Selection events in directing B cell development

Histology and Histopathology

Volumn 18, Issue 2, 2003, Pages 519-527

  Seagal, J ^a   Melamed, Doron ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

B cell development; B cell receptor; Negative selection; Positive selection; Receptor editing; Secondary immunoglobulin rearrangement

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR;

B LYMPHOCYTE; CELL MATURATION; CELL SELECTION; CELL SURVIVAL; GENE MUTATION; GENE REARRANGEMENT; GERM LINE; HOMEOSTASIS; HUMAN; IMMATURITY; LIFESPAN; LYMPHOCYTE DIFFERENTIATION; METABOLIC REGULATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; HUMANS; MICE; RECEPTORS, ANTIGEN, B-CELL; STEM CELLS;

EID: 0037379313     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (109)

1. Bain G., Maandag E.C., Izon D.J., Amsen D., Kruisbeek A.M., Weintraub B.C., Krop I., Schlissel M.S., Feeney A.J., Van Roon M. and et al. (1994). E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79, 885-892.
2. Bassing C.H., Swat W. and Alt F.W. (2002). The mechanism and regulation of chromosomal V(D)J recombination. Cell 109 Suppl, S45-55.
3. Bellan C., Lazzi S., Zazzi M., Lalinga A.V., Palummo N., Galieni P., Marafioti T., Tonini T., Cinti C., Leoncini L., Pileri S.A. and Tosi P. (2002). Immunoglobulin gene rearrangement analysis in composite hodgkin disease and large B-cell lymphoma: Evidence for receptor revision of immunoglobulin heavy chain variable region genes in Hodgkin-Reed-Sternberg cells? Diagn. Mol. Pathol. 11, 2-8.
4. Benschop R.J., Brandl E., Chan A.C. and Cambier J.C. (2001). Unique signaling properties of B cell antigen receptor in mature and immature B cells: Implications for tolerance and activation. J. Immunol. 167, 4172-4179.
5. Boekel E., Melchers F. and Rolink A. (1995). The status of Ig loci rearrangements in single cells from different stages of B cell development. Int. Immunol. 7, 1013-1019.
6. Bradl H. and Jack H.M. (2001). Surrogate light chain-mediated interaction of a soluble pre-B cell receptor with adherent cell lines. J. Immunol. 167, 6403-6411.
7. Brard F., Shannon M., Prak E.L., Litwin S. and Weigert M. (1999). Somatic mutation and light chain rearrangement generate autoimmunity in anti-single-stranded DNA transgenic MRL/lpr mice. J. Exp. Med. 190, 691-704.
8. Brodeur P.H., Osman G.E., Mackle J.J. and Lalor T.M. (1988). The organization of the mouse Igh-V locus. Dispersion, interspersion, and the evolution of VH gene family clusters. J. Exp. Med. 168, 2261-2278.
9. Buhl A.M., Nemazee D., Cambier J.C., Rickert R. and Hertz M. (2000). B-cell antigen receptor competence regulates B-lymphocyte selection and survival. Immunol. Rev. 176, 141-153.
10. Casellas R., Shih T.A., Kleinewietfeld M., Rakonjac J., Nemazee D., Rajewsky K. and Nussenzweig M.C. (2001). Contribution of receptor editing to the antibody repertoire. Science 291, 1541-1544.
11. Chan V.W., Meng F., Soriano P., DeFranco A.L. and Lowell C.A. (1997). Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity, 7, 69-81.
12. Chen C., Nagy Z., Prak E.L. and Weigert M. (1995). Immunoglobulin heavy chain gene replacement: A mechanism of receptor editing. Immunity 3, 747-755.
13. Chen C., Prak E.L. and Weigert M. (1997). Editing disease-associated autoantibodies. Immunity 6, 97-105.
14. Coleclough C., Perry R.P., Karjalainen K. and Weigert M. (1981). Aberrant rearrangements contribute significantly to the allelic exclusion of immunoglobulin gene expression. Nature 290, 372-378.
15. Constantinescu A. and Schlissel M.S. (1997). Changes in locus-specific V(D)J recombinase activity induced by immunoglobulin gene products during B cell development. J. Exp. Med. 185, 609-620.
