antibody synthesis II. Effect of antigen dose and of suppression by passive antibody on the affinity of antibody synthesized. J. Exp. Med., 127, 55-66.
39. Slifka, M K., Matloubian, M. and Ahmed, R. (1995) Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol., 69, 1895-1902.
40. Smith, K.G.C., Weiss, U., Rajewsky, K., Nossal, G.J.V. and Tarlinton, D.M. (1994) Bcl-2 increases memory B cell recruitment but does not perturb selection in germinal centers. Immunity, 1, 803-813.
41. Smith, K.G.C., Nossal, G.J.V. and Tarlinton, D.M. (1995) FAS is highly expressed in the germinal center, but is not required for regulation of the B cell response to antigen. Proc. Natl Acad. Sci. USA, 92, 11628-11632.
42. Smith, K.G.C., Hewitson, T.D., Nossal, G.J.V. and Tarlinton, D.M. (1996) The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol., 26, 444-448.
43. Steiner, L.A. and Eisen, H.N. (1967) The relative affinity of antibodies synthesized in the secondary response. J. Exp. Med., 126, 1185-1205.
44. Van Rooijen, N. (1991) Direct intrafollicular differentiation of memory B cells into plasma cells. Immunol. Today, 11, 154-157.
45. Van Rooijen, N., Claassen, E. and Eikelenboom, P. (1986) Is there a single differentiation pathway for all antibody-forming cells in the spleen? Immunol. Today, 7, 193-195.
46. Vitetta, E.S., Berton, M.T., Burger, C., Kepron, M., Lee, W.T. and Yin, X.M. (1991) Memory B and T cells. Annu. Rev. Immunol., 9, 193-217.
47. Weiss, U. and Rajewsky, K. (1990) The repertoire of somatic antibody mutants accumulating in the memory compartment after primary immunization is restricted through affinity maturation and mirrors that expressed in the secondary response. J. Exp. Med., 172, 1681-1689.
48. Weiss, U., Zoebelein, R. and Rajewsky, K. (1992) Accumulation of somatic mutants in the B cell compartment after primary immunization with a T cell-dependent antigen. Eur. J. Immunol., 22, 511-517.
49. Zachau, A.C., Strigard, K., Baig, S., Hojeberg, B. and Olsson, T. (1989) Distribution of plasma cells secreting antibodies against nervous tissue antigens during experimental allergic encephalomyelitis enumerated by a nitrocellulose immunospot assay. J. Neural. Sci., 91, 323-336.