Intestinal Bacteria Trigger T Cell-Independent Immunoglobulin A2 Class Switching by Inducing Epithelial-Cell Secretion of the Cytokine APRIL

Immunity

Volumn 26, Issue 6, 2007, Pages 812-826

  He, Bing ^a   Xu, Weifeng ^a   Santini, Paul A ^a,b   Polydorides, Alexandros D ^a   Chiu, April ^a   Estrella, Jeannelyn ^a   Shan, Meimei ^a   Chadburn, Amy ^a   Villanacci, Vincenzo ^c   Plebani, Alessandro ^d   Knowles, Daniel M ^a   Rescigno, Maria ^e   Cerutti, Andrea ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c Servizio di Anatomia Patologica   (Italy)

^d UNIVERSITY OF BRESCIA   (Italy)

^e EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

APRIL PROTEIN; BACTERIAL ENZYME; IMMUNOGLOBULIN A2; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 7; PROTEINASE; TOLL LIKE RECEPTOR;

ARTICLE; BACTERIAL COLONIZATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANTIGENS, CD40; B-LYMPHOCYTES; BACTERIA; BACTERIAL VACCINES; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN CLASS SWITCHING; INTESTINAL MUCOSA; INTESTINES; MOLECULAR SEQUENCE DATA; MUCOUS MEMBRANE; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 13;

EID: 34250205694     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2007.04.014     Document Type: Article

References (47)

