Advertisement

IgA Plasma Cell Development

  • Jo Spencer
  • Laurent Boursier
  • Jonathan D. Edgeworth

Evolution in biological systems is rarely wasteful; it involves both adaptation and conservation of resources. In this context especially, the quantity of IgA secreted onto mucosal surfaces and the cellular processes that generate it are all the more remarkable. Approximately 1010 plasma cells per meter of gut are situated in the diffuse connective tissue stroma between the epithelium and the muscularis mucosa referred to as the lamina propria (Fig. 2.1) (Brandtzaeg et al., 1999; Brandtzaeg and Pabst, 2004). These produce antibody, most of which is immumoglobin A (IgA), so that ~3–5g of IgA is actively transported each day into the lumen of the human gut (Conley and Delacroix, 1987). This secreted antibody has a critical role in maintaining homeostasis in an environment where the immune system and potentially proinflammatory bacterial stimuli are closely juxtaposed and separated by a single epithelial layer (Fagarasan et al., 2002). The aim of this chapter is to discuss the mechanisms that generate, diversify, and disseminate this extensive IgA-producing plasma cell population. There are considerable interspecies differences in mucosal lymphoid tissue that will be identified where relevant, but the final outcome in all species is the same: the production of the largest population of plasma cells in the body.

Keywords

Plasma Cell Lamina Propria Germinal Center Marginal Zone Malt Lymphoma 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akhiani, A. A., Schon, K., Franzen, L. E., Pappo, J., and Lycke, N. (2004). Helicobacter pylori-specific antibodies impair the development of gastritis, facilitate bacterial colonization, and counteract resistance against infection. J. Immunol. 172:5024–5033.PubMedGoogle Scholar
  2. Akhiani, A. A., Stensson, A., Schon, K., and Lycke, N. Y. (2005). IgA antibodies impair resistance against Helicobacter pylori infection: Studies on immune evasion in IL-10-deficient mice. IgA antibodies impair resistance against Helicobacter pylori infection: studies on immune evasion in IL-10-deficient mice. J. Immunol. 174:8144–8153.PubMedGoogle Scholar
  3. Amlot, P. L., Grennan, D., and Humphrey, J. H. (1985). Splenic dependence of the antibody response to thymus-independent (TI-2) antigens. Eur. J. Immunol. 15:508–512.PubMedCrossRefGoogle Scholar
  4. Amlot, P. L., and Hayes, A. E. (1985). Impaired human antibody response to the thymus-independent antigen, DNP-Ficoll, after splenectomy. Implications for post-splenectomy infections. Lancet 1:1008–1011.PubMedCrossRefGoogle Scholar
  5. Anderle, P., Rumbo, M., Sierro, F., Mansourian, R., Michetti, P., Roberts, M. A., and Kraehenbuhl, J.-P. (2005). Novel markers of the human follicle-associated epithelium identified by genomic profiling and microdissection. Gastroenterology 129:321–327.PubMedCrossRefGoogle Scholar
  6. Bhalla, D. K., Owen, R. L., Bhalla, D. K., and Owen, R. L. (1982). Cell renewal and migration in lymphoid follicles of Peyer’s patches and cecum:An autoradiographic study in mice. Gastroenterology 82:232–242.PubMedGoogle Scholar
