Intestinal IgA synthesis: A primitive form of adaptive immunity that regulates microbial communities in the gut

Seminars in Immunology

Volumn 19, Issue 2, 2007, Pages 127-135

  Suzuki, Keiichiro ^a   Ha, Seon ah ^a   Tsuji, Masayuki ^a   Fagarasan, Sidonia ^a  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

AID; Anaerobes; B cell homing; Gut homeostasis; Intestinal IgA

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN M;

B LYMPHOCYTE; BACTERIAL COLONIZATION; CELL MIGRATION; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNITY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; MICROFLORA; NONHUMAN; REVIEW; SYNTHESIS;

B-LYMPHOCYTES; BACTERIA; BACTERIAL PHYSIOLOGY; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN M; INTESTINAL MUCOSA; PLASMA CELLS;

EID: 34249298559     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2006.10.001     Document Type: Review

References (79)

1. Hooper L.V., and Gordon J.I. Commensal host-bacterial relationships in the gut. Science 292 (2001) 1115-1118
2. Backhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., and Gordon J.I. Host-bacterial mutualism in the human intestine. Science 307 (2005) 1915-1920
3. Sonnenburg J.L., Angenent L.T., and Gordon J.I. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine?. Nat Immunol 5 (2004) 569-573
4. 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
5. Ouellette A.J. Paneth cells and innate immunity in the crypt microenvironment. Gastroenterology 113 (1997) 1779-1784
6. Hooper L.V., Stappenbeck T.S., Hong C.V., and Gordon J.I. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 4 (2003) 269-273
7. van der Heijden P.J., Stok W., and Bianchi A.T. Contribution of immunoglobulin-secreting cells in the murine small intestine to the total 'background' immunoglobulin production. Immunology 62 (1987) 551-555
8. van Egmond M., Damen C.A., van Spriel A.B., Vidarsson G., van Garderen E., and van de Winkel J.G. IgA and the IgA Fc receptor. Trends Immunol 22 (2001) 205-211
9. Mostov K.E. Transepithelial transport of immunoglobulins. Annu Rev Immunol 12 (1994) 63-84
10. Craig S.W., and Cebra J.J. Peyer's patches: an enriched source of precursors for IgA-producing immunocytes in the rabbit. J Exp Med 134 (1971) 188-200
11. Brandtzaeg P., Baekkevold E.S., Farstad I.N., Jahnsen F.L., Johansen F.E., Nilsen E.M., et al. Regional specialization in the mucosal immune system: what happens in the microcompartments?. Immunol Today 20 (1999) 141-151
12. Fagarasan S., and Honjo T. Intestinal IgA synthesis: regulation of front-line body defences. Nat Rev Immunol 3 (2003) 63-72
13. Hamada H., Hiroi T., Nishiyama Y., Takahashi H., Masunaga Y., Hachimura S., et al. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J Immunol 168 (2002) 57-64
14. Fagarasan S., Muramatsu M., Suzuki K., Nagaoka H., Hiai H., and Honjo T. Critical roles of activation-induced cytidine deaminase (AID) in the homeostasis of gut flora. Science 298 (2002) 1424-1427
15. Pabst O., Herbrand H., Worbs T., Friedrichsen M., Yan S., Hoffmann M.W., et al. Cryptopatches and isolated lymphoid follicles: dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur J Immunol 35 (2005) 98-107
16. Nishikawa S., Honda K., Vieira P., and Yoshida H. Organogenesis of peripheral lymphoid organs. Immunol Rev 195 (2003) 72-80
17. Honda K., Nakano H., Yoshida H., Nishikawa S., Rennert P., Ikuta K., et al. Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J Exp Med 193 (2001) 621-630
18. Yoshida H., Naito A., Inoue J., Satoh M., Santee-Cooper S.M., Ware C.F., et al. Different cytokines induce surface lymphotoxin-alphabeta on IL-7 receptor-alpha cells that differentially engender lymph nodes and Peyer's patches. Immunity 17 (2002) 823-833
19. Lorenz R.G., Chaplin D.D., McDonald K.G., McDonough J.S., and Newberry R.D. Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin-sufficient B lymphocytes, lymphotoxin beta receptor, and TNF receptor I function. J Immunol 170 (2003) 5475-5482
20. McDonald K.G., McDonough J.S., and Newberry R.D. Adaptive immune responses are dispensable for isolated lymphoid follicle formation: antigen-naive, lymphotoxin-sufficient B lymphocytes drive the formation of mature isolated lymphoid follicles. J Immunol 174 (2005) 5720-5728
21. Finke D., Acha-Orbea H., Mattis A., Lipp M., and Kraehenbuhl J. CD4+CD3- cells induce Peyer's patch development: role of alpha4beta1 integrin activation by CXCR5. Immunity 17 (2002) 363-373
22. Cebra J.J., and Shroff K.E. Peyer's patches as inductive sites for IgA commitment. In: Ogra P., Mestecky J., Lamm M., Strobel W., McGhee J., and Bienenstock J. (Eds). Handbook of mucosal immunology (1994), Academic Press, San Diego 151-157
