Stromal cell independent B cell development in vitro: Generation and recovery of autoreactive clones

Journal of Immunological Methods

Volumn 354, Issue 1-2, 2010, Pages 53-67

  Holl, T Matt ^a   Haynes, Barton F ^a   Kelsoe, Garnett ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autoimmunity; B cell; BAFF; Development; Interleukin 7

Indexed keywords

B CELL ACTIVATING FACTOR; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN KAPPA CHAIN; IMMUNOGLOBULIN M; INTERLEUKIN 7; MEMBRANE ANTIGEN; RAG1 PROTEIN; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE; BONE MARROW CELL; C57BL 6 MOUSE; CELL CLONE; CELL CULTURE; CELL LINEAGE; CELL MATURATION; CELL STRAIN 3T3; CELL SURVIVAL; CONTROLLED STUDY; GENE ACTIVATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STROMA CELL;

ANIMALS; ANTIBODY FORMATION; ANTIGENS, SURFACE; AUTOANTIBODIES; AUTOIMMUNITY; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COMPLEMENT C4; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE REARRANGEMENT, B-LYMPHOCYTE; GENOTYPE; HOMEODOMAIN PROTEINS; IMMUNOGLOBULIN D; IMMUNOGLOBULIN ISOTYPES; IMMUNOGLOBULIN M; IMMUNOPHENOTYPING; INTERLEUKIN-7; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHENOTYPE; PRECURSOR CELLS, B-LYMPHOID; STROMAL CELLS; TIME FACTORS; TOLL-LIKE RECEPTORS;

ANIMALIA; MUS;

EID: 77949917469     PISSN: 00221759     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jim.2010.01.007     Document Type: Article

References (107)