16. De Wildt R.M., Hoet R.M., Van Venrooij W.J., Tomlinson I.M. and Winter G. (1999). Analysis of heavy and light chain pairings indicates that receptor editing shapes the human antibody repertoire. J. Mol. Biol. 285, 895-901.
17. Dorner T., Foster S.J., Farner N.L. and Lipsky P.E. (1998). Immunoglobulin kappa chain receptor editing in systemic lupus erythematosus. J. Clin. Invest. 102, 688-694.
18. Ehlich A., Schaal S., Gu H., Kitamura D., Muller W. and Rajewsky K. (1993). Immunoglobulin heavy and light chain genes rearrange independently at early stages of B cell development. Cell 72, 695-704.
19. Engel H., Rolink A. and Weiss S. (1999). B cells are programmed to activate kappa and lambda for rearrangement at consecutive developmental stages. Eur. J. Immunol. 29, 2167-2176.
20. Fulcher D.A., Lyons A.B., Korn S.L., Cook M.C., Koleda C., Parish C., Fazekas de St. Groth B. and Basten A. (1996). The fate of self-reactive B cells depends primarily on the degree of antigen receptor engagement and availability of T cell help. J. Exp. Med. 183, 2313-2328.
21. Gartner F., Alt F.W., Monroe R.J. and Seidl K.J. (2000). Antigen-independent appearance of recombination activating gene (RAG)-positive bone marrow B cells in the spleens of immunized mice. J. Exp. Med. 192, 1745-1754.
22. Gay D., Saunders T., Camper S. and Weigert M. (1993). Receptor editing: An approach by autoreactive B cells to escape tolerance. J. Exp. Med. 177, 999-1008.
23. George A.J. and Gray D. (1999). Receptor editing during affinity maturation. Immunol. Today 20, 196.
24. Goodnow C.C., Crosbie J., Adelstein S., Lavoie T.B., Smith-Gill S.J., Brink R.A., Pritchard-Briscoe H., Wotherspoon J.S., Loblay R.H. and Raphael K. (1988). Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334, 676-682.
25. Goossens T., Brauninger A., Klein U., Kuppers R. and Rajewsky K. (2001). Receptor revision plays no major role in shaping the receptor repertoire of human memory B cells after the onset of somatic hypermutation. Eur. J. Immunol. 31, 3638-3648.
26. Grawunder U., Leu T.M.J., Schatz D.G., Werner A., Rolink A.G., Melchers F. and Winkler T.H. (1995). Down-regulation of RAG1 and RAG2 gene expression in pre B cells after functional immunoglobulin heavy chain rearrangement. Immunity 3, 601-608.
27. Gu H., Tarlinton D., Muller W., Rajewsky K. and Forster I. (1991). Most peripheral B cells in mice are ligand selected. J. Exp. Med. 173, 1357-1371.
28. Han S., Dillon S.R., Zheng B., Shimoda M., Schlissel M.S. and Kelsoe G. (1997). V(D)J recombinase activity in a subset of germinal center B lymphocytes. Science 278, 301-305.
29. Han S., Zheng B., Schatz D.G., Spanopoulou E. and Kelsoe G. (1996). Neoteny in lymphocytes: Rag1 and Rag2 expression in germinal center B cells. Science 274, 2094-2097.
30. Harada K. and Yamagishi H. (1991). Lack of feedback inhibition of Vκ gene rearrangement by productively rearranged alleles. J. Exp. Med. 173, 409-415.
31. Hardy R.R., Carmack C.E., Shinton S.A., Kemp J.D. and Hayakawa K. (1991). Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173, 1213-1225.
32. Hartley S.B., Cooke M.P., Fulcher D.A., Harris A.W., Cory S., Basten A. and Goodnow C.C. (1993). Elimination of self-reactive B lymphocytes proceeds in two stages: Arrested development and cell death. Cell 72, 325-335.
33. Hartley S.B., Crosbie J., Brink R., Kantor A.B., Basten A. and Goodnow C.C. (1991). Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353, 765-769.
