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

doi:10.1084/jem.180.1.111

This Article

Full Text (PDF)

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JEM

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Murakami, M.

Articles by Honjo, T.

Search for Related Content

PubMed

PubMed Citation

Articles by Murakami, M.

Articles by Honjo, T.

Pubmed/NCBI databases

Medline Plus Health Information
Autoimmune Diseases

Social Bookmarking

What's this?

ARTICLES

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

M Murakami, T Tsubata, R Shinkura, S Nisitani, M Okamoto, H Yoshioka, T Usui, S Miyawaki and T Honjo
Department of Medical Chemistry, Faculty of Medicine, Kyoto University, Japan.

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.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Kataoka, K., Fujihashi, K., Sekine, S., Fukuiwa, T., Kobayashi, R., Suzuki, H., Nagata, H., Takatsu, K., Shizukuishi, S., McGhee, J. R., Fujihashi, K. (2007). Nasal Cholera Toxin Elicits IL-5 and IL-5 Receptor {alpha}-Chain Expressing B-1a B Cells for Innate Mucosal IgA Antibody Responses. J. Immunol. 178: 6058-6065 [Abstract] [Full Text]
Rui, L., Healy, J. I., Blasioli, J., Goodnow, C. C. (2006). ERK Signaling Is a Molecular Switch Integrating Opposing Inputs from B Cell Receptor and T Cell Cytokines to Control TLR4-Driven Plasma Cell Differentiation. J. Immunol. 177: 5337-5346 [Abstract] [Full Text]
Savitsky, D., Calame, K. (2006). B-1 B lymphocytes require Blimp-1 for immunoglobulin secretion. J. Exp. Med. 203: 2305-2314 [Abstract] [Full Text]
Ferry, H., Crockford, T. L., Leung, J. C. H., Cornall, R. J. (2006). Signals from a self-antigen induce positive selection in early B cell ontogeny but are tolerogenic in adults.. J. Immunol. 176: 7402-7411 [Abstract] [Full Text]
Wijburg, O. L.C., Uren, T. K., Simpfendorfer, K., Johansen, F.-E., Brandtzaeg, P., Strugnell, R. A. (2006). Innate secretory antibodies protect against natural Salmonella typhimurium infection. J. Exp. Med. 203: 21-26 [Abstract] [Full Text]
Askenase, P. W., Itakura, A., Leite-de-Moraes, M. C., Lisbonne, M., Roongapinun, S., Goldstein, D. R., Szczepanik, M. (2005). TLR-Dependent IL-4 Production by Invariant V{alpha}14+J{alpha}18+ NKT Cells to Initiate Contact Sensitivity In Vivo. J. Immunol. 175: 6390-6401 [Abstract] [Full Text]
Kikuchi, S., Amano, H., Amano, E., Fossati-Jimack, L., Santiago-Raber, M.-L., Moll, T., Ida, A., Kotzin, B. L., Izui, S. (2005). Identification of 2 major loci linked to autoimmune hemolytic anemia in NZB mice. Blood 106: 1323-1329 [Abstract] [Full Text]
Mori, S., Sakamoto, A., Yamashita, K., Fujimura, L., Arima, M., Hatano, M., Miyazaki, M., Tokuhisa, T. (2004). Effect of c-fos overexpression on development and proliferation of peritoneal B cells. Int Immunol 16: 1477-1486 [Abstract] [Full Text]
Yurino, H., Ishikawa, S., Sato, T., Akadegawa, K., Ito, T., Ueha, S., Inadera, H., Matsushima, K. (2004). Endocrine Disruptors (Environmental Estrogens) Enhance Autoantibody Production by B1 Cells. Toxicol Sci 81: 139-147 [Abstract] [Full Text]