1. Adams E., Basten A., Goodnow C.C. Intrinsic B-cell hyporesponsiveness accounts for self-tolerance in lysozyme/anti-lysozyme double-transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:5687.
2. Allman D., Pillai S. Peripheral B cell subsets. Curr. Opin. Immunol. 2008, 20:149.
3. Amano M., Baumgarth N., Dick M.D., Brossay L., Kronenberg M., Herzenberg L.A., Strober S. CD1 expression defines subsets of follicular and marginal zone B cells in the spleen: beta 2-microglobulin-dependent and independent forms. J. Immunol. 1998, 161:1710.
4. Baird A.M., Gerstein R.M., Berg L.J. The role of cytokine receptor signaling in lymphocyte development. Curr. Opin. Immunol. 1999, 11:157.
5. Batten M., Groom J., Cachero T.G., Qian F., Schneider P., Tschopp J., Browning J.L., Mackay F. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 2000, 192:1453.
6. Baumann B., Potash M.J., Kohler G. Consequences of frameshift mutations at the immunoglobulin heavy chain locus of the mouse. EMBO J. 1985, 4:351.
7. Benedict C.L., Kearney J.F. Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 1999, 10:607.
8. Benedict C.L., Gilfillan S., Thai T.H., Kearney J.F. Terminal deoxynucleotidyl transferase and repertoire development. Immunol. Rev. 2000, 175:150.
9. Billips L.G., Petitte D., Dorshkind K., Narayanan R., Chiu C.P., Landreth K.S. Differential roles of stromal cells, interleukin-7, and kit-ligand in the regulation of B lymphopoiesis. Blood 1992, 79:1185.
10. Billips L.G., Nunez C.A., Bertrand F.E., Stankovic A.K., Gartland G.L., Burrows P.D., Cooper M.D. Immunoglobulin recombinase gene activity is modulated reciprocally by interleukin 7 and CD19 in B cell progenitors. J. Exp. Med. 1995, 182:973.
11. Bowes T., Wagner E.R., Boffey J., Nicholl D., Cochrane L., Benboubetra M., Conner J., Furukawa K., Furukawa K., Willison H.J. Tolerance to self gangliosides is the major factor restricting the antibody response to lipopolysaccharide core oligosaccharides in Campylobacter jejuni strains associated with Guillain-Barre syndrome. Infect. Immun. 2002, 70:5008.
12. Bowie M.B., McKnight K.D., Kent D.G., McCaffrey L., Hoodless P.A., Eaves C.J. Hematopoietic stem cells proliferate until after birth and show a reversible phase-specific engraftment defect. J. Clin. Invest. 2006, 116:2808.
13. Bradley L.M., Haynes L., Swain S.L. IL-7: maintaining T-cell memory and achieving homeostasis. Trends. Immunol. 2005, 26:172.
14. Burton D.R., Desrosiers R.C., Doms R.W., Koff W.C., Kwong P.D., Moore J.P., Nabel G.J., Sodroski J., Wilson I.A., Wyatt R.T. HIV vaccine design and the neutralizing antibody problem. Nat. Immunol. 2004, 5:233.
15. Carsetti R., Rosado M.M., Wardmann H. Peripheral development of B cells in mouse and man. Immunol. Rev. 2004, 197:179.
16. Chen J., Alt F.W. Gene rearrangement and B-cell development. Curr. Opin. Immunol. 1993, 5:194.
17. Chen C., Nagy Z., Prak E.L., Weigert M. Immunoglobulin heavy chain gene replacement: a mechanism of receptor editing. Immunity 1995, 3:747.
18. -/- mice: enhanced affinity maturation but impaired antibody persistence. J. Immunol. 2000, 164:4522.
19. Chen Z., Koralov S.B., Kelsoe G. Complement C4 inhibits systemic autoimmunity through a mechanism independent of complement receptors CR1 and CR2. J. Exp. Med. 2000, 192:1339.
20. Chen Z., Koralov S.B., Kelsoe G. Regulation of humoral immune responses by CD21/CD35. Immunol. Rev. 2000, 176:194.
21. Cho S.K., Webber T.D., Carlyle J.R., Nakano T., Lewis S.M., Zuniga-Pflucker J.C. Functional characterization of B lymphocytes generated in vitro from embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9797.
22. Claudio E., Brown K., Park S., Wang H., Siebenlist U. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat. Immunol. 2002, 3:958.
23. Cobaleda C., Schebesta A., Delogu A., Busslinger M. Pax5: the guardian of B cell identity and function. Nat. Immunol. 2007, 8:463.
24. Collins L.S., Dorshkind K. A stromal cell line from myeloid long-term bone marrow cultures can support myelopoiesis and B lymphopoiesis. J. Immunol. 1987, 138:1082.
25. Cumano A., Dorshkind K., Gillis S., Paige C.J. The influence of S17 stromal cells and interleukin 7 on B cell development. Eur. J. Immunol. 1990, 20:2183.
26. Dorshkind K. Regulation of hemopoiesis by bone marrow stromal cells and their products. Annu. Rev. Immunol. 1990, 8:111.
27. Dorshkind K., Montecino-Rodriguez E. Fetal B-cell lymphopoiesis and the emergence of B-1-cell potential. Nat. Rev. Immunol. 2007, 7:213.
