Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells

Journal of Experimental Medicine

Volumn 188, Issue 9, 1998, Pages 1679-1689

  Klein, Ulf ^a   Rajewsky, Klaus ^a   Küppers, Ralf ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

B cell; CD27; Immunoglobulin D; Memory B cell; Somatic hypermutation

Indexed keywords

CD27 ANTIGEN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M;

ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOGLOBULIN VARIABLE REGION; MEMORY CELL; PHENOTYPE; PLASMA CELL; PRIORITY JOURNAL; SOMATIC MUTATION;

ADULT; ANTIGENS, CD27; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; BIOLOGICAL MARKERS; GENE REARRANGEMENT, B-LYMPHOCYTE, HEAVY CHAIN; GENE REARRANGEMENT, B-LYMPHOCYTE, LIGHT CHAIN; GENES, IMMUNOGLOBULIN; HUMANS; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGIC MEMORY; MUTATION;

EID: 0032476611     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.9.1679     Document Type: Article

References (51)

1. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature. 381:751-758.
2. Huang, C., A.K. Stewart, R.S. Schwartz, and B.D. Stollar. 1992. Immunoglobulin heavy chain gene expression in peripheral blood B lymphocytes. J. Clin. Invest. 89:1331-1343.
3. van Es, J.H., F.H. Meyling, and T. Logtenberg. 1992. High frequency of somatically mutated IgM molecules in the human adult blood B cell repertoire. Eur. J. Immunol. 22:2761-2764.
4. Klein, U., R. Küppers, and K. Rajewsky. 1997. Evidence for a large compartment of IgM-expressing memory B cells in humans. Blood. 89:1288-1298.
5. Kindler, V., and R.H. Zubler. 1997. Memory, but not naive, peripheral blood B lymphocytes differentiate into Ig-secreting cells after CD40 ligation and costimulation with IL-4 and the differentiation factors IL-2, IL-10, and IL-3. J. Immunol. 159:2085-2090.
6. Dunn-Walters, D.K., P.G. Isaacson, and J. Spencer. 1995. Analysis of mutations in immunoglobulin heavy chain variable region genes of microdissected marginal zone (MGZ) B cells suggests that the MGZ of human spleen is a reservoir of memory B cells. J. Exp. Med. 182:559-566.
7. Kraal, G. 1992. Cells in the marginal zone of the spleen. Int. Rev. Cytol. 132:31-74.
8. Nicholson, I.C., M.J. Brisco, and H. Zola. 1995. Memory B lymphocytes in human tonsil do not express surface IgD. J. Immunol. 154:1105-1113.
9. Pascual, V., Y.J. Liu, A. Magalski, O. de Bouteiller, J. Banchereau, and J.D. Capra. 1994. Analysis of somatic mutation in five B cell subsets of human tonsil. J. Exp. Med. 180: 329-339.
10. Klein, U., R. Küppers, and K. Rajewsky. 1994. Variable region gene analysis of B cell subsets derived from a 4-year-old child: somatically mutated memory B cells accumulate in the peripheral blood already at young age. J. Exp. Med. 180: 1383-1393.
11. + B cells, the major B cell subset in the peripheral blood, express V kappa genes with no or little somatic mutation throughout life. Eur. J. Immunol. 23:3272-3277.
12. - germinal center B cells can express up to 80 mutations in the variable region of their IgD transcripts. Immunity. 4:603-613.
13. Paramithiotis, E., and M.D. Cooper. 1997. Memory B lymphocytes migrate to the bone marrow in humans. Proc. Natl. Acad. Sci. USA. 94:208-212.
14. H gene, Cμ-Cδ switch, and λ light chain expression. J. Exp. Med. 187:1169-1178.
15. + B lymphocyte subset. J. Immunol. 148:3700-3705.
16. + B cells and helper T cells in immunoglobulin production. Eur. J. Immunol. 27:2073-2079.
17. Scheffold, A., S. Miltenyi, and A. Radbruch. 1995. Magnetofluorescent liposomes for increased sensitivity of immunofluorescence. Immunotechnology. 1:127-137.