34. Healy J.I. and Goodnow C.C. (1998). Positive versus negative signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 16, 645-670.
35. Hertz M. and Nemazee D. (1997). BCR ligation induces receptor editing in IgM+IgD- bone marrow B cells in vitro. Immunity 6, 429-436.
36. Hertz M. and Nemazee D. (1998). Receptor editing and commitment in B lymphocytes. Curr. Opin. Immunol. 10, 208-213.
37. Hikida M., Mori M., Takai T., Tomochika K., Hamatani K. and Ohmori H. (1996). Reexpression of RAG-1 and RAG-2 genes in activated mature mouse B cells. Science 274, 2092-2094.
38. Hikida M., Nakayama Y., Yamashita Y., Kumazawa Y., Nishikawa S.I. and Ohmori H. (1998). Expression of recombination activating genes in germinal center B cells: Involvement of interleukin 7 (IL-7) and the IL-7 receptor. J. Exp. Med. 188, 365-372.
39. Itoh K., Meffre E., Albesiano E., Farber A., Dines D., Stein P., Asnis S.E., Furie R.A., Jain R.I. and Chiorazzi N. (2000). Immunoglobulin heavy chain variable region gene replacement as a mechanism for receptor revision in rheumatoid arthritis synovial tissue B lymphocytes. J. Exp. Med. 192, 1151-1164.
40. Jumaa H., Wollscheid B., Mitterer M., Wienands J., Reth M. and Nielsen P.J. (1999). Abnormal development and function of B lymphocytes in mice deficient for the signaling adaptor protein SLP-65. Immunity 11, 547-554.
41. Khan W.N., Alt F.W., Gerstein R.M., Malynn B.A., Larsson I., Rathbun G., Davidson L., Muller S., Kantor A.B. and Herzenberg L.A. (1995). Defective B cell development and function in Btk-deficient mice. Immunity 3, 283-299.
42. Kitamura D. and Rajewsky K. (1992). Targeted disruption of mu chain membrane exon causes loss of heavy-chain allelic exclusion. Nature 356, 154-156.
43. Kleinfield R., Hardy R.R., Tarlinton D., Dangl J., Herzenberg L.A. and Weigert M. (1986). Recombination between an expressed immunoglobulin heavy-chain gene and a germline variable gene segment in a Ly 1+ B-cell lymphoma. Nature 322, 843-846.
44. Kouskoff V., Lacaud G. and Nemazee D. (2000). T cell-independent rescue of B lymphocytes from peripheral immune tolerance. Science 287, 2501-2503.
45. Kuwata N., Igarashi H., Ohmura T., Aizawa S. and Sakaguchi N. (1999). Cutting edge: Absence of expression of RAG1 in peritoneal B-1 cells detected by knocking into RAG1 locus with green fluorescent protein gene. J. Immunol. 163, 6355-6359.
46. Lam K.P., Kuhn R. and Rajewsky K. (1997). In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90, 1073-1083.
47. Lawton A.D., Asofsky R., Hylton M.B. and Cooper M.D. (1972). Suppression of immunoglobulin class synthesis in mice. I. Effects of treatment with antibody to -chain. J. Exp. Med. 135, 277-297.
48. Levy S., Campbell M.J. and Levy R. (1989). Functional immunoglobulin light chain genes are replaced by ongoing rearrangements of germline V kappa genes to downstream J kappa segment in a murine B cell line. J. Exp. Med. 170, 1-13.
49. Lin H. and Grosschedl R. (1995). Failure of B-cell differentiation in mice lacking the transcription factor EBF. Nature 376, 263-267.
50. Li H., Jiang Y., Prak E.L., Radic M. and Weigert M. (2001). Editors and editing of anti-DNA receptors. Immunity 15, 947-957.
51. Loder F., Mutschler B., Ray R.J., Paige C.J., Sideras P., Torres R., Lamers M.C. and Carsetti R. (1999). B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190, 75-89.
52. Loffert D., Ehlich A., Muller W. and Rajewsky K. (1996). Surrogate light chain expression is required to establish immunoglobulin heavy chain allelic exclusion during early B cell development. Immunity 4, 133-144.
