Signals from a self-antigen induce positive selection in early B cell ontogeny but are tolerogenic in adults

Journal of Immunology

Volumn 176, Issue 12, 2006, Pages 7402-7411

  Ferry, Helen ^a   Crockford, Tanya L ^a   Leung, Janson C H ^a   Cornall, Richard J ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Henry Wellcome Building of Molecular Physiology ^*  (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; AUTOANTIGEN; B LYMPHOCYTE RECEPTOR; COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; LYSOZYME;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL SELECTION; CELL SUBPOPULATION; CONTROLLED STUDY; EGG; EXPOSURE; FETUS; HEN; IMMUNOLOGICAL TOLERANCE; MOUSE; NEWBORN; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENE;

EID: 33744905326     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.12.7402     Document Type: Article

References (65)

1. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300.
2. Ansel, K. M., R. B. Harris, and J. G. Cyster. 2002. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 16: 67-76.
3. Arnold, L. W., C. A. Pennell, S. K. McCray, and S. H. Clarke. 1994. Development of B-1 cells: segregation of phosphatidyl choline-specific B cells to the B-1 population occurs after immunoglobulin gene expression. J. Exp. Med 179: 1585-1595.
4. Hardy, R. R., C. E. Carmack, S. A. Shinton, R. J. Riblet, and K. Hayakawa. 1989. A single VH gene is utilized predominantly in anti-BrMRBC hybridomas derived from purified Ly-1 B cells: definition of the VH11 family. J. Immunol. 142: 3643-3651.
5. H12 B cell differentiation toward a single B-1 cell specificity. J. Exp. Med. 190: 903-914.
6. Lesley, R., Y. Xu, S. L. Kalled, D. M. Hess, S. R. Schwab, H. B. Shu, and J. G. Cyster. 2004. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20: 441-453.
7. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377.
8. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629.
9. Martin, F., and J. F. Kearney. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2: 323-335.
10. Cancro, M. P., and J. F. Kearney. 2004. B cell positive selection: road map to the primary repertoire? J. Immunol. 173: 15-19.
11. Wang, H., and S. H. Clarke. 2004. Regulation of B-cell development by antibody specificity. Curr. Opin. Immunol. 16: 246-250.
12. Wen, L., J. Brill-Dashoff, S. A. Shinton, M. Asano, R. R. Hardy, and K. Hayakawa. 2005. Evidence of marginal-zone B cell-positive selection in spleen. Immunity 23: 297-308.
13. Chan, V. W., F. Meng, P. Soriano, A. L. DeFranco, and C. A. Lowell. 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.
14. Nishizumi, H., I. Taniuchi, Y. Yamanashi, D. Kitamura, D. Ilic, S. Mori, T. Watanabe, and T. Yamamoto. 1995. Impaired proliferation of peripheral B cells and indication of autoimmune disease in Lyn-deficient mice. Immunity 3: 549-560.
15. Hibbs, M. L., D. M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S. A. Stacker, and A. R. Dunn. 1995. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83: 301-311.
16. Sato, S., A. S. Miller, M. Inaoki, C. B. Bock, P. J. Jansen, M. L. Tang, and T. F. Tedder. 1996. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5: 551-562.
17. O'Keefe, T. L., G. T. Williams, S. L. Davies, and M. S. Neuberger. 1996. Hyperresponsive B cells in CD22-deficient mice. Science 274: 798-801.
18. Saitoh, Y., G. Kelsoe, C. Bona, and A. Kaushik. 1995. Skewed VH and Vκ gene family expression and pairing occurs among B lymphocytes in autoimmune motheaten mice. Autoimmunity 21: 185-193.
19. Sato, S., N. Ono, D. A. Steeber, D. S. Pisetsky, and T. F. Tedder. 1996. CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J. Immunol. 157: 4371-4378.
20. Cyster, J. G., and C. C. Goodnow. 1995. Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 2: 13-24.
21. Heltemes, L. M., and T. Manser. 2002. Level of B cell antigen receptor surface expression influences both positive and negative selection of B cells during primary development. J. Immunol. 169: 1283-1292.