23. Tseng J. Transfer of lymphocytes of Peyer's patches between immunoglobulin allotype congenic mice: repopulation of the IgA plasma cells in the gut lamina propria. J Immunol 127 (1981) 2039-2043
24. Tseng J. A population of resting IgM-IgD double-bearing lymphocytes in Peyer's patches: the major precursor cells for IgA plasma cells in the gut lamina propria. J Immunol 132 (1984) 2730-2735
25. Butcher E.C., Rouse R.V., Coffman R.L., Nottenburg C.N., Hardy R.R., and Weissman I.L. Surface phenotype of Peyer's patch germinal center cells: implications for the role of germinal centers in B cell differentiation. J Immunol 129 (1982) 2698-2707
26. Weinstein P.D., and Cebra J.J. The preference for switching to IgA expression by Peyer's patch germinal center B cells is likely due to the intrinsic influence of their microenvironment. J Immunol 147 (1991) 4126-4135
27. Strobel W., Fagarasan S., and Lycke N. IgA B cell development. In: Mestecky J., Lamm M., McGhee J., Bienenstock J., Mayer L., and Strobel W. (Eds). Mucosal immunology (2005), Academic Press, San Diego 583-616
28. Cebra J.J. Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69 (1999) 1046S-1051S
29. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., and Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102 (2000) 553-563
30. 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
31. Kinoshita K., Harigai M., Fagarasan S., Muramatsu M., and Honjo T. A hallmark of active class switch recombination: transcripts directed by I promoters on looped-out circular DNAs. Proc Natl Acad Sci USA 98 (2001) 12620-12623
32. Lycke N. T cell and cytokine regulation of the IgA response. In: MacDonald T. (Ed). Mucosal T cells (1998), Karger, Basel 209-234
33. Iwasaki A., and Kelsall B.L. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 190 (1999) 229-239
34. 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
35. Gardby E., Wrammert J., Schon K., Ekman L., Leanderson T., and Lycke N. Strong differential regulation of serum and mucosal IgA responses as revealed in CD28-deficient mice using cholera toxin adjuvant. J Immunol 170 (2003) 55-63
36. Kroese F.G., Butcher E.C., Stall A.M., Lalor P.A., Adams S., and 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 1 (1989) 75-84
37. Fagarasan S., Watanabe N., and Honjo T. Generation, expansion, migration and activation of mouse B1 cells. Immunol Rev 176 (2000) 205-215
38. Fagarasan S., Shinkura R., Kamata T., Nogaki F., Ikuta K., Tashiro K., et al. Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med 191 (2000) 1477-1486
39. Fagarasan S., and Honjo T. T-Independent immune response: new aspects of B cell biology. Science 290 (2000) 89-92
40. Macpherson A.J., Gatto D., Sainsbury E., Harriman G.R., Hengartner H., and Zinkernagel R.M. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288 (2000) 2222-2226
41. Eberl G., and Littman D.R. Thymic origin of intestinal alphabeta T cells revealed by fate mapping of RORgammat+ cells. Science 305 (2004) 248-251
42. Kang H.S., Chin R.K., Wang Y., Yu P., Wang J., Newell K.A., et al. Signaling via LTbetaR on the lamina propria stromal cells of the gut is required for IgA production. Nat Immunol 3 (2002) 576-582
43. Ryffel B., Le Hir M., Muller M., and Eugster H.P. Correction of the TNF-LT alpha-deficient phenotype by bone marrow transplantation. Dev Immunol 6 (1998) 253-260
44. Guy-Grand D., Griscelli C., and Vassalli P. The gut-associated lymphoid system: nature and properties of the large dividing cells. Eur J Immunol 4 (1974) 435-443
45. McWilliams M., Phillips-Quagliata J.M., and Lamm M.E. Mesenteric lymph node B lymphoblasts which home to the small intestine are precommitted to IgA synthesis. J Exp Med 145 (1977) 866-875
46. Youngman K., Lazarus N., and Butcher E. Lymphocyte homing:chemokines and adhesion molecules in T cell and IgA plasma cell localization in the mucosal immune system. In: Mestecky J., Lamm M., McGhee J., Bienenstock J., Mayer L., and Strobel W. (Eds). Mucosal immunology (2005), Academic Press, San Diego 667-680
47. Berlin C., Berg E.L., Briskin M.J., Andrew D.P., Kilshaw P.J., Holzmann B., et al. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 74 (1993) 185
48. Bowman E.P., Kuklin N.A., Youngman K.R., Lazarus N.H., Kunkel E.J., Pan J., et al. The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J Exp Med 195 (2002) 269-275
49. Kunkel E.J., and Butcher E.C. Chemokines and the tissue-specific migration of lymphocytes. Immunity 16 (2002) 1-4
50. Pabst O., Ohl L., Wendland M., Wurbel M.A., Kremmer E., Malissen B., et al. Chemokine receptor CCR9 contributes to the localization of plasma cells to the small intestine. J Exp Med 199 (2004) 411-416
