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. 1994 Jul 1;180(1):111–121. doi: 10.1084/jem.180.1.111

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

PMCID: PMC2191544  PMID: 8006578

Abstract

About a half of the antierythrocyte autoantibody transgenic (autoAb Tg) mice, in which almost all B cells are detected in the spleen, lymph nodes, and Peyer's patches, but not in the peritoneal cavity, suffer from autoimmune hemolytic anemia. The occurrence of this disease is strongly linked to production of autoAb by activated peritoneal B-1 cells in the Tg mice. In this study, we have shown that oral administration of lipopolysaccharides (LPS) activated B-1 cells in the lamina propria of the gut as well as the peritoneal cavity in the healthy Tg mice and induced the autoimmune symptoms in all the Tg mice. The activation of peritoneal and lamina propria B-1 cells by enteric LPS is found not only in the anti-RBC autoAb Tg mice and normal mice but also in the aly mice which congenitally lack lymph nodes and Peyer's patches. These results suggest that B-1 cells in the two locations may form a common pool independent of Peyer's patches and lymph nodes, and can be activated by enteric thymus-independent antigens or polyclonal activators such as LPS. The induction of autoimmune hemolytic anemia in the Tg mice by enteric LPS through the activation of B-1 cells in the lamina propria of gut and in the peritoneal cavity suggests that B-1 cells and bacterial infection may play a pathogenic role in the onset of autoimmune diseases.

