The human intestinal igA response; burning questions

Frontiers in Immunology

Volumn 3, Issue MAY, 2012, Pages

  Spencer, Jo ^a   Klavinskis, Linda S ^a   Fraser, Louise D ^a  

^a ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

Gut associated lymphoid tissue; Human; Iga

Indexed keywords

EID: 84870252859     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00108     Document Type: Review

References (100)

1. Barone, F., Patel, P., Sanderson, J., and Spencer, J. (2009). Gut-associated lymphoid tissue contains the mol-ecular machinery to support T-cell dependent and T-cell-independent class switch recombination. Mucosal Immunol. 2, 495-503.
2. Barone, F., and Spencer, J. (2010). Gut-associated lymphoid tissue contains the molecular machinery to support T-cell-dependent and T-cell-independent class switch recombi-nation. Mucosal Immunol. 3, 94-95.
3. Barone, F., Vossenkamper, A., Bour-sier, L., Su, W., Watson, A., John, S., Dunn-Walters, D. K., Fields, P., Wijetilleka, S., Edgeworth, J. D., and Spencer, J. (2011). IgA-producing plasma cells originate from germi-nal centers that are induced by B-cell receptor engagement in humans. Gastroenterology 140, 947-956.
4. Belnoue, E., Tougne, C., Rochat, A. F., Lambert, P. H., Pinschewer, D. D., and Siegrist, C. A. (2012). Hom-ing and adhesion patterns deter-mine the cellular composition of the bone marrow plasma cell niche. J. Immunol. 188, 1283-1291.
5. Benckert, J., Schmolka, N., Kreschel, C., Zoller, M. J., Sturm, A.,Wiedenmann, B., and Wardemann, H. (2011). The majority of intesti-nal IgA+ and IgG+ plasmablasts in the human gut are antigen-specific. J. Clin. Invest. 121, 1946-1955.
6. Bergqvist, P., Gardby, E., Stensson, A., Bemark, M., and Lycke, N. Y. (2006). Gut IgA class switch recom-bination in the absence of CD40 does not occur in the lamina pro-pria and is independent of ger-minal centers. J. Immunol. 177, 7772-7783.
7. Bergqvist, P., Stensson, A., Lycke, N. Y., and Bemark, M. (2010). T cell-independent IgA class switch recom-bination is restricted to the GALT and occurs prior to manifest ger-minal center formation. J. Immunol. 184, 3545-3553.
8. Berkowska, M. A., Driessen, G. J., Bikos, V., Grosserichter-Wagener, C., Stam-atopoulos, K., Cerutti, A., He, B., Biermann, K., Lange, J. F., van der Burg, M., van Dongen, J. J., and van Zelm, M. C. (2011). Human mem-ory B cells originate from three dis-tinct germinal center-dependent and -independent maturation pathways. Blood 118, 2150-2158.
9. Blutt, S., and Conner, M. (2010). Viral induced T cell independent Bcell activation. J. Immunol. 184, 38.13.
10. Blutt, S. E., Warfield, K. L., Estes, M. K., and Conner, M. E. (2008). Differen-tial requirements for T cells in virus-like particle-and rotavirus-induced protective immunity. J. Virol. 82, 3135-3138.
11. Bourke, E., Bosisio, D., Golay, J., Polentarutti, N., and Mantovani, A. (2003). The toll-like receptor reper-toire of human B lymphocytes: inducible and selective expression of TLR9 and TLR10 in normal and transformed cells. Blood 102, 956-963.
12. Boursier, L., Dunn-Walters, D. K., and Spencer, J. (1999). Characteristics of IgVH genes used by human intesti-nal plasma cells from childhood. Immunology 97, 558-564.
13. Boursier, L., Gordon, J. N., Thiag-amoorthy, S., Edgeworth, J. D., and Spencer, J. (2005). Human intesti-nal IgA response is generated in the organized gut-associated lymphoid tissue but not in the lamina propria. Gastroenterology 128, 1879-1889.