28. Dudley D.D., Chaudhuri J., Bassing C.H., Alt F.W. Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences. Adv. Immunol. 2005, 86:43.
29. Ekiert D.C., Bhabha G., Elsliger M.A., Friesen R.H., Jongeneelen M., Throsby M., Goudsmit J., Wilson I.A. Antibody recognition of a highly conserved influenza virus epitope. Science 2009, 324:246.
30. Erikson J., Radic M.Z., Camper S.A., Hardy R.R., Carmack C., Weigert M. Expression of anti-DNA immunoglobulin transgenes in non-autoimmune mice. Nature 1991, 349:331.
31. Feeney A.J. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J. Exp. Med. 1990, 172:1377.
32. Fischer M.B., Ma M., Goerg S., Zhou X., Xia J., Finco O., Han S., Kelsoe G., Howard R.G., Rothstein T.L., Kremmer E., Rosen F.S., Carroll M.C. Regulation of the B cell response to T-dependent antigens by classical pathway complement. J. Immunol. 1996, 157:549.
33. Fluckiger A.C., Sanz E., Garcia-Lloret M., Su T., Hao Q.L., Kato R., Quan S., de la Hera A., Crooks G.M., Witte O.N., Rawlings D.J. In vitro reconstitution of human B-cell ontogeny: from CD34(+) multipotent progenitors to Ig-secreting cells. Blood 1998, 92:4509.
34. Gay D., Saunders T., Camper S., Weigert M. Receptor editing: an approach by autoreactive B cells to escape tolerance. J. Exp. Med. 1993, 177:999.
35. Gilkeson G.S., Pippen A.M., Pisetsky D.S. Induction of cross-reactive anti-dsDNA antibodies in preautoimmune NZB/NZW mice by immunization with bacterial DNA. J. Clin. Invest. 1995, 95:1398.
36. Goodnow C.C. Transgenic mice and analysis of B-cell tolerance. Annu. Rev. Immunol. 1992, 10:489.
37. Gorelik L., Cutler A.H., Thill G., Miklasz S.D., Shea D.E., Ambrose C., Bixler S.A., Su L., Scott M.L., Kalled S.L. Cutting edge: BAFF regulates CD21/35 and CD23 expression independent of its B cell survival function. J. Immunol. 2004, 172:762.
38. Han S., Dillon S.R., Zheng B., Shimoda M., Schlissel M.S., Kelsoe G. V(D)J recombinase activity in a subset of germinal center B lymphocytes. Science 1997, 278:301.
39. Hardy R.R. B-1 B cells: development, selection, natural autoantibody and leukemia. Curr. Opin. Immunol. 2006, 18:547.
40. Hardy R.R., Hayakawa K. B cell development pathways. Annu. Rev. Immunol. 2001, 19:595.
41. Hardy R.R., Carmack C.E., Shinton S.A., Kemp J.D., Hayakawa K. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 1991, 173:1213.
42. Hartley S.B., Crosbie J., Brink R., Kantor A.B., Basten A., Goodnow C.C. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 1991, 353:765.
43. Hartley S.B., Cooke M.P., Fulcher D.A., Harris A.W., Cory S., Basten A., Goodnow C.C. Elimination of self-reactive B lymphocytes proceeds in two stages: arrested development and cell death. Cell 1993, 72:325.
44. Hayakawa K., Hardy R.R., Herzenberg L.A. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 1985, 161:1554.
45. Hayakawa K., Hardy R.R., Stall A.M., Herzenberg L.A. Immunoglobulin-bearing B cells reconstitute and maintain the murine Ly-1 B cell lineage. Eur. J. Immunol. 1986, 16:1313.
46. Haynes B.F., Fleming J., St Clair E.W., Katinger H., Stiegler G., Kunert R., Robinson J., Scearce R.M., Plonk K., Staats H.F., Ortel T.L., Liao H.X., Alam S.M. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 2005, 308:1906.
47. Hess J., Werner A., Wirth T., Melchers F., Jack H.M., Winkler T.H. Induction of pre-B cell proliferation after de novo synthesis of the pre-B cell receptor. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:1745.
48. Jacob J., Kelsoe G., Rajewsky K., Weiss U. Intraclonal generation of antibody mutants in germinal centres. Nature 1991, 354:389.
49. Kaech S.M., Hemby S., Kersh E., Ahmed R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 2002, 111:837.
50. Kieper W.C., Jameson S.C. Homeostatic expansion and phenotypic conversion of naive T cells in response to self peptide/MHC ligands. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:13306.
51. Kikuchi K., Kondo M. Developmental switch of mouse hematopoietic stem cells from fetal to adult type occurs in bone marrow after birth. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17852.
52. Kondo M., Weissman I.L., Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997, 91:661.
53. Lang J., Arnold B., Hammerling G., Harris A.W., Korsmeyer S., Russell D., Strasser A., Nemazee D. Enforced Bcl-2 expression inhibits antigen-mediated clonal elimination of peripheral B cells in an antigen dose-dependent manner and promotes receptor editing in autoreactive, immature B cells. J. Exp. Med. 1997, 186:1513.
54. Lazorchak A.S., Schlissel M.S., Zhuang Y. E2A and IRF-4/Pip promote chromatin modification and transcription of the immunoglobulin kappa locus in pre-B cells. Mol. Cell. Biol. 2006, 26:810.