  7. Bos, N. A., Bun, J. C., Popma, S. H., Cebra, E. R., Deenen, G. J., van der Cammen, M. J., Kroese, F. G., and Cebra, J. J. (1996). Monoclonal immunoglobulin A derived from peritoneal B cells is encoded by both germ line and somatically mutated VH genes and is reactive with commensal bacteria. Infect. Immun. 64:616–623.PubMedGoogle Scholar
  8. Boursier, L., Dunn-Walters, D. K., and Spencer, J. (1999). Characteristics of IgVH genes used by human intestinal plasma cells from childhood. Immunology 97:558–564.PubMedCrossRefGoogle Scholar
  9. Boursier, L., Farstad, I. N., Mellembakken, J. R., Brandtzaeg, P., and Spencer, J. (2002). IgVH gene analysis suggests that peritoneal B cells do not contribute to the gut immune system in man. Eur. J. Immunol. 32:2427–2436.PubMedCrossRefGoogle Scholar
  10. Boursier, L., Gordon, J. N., Thiagamoorthy, S., Edgeworth, J. D., and Spencer J. (2005). Human intestinal IgA response is generated in the organized gut-associated lymphoid tissue but not in the lamina propria. Human intestinal IgA response is generated in the organized gut-associated lymphoid tissue but not in the lamina propria. Gastroenterology 128:1879–1889.PubMedCrossRefGoogle Scholar
  11. Bowman, E. P., Kuklin, N. A., Youngman, K. R., Lazarus, N. H., Kunkel, E. J., Pan, J., Greenberg, H. B., and Butcher, E. C. (2002). The intestinal chemokine thymus-expressed chemokine (CCL25) attracts IgA antibody-secreting cells. J. Exp. Med. 195:269–275.PubMedCrossRefGoogle Scholar
  12. Brandtzaeg, P., Farstad, I. N., Johansen, F. E., Morton, H. C., Norderhaug, I. N., and Yamanaka, T. (1999). The B-cell system of human mucosae and exocrine glands. Immunol. Rev. 171:45–87.PubMedCrossRefGoogle Scholar
  13. Brandtzaeg, P., Kett, K., Rognum, T. O., Soderstrom, R., Bjorkander, J., Soderstrom, T., Petrusson, B., and Hanson, L. A. (1986). Distribution of mucosal IgA and IgG subclass-producing immunocytes and alterations in various disorders. Monogr. Allergy 20:179–194.PubMedGoogle Scholar
  14. Brandtzaeg, P., and Pabst, R. (2004). Let’s go mucosal: Communication on slippery ground. Trends Immunol. 25:570–577.PubMedCrossRefGoogle Scholar
  15. Briere, F., Defrance, T., Vanbervliet, B., Bridon, J.-M., Durand, I., Rousset, F., and Banchereau, J. (1995). Transforming growth factor B (TGF ) directs IgA1 and IgA2 switching in human naive B cells. Adv. Exp. Med. Biol. 371A:21–26.PubMedGoogle Scholar
  16. Briskin, M. J., McEvoy, L. M., and Butcher, E. C. (1993). MAdCAM-1 has homology to immunoglobulin and mucin-like adhesion receptors and to IgA1. Nature 363:461–464.PubMedCrossRefGoogle Scholar
  17. Butcher, E. C., Rouse, R. V., Coffman, R. L., Nottenburg, C. N., Hardy, R. R., and Weissman, I. L. (1982). Surface phenotype of Peyer’s patch germinal center cells: Implications for the role of germinal centers in B cell differentiation. J. Immunol. 129:2698–2707.PubMedGoogle Scholar
  18. Casola, S., Otipoby, K. L., Alimzhanov, M., Humme, S., Uyttersprot, N., Kutok, J. L., Carroll, M. C., and Rajewsky, K. (2004). B cell receptor signal strength determines B cell fate. Nat. Immunol. 5:317–327.PubMedCrossRefGoogle Scholar
  19. Cazac, B. B., and Roes, J. (2000). TGF-b receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 13:443–451.PubMedCrossRefGoogle Scholar
  20. Claassen, E., Kors, N., Dijkstra, C.D., and van Rooijen, N. (1986). Marginal zone of the spleen and the development and localization of specific antibody-forming cells against thymus-dependent and thymus-independent type-2 antigens. Immunology 57:399–403.PubMedGoogle Scholar
