Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
American Association for Cancer Research

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 3 December 1999:
Vol. 286. no. 5446, pp. 1965 - 1968
DOI: 10.1126/science.286.5446.1965

Reports

Organogenic Role of B Lymphocytes in Mucosal Immunity

Tatyana V. Golovkina, 1 Mark Shlomchik, 23 Lynn Hannum, 2 Alexander Chervonsky 1*

Follicle-associated epithelium (FAE) in the intestinal Peyer's patches contains M cells that deliver pathogens to organized lymphoid tissue. Development of Peyer's patches, FAE, and M cells was found to be impaired in mice that had no B cells. Transgenic expression of membrane-bound immunoglobulin M restored B cells and FAE development. The lack of M cells abrogated infection with a milk-borne retrovirus. Thus, in addition to secretion of antibodies and presentation of antigens, B cells are important for organogenesis of the mucosal immune barriers.

1 Jackson Laboratory, 600 Main Street, Bar Harbor, ME 04609, USA.
2 Section of Immunobiology,
3 Department of Laboratory Medicine, Yale University School of Medicine, New Haven, CT 06510, USA.
*   To whom correspondence should be addressed. E-mail: avc{at}aretha.jax.org


Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Differentiation of a murine intestinal epithelial cell line (MIE) toward the M cell lineage.
T. Kanaya, K. Miyazawa, I. Takakura, W. Itani, K. Watanabe, S. Ohwada, H. Kitazawa, M. T. Rose, H. R. McConochie, H. Okano, et al. (2008)
Am J Physiol Gastrointest Liver Physiol 295, G273-G284
   Abstract »    Full Text »    PDF »
Villous B Cells of the Small Intestine Are Specialized for Invariant NK T Cell Dependence.
P. Velazquez, B. Wei, M. McPherson, L. M. A. Mendoza, S. L. Nguyen, O. Turovskaya, M. Kronenberg, T. T. Huang, M. Schrage, L. N. Lobato, et al. (2008)
J. Immunol. 180, 4629-4638
   Abstract »    Full Text »    PDF »
Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice.
J.-D. Bouaziz, K. Yanaba, G. M. Venturi, Y. Wang, R. M. Tisch, J. C. Poe, and T. F. Tedder (2007)
PNAS 104, 20878-20883
   Abstract »    Full Text »    PDF »
Interactions between epithelial cells and leukocytes in immunity and tissue homeostasis.
R. Shaykhiev and R. Bals (2007)
J. Leukoc. Biol. 82, 1-15
   Abstract »    Full Text »    PDF »
Critical Role of Dendritic Cells in Mouse Mammary Tumor Virus In Vivo Infection.
M. C. Courreges, D. Burzyn, I. Nepomnaschy, I. Piazzon, and S. R. Ross (2007)
J. Virol. 81, 3769-3777
   Abstract »    Full Text »    PDF »
CC Chemokine Receptor 6 Expression by B Lymphocytes Is Essential for the Development of Isolated Lymphoid Follicles.
K. G. McDonald, J. S. McDonough, C. Wang, T. Kucharzik, I. R. Williams, and R. D. Newberry (2007)
Am. J. Pathol. 170, 1229-1240
   Abstract »    Full Text »    PDF »
Fitness of Cell-Mediated Immunity Independent of Repertoire Diversity.
M. AbuAttieh, M. Rebrovich, P. J. Wettstein, Z. Vuk-Pavlovic, A. H. Limper, J. L. Platt, and M. Cascalho (2007)
J. Immunol. 178, 2950-2960
   Abstract »    Full Text »    PDF »
Host B cells produce IL-10 following TBI and attenuate acute GVHD after allogeneic bone marrow transplantation.
V. Rowe, T. Banovic, K. P. MacDonald, R. Kuns, A. L. Don, E. S. Morris, A. C. Burman, H. M. Bofinger, A. D. Clouston, and G. R. Hill (2006)
Blood 108, 2485-2492
   Abstract »    Full Text »    PDF »
Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine.
P. D. Barnes, M. A. Bergman, J. Mecsas, and R. R. Isberg (2006)
J. Exp. Med. 203, 1591-1601
   Abstract »    Full Text »    PDF »
Sequences within the gag Gene of Mouse Mammary Tumor Virus Needed for Mammary Gland Cell Transformation..
I. Swanson, B. A. Jude, A. R. Zhang, A. Pucker, Z. E. Smith, and T. V. Golovkina (2006)
J. Virol. 80, 3215-3224
   Abstract »    Full Text »    PDF »
Transepithelial Pathogen Uptake into the Small Intestinal Lamina Propria.
A. Vallon-Eberhard, L. Landsman, N. Yogev, B. Verrier, and S. Jung (2006)