55. Lee D.J., Abeyratne A., Carson D.A., Corr M. Induction of an antigen-specific, CD1-restricted cytotoxic T lymphocyte response in vivo. J. Exp. Med. 1998, 187:433.
56. Li Y.S., Hayakawa K., Hardy R.R. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J. Exp. Med. 1993, 178:951.
57. Li Z., Dordai D.I., Lee J., Desiderio S. A conserved degradation signal regulates RAG-2 accumulation during cell division and links V(D)J recombination to the cell cycle. Immunity 1996, 5:575.
58. Lopes-Carvalho T., Kearney J.F. Development and selection of marginal zone B cells. Immunol. Rev. 2004, 197:192.
59. Luo X.M., Maarschalk E., O'Connell R.M., Wang P., Yang L., Baltimore D. Engineering human hematopoietic stem/progenitor cells to produce a broadly neutralizing anti-HIV antibody after in vitro maturation to human B lymphocytes. Blood 2009, 113:1422.
60. Mackay F., Woodcock S.A., Lawton P., Ambrose C., Baetscher M., Schneider P., Tschopp J., Browning J.L. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 1999, 190:1697.
61. Mackay F., Schneider P., Rennert P., Browning J. BAFF and APRIL: a tutorial on B cell survival. Annu. Rev. Immunol. 2003, 21:231.
62. Market E., Papavasiliou F.N. V(D)J recombination and the evolution of the adaptive immune system. PLoS Biol. 2003, 1:E16.
63. Martin F., Kearney J.F. B1 cells: similarities and differences with other B cell subsets. Curr. Opin. Immunol. 2001, 13:195.
64. McKearn J.P., Baum C., Davie J.M. Cell surface antigens expressed by subsets of pre-B cells and B cells. J. Immunol. 1984, 132:332.
65. Meffre E., Schaefer A., Wardemann H., Wilson P., Davis E., Nussenzweig M.C. Surrogate light chain expressing human peripheral B cells produce self-reactive antibodies. J. Exp. Med. 2004, 199:145.
66. Melamed D., Kench J.A., Grabstein K., Rolink A., Nemazee D. A functional B cell receptor transgene allows efficient IL-7- independent maturation of B cell precursors. J. Immunol. 1997, 159:1233.
67. Nagasawa T. Microenvironmental niches in the bone marrow required for B-cell development. Nat. Rev. Immunol. 2006, 6:107.
68. Nakano T., Kodama H., Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science 1994, 265:1098.
69. Nemazee D.A., Burki K. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 1989, 337:562.
70. Nisitani S., Tsubata T., Murakami M., Okamoto M., Honjo T. The bcl-2 gene product inhibits clonal deletion of self-reactive B lymphocytes in the periphery but not in the bone marrow. J. Exp. Med. 1993, 178:1247.
71. Nitschke L. The role of CD22 and other inhibitory co-receptors in B-cell activation. Curr. Opin. Immunol. 2005, 17:290.
72. Oliver A.M., Martin F., Gartland G.L., Carter R.H., Kearney J.F. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 1997, 27:2366.
73. Oliver A.M., Martin F., Kearney J.F. IgMhighCD21high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J. Immunol. 1999, 162:7198.
74. Pelletier M., Thompson J.S., Qian F., Bixler S.A., Gong D., Cachero T., Gilbride K., Day E., Zafari M., Benjamin C., Gorelik L., Whitty A., Kalled S.L., Ambrose C., Hsu Y.M. Comparison of soluble decoy IgG fusion proteins of BAFF-R and BCMA as antagonists for BAFF. J. Biol. Chem. 2003, 278:33127.
75. Pereira J.P., An J., Xu Y., Huang Y., Cyster J.G. Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids. Nat. Immunol. 2009, 10:403.
76. Pillai S., Cariappa A., Moran S.T. Marginal zone B cells. Annu. Rev. Immunol. 2005, 23:161.
77. Pranzatelli M.R., Tate E.D., Hoefgen E.R., Swan J.A., Colliver J.A. Therapeutic down-regulation of central and peripheral B-cell-activating factor (BAFF) production in pediatric opsoclonus-myoclonus syndrome. Cytokine 2008, 44:26.
78. Radic M.Z., Erikson J., Litwin S., Weigert M. B lymphocytes may escape tolerance by revising their antigen receptors. J. Exp. Med. 1993, 177:1165.
79. Ray R.J., Stoddart A., Pennycook J.L., Huner H.O., Furlonger C., Wu G.E., Paige C.J. Stromal cell-independent maturation of IL-7-responsive pro-B cells. J. Immunol. 1998, 160:5886.
80. Rohatgi S., Ganju P., Sehgal D. Systematic design and testing of nested (RT-)PCR primers for specific amplification of mouse rearranged/expressed immunoglobulin variable region genes from small number of B cells. J. Immunol. Methods 2008, 339:205.
81. Rolink A., Kudo A., Karasuyama H., Kikuchi Y., Melchers F. Long-term proliferating early pre B cell lines and clones with the potential to develop to surface Ig-positive, mitogen reactive B cells in vitro and in vivo. EMBO J. 1991, 10:327.
