Reports

Generation of Gut-Homing IgA-Secreting B Cells by Intestinal Dendritic Cells

J. Rodrigo Mora,^1* Makoto Iwata,^2* Bertus Eksteen,^3* Si-Young Song,² Tobias Junt,¹ Balimkiz Senman,¹ Kevin L. Otipoby,¹ Aya Yokota,² Hajime Takeuchi,² Paola Ricciardi-Castagnoli,⁴ Klaus Rajewsky,¹ David H. Adams,³ Ulrich H. von Andrian¹

Normal intestinal mucosa contains abundant immunoglobulin A (IgA)–secreting cells, which are generated from B cells in gut-associated lymphoid tissues (GALT). We show that dendritic cells (DC) from GALT induce T cell–independent expression of IgA and gut-homing receptors on B cells. GALT-DC–derived retinoic acid (RA) alone conferred gut tropism but could not promote IgA secretion. However, RA potently synergized with GALT-DC–derived interleukin-6 (IL-6) or IL-5 to induce IgA secretion. Consequently, mice deficient in the RA precursor vitamin A lacked IgA-secreting cells in the small intestine. Thus, GALT-DC shape mucosal immunity by modulating B cell migration and effector activity through synergistically acting mediators.

¹ CBR Institute for Biomedical Research and Department of Pathology, Harvard Medical School, Boston, MA 02115, USA.
² Faculty of Pharmaceutical Sciences at Kagawa Campus, Tokushima Bunri University, Sanuki-shi, Kagawa 769-2193, Japan.
³ MRC Centre for Immune Regulation, University of Birmingham, Birmingham B15 2TT, UK.
⁴ Department of Biotechnology and Bioscience, University of Milano-Bicocca, Piazza della Scienza 2, Milan, Italy.

^* These authors contributed equally to this work.

To whom correspondence should be addressed. E-mail: uva{at}cbr.med.harvard.edu (U.H.V.A.); mora{at}cbr.med.harvard.edu (J.R.M.)

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Stromal Cells Confer Lymph Node-Specific Properties by Shaping a Unique Microenvironment Influencing Local Immune Responses.

M. Ahrendt, S. I. Hammerschmidt, O. Pabst, R. Pabst, and U. Bode (2008)
J. Immunol. 181, 1898-1907
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Discriminating gene expression profiles of memory B cell subpopulations.

G. R.A. Ehrhardt, A. Hijikata, H. Kitamura, O. Ohara, J.-Y. Wang, and M. D. Cooper (2008)
J. Exp. Med.
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Deficiency of Indoleamine 2,3-Dioxygenase Enhances Commensal-Induced Antibody Responses and Protects against Citrobacter rodentium-Induced Colitis.

L. Harrington, C. V. Srikanth, R. Antony, S. J. Rhee, A. L. Mellor, H. N. Shi, and B. J. Cherayil (2008)
Infect. Immun. 76, 3045-3053
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Nonmucosal Alphavirus Vaccination Stimulates a Mucosal Inductive Environment in the Peripheral Draining Lymph Node.

J. M. Thompson, M. G. Nicholson, A. C. Whitmore, M. Zamora, A. West, A. Iwasaki, H. F. Staats, and R. E. Johnston (2008)
J. Immunol. 181, 574-585
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Immunology of the gut and liver: a love/hate relationship.

D H Adams, B Eksteen, and S M Curbishley (2008)
Gut 57, 838-848
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CCL25 and CCL28 promote {alpha}4{beta}7-integrin-dependent adhesion of lymphocytes to MAdCAM-1 under shear flow.

A. Miles, E. Liaskou, B. Eksteen, P. F. Lalor, and D. H. Adams (2008)
Am J Physiol Gastrointest Liver Physiol 294, G1257-G1267
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Sphingosine 1-phosphate-dependent trafficking of peritoneal B cells requires functional NF{kappa}B-inducing kinase in stromal cells.

J. Kunisawa, M. Gohda, Y. Kurashima, I. Ishikawa, M. Higuchi, and H. Kiyono (2008)
Blood 111, 4646-4652
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Sphingosine 1-Phosphate Regulates the Egress of IgA Plasmablasts from Peyer's Patches for Intestinal IgA Responses.

M. Gohda, J. Kunisawa, F. Miura, Y. Kagiyama, Y. Kurashima, M. Higuchi, I. Ishikawa, I. Ogahara, and H. Kiyono (2008)
J. Immunol. 180, 5335-5343
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Cutting Edge: Langerin+ Dendritic Cells in the Mesenteric Lymph Node Set the Stage for Skin and Gut Immune System Cross-Talk.