  21. Clemens, J. D., Sack, D. A., Harris, J. R., Chakraborty, J., Khan, M. R., Stanton, B. F., Kay, B. A., Khan, M. U., Yunus, M., Atkinson, W., and Holmgren, J. (1986). Field trial of oral cholera vaccines in Bangladesh. Lancet 328:124–127.CrossRefGoogle Scholar
  22. Conley, M. E., and Delacroix, D. L. (1987). Intravascular and mucosal immunoglobulin A: Two separate but related systems of immune defense? Ann. Intern. Med. 106:892–899.PubMedGoogle Scholar
  23. Cornes, J. S. (1965) Number, size and distribution of Peyer’s patches in the human small intestine. Gut 6:225–233.PubMedCrossRefGoogle Scholar
  24. Craig, S. W., and Cebra, J. J. (1971) Peyer’s patches: An enriched source of precursors for IgA-producing immunocytes in the rabbit. J. Exp. Med. 134:188–200.PubMedCrossRefGoogle Scholar
  25. Defrance, T., Vanbervliet, B., Briere, F., Durand, I., Rousset, F., and Banchereau, J. (1992). Interleukin 10 and transforming growth factor b cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J. Exp. Med. 175:671–682.PubMedCrossRefGoogle Scholar
  26. Du, M., Diss, T. C., Xu, C., Peng, H., Isaacson, P.G., and Pan, L. (1996). Ongoing mutation in MALT lymphoma immunoglobulin gene suggests that antigen stimulation plays a role in the clonal expansion. Leukemia 10:1190–1197.PubMedGoogle Scholar
  27. Dukes, C., and Bussey, H. J. R. (1926). The number of lymphoid follicles of the human large intestine. J. Pathol. Bacteria 29:111–116.CrossRefGoogle Scholar
  28. Dunn-Walters, D. K., Isaacson, P. G., and Spencer, J. (1996). Sequence analysis of rearranged IgVH genes from microdissected human Peyer’s patch marginal zone B cells. Immunology 88:618–624.PubMedGoogle Scholar
  29. Dunn-Walters, D. K., Isaacson, P. G., and Spencer, J. (1997). Sequence analysis of human IgVH genes indicates that ileal lamina propria plasma cells are derived from Peyer’s patches. Eur. J. Immunol. 27:463–467.PubMedCrossRefGoogle Scholar
  30. Dunn-Walters, D. K. and Spencer J. (1998). Strong intrinsic biases towards mutation and conservation of bases in human IgVH genes during somatic hypermutation prevent statistical analysis of antigen selection. Immunology 95:339–345.PubMedCrossRefGoogle Scholar
  31. DuPont, H. L., Hornick, R. B., Snyder, M. J., Libonati, J. P., Formal, S. B., and Gangarosa, E. J. (1972). Immunity in shigellosis. II. Protection induced by oral live vaccine or primary infection. J. Infect. Dis. 125:12–16.PubMedGoogle Scholar
  32. Fagarasan, S., Kinoshita, K., Muramatsu, M., Ikuta, K., and Honjo, T. (2001). In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413:639–643.PubMedCrossRefGoogle Scholar
  33. Fagarasan, S., Muramatsu, M., Suzuki, K., Nagaoka, H., Hiai, H., and Honjo, T. (2002). Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science 298:1424–1427.PubMedCrossRefGoogle Scholar
  34. Falini, B., Tiacci, E., Pucciarini, A., Bigerna, B., Kurth, J., Hatzivassiliou, G., Droetto, S., Galletti, B. V., Gambacorta, M., Orazi, A., Pasqualucci, L., Miller, I., Kuppers, R., Dalla-Favera, R., and Cattoretti, G. (2003). Expression of the IRTA1 receptor identifies intraepithelial and subepithelial marginal zone B cells of the mucosa-associated lymphoid tissue (MALT). Blood 102:3684–3692.PubMedCrossRefGoogle Scholar