82. Rolink A., Streb M., Melchers F. The kappa/lambda ratio in surface immunoglobulin molecules on B lymphocytes differentiating from DHJH-rearranged murine pre-B cell clones in vitro. Eur. J. Immunol. 1991, 21:2895.
83. Rolink A.G., Tschopp J., Schneider P., Melchers F. BAFF is a survival and maturation factor for mouse B cells. Eur. J. Immunol. 2002, 32:2004.
84. Sandel P.C., Monroe J.G. Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 1999, 10:289.
85. Sandel P.C., Gendelman M., Kelsoe G., Monroe J.G. 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. 2001, 166:5935.
86. Schiemann B., Gommerman J.L., Vora K., Cachero T.G., Shulga-Morskaya S., Dobles M., Frew E., Scott M.L. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 2001, 293:2111.
87. Schmitt T.M., de Pooter R.F., Gronski M.A., Cho S.K., Ohashi P.S., Zuniga-Pflucker J.C. Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro. Nat. Immunol. 2004, 5:410.
88. Schneider P., MacKay F., Steiner V., Hofmann K., Bodmer J.L., Holler N., Ambrose C., Lawton P., Bixler S., Acha-Orbea H., Valmori D., Romero P., Werner-Favre C., Zubler R.H., Browning J.L., Tschopp J. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J. Exp. Med. 1999, 189:1747.
89. Shimizu T., Mundt C., Licence S., Melchers F., Martensson I.L. VpreB1/VpreB2/lambda 5 triple-deficient mice show impaired B cell development but functional allelic exclusion of the IgH locus. J. Immunol. 2002, 168:6286.
90. Shlomchik M., Mascelli M., Shan H., Radic M.Z., Pisetsky D., Marshak-Rothstein A., Weigert M. Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation. J. Exp. Med. 1990, 171:265.
91. Silveira P.A., Dombrowsky J., Johnson E., Chapman H.D., Nemazee D., Serreze D.V. B cell selection defects underlie the development of diabetogenic APCs in nonobese diabetic mice. J. Immunol. 2004, 172:5086.
92. Snapper C.M., Yamada H., Smoot D., Sneed R., Lees A., Mond J.J. Comparative in vitro analysis of proliferation, Ig secretion, and Ig class switching by murine marginal zone and follicular B cells. J. Immunol. 1993, 150:2737.
93. Surh C.D., Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 1994, 372:100.
94. ten Boekel E., Melchers F., Rolink A. The status of Ig loci rearrangements in single cells from different stages of B cell development. Int. Immunol. 1995, 7:1013.
95. Thompson J.S., Bixler S.A., Qian F., Vora K., Scott M.L., Cachero T.G., Hession C., Schneider P., Sizing I.D., Mullen C., Strauch K., Zafari M., Benjamin C.D., Tschopp J., Browning J.L., Ambrose C. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 2001, 293:2108.
96. Tiegs S.L., Russell D.M., Nemazee D. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 1993, 177:1009.
97. Tokoyoda K., Egawa T., Sugiyama T., Choi B.I., Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 2004, 20:707.
98. + memory B cell development. J. Exp. Med. 2006, 203:393.
99. Tuscano J.M., Harris G.S., Tedder T.F. B lymphocytes contribute to autoimmune disease pathogenesis: current trends and clinical implications. Autoimmun. Rev. 2003, 2:101.
100. Tze L.E., Baness E.A., Hippen K.L., Behrens T.W. Ig light chain receptor editing in anergic B cells. J. Immunol. 2000, 165:6796.
101. Tze L.E., Hippen K.L., Behrens T.W. Late immature B cells (IgMhighIgDneg) undergo a light chain receptor editing response to soluble self-antigen. J. Immunol. 2003, 171:678.
102. Tze L.E., Schram B.R., Lam K.P., Hogquist K.A., Hippen K.L., Liu J., Shinton S.A., Otipoby K.L., Rodine P.R., Vegoe A.L., Kraus M., Hardy R.R., Schlissel M.S., Rajewsky K., Behrens T.W. Basal immunoglobulin signaling actively maintains developmental stage in immature B cells. PLoS Biol. 2005, 3:e82.
103. Ueda Y., Kondo M., Kelsoe G. Inflammation and the reciprocal production of granulocytes and lymphocytes in bone marrow. J. Exp. Med. 2005, 201:1771.
104. Ueda Y., Liao D., Yang K., Patel A., Kelsoe G. T-independent activation-induced cytidine deaminase expression, class-switch recombination, and antibody production by immature/transitional 1 B cells. J. Immunol. 2007, 178:3593.
105. Wardemann H., Yurasov S., Schaefer A., Young J.W., Meffre E., Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors. Science 2003, 301:1374.
106. Wardemann H., Hammersen J., Nussenzweig M.C. Human autoantibody silencing by immunoglobulin light chains. J. Exp. Med. 2004, 200:191.
107. Yu X., McGraw P.A., House F.S., Crowe J.E. An optimized electrofusion-based protocol for generating virus-specific human monoclonal antibodies. J. Immunol. Methods 2008, 336:142.