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Selected References

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  1. Bandeira A., Itohara S., Bonneville M., Burlen-Defranoux O., Mota-Santos T., Coutinho A., Tonegawa S. Extrathymic origin of intestinal intraepithelial lymphocytes bearing T-cell antigen receptor gamma delta. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):43–47. doi: 10.1073/pnas.88.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cong Y. Z., Rabin E., Wortis H. H. Treatment of murine CD5- B cells with anti-Ig, but not LPS, induces surface CD5: two B-cell activation pathways. Int Immunol. 1991 May;3(5):467–476. doi: 10.1093/intimm/3.5.467. [DOI] [PubMed] [Google Scholar]
  3. Davies M. D., Parrott D. M. Preparation and purification of lymphocytes from the epithelium and lamina propria of murine small intestine. Gut. 1981 Jun;22(6):481–488. doi: 10.1136/gut.22.6.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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 Jan 24;349(6307):331–334. doi: 10.1038/349331a0. [DOI] [PubMed] [Google Scholar]
  5. 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., Raphael K. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature. 1988 Aug 25;334(6184):676–682. doi: 10.1038/334676a0. [DOI] [PubMed] [Google Scholar]
  6. Goverman J., Woods A., Larson L., Weiner L. P., Hood L., Zaller D. M. Transgenic mice that express a myelin basic protein-specific T cell receptor develop spontaneous autoimmunity. Cell. 1993 Feb 26;72(4):551–560. doi: 10.1016/0092-8674(93)90074-z. [DOI] [PubMed] [Google Scholar]
  7. Gregersen P. K., Silver J., Winchester R. J. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987 Nov;30(11):1205–1213. doi: 10.1002/art.1780301102. [DOI] [PubMed] [Google Scholar]
  8. Hardy R., Hayakawa K. Generation of Ly-1 B cells from developmentally distinct precursors. Enrichment by stromal-cell culture or cell sorting. Ann N Y Acad Sci. 1992 May 4;651:99–111. doi: 10.1111/j.1749-6632.1992.tb24600.x. [DOI] [PubMed] [Google Scholar]
  9. 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 Oct 24;353(6346):765–769. doi: 10.1038/353765a0. [DOI] [PubMed] [Google Scholar]
  10. Hayakawa K., Hardy R. R., Parks D. R., Herzenberg L. A. The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice. J Exp Med. 1983 Jan 1;157(1):202–218. doi: 10.1084/jem.157.1.202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Herman A., Kappler J. W., Marrack P., Pullen A. M. Superantigens: mechanism of T-cell stimulation and role in immune responses. Annu Rev Immunol. 1991;9:745–772. doi: 10.1146/annurev.iy.09.040191.003525. [DOI] [PubMed] [Google Scholar]
  12. Herzenberg L. A., Stall A. M., Lalor P. A., Sidman C., Moore W. A., Parks D. R., Herzenberg L. A. The Ly-1 B cell lineage. Immunol Rev. 1986 Oct;93:81–102. doi: 10.1111/j.1600-065x.1986.tb01503.x. [DOI] [PubMed] [Google Scholar]
  13. Honjo T. Immunoglobulin genes. Annu Rev Immunol. 1983;1:499–528. doi: 10.1146/annurev.iy.01.040183.002435. [DOI] [PubMed] [Google Scholar]
  14. Hsu S. M., Raine L., Fanger H. A comparative study of the peroxidase-antiperoxidase method and an avidin-biotin complex method for studying polypeptide hormones with radioimmunoassay antibodies. Am J Clin Pathol. 1981 May;75(5):734–738. doi: 10.1093/ajcp/75.5.734. [DOI] [PubMed] [Google Scholar]
  15. Izui S., Lambert P. H., Fournié G. J., Türler H., Miescher P. A. Features of systemic lupus erythematosus in mice injected with bacterial lipopolysaccharides: identificantion of circulating DNA and renal localization of DNA-anti-DNA complexes. J Exp Med. 1977 May 1;145(5):1115–1130. doi: 10.1084/jem.145.5.1115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kantor A. B., Stall A. M., Adams S., Herzenberg L. A., Herzenberg L. A. Differential development of progenitor activity for three B-cell lineages. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3320–3324. doi: 10.1073/pnas.89.8.3320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kelly J., Whelan C. A., Weir D. G., Feighery C. Removal of endogenous peroxidase activity from cryostat sections for immunoperoxidase visualisation of monoclonal antibodies. J Immunol Methods. 1987 Jan 26;96(1):127–132. doi: 10.1016/0022-1759(87)90376-0. [DOI] [PubMed] [Google Scholar]
  18. Kroese F. G., Butcher E. C., Stall A. M., Lalor P. A., Adams S., Herzenberg L. A. Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int Immunol. 1989;1(1):75–84. doi: 10.1093/intimm/1.1.75. [DOI] [PubMed] [Google Scholar]
  19. Murakami K., Muruyama H., Hosono M., Sinagawa K., Yamada J., Kuribayashi K., Masuda T. Germ-free condition and the susceptibility of BALB/c mice to post-thymectomy autoimmune gastritis. Autoimmunity. 1992;12(1):69–70. doi: 10.3109/08916939209146132. [DOI] [PubMed] [Google Scholar]
  20. Nemazee D. A., Bürki K. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature. 1989 Feb 9;337(6207):562–566. doi: 10.1038/337562a0. [DOI] [PubMed] [Google Scholar]
  21. Oldstone M. B. Molecular mimicry and autoimmune disease. Cell. 1987 Sep 11;50(6):819–820. doi: 10.1016/0092-8674(87)90507-1. [DOI] [PubMed] [Google Scholar]
  22. Scher I. CBA/N immune defective mice; evidence for the failure of a B cell subpopulation to be expressed. Immunol Rev. 1982;64:117–136. doi: 10.1111/j.1600-065x.1982.tb00421.x. [DOI] [PubMed] [Google Scholar]
  23. Smith H. R., Steinberg A. D. Autoimmunity--a perspective. Annu Rev Immunol. 1983;1:175–210. doi: 10.1146/annurev.iy.01.040183.001135. [DOI] [PubMed] [Google Scholar]
  24. Solvason N., Lehuen A., Kearney J. F. An embryonic source of Ly1 but not conventional B cells. Int Immunol. 1991 Jun;3(6):543–550. doi: 10.1093/intimm/3.6.543. [DOI] [PubMed] [Google Scholar]
  25. Stall A. M., Adams S., Herzenberg L. A., Kantor A. B. Characteristics and development of the murine B-1b (Ly-1 B sister) cell population. Ann N Y Acad Sci. 1992 May 4;651:33–43. doi: 10.1111/j.1749-6632.1992.tb24591.x. [DOI] [PubMed] [Google Scholar]
  26. Todd J. A., Bell J. I., McDevitt H. O. HLA-DQ beta gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature. 1987 Oct 15;329(6140):599–604. doi: 10.1038/329599a0. [DOI] [PubMed] [Google Scholar]
  27. Van der Heijden P. J., Stok W. Improved procedure for the isolation of functionally active lymphoid cells from the murine intestine. J Immunol Methods. 1987 Nov 5;103(2):161–167. doi: 10.1016/0022-1759(87)90285-7. [DOI] [PubMed] [Google Scholar]

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