Lauder, A. J., Jolin, H. E., Smith, P., van den Berg, J. G., Jones, A., Wisden, W., Smith, K. G. C., Dasvarma, A., Fallon, P. G., McKenzie, A. N. J. (2004). Lymphomagenesis, Hydronephrosis, and Autoantibodies Result from Dysregulation of IL-9 and Are Differentially Dependent on Th2 Cytokines. J. Immunol. 173: 113-122 [Abstract] [Full Text]
Cole, M. F., Evans, M. K., Kirchherr, J. L., Sheridan, M. J., Bowden, G. H. W. (2004). Study of Humoral Immunity to Commensal Oral Bacteria in Human Infants Demonstrates the Presence of Secretory Immunoglobulin A Antibodies Reactive with Actinomyces naeslundii Genospecies 1 and 2 Ribotypes. CVI 11: 473-482 [Abstract] [Full Text]
Ito, T., Ishikawa, S., Sato, T., Akadegawa, K., Yurino, H., Kitabatake, M., Hontsu, S., Ezaki, T., Kimura, H., Matsushima, K. (2004). Defective B1 Cell Homing to the Peritoneal Cavity and Preferential Recruitment of B1 Cells in the Target Organs in a Murine Model for Systemic Lupus Erythematosus. J. Immunol. 172: 3628-3634 [Abstract] [Full Text]
Shen, C.-R., Youssef, A.-R., Devine, A., Bowie, L., Hall, A. M., Wraith, D. C., Elson, C. J., Barker, R. N. (2003). Peptides containing a dominant T-cell epitope from red cell band 3 have in vivo immunomodulatory properties in NZB mice with autoimmune hemolytic anemia. Blood 102: 3800-3806 [Abstract] [Full Text]
Ferry, H., Jones, M., Vaux, D. J., Roberts, I. S.D., Cornall, R. J. (2003). The Cellular Location of Self-antigen Determines the Positive and Negative Selection of Autoreactive B Cells. J. Exp. Med. 198: 1415-1425 [Abstract] [Full Text]
Ishikawa, S., Sato, T., Abe, M., Nagai, S., Onai, N., Yoneyama, H., Zhang, Y.-y., Suzuki, T., Hashimoto, S.-i., Shirai, T., Lipp, M., Matsushima, K. (2001). Aberrant High Expression of B Lymphocyte Chemokine (BLC/CXCL13) by C11b+CD11c+ Dendritic Cells in Murine Lupus and Preferential Chemotaxis of B1 Cells Towards BLC. J. Exp. Med. 193: 1393-1402 [Abstract] [Full Text]
BOS, N A, JIANG, H-Q, CEBRA, J J (2001). T cell control of the gut IgA response against commensal bacteria. Gut 48: 762-764 [Full Text]
Koide, N., Sugiyama, T., Kato, Y., Chakravortty, D., Mya Mya Mu, , Yoshida, T., Hamano, T., Yokochi, T. (2001). Mouse B1 cell line responds to lipopolysaccharide via membrane-bound CD14. Innate Immunity 7: 39-43 [Abstract]
Watanabe, N., Ikuta, K., Fagarasan, S., Yazumi, S., Chiba, T., Honjo, T. (2000). Migration and Differentiation of Autoreactive B-1 Cells Induced by Activated {gamma}/{delta} T Cells in Antierythrocyte Immunoglobulin Transgenic Mice. J. Exp. Med. 192: 1577-1586 [Abstract] [Full Text]
Ohdan, H., Swenson, K. G., Kruger Gray, H. S., Yang, Y.-G., Xu, Y., Thall, A. D., Sykes, M. (2000). Mac-1-Negative B-1b Phenotype of Natural Antibody-Producing Cells, Including Those Responding to Gal{alpha}1,3Gal Epitopes in {alpha}1,3-Galactosyltransferase-Deficient Mice. J. Immunol. 165: 5518-5529 [Abstract] [Full Text]
Hiroi, T., Yanagita, M., Ohta, N., Sakaue, G., Kiyono, H. (2000). IL-15 and IL-15 Receptor Selectively Regulate Differentiation of Common Mucosal Immune System-Independent B-1 Cells for IgA Responses. J. Immunol. 165: 4329-4337 [Abstract] [Full Text]
Chen, M., Aosai, F., Mun, H.-S., Norose, K., Hata, H., Yano, A. (2000). Anti-HSP70 Autoantibody Formation by B-1 Cells in Toxoplasma gondii-Infected Mice. Infect. Immun. 68: 4893-4899 [Abstract] [Full Text]