S.-Y. Chang, H.-R. Cha, O. Igarashi, P. D. Rennert, A. Kissenpfennig, B. Malissen, M. Nanno, H. Kiyono, and M.-N. Kweon (2008)
J. Immunol. 180, 4361-4365
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Docosahexaenoic Acid-Enriched Fish Oil Consumption Modulates Immunoglobulin Responses to and Clearance of Enteric Reovirus Infection in Mice.

E. Beli, M. Li, C. Cuff, and J. J. Pestka (2008)
J. Nutr. 138, 813-819
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Effects of adding fibrous feedstuffs to the diet of young pigs on growth performance, intestinal cytokines, and circulating acute-phase proteins.

T. E. Weber, C. J. Ziemer, and B. J. Kerr (2008)
J Anim Sci 86, 871-881
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Broad dispersion and lung localization of virus-specific memory B cells induced by influenza pneumonia.

H. M. Joo, Y. He, and M. Y. Sangster (2008)
PNAS 105, 3485-3490
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1,25-Dihydroxyvitamin D3 Induces CCR10 Expression in Terminally Differentiating Human B Cells.

A.-K. Shirakawa, D. Nagakubo, K. Hieshima, T. Nakayama, Z. Jin, and O. Yoshie (2008)
J. Immunol. 180, 2786-2795
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Organ-derived dendritic cells have differential effects on alloreactive T cells.

T. D. Kim, T. H. Terwey, J. L. Zakrzewski, D. Suh, A. A. Kochman, M. E. Chen, C. G. King, C. Borsotti, J. Grubin, O. M. Smith, et al. (2008)
Blood 111, 2929-2940
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Lung Dendritic Cells Have a Potent Capability to Induce Production of Immunoglobulin A.

T. Naito, T. Suda, K. Suzuki, Y. Nakamura, N. Inui, J. Sato, K. Chida, and H. Nakamura (2008)
Am. J. Respir. Cell Mol. Biol. 38, 161-167
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Colonic Patches Direct the Cross-Talk Between Systemic Compartments and Large Intestine Independently of Innate Immunity.

S.-Y. Chang, H.-R. Cha, S. Uematsu, S. Akira, O. Igarashi, H. Kiyono, and M.-N. Kweon (2008)
J. Immunol. 180, 1609-1618
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Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway.

K. M. Elias, A. Laurence, T. S. Davidson, G. Stephens, Y. Kanno, E. M. Shevach, and J. J. O'Shea (2008)
Blood 111, 1013-1020
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Retinoids Accelerate B Lineage Lymphoid Differentiation.

X. Chen, B. L. Esplin, K. P. Garrett, R. S. Welner, C. F. Webb, and P. W. Kincade (2008)
J. Immunol. 180, 138-145
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Retinol Combined with Retinoic Acid Increases Retinol Uptake and Esterification in the Lungs of Young Adult Rats when Delivered by the Intramuscular as well as Oral Routes.

A. C. Ross and N.-q. Li (2007)
J. Nutr. 137, 2371-2376
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Lymphoma dissemination: the other face of lymphocyte homing.

S. T. Pals, D. J. J. de Gorter, and M. Spaargaren (2007)
Blood 110, 3102-3111
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The yin and yang of intestinal epithelial cells in controlling dendritic cell function.

I. D. Iliev, G. Matteoli, and M. Rescigno (2007)
J. Exp. Med. 204, 2253-2257
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In Vitro Induction of Mucosa-Type Dendritic Cells by All-Trans Retinoic Acid.

L. Saurer, K. C. McCullough, and A. Summerfield (2007)
J. Immunol. 179, 3504-3514
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Vitamin A Metabolites Induce Gut-Homing FoxP3+ Regulatory T Cells.

S. G. Kang, H. W. Lim, O. M. Andrisani, H. E. Broxmeyer, and C. H. Kim (2007)
J. Immunol. 179, 3724-3733
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Th2 Differentiation in Distinct Lymph Nodes Influences the Site of Mucosal Th2 Immune-Inflammatory Responses.

D. Alvarez, J. L. Arkinson, J. Sun, R. Fattouh, T. Walker, and M. Jordana (2007)
J. Immunol. 179, 3287-3296
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Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid.

C.-M. Sun, J. A. Hall, R. B. Blank, N. Bouladoux, M. Oukka, J. R. Mora, and Y. Belkaid (2007)
J. Exp. Med. 204, 1775-1785
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