14. Bouskra, D., Brézillon, C., Bérard, M., Werts, C., Varona, R., Boneca, I. G., and Eberl, G. (2008). Lymphoid tis-sue genesis induced by commensals through NOD1 regulates intesti-nal homeostasis. Nature 456, 507-510.
15. Brandtzaeg, P. (2009). Mucosal immunity: induction, dissemination, and effector functions. Scand. J. Immunol. 70, 505-515.
16. Brandtzaeg, P. (2010). Function of mucosa-associated lymphoid tissue in antibody formation. Immunol. Invest. 39, 303-355.
17. 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.
18. Brandtzaeg, P., and Pabst, R. (2004). Let's go mucosal: communication on slippery ground. Trends Immunol. 25, 570-577.
19. 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.
20. Cerutti, A. (2008a). Location, location, location: B-cell differentiation in the gut lamina propria. Mucosal Immunol. 1, 8-10.
21. Cerutti, A. (2008b). The regulation of IgA class switching. Nat. Rev. Immunol. 8, 421-434.
22. Cerutti, A., Cols, M., Gentile, M., Cassis, L., Barra, C. M., He, B., Puga, I., and Chen, K. (2011). Regulation of mucosal IgA responses: lessons from primary immunodeficiencies. Ann. N. Y. Acad. Sci. 1238, 132-144.
23. Chabot, S., Wagner, J. S., Farrant, S., and Neutra, M. R. (2006). TLRs regulate the gatekeeping functions of the intestinal follicleassociated epithelium. J. Immunol. 176, 4275-4283.
24. 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.
25. Cornes, J. S. (1965). Number, size, and distribution of Peyer's patches in the human small intestine: part I The development of Peyer's patches. Gut 6, 225-229.
26. Craig,V. J., Arnold, I., Gerke, C., Huynh, M. Q., Wündisch, T., Neubauer, A., Renner, C., Falkow, S., and Müller, A. (2010). Gastric MALT lymphoma B cells express polyreactive, somatically mutated immunoglobulins. Blood 115, 581-591.
27. Di Niro, R., Mesin, L., Raki, M., Zheng, N. Y., Lund-Johansen, F., Lundin, K. E., Charpilienne,A., Poncet, D., Wilson, P. C., and Sollid, L. M. (2010). Rapid generation of rotavirusspecific human monoclonal antibodies from smallintestinal mucosa. J. Immunol. 185, 5377-5383.
28. Di Niro, R., Mesin, L., Zheng, N. Y., Stamnaes, J., Morrissey, M., Lee, J. H., Huang, M., Iversen, R., du Pré, M. F., Qiao, S. W., Lundin, K. E., Wilson, P. C., and Sollid, L. M. (2012). High abundance of plasma cells secreting transglutaminase 2-specific IgA autoantibodies with limited somatic hypermutation in celiac disease intestinal lesions. Nat Med. 18, 441-445.
29. Dunn-Walters, D. K., Boursier, L., and Spencer, J. (1997). Hypermutation, diversity and dissemination of human intestinal lamina propria plasma cells. Eur. J. Immunol. 27, 2959-2964.
30. Dunn-Walters,D. K.,Hackett,M.,Boursier, L., Ciclitira, P. J., Morgan, P., Challacombe, S. J., and Spencer, J. (2000). Characteristics of human IgA and IgM genes used by plasma cells in the salivary gland resemble those used in duodenum but not those used in the spleen. J. Immunol. 164, 1595-1601.
31. 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.
32. 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.
33. 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.
34. Ferrari, S., Giliani, S., Insalaco, A., Al-Ghonaium,A.,Soresina,A. R.,Loubser, M., Avanzini, M. A., Marconi, M., Badolato, R., and Ugazio, A. G. (2001). Mutations of CD40 gene cause an autosomal recessive form of immunodeficiency with hyper IgM. Proc. Natl. Acad. Sci. U.S.A. 98, 12614-12619.
35. Franco, M. A., and Greenberg, H. B. (1997). Immunity to rotavirus in T cell deficient mice. Virology 238, 169-179.
36. Garside, P., Ingulli, E., Merica, R. R., Johnson,J. G.,Noelle,R. J.,and Jenkins, M. K. (1998). Visualization of specific B and T lymphocyte interactions in the lymph node. Science 281, 96-99.