53. Lu L. and Osmond D.G. (1997). Apoptosis during B lymphopoiesis in mouse bone marrow. J. Immunol. 158, 5136-5145.
54. Magari M., Sawatari T., Kawano Y., Cascalho M., Wabl M., Kanayama N., Hikida M. and Ohmori H. (2002). Contribution of light chain rearrangement in peripheral B cells to the generation of high-affinity antibodies. Eur. J. Immunol. 32, 957-966.
55. Martin F. and Kearney J.F. (2000). Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19, and btk. Immunity 12, 39-49.
56. Meade J., Fernandez C. and Turner M. (2002). The tyrosine kinase Lyn is required for B cell development beyond the T1 stage in the spleen: Rescue by over-expression of Bcl-2. Eur. J. Immunol. 32, 1029-1034.
57. Meffre E., Casellas R. and Nussenzweig M.C. (2000). Antibody regulation of B cell development. Nat. Immunol. 1, 379-385.
58. Meffre E., Davis E., Schiff C., Cunningham-Rundles C., Ivashkiv L.B., Staudt L.M., Young J.W. and Nussenzweig M.C. (2000). Circulating human B cells that express surrogate light chains and edited receptors. Nat. Immunol. 1, 207-213.
59. Meffre E., Papavasiliou F., Cohen P., De Bouteiller O., Bell D., Karasuyama H., Schiff C., Banchereau J., Liu Y.J. and Nussenzweig M.C. (1998). Antigen receptor engagement turns off the V(D)J recombination machinery in human tonsil B cells. J. Exp. Med. 188, 765-772.
60. Melamed D. and Nemazee D. (1997). Self-antigen does not accelerate immature B cell apoptosis, but stimulates receptor editing as a consequence of developmental arrest. Proc. Natl. Acad. Sci. USA 94, 9267-9272.
61. Melamed D., Benschop R.J., Cambier J.C. and Nemazee D. (1998). Developmental regulation of B lymphocyte immune tolerance compartmentalizes clonal selection from receptor selection. Cell 92, 173-182.
62. Melamed D., Miri E., Leider N. and Nemazee D. (2000). Unexpected autoantibody production in membrane Ig-&mgr;-Deficient/Ipr mice [In Process Citation]. J. Immunol. 165, 4353-4358.
63. Melchers F., Ten Boekel E., Seidl T., Kong X.C., Yamagami T., Onishi K., Shimizu T., Rolink A.G. and Andersson J. (2000). Repertoire selection by pre-B-cell receptors and B-cell receptors, and genetic control of B-cell development from immature to mature B cells. Immunol. Rev. 175, 33-46.
64. Melchers F., Ten Boekel E., Yamagami T., Andersson J. and Rolink A. (1999). The roles of preB and B cell receptors in the stepwise allelic exclusion of mouse IgH and L chain gene loci. Semin. Immunol. 11, 307-317.
65. Minegishi Y. and Conley M.E. (2001). Negative selection at the pre-BCR checkpoint elicited by human mu heavy chains with unusual CDR3 regions. Immunity 14, 631-641.
66. Monroe J.G. (1996). Tolerance sensitivity of immature-stage B cells. J. Immunol. 156, 2657-2660.
67. Monroe R.J., Seidl K.J., Gaertner F., Han S., Chen F., Sekiguchi J., Wang J., Ferrini R., Davidson L., Kelsoe G. and Alt F.W. (1999). RAG2:GFP knockin mice reveal novel aspects of RAG2 expression in primary and peripheral lymphoid tissues. Immunity 11, 201-212.
68. Nagaoka H., Gonzalez-Aseguinolaza G., Tsuji M. and Nussenzweig M.C. (2000). Immunization and infection change the number of recombination activating gene (RAG)-expressing B cells in the periphery by altering immature lymphocyte production. J. Exp. Med. 191, 2113-2120.
69. Nemazee D. (2000). Receptor selection in B and T lymphocytes. Annu. Rev. Immunol. 18, 19-51.
70. Nemazee D. and Weigert M. (2000). Revising B cell receptors. J. Exp. Med. 191, 1813-1817.
71. Nemazee D.A. and Burki K. (1989). Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-μHC class I antibody genes. Nature 337, 562-566.