J. Immunol. 176, 2465-2469
   Abstract »    Full Text »    PDF »
Molecular and Cellular Basis of the Retrovirus Resistance in I/LnJ Mice.
L. K. Case, A. Purdy, and T. V. Golovkina (2005)
J. Immunol. 175, 7543-7549
   Abstract »    Full Text »    PDF »
Role of Interferon-{gamma} in a Mouse Model of Allergic Conjunctivitis.
M. E. Stern, K. Siemasko, J. Gao, A. Duong, C. Beauregard, V. Calder, and J. Y. Niederkorn (2005)
Invest. Ophthalmol. Vis. Sci. 46, 3239-3246
   Abstract »    Full Text »    PDF »
Mucosal B Cell Deficiency in IgA-/- Mice Abrogates the Development of Allergic Lung Inflammation.
P. M. Arnaboldi, M. J. Behr, and D. W. Metzger (2005)
J. Immunol. 175, 1276-1285
   Abstract »    Full Text »    PDF »
Roles of CD4+ T-Cell-Independent and -Dependent Antibody Responses in the Control of Influenza Virus Infection: Evidence for Noncognate CD4+ T-Cell Activities That Enhance the Therapeutic Activity of Antiviral Antibodies.
K. Mozdzanowska, M. Furchner, D. Zharikova, J. Feng, and W. Gerhard (2005)
J. Virol. 79, 5943-5951
   Abstract »    Full Text »    PDF »
Defects in CD8+ Regulatory T Cells in the Lamina Propria of Patients with Inflammatory Bowel Disease.
J. Brimnes, M. Allez, I. Dotan, L. Shao, A. Nakazawa, and L. Mayer (2005)
J. Immunol. 174, 5814-5822
   Abstract »    Full Text »    PDF »
Isolated Lymphoid Follicles Can Function as Sites for Induction of Mucosal Immune Responses.
R. G. LORENZ and R. D. NEWBERRY (2004)
Ann. N.Y. Acad. Sci. 1029, 44-57
   Abstract »    Full Text »    PDF »
Lymphotoxin and TNF Produced by B Cells Are Dispensable for Maintenance of the Follicle-Associated Epithelium but Are Required for Development of Lymphoid Follicles in the Peyer's Patches.
A. V. Tumanov, D. V. Kuprash, J. A. Mach, S. A. Nedospasov, and A. V. Chervonsky (2004)
J. Immunol. 173, 86-91
   Abstract »    Full Text »    PDF »
Clearance of Citrobacter rodentium Requires B Cells but Not Secretory Immunoglobulin A (IgA) or IgM Antibodies.
C. Maaser, M. P. Housley, M. Iimura, J. R. Smith, B. A. Vallance, B. B. Finlay, J. R. Schreiber, N. M. Varki, M. F. Kagnoff, and L. Eckmann (2004)
Infect. Immun. 72, 3315-3324
   Abstract »    Full Text »    PDF »
Intestinal villous M cells: An antigen entry site in the mucosal epithelium.
M. H. Jang, M.-N. Kweon, K. Iwatani, M. Yamamoto, K. Terahara, C. Sasakawa, T. Suzuki, T. Nochi, Y. Yokota, P. D. Rennert, et al. (2004)
PNAS 101, 6110-6115
   Abstract »    Full Text »    PDF »
Fate of MHC-Matched Corneal Allografts in Th1-Deficient Hosts.
S. L. Hargrave, C. Hay, J. Mellon, E. Mayhew, and J. Y. Niederkorn (2004)
Invest. Ophthalmol. Vis. Sci. 45, 1188-1193
   Abstract »    Full Text »    PDF »
Modulating the intestinal immune system: the role of lymphotoxin and GALT organs.
T W Spahn and T Kucharzik (2004)
Gut 53, 456-465
   Full Text »    PDF »
Role of {gamma}{delta}T Cells in the Inflammatory Response of Experimental Colitis Mice.
T. Tsuchiya, S. Fukuda, H. Hamada, A. Nakamura, Y. Kohama, H. Ishikawa, K. Tsujikawa, and H. Yamamoto (2003)
J. Immunol. 171, 5507-5513
   Abstract »    Full Text »    PDF »
Vimentin-positive Cells in the Epithelium of Rabbit Ileal Villi Represent Cup Cells but not M-cells.
C. Ramirez and A. Gebert (2003)
J. Histochem. Cytochem. 51, 1533-1544
   Abstract »    Full Text »    PDF »
Isolated Lymphoid Follicle Formation Is Inducible and Dependent Upon Lymphotoxin-Sufficient B Lymphocytes, Lymphotoxin {beta} Receptor, and TNF Receptor I Function.
R. G. Lorenz, D. D. Chaplin, K. G. McDonald, J. S. McDonough, and R. D. Newberry (2003)
J. Immunol. 170, 5475-5482
   Abstract »    Full Text »    PDF »
Oral Prion Infection Requires Normal Numbers of Peyer's Patches but Not of Enteric Lymphocytes.
M. Prinz, G. Huber, A. J. S. Macpherson, F. L. Heppner, M. Glatzel, H.-P. Eugster, N. Wagner, and A. Aguzzi (2003)
Am. J. Pathol. 162, 1103-1111
   Abstract »    Full Text »    PDF »