  35. Farstad, I. N., Carlsen, H., Morton, H. C., and Brandtzaeg, P. (2000). Immunoglobulin A cell distribution in the human small intestine: Phenotypic and functional characteristics. Immunology 101:354–363.PubMedCrossRefGoogle Scholar
  36. Farstad, I. N., Halstensen, T. S., Fausa, O., and Brandtzaeg, P. (1994). Heterogeneity of M-cell-associated B and T cells in human Peyer’s patches. Immunology 83:457–464.PubMedGoogle Scholar
  37. Farstad, I. N., Halstensen, T. S., Lazarovits, A. I., Norstein, J., Fausa, O., and Brandtzaeg, P. (1995). Human intestinal B-cell blasts and plasma cells express the mucosal homing receptor integrin a4b7. Scand. J. Immunol. 42:662–672.PubMedCrossRefGoogle Scholar
  38. Fayette, J., Dubois, B., Vandenabeele, S., Bridon, J.-M., Vanbervliet, B., Durand, I., Banchereau, J., Caux, C., and Brière, F. (1997). Human dendritic cells skew isotype switching of CD40-activated naive B cells towards IgA1 and IgA2. J. Exp. Med. 185:1909–1918.PubMedCrossRefGoogle Scholar
  39. Finke, D., Acha-Orbea, H., Mattis, A., Lipp, M., and Kraehenbuhl, J. (2002). CD4+CD3 cells induce Peyer’s patch development: role of y441 integrin activation by CXCR5. Immunity 17:363–373.PubMedCrossRefGoogle Scholar
  40. Fischer, M., and Kuppers, R. (1998). Human IgA- and IgM-secreting intestinal plasma cells carry heavily mutated VH region genes. Eur. J. Immunol. 28:2971–2977.PubMedCrossRefGoogle Scholar
  41. Formal, S. B., Kent, T. H., May, H. C., Palmer, A., Falkow, S., and LaBrec, E. H. (1966). Protection of monkeys against experimental shigellosis with a living attenuated oral polyvalent dysentery vaccine. J. Bacteriol. 92:17–22.PubMedGoogle Scholar
  42. Gardby, E., Wrammert, J., Schon, K., Ekman, L., Leanderson, T., and Lycke, N. (2003). Strong differential regulation of serum and mucosal IgA responses as revealed in CD28-deficient mice using cholera toxin adjuvant. J. Immunol. 170:55–63.PubMedGoogle Scholar
  43. Genta, R. M., Hamner, H. W., and Graham, D. Y. (1993). Gastric lymphoid follicles in Helicobacter pylori infection: Frequency, distribution, and response to triple therapy. Hum. Pathol. 24:577–583.PubMedCrossRefGoogle Scholar
  44. Goodrich, M. E., and McGee, D. W. (1998). Regulation of mucosal B cell immunoglobulin secretion by intestinal epithelial cell-derived cytokines. Cytokine 10:948–955.PubMedCrossRefGoogle Scholar
  45. Gowans, J. L., and Knight, E. J. (1964). The route of recirculation of lymphocytes in the rat. Proc. R. Soc. Lond. B: Biol. Sci. 159:257–282.CrossRefGoogle Scholar
  46. Guilliano, M. J., Foxx-Orenstein, A. E., and Lebman, D. A. (2001). The microenvironment of human Peyer’s patches inhibits the increase in CD38 expression associated with the germinal center reaction. J. Immunol. 166:2179–2185.PubMedGoogle Scholar
  47. Hamada, H., Hiroi, T., Nishiyama, Y., Takahashi, H., Masunaga, Y., Hachimura, S., Kaminogawa, S., Takahashi-Iwanaga, H., Iwanaga, T., Kiyono, H., Yamamoto, H., and Ishikawa, H. (2002). Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J. Immunol. 168:57–64.PubMedGoogle Scholar
  48. Hardie, D. L., Johnson, G. D., Khan, M., and MacLennan I. C. (1993). Quantitative analysis of molecules which distinguish functional compartments within germinal centers. Eur J Immunol. 23:997–1004.PubMedCrossRefGoogle Scholar