72. Nossal G.J. (1983). Cellular mechanisms of immunologic tolerance. Ann. Rev. Immunol. 1, 33-62.
73. Nussenzweig M.C. (1998). Immune receptor editing: Revise and select. Cell 95, 875-878.
74. Nutt S.L., Eberhard D., Horcher M., Rolink A.G. and Busslinger M. (2001). Pax5 determines the identity of B cells from the beginning to the end of B-lymphopoiesis. Int. Rev. Immunol. 20, 65-82.
75. Papavasiliou F., Casellas R., Suh H., Qin X.F., Besmer E., Pelanda R., Nemazee D., Rajewsky K. and Nussenzweig M.C. (1997). V(D)J recombination in mature B cells: A mechanism for altering antibody responses. Science 278, 298-301.
76. Papavasiliou F., Misulovin Z., Suh H. and Nussenzweig M.C. (1995). The role of Ig beta in precursor B cell transition and allelic exclusion. Science 268, 408-411.
77. Pelanda R., Schwers S., Sonoda E., Torres R.M., Nemazee D. and Rajewsky K. (1997). Receptor editing in a transgenic mouse model: Site, efficiency and role in B cell tolerance and antibody diversification. Immunity 7, 765-775.
78. Pewzner-Jung Y., Friedmann D., Sonoda E., Jung S., Rajewsky K. and Eilat D. (1998). B cell deletion, energy, and receptor editing in "knock in" mice targeted with a germline-encoded or somatically mutated anti-DNA heavy chain. J. Immunol. 161, 4634-4645.
79. Radic M.Z. and Zouali M. (1996). Receptor editing, immune diversification, and self-tolerance. Immunity 5, 505-511.
80. Radic M.Z., Erikson J., Litwin S. and Weigert M. (1993). B lymphocytes may escape tolerance by revising their antigen receptors. J. Exp. Med. 177, 1165-1173.
81. Rajewsky K. (1996). Clonal selection and learning in the antibody system. Nature 381, 751-758.
82. Reichlin A., Hu Y., Meffre E., Nagaoka H., Gong S., Kraus M., Rajewsky K. and Nussenzweig M.C. (2001). B cell development is arrested at the immature B cell stage in mice carrying a mutation in the cytoplasmic domain of immunoglobulin beta. J. Exp. Med. 193, 13-23.
83. Reth M., Gehrmann P., Petrac E. and Wiese P. (1986). A novel VH to VHDJH joining mechanism in heavy-chain-negative (null) pre-B cells results in heavy-chain production. Nature 322, 840-842.
84. Reth M., Wienands J. and Schamel W.W. (2000). An unsolved problem of the clonal selection theory and the model of an oligomeric B-cell antigen receptor. Immunol. Rev. 176, 10-18.
85. Retter M.W. and Nemazee D. (1998). Receptor editing occurs frequently during normal B cell development. J. Exp. Med. 188, 1231-1238.
86. + B cells can continue to rearrange kappa and lambda L chain gene loci. J. Exp. Med. 178, 1263-1270.
87. Rolink A.G., Nutt S.L., Melchers F. and Busslinger M. (1999). Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors. Nature 401, 603-606.
88. Rolink A.G., Schaniel C., Andersson J. and Melchers F. (2001). Selection events operating at various stages in B cell development. Curr. Opin. Immunol. 13, 202-207.
89. Rolink A.G., Ten Boekel E., Yamagami T., Ceredig R., Andersson J. and Melchers F. (1999). B cell development in the mouse from early progenitors to mature B cells. Immunol. Lett. 68, 89-93.
90. Roth P.E., Doglio L., Manz J.T., Kim J.Y., Lo D. and Storb U. (1993). Immunoglobulin gamma 2b transgenes inhibit heavy chain gene rearrangement, but cannot promote B cell development. J. Exp. Med. 178, 2007-2021.
91. Russell D.M., Dembic Z., Morahan G., Miller J.F., Burki K. and Nemazee D. (1991). Peripheral deletion of self-reactive B cells. Nature 354, 308-311.