37. Gibbons, D. L., and Spencer, J. (2011). Mouse and human intestinal immunity: same ballpark,different players; different rules, same score. Mucosal Immunol. 4, 148-157.
38. 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.
39. Greiner, A., Marx, A., Heesemann, J., Leebmann, J., Schmausser, B., and Müller-Hermelink, H. K. (1994). Idiotype identity in a MALT-type lymphoma and B cells in Helicobacter pylori associated chronic gastritis. Lab. Invest. 70, 572-578.
40. Hapfelmeier, S., Lawson, M. A., Slack, E., Kirundi, J. K., Stoel, M., Heikenwalder,M.,Cahenzli,J.,Velykoredko, Y., Balmer, M. L., Endt, K., Geuking, M. B., Curtiss, R. III, McCoy, K. D., and Macpherson, A. J. (2010). Reversible microbial colonization of germfree mice reveals the dynamics of IgA immune responses. Science 328, 1705-1709.
41. Hardenberg, G., Planelles, L., Schwarte, C. M., van Bostelen, L., Le Huong, T., Hahne,M.,and Medema,J. P. (2007). Specific TLR ligands regulate APRIL secretion by dendritic cells in a PKR-dependent manner. Eur. J. Immunol. 37, 2900-2911.
42. He,B.,Xu,W.,Santini,P.A.,Polydorides, A. D., Chiu, A., Estrella, J., Shan, M., Chadburn, A.,Villanacci,V., Plebani, A., Knowles, D. M., Rescigno, M., and Cerutti, A. (2007). Intestinal bacteria trigger T cellindependent immunoglobulin A(2) class switching by inducing epithelialcell secretion of the cytokine APRIL. Immunity 26, 812-826.
43. 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.
44. Husband,A. J.,and Gowans,J. L. (1978). The origin and antigendependent distribution of IgA-containing cells in the intestine. J. Exp. Med. 148, 1146-1160.
45. Hussell, T., Isaacson, P. G., Crabtree, J. E., Dogan, A., and Spencer, J. (1993). Immunoglobulin specificity of low grade B cell gastrointestinal lymphoma of mucosaassociated lymphoid tissue (MALT) type. Am. J. Pathol. 142, 285-292.
46. Hussell,T.,Isaacson,P. G.,Crabtree,J. E., and Spencer, J. (1996). Helicobacter pylorispecific tumourinfiltrating T cells provide contact dependent help for the growth of malignant B cells in lowgrade gastric lymphoma of mucosaassociated lymphoid tissue. J. Pathol. 178, 122-127.
47. Isaacson, P. G., and Spencer, J. (1987). Malignant lymphoma of mucosaassociated lymphoid tissue. Histopathology 11, 445-462.
48. Ishikawa, H., Saito, H., Suzuki, K., Oida, T., and Kanamori, Y. (1999). New gut associated lymphoid tissue "cryptopatches" breed murine intestinal intraepithelial T cell precursors. Immunol. Res. 20, 243-250.
49. Kaminski, D. A., and Stavnezer, J. (2004). Antibody class switching: uncoupling S region accessibility from transcription. Trends Genet. 20, 337-340.
50. Kanamori, Y., Ishimaru, K., Nanno, M., Maki, K., Ikuta, K., Nariuchi, H., and Ishikawa, H. (1996). Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of ckit+ IL-7R+ Thy1+ lymphohemopoietic progenitors develop. J. Exp. Med. 184, 1449-1459.
51. Kett, K., Baklien, K., Bakken, A., Kral, J. G., Fausa, O., and Brandtzaeg, P. (1995). Intestinal B-cell isotype response in relation to local bacterial load: evidence for immunoglobulin A subclass adaptation. Gastroenterology 109, 819-825.
52. Kett, K., and Brandtzaeg, P. (1987). Local IgA subclass alterations in ulcerative colitis and Crohn's disease of the colon. Gut 28, 1013-1021.