  49. Haubrich, W. S. (2005). Peyer of Peyer’s patches. Gastroenterology 129:85.CrossRefGoogle Scholar
  50. Holmgren, J., Lycke, N., and Czerkinsky, C. (1993). Cholera toxin and cholera B subunit as oral-mucosal adjuvant and antigen vector systems. Vaccine 11:1179–1184.PubMedCrossRefGoogle Scholar
  51. Holtmeier, W., Hennemann, A., and Caspary, W. F. (2000). IgA and IgM V(H) repertoires in human colon: Evidence for clonally expanded B cells that are widely disseminated. Gastroenterology 119:1253–1266.PubMedCrossRefGoogle Scholar
  52. Husband, A. J., (1982). Kinetics of extravasation and redistribution of IgA-specific antibody-containing cells in the intestine. J. Immunol. 128:1355–1359.PubMedGoogle Scholar
  53. Husband, A. J. and Gowans, J. L. (1978). The origin and antigen-dependent distribution of IgA-containing cells in the intestine. J. Exp. Med. 148:1146–1160.PubMedCrossRefGoogle Scholar
  54. Kroese, F. G., Butcher, E. C., Stall, A. M., Lalor, P. A., Adams, S., and Herzenberg, L. A. (1989). Many of the IgA producing plasma cells in murine gut are derived from self-replenishing precursors in the peritoneal cavity. Int. Immunol. 1:75–78.PubMedCrossRefGoogle Scholar
  55. Kunkel, E. J., and Butcher, E. C. (2003). Plasma-cell homing. Nat. Rev. Immunol. 3:822–829.PubMedCrossRefGoogle Scholar
  56. Kunkel, E. J., Kim, C. H., Lazarus, N. H., Vierra, M. A., Soler, D., Bowman, E. P., and Butcher, E. C. (2003). CCR10 expression is a common feature of circulating and mucosal epithelial tissue IgA Ab-secreting cells. J. Clin. Invest. 111:1001–1010.PubMedGoogle Scholar
  57. Kweon, M. N., Yamamoto, M., Rennert, P. D., Park, E. J., Lee, A. Y., Chang, S. Y., Hiroi, T., Nanno, M., and Kiyono, H. (2005). Prenatal blockage of lymphotoxin p receptor and TNF receptor p55 signaling cascade resulted in the acceleration of tissue genesis for isolated lymphoid follicles in the large intestine. J. Immunol. 174:4365–4372.PubMedGoogle Scholar
  58. Lanning, D. K., Rhee, K. J., and Knight, K. L. (2005). Intestinal bacteria and development of the B-lymphocyte repertoire. Trends Immunol. 26:419–425.PubMedCrossRefGoogle Scholar
  59. Lanning, D., Zhu, X., Zhai, S. K., and Knight, K. L. (2000). Development of the antibody repertoire in rabbit: gut-associated lymphoid tissue, microbes, and selection. Immunol Rev. 175:214–228.PubMedCrossRefGoogle Scholar
  60. Litinskiy, M. B., Nardelli, B., Hilbert, D. M., He, B., Schaffer, A., Casali, P., and Cerutti, A. (2002). DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3:822–829.PubMedCrossRefGoogle Scholar
  61. Liu, Y.-J., Malisan, F., de Bouteiller, O., Guret, C., Lebecque, S., Banchereau, J., Mills, F. C., Max, E. E., and Martinez-Valdez, H. (1996). Within germinal centers, isotype switching of immunoglobulin genes occurs after the onset of somatic mutation. Immunity 4:241–250.PubMedCrossRefGoogle Scholar
  62. Liu, Y.-J., Oldfield. S., and MacLennan, I. C. (1988). Memory B cells in T cell-dependent antibody responses colonize the splenic marginal zones. Eur. J. Immunol. 18:355–362.PubMedCrossRefGoogle Scholar
  63. Lorenz, R. G., and Newberry, R. D. (2004). Isolated lymphoid follicles can function as sites for induction of mucosal immune responses. Ann. NY Acad. Sci. 1029:44–57.PubMedCrossRefGoogle Scholar