22. Watanabe, N., S. Nisitani, K. Ikuta, M. Suzuki, T. Chiba, and T. Honjo. 1999. Expression levels of B cell surface immunoglobulin regulate efficiency of allelic exclusion and size of autoreactive B-1 cell compartment. J. Exp. Med. 190: 461-469.
23. Sanchez, P., A. M. Crain-Denoyelle, P. Daras, M. C. Gendron, and C. Kanellopoulos-Langevin. 2000. The level of expression of μ heavy chain modifies the composition of peripheral B cell subpopulations. Int. Immunol. 12: 1459-1466.
24. Lam, K. P., and K. Rajewsky. 1999. B cell antigen receptor specificity and surface density together determine B-1 versus B-2 cell development. J. Exp. Med. 190: 471-477.
25. Casola, S., K. L. Otipoby, M. Alimzhanov, S. Humme, N. Uyttersprot, J. L. Kutok, M. C. Carroll, and K. Rajewsky. 2004. B cell receptor signal strength determines B cell fate. Nat. Immunol. 5: 317-327.
26. Goodnow, C. C., J. G. Cyster, S. B. Hartley, S. E. Bell, M. P. Cooke, J. I. Healy, S. Akkaraju, I. C. Rathmell, S. L. Pogue, and K. P. Shokat. 1995. Self-tolerance checkpoints in B lymphocyte development. Adv. Immunol. 59: 279-368.
27. Hartley, S. B., J. Crosbie, R. Brink, A. B. Kantor, A. Basten, and C. C. Goodnow. 1991. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353: 765-769.
28. Hartley, S. B., M. P. Cooke, D. A. Fulcher, A. W. Harris, S. Cory, A. Basten, and C. C. Goodnow. 1993. Elimination of self-reactive B lymphocytes proceeds in two stages: arrested development and cell death. Cell 72: 325-335.
29. Goodnow, C. C., J. Crosbie, H. Jorgensen, R. A. Brink, and A. Basten. 1989. Induction of self-tolerance in mature peripheral B lymphocytes. Nature 342: 385-391.
30. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, I. S. Wotherspoon, R. H. Loblay, K. Raphael, et al. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334: 676-682.
31. Cooke, M. P., A. W. Heath, K. M. Shokat, Y. Zeng, F. D. Finkelman, P. S. Linsley, M. Howard, and C. C. Goodnow. 1994. Immunoglobulin signal transduction guides the specificity of B cell-T cell interactions and is blocked in tolerant self-reactive B cells. J. Exp. Med. 179: 425-438.
32. Healy, J. I., R. E. Dolmetsch, R. S. Lewis, and C. C. Goodnow. 1998. Quantitative and qualitative control of antigen receptor signalling in tolerant B lymphocytes. Novartis Found Symp. 215: 137-144.
33. Cyster, J. G., and C. C. Goodnow. 1997. Tuning antigen receptor signaling by CD22: integrating cues from antigens and the microenvironment. Immunity 6: 509-517.
34. Cornall, R. J., J. G. Cyster, M. L. Hibbs, A. R. Dunn, K. L. Otipoby, E. A. Clark, and C. C. Goodnow. 1998. Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8: 497-508.
35. Ferry, H., M. Jones, D. J. Vaux, I. S. Roberts, and R. J. Cornall. 2003. The cellular location of self-antigen determines the positive and negative selection of autoreactive B cells. J. Exp. Med. 198: 1415-1425.
36. Adelstein, S., H. Pritchard-Briscoe, T. A. Anderson, J. Crosbie, G. Gammon, R. H. Loblay, A. Basten, and C. C. Goodnow. 1991. Induction of self-tolerance in T cells but not B cells of transgenic mice expressing little self antigen. Science 251: 1223-1225.
37. Hayakawa, K., R. R. Hardy, and L. A. Herzenberg. 1985. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161: 1554-1568.
38. Kantor, A. B., A. M. Stall, S. Adams, and L. A. Herzenberg. 1992. Differential development of progenitor activity for three B-cell lineages. Proc. Natl. Acad. Sci. USA 89: 3320-3324.
39. H sequences from B-1a, B-1b, and conventional B cells. J. Immunol. 158: 1175-1186.
40. Benedict, C. L., and J. F. Kearney. 1999. Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 10: 607-617.
41. Kawahara, T., H. Ohdan, G. Zhao, Y. G. Yang, and M. Sykes. 2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171: 5406-5414.
42. Youinou, P., L. Mackenzie, P. Katsikis, G. Merdrignac, D. A. Isenberg, N. Tuaillon, A. Lamour, P. Le Goff, J. Jouquan, A. Drogou, et al. 1990. The relationship between CD5-expressing B lymphocytes and serologic abnormalities in rheumatoid arthritis patients and their relatives. Arthritis Rheum. 33: 339-348.