Kamata, T., Nogaki, F., Fagarasan, S., Sakiyama, T., Kobayashi, I., Miyawaki, S., Ikuta, K., Muso, E., Yoshida, H., Sasayama, S., Honjo, T. (2000). Increased Frequency of Surface IgA-Positive Plasma Cells in the Intestinal Lamina Propria and Decreased IgA Excretion in Hyper IgA (HIGA) Mice, a Murine Model of IgA Nephropathy with Hyperserum IgA. J. Immunol. 165: 1387-1394 [Abstract] [Full Text]
Satoh, M., Weintraub, J. P., Yoshida, H., Shaheen, V. M., Richards, H. B., Shaw, M., Reeves, W. H. (2000). Fas and Fas Ligand Mutations Inhibit Autoantibody Production in Pristane-Induced Lupus. J. Immunol. 165: 1036-1043 [Abstract] [Full Text]
Saitoh–Inagawa, W., Hiroi, T., Yanagita, M., Iijima, H., Uchio, E., Ohno, S., Aoki, K., Kiyono, H. (2000). Unique Characteristics of Lacrimal Glands as a Part of Mucosal Immune Network: High Frequency of IgA-Committed B-1 Cells and NK1.1+ {alpha}{beta} T Cells. IOVS 41: 138-144 [Abstract] [Full Text]
Kuwata, N., Igarashi, H., Ohmura, T., Aizawa, S., 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 [Abstract] [Full Text]
Fossati-Jimack, L., Reininger, L., Chicheportiche, Y., Clynes, R., Ravetch, J. V., Honjo, T., Izui, S. (1999). High Pathogenic Potential of Low-Affinity Autoantibodies in Experimental Autoimmune Hemolytic Anemia. J. Exp. Med. 190: 1689-1696 [Abstract] [Full Text]
Watanabe, N., Nisitani, S., Ikuta, K., Suzuki, M., Chiba, T., Honjo, T. (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: 461-470 [Abstract] [Full Text]
Sakiyama, T., Ikuta, K., Nisitani, S., Takatsu, K., Honjo, T. (1999). Requirement of IL-5 for induction of autoimmune hemolytic anemia in anti-red blood cell autoantibody transgenic mice. Int Immunol 11: 995-1000 [Abstract] [Full Text]
Hiroi, T., Yanagita, M., Iijima, H., Iwatani, K., Yoshida, T., Takatsu, K., Kiyono, H. (1999). Deficiency of IL-5 Receptor {alpha}-Chain Selectively Influences the Development of the Common Mucosal Immune System Independent IgA-Producing B-1 Cell in Mucosa-Associated Tissues. J. Immunol. 162: 821-828 [Abstract] [Full Text]
Itoh, M., Ishihara, K., Hiroi, T., Ok Lee, B., Maeda, H., Iijima, H., Yanagita, M., Kiyono, H., Hirano, T. (1998). Deletion of Bone Marrow Stromal Cell Antigen-1 (CD157) Gene Impaired Systemic Thymus Independent-2 Antigen-Induced IgG3 and Mucosal TD Antigen-Elicited IgA Responses. J. Immunol. 161: 3974-3983 [Abstract] [Full Text]
Gardby, E., Lane, P., Lycke, N. Y. (1998). Requirements for B7-CD28 Costimulation in Mucosal IgA Responses: Paradoxes Observed in CTLA4-H{gamma}1 Transgenic Mice. J. Immunol. 161: 49-59 [Abstract] [Full Text]
Boes, M., Esau, C., Fischer, M. B., Schmidt, T., Carroll, M., Chen, J. (1998). Enhanced B-1 Cell Development, But Impaired IgG Antibody Responses in Mice Deficient in Secreted IgM. J. Immunol. 160: 4776-4787 [Abstract] [Full Text]
Mizoguchi, A., Mizoguchi, E., Smith, R. N., Preffer, F. I., Bhan, A. K. (1997). Suppressive Role of B Cells in Chronic Colitis of �T Cell Receptor alpha �Mutant Mice. J. Exp. Med. 186: 1749-1756 [Abstract] [Full Text]
Tarakhovsky, A. (1997). Bar Mitzvah for B-1 Cells: How Will They Grow Up?. J. Exp. Med. 185: 981-984 [Full Text]
Murakami, M., Nakajima, K., Yamazaki, K.-i., Muraguchi, T., Serikawa, T., Honjo, T. (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 [Abstract] [Full Text]