  64. Lue, C., van den Wall Bake, A. W., Prince, S. J., Julian, B. A., Tseng, M. L., Radl, J., Elson, C. O., and Mestecky J. (1994). Intraperitoneal immunization of human subjects with tetanus toxoid induces specific antibody-secreting cells in the peritoneal cavity and in the circulation, but fails to elicit a secretory IgA response. Clin. Exp. Immunol. 96:356–363.PubMedCrossRefGoogle Scholar
  65. McDonald, K. G., McDonough, J. S., and Newberry, R. D. (2005). 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. 174:5720–5728.PubMedGoogle Scholar
  66. MacDonald, T. T., Spencer, J., Viney, J. L., Williams, C. B., and Walker-Smith, J. A. (1987). Selective biopsy of human Peyer’s patches during ileal endoscopy. Gastroenterology 93:1356–1362.PubMedGoogle Scholar
  67. Macpherson, A. J., Gatto, D., Sainsbury, E., Harriman, G. R., Hengartner, H., and Zinkernagel, R. M. (2000). A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288:2222–2226.PubMedCrossRefGoogle Scholar
  68. Macpherson, A. J., Lamarre, A., McCoy, K., Harriman, G. R., Odermatt, B., Dougan, G., Hengartner, H., and Zinkernagel, R. M. (2001). IgA production without H or chain expression in developing B cells. Nat. Immunol. 2:625–631.PubMedCrossRefGoogle Scholar
  69. Macpherson, A. J., and Uhr T. (2004). Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303:1662–1665.PubMedCrossRefGoogle Scholar
  70. Medina, F., Segundo, C., Campos-Caro, A., González-García, I., and Brieva, J. A. (2002). The heterogeneity shown by human plasma cells from tonsil, blood, and bone marrow reveals graded stages of increasing maturity, but local profiles of adhesion molecule expression. Blood 99:2154–2161.PubMedCrossRefGoogle Scholar
  71. Medina, F., Segundo, C., Campos-Caro, A., Salcedo, I., Garcia-Poley, A., and Brieva, J. A. (2003). Isolation, maturational level, and functional capacity of human colon lamina propria plasma cells. Gut 52:383–389.PubMedCrossRefGoogle Scholar
  72. Mel, D. M., Terzin, A. L., and Vuksic, L. (1965). Studies on vaccination against bacillary dysentery. 3. Effective oral immunization against Shigella flexneri 2a in a field trial. Bull. World Health Org. 32:647–655.PubMedGoogle Scholar
  73. Michetti, P., Mahan, M. J., Slauch, J. M., Mekalanos, J. J., and Neutra, M. R. (1992). Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. 60:1786–1792.Google Scholar
  74. Moghaddami, M., Cummins, A., and Mayrhofer, G. (1998). Lymphocyte-filled villi: Comparison with other lymphoid aggregations in the mucosa of the human small intestine. Gastroenterology 115:1414–1425.PubMedCrossRefGoogle Scholar
  75. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., and Honjo, T. (2000). Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–563.PubMedCrossRefGoogle Scholar
  76. Murakami, M., Tsubata, T., Shinkura, R., Nisitani, S., Okamoto, M., Yoshioka, H., Usui, T., Miyawaki, S., and Honjo T. (1994). 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. J. Exp. Med. 180:111–121.PubMedCrossRefGoogle Scholar
  77. Nishikawa, S., Honda, K., Vieira, P., and Yoshida, H. (2003). Organogenesis of peripheral lymphoid organs. Immunol. Rev. 195:72–80.PubMedCrossRefGoogle Scholar