92. Sandel P.C., Gendelman M., Kelsoe G. and Monroe J.G. (2001). Definition of a novel cellular constituent of the bone marrow that regulates the response of immature B cells to B cell antigen receptor engagement. J. Immunol. 166, 5935-5944.
93. Sandel P.C. and Monroe J.G. (1999). Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 10, 289-299.
94. Shivtiel S., Leider N. and Melamed D. (2002). Receptor editing in CD45-deficient immature B cells. Eur. J. Immunol. 32, 2264-2273.
95. Shivtiel S., Leider N., Sadeh O., Kraiem Z. and Melamed D. (2002). Impaired light chain allelic exclusion and lack of positive selection in immature B cells expressing incompetent receptor deficient of CD19. J. Immunol. 168, 5596-5604.
96. Sproul T.W., Malapati S., Kim J. and Pierce S.K. (2000). Cutting edge: B cell antigen receptor signaling occurs outside lipid rafts in immature B cells. J. Immunol. 165, 6020-6023.
97. Sun T., Clark M.R. and Storb U. (2002). A point mutation in the constant region of Ig lambda1 prevents normal B cell development due to defective BCR signaling. Immunity 16, 245-255.
98. Tedford K., Nitschke L., Girkontaite I., Charlesworth A., Chan G., Sakk V., Barbacid M. and Fischer K.D. (2001). Compensation between Vav-1 and Vav-2 in B cell development and antigen receptor signaling. Nat. Immunol. 2, 548-555.
99. Ten Boekel E., Melchers F. and Rolink A.G. (1997). Changes in the V(H) gene repertoire of developing precursor B lymphocytes in mouse bone marrow mediated by the pre-B cell receptor. Immunity 7, 357-368.
100. Ten Boekel E., Melchers F. and Rolink A.G. (1998). Precursor B cells showing H chain allelic inclusion display allelic exclusion at the level of pre-B cell receptor surface expression. Immunity 8, 199-207.
101. Tiegs S.L., Russell D.M. and Nemazee D. (1993). Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177, 1009-1020.
102. Torres R.M., Flaswinkel H., Reth M. and Rajewsky K. (1996). Aberrant B cell development and immune response in mice with a compromised BCR complex. Science 272, 1804-1808.
103. Torres R.M. and Hafen K. (1999). A negative regulatory role for Ig-alpha during B cell development. Immunity 11, 527-536.
104. Turner M., Gulbranson-Judge A., Quinn M.E., Walters A.E., MacLennan I.C. and Tybulewicz V.L. (1997). Syk tyrosine kinase is required for the positive selection of immature B cells into the recirculating B cell pool. J. Exp. Med. 186, 2013-2021.
105. Wasserman R., Li Y.S., Shinton S.A., Carmack C.E., Manser T., Wiest D.L., Hayakawa K. and Hardy R.R. (1998). A novel mechanism for B cell repertoire maturation based on response by B cell precursors to pre-B receptor assembly. J. Exp. Med. 187, 259-264.
106. Wilson P.C., Wilson K., Liu Y.J., Banchereau J., Pascual V. and Capra J.D. (2000). Receptor revision of immunoglobulin heavy chain variable region genes in normal human B lymphocytes. J. Exp. Med. 191, 1881-1894.
107. Yachimovich N., Mostoslavsky G., Yarkoni Y., Verbovetski I. and Eilat D. (2002). The efficiency of B cell receptor (BCR) editing is dependent on BCR light chain rearrangement status. Eur. J. Immunol. 32, 1164-1174.
108. Yamagami T., Ten Boekel E., Andersson J., Rolink A. and Melchers F. (1999). Frequencies of multiple IgL chain gene rearrangements in single normal or kappaL chain-deficient B lineage cells. Immunity 11, 317-327.
109. Yu W., Nagaoka H., Jankovic M., Misulovin Z., Suh H., Rolink A., Melchers F., Meffre E. and Nussenzweig M.C. (1999). Continued RAG expression in late stages of B cell development and no apparent re-induction after immunization. Nature 400, 682-687.