1. Abreu M.T., Fukata M., and Arditi M. TLR signaling in the gut in health and disease. J. Immunol. 174 (2005) 4453-4460
2. Brandtzaeg P., Baekkevold E.S., and Morton H.C. From B to A the mucosal way. Nat. Immunol. 2 (2001) 1093-1094
3. Calame K.L. Plasma cells: finding new light at the end of B cell development. Nat. Immunol. 2 (2001) 1103-1108
4. Castigli E., Alt F.W., Davidson L., Bottaro A., Mizoguchi E., Bhan A.K., and Geha R.S. CD40-deficient mice generated by recombination-activating gene-2-deficient blastocyst complementation. Proc. Natl. Acad. Sci. USA 91 (1994) 12135-12139
5. Castigli E., Scott S., Dedeoglu F., Bryce P., Jabara H., Bhan A.K., Mizoguchi E., and Geha R.S. Impaired IgA class switching in APRIL-deficient mice. Proc. Natl. Acad. Sci. USA 101 (2004) 3903-3908
6. Castigli E., Wilson S.A., Scott S., Dedeoglu F., Xu S., Lam K.P., Bram R.J., Jabara H., and Geha R.S. TACI and BAFF-R mediate isotype switching in B cells. J. Exp. Med. 201 (2005) 35-39
7. Cattoretti G., Buttner M., Shaknovich R., Kremmer E., Alobeid B., and Niedobitek G. Nuclear and cytoplasmic AID in extrafollicular and germinal center B cells. Blood 107 (2006) 3967-3975
8. Cerutti A., Zan H., Kim E.C., Shah S., Schattner E.J., Schaffer A., and Casali P. Ongoing in vivo immunoglobulin class switch DNA recombination in chronic lymphocytic leukemia B cells. J. Immunol. 169 (2002) 6594-6603
9. Chaudhuri J., and Alt F.W. Class-switch recombination: interplay of transcription, DNA deamination and DNA repair. Nat. Rev. Immunol. 4 (2004) 541-552
10. Coffman R.L., Lebman D.A., and Shrader B. Transforming growth factor beta specifically enhances IgA production by lipopolysaccharide-stimulated murine B lymphocytes. J. Exp. Med. 170 (1989) 1039-1044
11. Crago S.S., Kutteh W.H., Moro I., Allansmith M.R., Radl J., Haaijman J.J., and Mestecky J. Distribution of IgA1-, IgA2-, and J chain-containing cells in human tissues. J. Immunol. 132 (1984) 16-28
12. Fagarasan S., and Honjo T. Intestinal IgA synthesis: regulation of front-line body defences. Nat. Rev. Immunol. 3 (2003) 63-72
13. Fagarasan S., Kinoshita K., Muramatsu M., Ikuta K., and Honjo T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413 (2001) 639-643
14. Fagarasan S., Muramatsu M., Suzuki K., Nagaoka H., Hiai H., and Honjo T. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science 298 (2002) 1424-1427
15. Fayette J., Dubois B., Vandenabeele S., Bridon J.M., Vanbervliet B., Durand I., Banchereau J., Caux C., and Briere F. Human dendritic cells skew isotype switching of CD40-activated naive B cells towards IgA1 and IgA2. J. Exp. Med. 185 (1997) 1909-1918
16. Ferrari S., Giliani S., Insalaco A., Al-Ghonaium A., Soresina A.R., Loubser M., Avanzini M.A., Marconi M., Badolato R., Ugazio A.G., et al. Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc. Natl. Acad. Sci. USA 98 (2001) 12614-12619
17. He B., Qiao X., and Cerutti A. CpG DNA induces IgG class switch DNA recombination by activating human B cells through an innate pathway that requires TLR9 and cooperates with IL-10. J. Immunol. 173 (2004) 4479-4491
18. Hel Z., McGhee J.R., and Mestecky J. HIV infection: first battle decides the war. Trends Immunol. 27 (2006) 274-281
19. Honjo T., Kinoshita K., and Muramatsu M. Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu. Rev. Immunol. 20 (2002) 165-196
20. Jain A., Ma C.A., Lopez-Granados E., Means G., Brady W., Orange J.S., Liu S., Holland S., and Derry J.M. Specific NEMO mutations impair CD40-mediated c-Rel activation and B cell terminal differentiation. J. Clin. Invest. 114 (2004) 1593-1602
21. Kato A., Truong-Tran A.Q., Scott A.L., Matsumoto K., and Schleimer R.P. Airway epithelial cells produce B cell-activating factor of TNF family by an IFN-beta-dependent mechanism. J. Immunol. 177 (2006) 7164-7172
22. Kett K., Brandtzaeg P., Radl J., and Haaijman J.J. Different subclass distribution of IgA-producing cells in human lymphoid organs and various secretory tissues. J. Immunol. 136 (1986) 3631-3635
23. Klein U., Casola S., Cattoretti G., Shen Q., Lia M., Mo T., Ludwig T., Rajewsky K., and Dalla-Favera R. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 7 (2006) 773-782
24. Litinskiy M.B., Nardelli B., Hilbert D.M., He B., Schaffer A., Casali P., and Cerutti A. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3 (2002) 822-829
25. Lue C., Tarkowski A., and Mestecky J. Systemic immunization with pneumococcal polysaccharide vaccine induces a predominant IgA2 response of peripheral blood lymphocytes and increases of both serum and secretory anti-pneumococcal antibodies. J. Immunol. 140 (1988) 3793-3800
26. Macpherson A.J. IgA adaptation to the presence of commensal bacteria in the intestine. Curr. Top. Microbiol. Immunol. 308 (2006) 117-136
27. Macpherson A.J., and Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303 (2004) 1662-1665
28. Mestecky J., Russell M.W., and Elson C.O. Intestinal IgA: novel views on its function in the defence of the largest mucosal surface. Gut 44 (1999) 2-5
29. Mora J.R., Iwata M., Eksteen B., Song S.Y., Junt T., Senman B., Otipoby K.L., Yokota A., Takeuchi H., Ricciardi-Castagnoli P., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314 (2006) 1157-1160
30. Nagler-Anderson C. Man the barrier! Strategic defences in the intestinal mucosa. Nat. Rev. Immunol. 1 (2001) 59-67
31. Neutra M.R., Mantis N.J., and Kraehenbuhl J.P. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. 2 (2001) 1004-1009
32. Odegard V.H., and Schatz D.G. Targeting of somatic hypermutation. Nat. Rev. Immunol. 6 (2006) 573-583
33. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004) 229-241
34. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., Granucci F., Kraehenbuhl J.P., and Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2 (2001) 361-367
35. Rimoldi M., Chieppa M., Salucci V., Avogadri F., Sonzogni A., Sampietro G.M., Nespoli A., Viale G., Allavena P., and Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6 (2005) 507-514
36. Salzer U., Chapel H.M., Webster A.D., Pan-Hammarstrom Q., Schmitt-Graeff A., Schlesier M., Peter H.H., Rockstroh J.K., Schneider P., Schaffer A.A., et al. Mutations in TNFRSF13B encoding TACI are associated with common variable immunodeficiency in humans. Nat. Genet. 37 (2005) 820-828
37. Sato A., Hashiguchi M., Toda E., Iwasaki A., Hachimura S., and Kaminogawa S. CD11b+ Peyer's patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J. Immunol. 171 (2003) 3684-3690
38. Schlissel M.S. Regulating antigen-receptor gene assembly. Nat. Rev. Immunol. 3 (2003) 890-899
39. Schneider P. The role of APRIL and BAFF in lymphocyte activation. Curr. Opin. Immunol. 17 (2005) 282-289
40. Stavnezer J. Antibody class switching. Adv. Immunol. 61 (1996) 79-146
41. Suzuki K., Meek B., Doi Y., Honjo T., and Fagarasan S. Two distinctive pathways for recruitment of naive and primed IgM+ B cells to the gut lamina propria. Proc. Natl. Acad. Sci. USA 102 (2005) 2482-2486
42. Takeda K., Kaisho T., and Akira S. Toll-like receptors. Annu. Rev. Immunol. 21 (2003) 335-376
43. Tarkowski A., Lue C., Moldoveanu Z., Kiyono H., McGhee J.R., and Mestecky J. Immunization of humans with polysaccharide vaccines induces systemic, predominantly polymeric IgA2-subclass antibody responses. J. Immunol. 144 (1990) 3770-3778
44. Weller S., Braun M.C., Tan B.K., Rosenwald A., Cordier C., Conley M.E., Plebani A., Kumararatne D.S., Bonnet D., Tournilhac O., et al. Human blood IgM "memory" B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104 (2004) 3647-3654
45. Wilson E., and Butcher E.C. CCL28 controls immunoglobulin (Ig)A plasma cell accumulation in the lactating mammary gland and IgA antibody transfer to the neonate. J. Exp. Med. 200 (2004) 805-809
46. Xu W., He B., Chiu A., Chadburn A., Shan M., Buldys M., Ding A., Knowles D.M., Santini P.A., and Cerutti A. Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat. Immunol. 8 (2007) 294-303
47. Ziegler S.F., and Liu Y.J. Thymic stromal lymphopoietin in normal and pathogenic T cell development and function. Nat. Immunol. 7 (2006) 709-714