  78. Ogra, P. L., and Karzon, D. T. (1969). Distribution of poliovirus antibody in serum, nasopharynx and alimentary tract following segmental immunization of lower alimentary tract with poliovaccine. J. Immunol. 102:1423–1430.PubMedGoogle Scholar
  79. O’Leary, A. D., and Sweeney, E. C. (1986). Lymphoglandular complexes of the colon: Structure and distribution. Histopathology 10:267–283.PubMedCrossRefGoogle Scholar
  80. Owen, R. L., and Jones, A. L. (1974). Epithelial cell specialization within human Peyer’s patches: An ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203.PubMedGoogle Scholar
  81. Pan, J., Kunkel, E. J., Gosslar, U., Lazarus, N., Langdon, P., Broadwell, K., Vierra, M. A., Genovese, M. C., Butcher, E. C., and Soler, D. (2000). A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J. Immunol. 165:2943–2949.PubMedGoogle Scholar
  82. Pappo, J., and Owen, R. L. (1988). Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 95:1173–1177.PubMedGoogle Scholar
  83. Pascual, V., Liu, Y.-J., Magalski, A., de Bouteiller, O., Banchereau, J., and Capra, J. D. (1994). Analysis of somatic mutation in five B cell subsets of human tonsil. J. Exp. Med. 180:329–339.PubMedCrossRefGoogle Scholar
  84. Phalipon, A., Kaufmann, M., Michetti, P., Cavaillon, J.-M., Huerre, M., Sansonetti, P., and Kraehenbuhl, J.-P. (1995). Monoclonal immunoglobulin A antibody directed against serotype-specific epitope of Shigella flexneri lipopolysaccharide protects against murine experimental shigellosis. J. Exp. Med. 182:769–778.PubMedCrossRefGoogle Scholar
  85. Rescigno, M., Urbano. M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J.-P., and Ricciardi-Castagnoli, P. (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2:361–367.PubMedCrossRefGoogle Scholar
  86. Reynaud, C.-A., Garcia, C., Hein, W. R., and Weill, J.-C. (1995). Hypermutation generating the sheep immunoglobulin repertoire is an antigen-independent process. Cell 80:115–125.PubMedCrossRefGoogle Scholar
  87. Salmi, M., and Jalkanen, S. (2005). Lymphocyte homing to the gut: Attraction, adhesion, and commitment. Immunol. Rev. 206:100–113.PubMedCrossRefGoogle Scholar
  88. Shikina, T., Hiroi, T., Iwatani, K., Jang, M. H., Fukuyama, S., Tamura, M., Kubo, T., Ishikawa, H., and Kiyono, H. (2004). IgA class switch occurs in the organized nasopharynx- and gut-associated lymphoid tissue, but not in the diffuse lamina propria of airways and gut. J Immunol. 172:6259–6264.PubMedGoogle Scholar
  89. Sierro, F., Pringault, E., Assman, P. S., Kraehenbuhl, J.-P., and Debard, N. (2000). Transient expression of M-cell phenotype by enterocyte-like cells of the follicle-associated epithelium of mouse Peyer’s patches. Gastroenterology 119:734–743.PubMedCrossRefGoogle Scholar
  90. Simmons, D. A., and Romanowska, E. (1987). Structure and biology of Shigella flexneri O antigens. J. Med. Microbiol. 23:289–302.PubMedCrossRefGoogle Scholar
  91. Smith, M. W. (1985). Selective expression of brush border hydrolases by mouse Peyer’s patch and jejunal villus enterocytes. J. Cell. Physiol. 124:219–225.PubMedCrossRefGoogle Scholar
  92. Spencer, J., Finn, T., and Isaacson, P. G. (1986a) Human Peyer’s patches: An immunohistochemical study. Gut 27:405–410.PubMedCrossRefGoogle Scholar
  93. Spencer, J., MacDonald, T. T., Finn, T., and Isaacson, P. G. (1986b). The development of gut associated lymphoid tissue in the terminal ileum of fetal human intestine. Clin. Exp. Immunol. 64:536–543.PubMedGoogle Scholar