18. Fischer, M., U. Klein, and R. Küppers. 1997. Molecular single-cell analysis reveals that CD5-positive peripheral blood B cells in healthy humans are characterized by rearranged Vκ genes lacking somatic mutation. J. Clin. Invest. 100:1667-1676.
19. Küppers, R., M.L. Hansmann, and K. Rajewsky. 1997. Micromanipulation and PCR analysis of single cells from tissue sections. In Handbook of Experimental Immunology. 5th ed. L.A. Herzenberg, L.A. Herzenberg, D. Weir, and D. Blackwell, editors. Blackwell Science Ltd., Oxford. 206.1-206.4.
20. Goossens, T., U. Klein, and R. Küppers. 1998. Frequent occurrence of deletions and duplications during somatic hypermutation: implications for oncogene translocations and heavy chain disease. Proc. Natl. Acad. Sci. USA. 95:2463-2468.
21. Braeuninger, A., R. Küppers, J.G. Strickler, H.H. Wacker, K. Rajewsky, and M.L. Hansmann. 1997. Hodgkin and Reed-Sternberg cells in lymphocyte predominant Hodgkin disease represent clonal populations of germinal center-derived tumor B cells. Proc. Natl. Acad. Sci. USA. 94:9337-9342.
22. Rassenti, L.Z., and T.J. Kipps. 1997. Lack of allelic exclusion in B cell chronic lymphocytic leukemia. J. Exp. Med. 185: 1435-1445.
23. Wilson, P.C., O. de Bouteiller, Y.J. Liu, K. Potter, J. Banchereau, J.D. Capra, and V. Pascual. 1998. Somatic hypermutation introduces insertions and deletions into immunoglobulin V genes. J. Exp. Med. 187:59-70.
24. Klein, U., T. Goossens, M. Fischer, H. Kanzler, A. Braeuninger, K. Rajewsky, and R. Küppers. 1998. Somatic hypermutation in normal and transformed human B cells. Immunol. Rev. 162:261-280.
25. Feddersen, R.M., D.J. Martin, and B.C. Van Ness. 1990. The frequency of multiple recombination events occurring at the human Ig kappa L chain locus. J. Immunol. 144:1088-1093.
26. Betz, A.G., C. Milstein, A. Gonzalez-Fernandez, R. Pannell, T. Larson, and M.S. Neuberger. 1994. Elements regulating somatic hypermutation of an immunoglobulin kappa gene: critical role for the intron enhancer/matrix attachment region. Cell. 77:239-248.
27. Küppers, R., M. Hajadi, L. Plank, K. Rajewsky, and M.L. Hansmann. 1996. Molecular Ig gene analysis reveals that monocytoid B cell lymphoma is a malignancy of mature B cells carrying somatically mutated V region genes and suggests that rearrangement of the kappa-deleting element (resulting in deletion of the Ig kappa enhancers) abolishes somatic hypermutation in the human. Eur. J. Immunol. 26: 1794-1800.
28. Liu, Y.J., J. Zhang, P.J. Lane, E.Y. Chan, and I.C. MacLennan. 1991. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur. J. Immunol. 21:2951-2962.
29. Arpin, C., J. Banchereau, and Y.J. Liu. 1997. Memory B cells are biased towards terminal differentiation: a strategy that may prevent repertoire freezing. J. Exp. Med. 186:931-940.
30. Lebecque, S., O. de Bouteiller, C. Arpin, J. Banchereau, and Y.J. Liu. 1997. Germinal center founder cells display propensity for apoptosis before onset of somatic mutation. J. Exp. Med. 185:563-571.
31. Lens, S.M.A., R.M.J. Keehnen, M.H.J. van Oers, R.A.W. van Lier, S.T. Pals, and G. Koopman. 1996. Identification of a novel subpopulation of germinal center B cells characterized by expression of IgD and CD70. Eur. J. Immunol. 26: 1007-1011.
32. Lens, S.M.A., R. de Jong, B. Hooibrink, G. Koopman, M.H.J. van Oers, and R.A.W. van Lier. 1996. Phenotype and function of human B cells expressing CD70 (CD27 ligand). Eur. J. Immunol. 26:2964-2971.