53. Kett, K., Brandtzaeg, P., Radl, J., and Haaijman, J. J. (1986). Different subclass distribution of IgA-producing cells in human lymphoid organs and various secretory tissues. J. Immunol. 136, 3631-3635.
54. Kroese, F. G., Butcher, E. C., Stall, A. M, and Herzenberg, L. A. (1989). A major peritoneal reservoir of precursors for intestinal IgA plasma cells. Immunol. Invest. 18, 47-58.
55. Kunkel, E. J., Campbell, J. J., Haraldsen, G., Pan, J., Boisvert, J., Roberts, A. I., Ebert, E. C., Vierra, M. A., Goodman, S. B., Genovese, M. C., Wardlaw, A. J., Greenberg, H. B., Parker, C. M., Butcher, E. C., Andrew, D. P., Agace,W. W. (2000) Lymphocyte CC chemokine receptor 9 and epithelial thymusexpressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissuespecific chemokines as an organizing principle in regional immunity. J. Exp. Med. 192, 761-767.
56. Levesque, M. C., Moody, M. A, Hwan, K-K., Marshall, D. J, Whitesides, J. F., Amos, J. D., Gurley, T. C., Allgood, S., Haynes, B. B., Vandergrift, N. A., Plonk, S., Parker, D. C., Cohen, M. S., Tomaras, G. D., Goepfert, P. A., Shaw, G. M., Schmitz, J. E., Eron, J. J., Shaheen, N. J., Hicks, C. B., Liao, H-X., Markowitz, M., Kelsoe, G., Margolis, D. M., and Haynes, B. F. (2009). Polyclonal B cell differentiation and loss of gastrointestinal tract germinal centers in the earliest stages of HIV-1 infection. PLoS Med. 6, e1000107. doi:10.1371/journal.pmed.1000107
57. Levine, M. M., Kotloff, K. L., Barry, E. M., Pasetti, M. F., and Sztein, M. B. (2007). Clinical trials of Shigella vaccines: two steps forward and one step back on a long, hard road. Nat. Rev. Microbiol. 5, 540-553.
58. Lindner, C., Wahl, B., Föhse, L., Suerbaum, S., Macpherson, A. J., Prinz, I., and Pabst, O. (2012). Age, microbiota, and T cells shape diverse individual IgA repertoires in the intestine. J. Exp. Med. 209, 365-377.
59. 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.
60. McIntyre,T. M.,Kehry,M. R.,and Snapper, C. M. (1995). Novel in vitro model for highrate IgA class switching. J. Immunol. 154, 3156-3161.
61. Medina, F., Segundo, C., Campos-Caro, A., Salcedo, I., García-Poley, A., and Brieva, J. A. (2003). Isolation, maturational level, and functional capacity of human colon lamina propria plasma cells. Gut 52, 383-389.
62. Mesin, L., Di Niro, R., Thompson, K. M., Lundin, K. E., and Sollid, L. M. (2011). Longlived plasma cells from human small intestine biopsies secrete immunoglobulins for many weeks in vitro. J. Immunol. 187, 2867-2874.
63. Mobley, H. L. (1996). The role of Helicobacter pylori urease in the pathogenesis of gastritis and peptic ulceration. Aliment. Pharmacol. Ther. 10(Suppl. 1), 57-64.
64. Moghaddami, M., Cummins, A., and Mayrhofer, G. (1998). Lymphocytefilled villi: comparison with other lymphoid aggregations in the mucosa of the human small intestine. Gastroenterology 115, 1414-1425.
65. Morteau, O., Gerard, C., Lu, B., Ghiran, S., Rits, M., Fujiwara, Y., Law, Y., Distelhorst, K., Nielsen, E. M., Hill, E. D., Kwan, R., Lazarus, N. H., Butcher, E. C., and Wilson, E. (2008). An indispensable role for the chemokine receptor CCR10 in IgA antibodysecreting cell accumulation. J. Immunol. 181, 6309-6315.
66. 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. JExp.Med.180, 111-121.
67. Niess, J. H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B. A., Vyas, J. M., Boes, M., Ploegh, H. L., Fox, J. G., Littman, D. R., and Reinecker, H. C. (2005). CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307, 254-258.