43. Dauphinee, M., Z. Tovar, and N. Talal. 1988. B cells expressing CD5 are increased in Sjogren's syndrome. Arthritis Rheum. 31: 642-647.
44. + B cells and natural IgM-secreting cells: reconstitution potential of adult bone marrow, spleen and peritoneal cells. Eur. J. Immunol. 22: 1243-1251.
45. Herzenberg, L. A., A. M. Stall, P. A. Lalor, C. Sidman, W. A. Moore, and D. R. Parks. 1986. The Ly-1 B cell lineage. Immunol. Rev. 93: 81-102.
46. + B cells. Eur. J. Immunol. 26: 2537-2540.
47. Iacomini, J., and T. Imanishi-Kari. 1992. The effect of an immunoglobulin μ transgene on B cell maturation. Eur. J. Immunol. 22: 745-751.
48. + B cells both in vivo and in vitro. J. Immunol. 164: 4586-4593.
49. Hayakawa, K., M. Asano, S. A. Shinton, M. Gui, L. J. Wen, J. Dashoff, and R. R. Hardy. 2003. Positive selection of anti-thy-1 autoreactive B-1 cells and natural serum autoantibody production independent from bone marrow B cell development. J. Exp. Med. 197: 87-99.
50. Okamoto, M., M. Murakami, A. Shimizu, S. Ozaki, T. Tsubata, S. Kumagai, and T. Honjo. 1992. A transgenic model of autoimmune hemolytic anemia. J. Exp. Med. 175: 71-79.
51. Cambier, J. C., J. R. Kettman, E. S. Vitetta, and J. W. Uhr. 1976. Differential susceptibility of neonatal and adult murine spleen cells to in vitro induction of B-cell tolerance. J. Exp. Med. 144: 293-297.
52. Cyster, J. G., J. I. Healy, K. Kishihara, T. W. Mak, M. L. Thomas, and C. C. Goodnow. 1996. Regulation of B-lymphocyte negative and positive selection by tyrosine phosphatase CD45. Nature 381: 325-328.
53. Kenny, J. J., L. J. Rezanka, A. Lustig, R. T. Fischer, J. Yoder, S. Marshall, and D. L. Longo. 2000. Autoreactive B cells escape clonal deletion by expressing multiple antigen receptors. J. Immunol. 164: 4111-4119.
54. Hartley, S. B., and C. C. Goodnow. 1994. Censoring of self-reactive B cells with a range of receptor affinities in transgenic mice expressing heavy chains for a lysozyme-specific antibody. Int. Immunol. 6: 1417-1425.
55. Gaudin, E., Y. Hao, M. M. Rosado, R. Chaby, R. Girard, and A. A. Freitas. 2004. Positive selection of B cells expressing low densities of self-reactive BCRs. J. Exp. Med. 199: 843-853.
56. Akkaraju, S., K. Canaan, and C. C. Goodnow. 1997. Self-reactive B cells are not eliminated or inactivated by autoantigen expressed on thyroid epithelial cells. J. Exp. Med. 186: 2005-2012.
57. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
58. Murakami, M., T. Tsubata, R. Shinkura, S. Nisitani, M. Okamoto, H. Yoshioka, T. Usui, S. Miyawaki, and T. Honjo. 1994. Oral administration of lipopolysaccharides activates B-1 cells in the peritoneal cavity and lamina propria of the gut and induces autoimmune symptoms in an autoantibody transgenic mouse. J. Exp. Med. 180: 111-121.
59. Murakami, M., K. Nakajima, K. Yamazaki, T. Muraguchi, T. Serikawa, and T. Honjo. 1997. Effects of breeding environments on generation and activation of autoreactive B-1 cells in anti-red blood cell autoantibody transgenic mice. J. Exp. Med. 185: 791-794.
60. Feeney, A. J. 1990. Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences. J. Exp. Med. 172: 1377-1390.
61. Feeney, A. J. 1991. Predominance of the prototypic T15 anti-phosphorylcholine junctional sequence in neonatal pre-B cells. J. Immunol. 147: 4343-4350.
62. Boes, M., T. Schmidt, K. Linkemann, B. C. Beaudette, A. Marshak-Rothstein, and J. Chen. 2000. Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc. Natl. Acad. Sci. USA 97: 1184-1189.
63. Ehrenstein, M. R., H. T. Cook, and M. S. Neuberger. 2000. Deficiency in serum immunoglobulin (Ig)M predisposes to development of IgG autoantibodies. J. Exp. Med. 191: 1253-1258.
64. Boes, M., A. P. Prodeus, T. Schmidt, M. C. Carroll, and J. Chen. 1998. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J. Exp. Med. 188: 2381-2386.
65. Briles, D. E., M. Nahm, K. Schroer, J. Davie, P. Baker, J. Kearney, and R. Barletta. 1981. Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J. Exp. Med. 153: 694-705.