Competition for self ligands restrains homeostatic proliferation of naive CD4 T cells.
C. T. Moses, K. M. Thorstenson, S. C. Jameson, and A. Khoruts (2003)
PNAS 100, 1185-1190
   Abstract »    Full Text »    PDF »
Microbial Colonization Drives Lymphocyte Accumulation and Differentiation in the Follicle-Associated Epithelium of Peyer's Patches.
T. Yamanaka, L. Helgeland, I. N. Farstad, H. Fukushima, T. Midtvedt, and P. Brandtzaeg (2003)
J. Immunol. 170, 816-822
   Abstract »    Full Text »    PDF »
Overexpression of arginase I in enterocytes of transgenic mice elicits a selective arginine deficiency and affects skin, muscle, and lymphoid development.
W. J de Jonge, M. M Hallemeesch, K. L Kwikkers, J. M Ruijter, C. de Gier-de Vries, M. A van Roon, A. J Meijer, B. Marescau, P. P De Deyn, N. E. Deutz, et al. (2002)
Am. J. Clinical Nutrition 76, 128-140
   Abstract »    Full Text »    PDF »
Homeostatic Regulation of Intestinal Villous Epithelia by B Lymphocytes.
Y. Nishiyama, H. Hamada, S. Nonaka, H. Yamamoto, M. Nanno, Y. Katayama, H. Takahashi, and H. Ishikawa (2002)
J. Immunol. 168, 2626-2633
   Abstract »    Full Text »    PDF »
Splenic T Zone Development Is B Cell Dependent.
V. N. Ngo, R. J. Cornall, and J. G. Cyster (2001)
J. Exp. Med. 194, 1649-1660
   Abstract »    Full Text »    PDF »
Role of B cells as antigen-presenting cells in vivo revisited: antigen-specific B cells are essential for T cell expansion in lymph nodes and for systemic T cell responses to low antigen concentrations.
A. Rivera, C.-C. Chen, N. Ron, J. P. Dougherty, and Y. Ron (2001)
Int. Immunol. 13, 1583-1593
   Abstract »    Full Text »    PDF »
Neuroinvasion by a Creutzfeldt-Jakob disease agent in the absence of B cells and follicular dendritic cells.
M. J. Shlomchik, K. Radebold, N. Duclos, and L. Manuelidis (2001)
PNAS
   Abstract »    Full Text »    PDF »
The Role of Dendritic Cells, B Cells, and M Cells in Gut-Oriented Immune Responses.
O. Alpan, G. Rudomen, and P. Matzinger (2001)
J. Immunol. 166, 4843-4852
   Abstract »    Full Text »    PDF »
B Cell-Deficient ({micro}MT) Mice Have Alterations in the Cytokine Microenvironment of the Gut-Associated Lymphoid Tissue (GALT) and a Defect in the Low Dose Mechanism of Oral Tolerance.
P. A. Gonnella, H. P. Waldner, and H. L. Weiner (2001)
J. Immunol. 166, 4456-4464
   Abstract »    Full Text »    PDF »
Mycobacterium avium Invades the Intestinal Mucosa Primarily by Interacting with Enterocytes.
F. J. Sangari, J. Goodman, M. Petrofsky, P. Kolonoski, and L. E. Bermudez (2001)
Infect. Immun. 69, 1515-1520
   Abstract »    Full Text »    PDF »
IgA Immunodeficiency Leads to Inadequate Th Cell Priming and Increased Susceptibility to Influenza Virus Infection.
B. P. Arulanandam, R. H. Raeder, J. G. Nedrud, D. J. Bucher, J. Le, and D. W. Metzger (2001)
J. Immunol. 166, 226-231
   Abstract »    Full Text »    PDF »
Unsolved mysteries of intestinal M cells.
C NICOLETTI (2000)
Gut 47, 735-739
   Full Text »    PDF »
Genetics of Mouse Mammary Tumor Virus-Induced Mammary Tumors: Linkage of Tumor Induction to the gag Gene.
L. M. Hook, Y. Agafonova, S. R. Ross, S. J. Turner, and T. V. Golovkina (2000)
J. Virol. 74, 8876-8883
   Abstract »    Full Text »
Protective Immunity to Bordetella pertussis Requires Both B Cells and CD4+ T Cells for Key Functions Other than Specific Antibody Production.
M. Leef, K. L. Elkins, J. Barbic, and R. D. Shahin (2000)
J. Exp. Med. 191, 1841-1852
   Abstract »    Full Text »    PDF »
A Novel Mechanism of Resistance to Mouse Mammary Tumor Virus Infection.
T. V. Golovkina (2000)
J. Virol. 74, 2752-2759
   Abstract »    Full Text »
Neuroinvasion by a Creutzfeldt-Jakob disease agent in the absence of B cells and follicular dendritic cells.
M. J. Shlomchik, K. Radebold, N. Duclos, and L. Manuelidis (2001)
PNAS 98, 9289-9294
   Abstract »    Full Text »    PDF »



ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)