68. 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.
69. O'Leary, A. D., and Sweeney, E. C. (1986). Lymphoglandular complexes of the colon: structure and distribution. Histopathology 10, 267-283.
70. Pabst, O., Bernhardt, G., and Forster, R. (2007). The impact of cellbound antigen transport on mucosal tolerance induction. J. Leukoc. Biol. 82, 795-800.
71. Pabst,O.,and Mowat,A. M. (2012). Oral tolerance to food protein. Mucosal Immunol. doi:10.1038/mi.2012.4. [Epub ahead of print].
72. 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.
73. Passwell, J. H., Ashkenasi, S., Harlev, E., Miron, D., Ramon, R., Farzam, N., Lerner-Geva, L., Levi, Y., Chu, C., Shiloach, J., Robbins, J. B., Schneerson, R., and Israel Shigella Group. (2003). Safety and immunogenicity of Shigella sonnei-CRM9 and Shigella flexneri type 2arEPAsucc conjugate vaccines in oneto fouryear old children. Pediatr. Infect. Dis. J. 22, 701-706.
74. Phalipon, A., Costachel, C., Grandjean, C., Thuizat, A., Guerreiro, C., Tanguy, M., Nato, F., Vulliez-Le Normand, B., Bélot, F., Wright, K., Marcel-Peyre, V., Sansonetti, P. J., and Mulard, L. A. (2006). Characterization of functional oligosaccharide mimics of the Shigella flexneri serotype 2a O-antigen: implications for the development of a chemically defined glycoconjugate vaccine. J. Immunol. 176, 1686-1694.
75. Picard, C., von Bernuth, H., Ghandil, P., Chrabieh, M., Levy, O., Arkwright, P. D., McDonald, D., Geha, R. S., Takada, H., Krause, J. C., Creech, C. B., Ku, C. L., Ehl, S., Maródi, L., Al-Muhsen, S., Al-Hajjar, S., Al-Ghonaium, A., Day-Good, N. K., Holland, S. M., Gallin, J. I., Chapel, H., Speert, D. P., Rodriguez-Gallego, C., Colino, E., Garty, B. Z., Roifman, C., Hara, T., Yoshikawa, H., Nonoyama, S., Domachowske, J., Issekutz, A. C., Tang, M., Smart, J., Zitnik, S. E., Hoarau, C., Kumararatne, D. S., Thrasher, A. J., Davies, E. G., Bethune, C., Sirvent, N., de Ricaud, D., Camcioglu, Y., Vasconcelos, J., Guedes, M., Vitor, A. B., Rodrigo, C., Almazán, F., Méndez, M., Aróstegui, J. I., Alsina, L., Fortuny, C., Reichenbach, J., Verbsky, J. W., Bossuyt, X., Doffinger, R., Abel, L., Puel, A., and Casanova, J. L. (2010). Clinical features and outcome of patients with IRAK-4 and MyD88 deficiency. Medicine (Baltimore) 89, 403-425.
76. Pollard, A. J., Perrett, K. P., and Beverley, P. C. (2009). Maintaining protection against invasive bacteria with proteinpolysaccharide conjugate vaccines. Nat. Rev. Immunol. 9, 213-220.
77. Rasolofo-Razanamparany, V., Cassel-Beraud, A. M., Roux, J., Sansonetti, P. J., and Phalipon, A. (2001). Predominance of serotypespecific mucosal antibody response in Shigella flexneriinfected humans living in an area of endemicity. Infect. Immun. 69, 5230-5234.
78. Renz, H., Brandtzaeg, P., and Hornef, M. (2011). The impact of perinatal immune development on mucosal homeostasis and chronic inflammation. Nat. Rev. Immunol. 12, 9-23.
79. 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.
80. Simon, J. K., Maciel, M. Jr., Weld, E. D., Wahid, R., Pasetti, M. F., Picking, W. L., Kotloff, K. L., Levine, M. M., and Sztein, M. B. (2011a). Antigenspecific IgA B memory cell responses to Shigella antigens elicited in volunteers immunized with live attenuated Shigella flexneri 2a oral vaccine candidates. Clin. Immunol. 139, 185-192.