33. Maurer, D., W. Holter, O. Majdic, G.F. Fischer, and W. Knapp. 1990. CD27 expression by a distinct subpopulation of human B lymphocytes. Eur. J. Immunol. 20:2679-2684.
34. Reynaud, C.A., C. Garcia, W.R. Hein, and J.C. Weill. 1995. Hypermutation generating the sheep immunoglobulin repertoire is an antigen-independent process. Cell. 80:115-125.
35. Klein, U., G. Klein, B. Ehlin-Henriksson, K. Rajewsky, and R. Küppers. 1995. Burkitt's lymphoma is a malignancy of mature B cells expressing somatically mutated V region genes. Mol. Med. 1:495-505.
36. Brezinschek, H., S.J. Foster, T. Dörner, R.I. Brezinschek, and P.E. Lipsky. 1998. Pairing of variable heavy and variable κ chains in individual naive and memory B cells. J. Immunol. 160:4762-4767.
37. Han, S., S.R. Dillon, B. Zheng, M. Shimoda, M.S. Schlissel, and G. Kelsoe. 1997. V(D)J recombinase activity in a subset of germinal center B lymphocytes. Science. 278:301-305.
38. Papavasiliou, F., R. Casellas, H. Suh, X.F. Qin, E. Besmer, R. Pelanda, D. Nemazee, K. Rajewsky, and M.C. Nussenzweig. 1997. V(D)J recombination in mature B cells: a mechanism for altering antibody responses. Science. 278:298-301.
39. Brezinschek, H.P., R.I. Brezinschek, and P.E. Lipsky. 1995. Analysis of the heavy chain repertoire of human peripheral B cells using single-cell polymerase chain reaction. J. Immunol. 155:190-202.
40. Kipps, T.J. 1989. The CD5 B cell. Adv. Immunol. 47:117-185.
41. Linton, P.J., D. Lo, L. Lai, G.J. Thorbecke, 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.
42. Stall, A.M., S.M. Wells, and K.P. Lam. 1996. B-1 cells: unique origins and functions. Semin. Immunol. 8:45-59.
43. Schittek, B., and K. Rajewsky. 1992. Natural occurrence and origin of somatically mutated memory B cells in mice. J. Exp. Med. 176:427-438.
44. Schirrmacher, V., and K. Rajewsky. 1970. Determination of antibody class in a system of cooperating antigenic determinants. J. Exp. Med. 132:1019-1034.
45. Lafrenz, D., S. Strober, and E. Vitetta. 1981. The relationship between surface immunoglobulin isotype and the immune function of murine B lymphocytes. V. High affinity secondary antibody responses are transferred by both IgD-positive and IgD-negative memory B cells. J. Immunol. 127:867-872.
46. Herzenberg, L.A., S.J. Black, T. Tokuhisa, and L.A. Herzenberg. 1980. Memory B cells at successive stages of differentiation. Affinity maturation and the role of IgD receptors. J. Exp. Med. 151:1071-1087.
47. Kobata, T., S. Jacquot, S. Kozlowski, K. Agematsu, S.F. Schlossman, and C. Morimoto. 1995. CD27-CD70 interactions regulate B-cell activation by T cells. Proc. Natl. Acad. Sci. USA. 92:11249-11253.
48. Agematsu, K., H. Nagumo, Y. Oguchi, T. Nakazawa, K. Fukushima, K. Yasui, T. Kobata, C. Morimoto, and A. Komiyama. 1998. Generation of plasma cells from peripheral blood memory B cells: synergistic effect of interleukin-10 and CD27/CD70 interaction. Blood. 91:173-180.
49. Winter, E., U. Krawinkel, and A. Radbruch. 1987. Directed Ig class switch recombination in activated murine B cells. EMBO (Eur. Mol. Biol. Organ.) J. 6:1663-1671.
50. Zhang, K., H.K. Cheah, and A. Saxon. 1994. Secondary deletional recombination of rearranged switch region in isotype-switched B cells. A mechanism for isotype stabilization. J. Immunol. 154:2237-2247.
51. Matsuda, F., E.K. Shin, H. Nagaoka, R. Matsumura, M. Haino, Y. Fukita, S. Takaishi, T. Imai, J.H. Riley, R. Anand, et al. 1993. Structure and physical map of 64 variable segments in the 3′ 0.8-megabase region of the human immunoglobulin heavy-chain locus. Nat. Genet. 3:88-94.