51. Cyster J.G. Homing of antibody secreting cells. Immunol Rev 194 (2003) 48-60
52. Shinkura R., Kitada K., Matsuda F., Tashiro K., Ikuta K., Suzuki M., et al. Alymphoplasia is caused by a point mutation in the mouse gene encoding Nf-kappa b-inducing kinase. Nat Genet 22 (1999) 74-77
53. 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
54. Newberry R.D., McDonough J.S., McDonald K.G., and Lorenz R.G. Postgestational lymphotoxin/lymphotoxin beta receptor interactions are essential for the presence of intestinal B lymphocytes. J Immunol 168 (2002) 4988-4997
55. Mora J.R., Bono M.R., Manjunath N., Weninger W., Cavanagh L.L., Rosemblatt M., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424 (2003) 88-93
56. Johansson-Lindbom B., Svensson M., Wurbel M.A., Malissen B., Marquez G., and Agace W. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med 198 (2003) 963-969
57. Iwata M., Hirakiyama A., Eshima Y., Kagechika H., Kato C., and Song S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21 (2004) 527-538
58. Kraehenbuhl J.P., and Neutra M.R. Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 16 (2000) 301-332
59. Macpherson A.J., and Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303 (2004) 1662-1665
60. Worbs T., Bode U., Yan S., Hoffmann M.W., Hintzen G., Bernhardt G., et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 203 (2006) 519-527
61. MacLennan I.C. Germinal centers. Annu Rev Immunol 12 (1994) 117-139
62. Honjo T., Kinoshita K., and Muramatsu M. Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu Rev Immunol 20 (2002) 165-196
63. Casola S., Otipoby K.L., Alimzhanov M., Humme S., Uyttersprot N., Kutok J.L., et al. B cell receptor signal strength determines B cell fate. Nat Immunol 5 (2004) 317-327
64. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2 (2001) 361-367
65. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 (2005) 254-258
66. Cheroutre H., and Madakamutil L. Acquired and natural memory T cells join forces at the mucosal front line. Nat Rev Immunol 4 (2004) 290-300
67. Litinskiy M.B., Nardelli B., Hilbert D.M., He B., Schaffer A., Casali P., et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 3 (2002) 822-829
68. Fagarasan S., and Honjo T. Regulation of IgA synthesis at mucosal surfaces. Curr Opin Immunol 16 (2004) 277-283
69. Russell M., and Kilian M. Biological activities of IgA. In: Mestecky J., Lamm M., McGhee J., Bienenstock J., Mayer L., and Strobel W. (Eds). Mucosal immunology (2005), Academic Press, San Diego 267-289
70. Harriman G.R., Bogue M., Rogers P., Finegold M., Pacheco S., Bradley A., et al. Targeted deletion of the IgA constant region in mice leads to IgA deficiency with alterations in expression of other Ig isotypes. J Immunol 162 (1999) 2521-2529
71. Lycke N., Erlandsson L., Ekman L., Schon K., and Leanderson T. Lack of J chain inhibits the transport of gut IgA and abrogates the development of intestinal antitoxic protection. J Immunol 163 (1999) 913-919
72. Wijburg O.L., Uren T.K., Simpfendorfer K., Johansen F.E., Brandtzaeg P., and Strugnell R.A. Innate secretory antibodies protect against natural Salmonella typhimurium infection. J Exp Med 203 (2006) 21-26
73. Johansen F.E., Pekna M., Norderhaug I.N., Haneberg B., Hietala M.A., Krajci P., et al. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/secretory component-deficient mice. J Exp Med 190 (1999) 915-922
74. Cunningham-Rundles C., Brandeis W.E., Good R.A., and Day N.K. Milk precipitins, circulating immune complexes, and IgA deficiency. Proc Natl Acad Sci USA 75 (1978) 3387-3389
75. Suzuki K., Meek B., Doi Y., Muramatsu M., Chiba T., Honjo T., et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci USA 101 (2004) 1981-1986
76. Jiang H.Q., Bos N.A., and Cebra J.J. Timing, localization, and persistence of colonization by segmented filamentous bacteria in the neonatal mouse gut depend on immune status of mothers and pups. Infect Immun 69 (2001) 3611-3617
77. Bastlein C., Burlefinger R., Holzberg E., Voeth C., Garbrecht M., and Ottenjann R. Common variable immunodeficiency syndrome and nodular lymphoid hyperplasia in the small intestine. Endoscopy 20 (1988) 272-275
78. Burt R.W., and Jacoby R.F. Polyposis syndromes. In: Yamada T., Alpers D., Laine L., Owyang C., and Powell D. (Eds). Textbook of gastroenterology (1999), Lippincott William & Wilkins, Philadelphia 1995-2022
79. Ha S.A., Tsuji M., Suzuki K., Meek B., Yasuda N., Kaisho T., et al. Regulation of B1 cell migration by signals through Toll-like receptors. J Exp Med. 203 11 (2006) 2541-2550