  94. Spencer, J., MacDonald. T. T., and Isaacson. P. G. (1987). Heterogeneity of non-lymphoid cells expressing HLA-D region antigens in human fetal gut. Clin. Exp. Immunol. 67:415–424.PubMedGoogle Scholar
  95. Tanaka, Y., Imai, T., Baba, M., Ishikawa, I., Uehira, M., Nomiyama, H., and Yoshie, O. (1999). Selective expression of liver and activation-regulated chemokine (LARC) in intestinal epithelium in mice and humans. Eur. J. Immunol. 29:633–642.PubMedCrossRefGoogle Scholar
  96. Tangye, S. G., Ferguson, A., Avery, D. T., Ma, C. S., and Hodgkin P. D. (2002). Isotype switching by human B cells is division-associated and regulated by cytokines. Isotype switching by human B cells is division-associated and regulated by cytokines. J. Immunol. 169:4298–4306.PubMedGoogle Scholar
  97. Thurnheer, M. C., Zuercher, A. W., Cebra, J. J., and Bos, N. A. (2003). B1 cells contribute to serum IgM, but not to intestinal IgA, production in gnotobiotic Ig allotype chimeric mice. J. Immunol. 170:4564–4571.PubMedGoogle Scholar
  98. Viau, M., and Zouali, M. (2005). B-lymphocytes, innate immunity, and autoimmunity. Clin. Immunol. 114:17–26.PubMedCrossRefGoogle Scholar
  99. Wijburg, O. L. C., Uren, T. K., Simpfendorfer, K., Johansen, F.-E., Brandtzaeg, P., and Strugnell, R.A. (2006). Innate secretory antibodies protect against natural Salmonella typhimurium infection. J. Exp. Med. 203:21–26.PubMedCrossRefGoogle Scholar
  100. Xu-Amano, J., Kiyono, H., Jackson, R. J., Staats, H. F., Fujihashi, K., Burrows, P. D., Elson, C. O., Pillai, S., and McGhee, J. R. (1993). Helper T cell subsets for immunoglobulin A responses: Oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J. Exp. Med. 178:1309–1320.PubMedCrossRefGoogle Scholar
  101. Yamanaka, T., Helgeland, L., Farstad, I. N., Fukushima, H., Midtvedt, T., and Brandtzaeg, P. (2003). Microbial colonization drives lymphocyte accumulation and differentiation in the follicle-associated epithelium of Peyer’s patches. J. Immunol. 170:816–822.PubMedGoogle Scholar
  102. Yamanaka, T., Straumfors, A., Morton, H., Fausa, O., Brandtzaeg, P., and Farstad, I. N. (2001). M cell pockets of human Peyer’s patches are specialized extensions of germinal centers. Eur. J. Immunol. 31:107–117.PubMedCrossRefGoogle Scholar
  103. Zan, H., Cerutti, A., Dramitinos, P., Schaffer, A., and Casali, P. (1998). CD40 engagement triggers switching to IgA1 and IgA2 in human B cells through induction of endogenous TGF-e: Evidence for TGF-: but not IL-10-dependent direct SµµSS and sequential SµµSS, S, SS DNA recombination. J. Immunol. 161:5217–5225.PubMedGoogle Scholar
  104. Zhao, X., Sato, A., Dela Cruz, C. S., Linehan, M., Luegering, A., Kucharzik, T., Shirakawa A. K., Marquez, G., Farber, J. M., Williams, I., and Iwasaki, A. (2003). CCL9 is secreted by the follicle-associated epithelium and recruits dome region Peyer’s patch CD11b+ dendritic cells. J. Immunol. 171:2797–2803.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Jo Spencer
    • 1
  • Laurent Boursier
    • 1
  • Jonathan D. Edgeworth
    • 2
  1. 1.Department of ImmunobiologyKings College London School of MedicineUK
  2. 2.Department of Nephrology & TransplantationKings College London School of MedicineUK

Personalised recommendations