81. Simon, R., Tennant, S. M., Wang, J. Y., Schmidlein, P. J., Lees, A., Ernst, R. K., Pasetti, M. F., Galen, J. E., and Levine, M. M. (2011b). Salmonella enterica serovar enteritidis core O polysaccharide conjugated to H:g,m flagellin as a candidate vaccine for protection against invasive infection with S. enteritidis. Infect. Immun. 79, 4240-4249.
82. Schneider, T., Ullrich, R., and Zeitz, M. (1996). The immunologic aspects of human immunodeficiency virus infection in the gastrointestinal tract. Semin. Gastrointest. Dis. 7, 19-29.
83. Spencer, J., Barone, F., and Dunn-Walters, D. (2009). Generation of Immunoglobulin diversity in human gutassociated lymphoid tissue. Semin. Immunol. 21, 139-146.
84. Su, W., Gordon, J. N., Barone, F., Boursier, L., Turnbull, W., Mendis, S., Dunn-Walters, D. K., and Spencer, J. (2008). Lambda light chain revision in the human intestinal IgA response. J. Immunol. 181, 1264-1271.
85. Suzuki, K., and Fagarasan, S. (2009). Diverse regulatory pathways for IgA synthesis in the gut. Mucosal Immunol. 2, 468-471.
86. Svenson, S. B., Nurminen, M., and Lindberg, A. A. (1979). Artificial Salmonella vaccines: O-antigenic oligosaccharideprotein conjugates induce protection against infection with Salmonella typhimurium. Infect. Immun. 1925, 863-872.
87. Tsuji, M., Suzuki, K., Kitamura, H., Maruya, M., Kinoshita, K., Ivanov, I. I., Itoh, K., Littman, D. R., and Fagarasan, S. (2008). Requirement for lymphoid tissueinducer cells in isolated follicle formation and T cellindependent immunoglobulinA generation in the gut. Immunity 29, 261-271.
88. Turner,J. R. (2000).'Putting the squeeze' on the tight junction: understanding cytoskeletal regulation. Semin. Cell Dev. Biol. 11,301-308.
89. VanCott, J. L., McNeal, M. M., Flint, J., Bailey, S. A., Choi, A. H., and Ward, R. L. (2001). Role for T cellindependent B cell activity in the resolution of primary rotavirus infection in mice. Eur. J. Immunol. 31, 3380-3387.
90. Wagner, M., Poeck, H., Jahrsdoerfer, B., Rothenfusser, S., Prell, D., Bohle, B., Tuma, E., Giese, T., Ellwart, J. W., Endres,S.,and Hartmann,G. (2004). IL-12p70-dependent Th1 induction by human B cells requires combined activation with CD40 ligand and CpG DNA. J. Immunol. 172, 954-963.
91. Wei, M., Shinkura, R., Doi, Y., Maruya, M., Fagarasan, S., and Honjo, T. (2011). Mice carrying a knockin mutation of Aicda resulting inadefectinsomatichypermutation have impaired gut homeostasis and compromised mucosal defense. Nat. Immunol. 12, 264-270.
92. Weitkamp, J. H., Kallewaard, N. L., Bowen, A. L., Lafleur, B. J., Greenberg, H. B., and Crowe, J. E. Jr. (2005). VH1-46 is the dominant immunoglobulin heavy chain gene segment in rotavirusspecific memory B cells expressing the intestinal homing receptor alpha4beta7. J. Immunol. 174, 3454-3460.
93. Weitkamp, J. H., Lafleur, B. J., and Crowe, J. E. Jr. (2006). Rotavirusspecific CD5+ B cells in young children exhibit a distinct antibody repertoire compared with CD5-B cells. Hum. Immunol. 67, 33-42.
94. Wijburg, O. L, 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.
95. Williams, G. T. (1992). "The stomach: developmental and inflammatory conditions,"in Oxford Text Book of Pathology,eds J. O.'D. McGee,P. G. Isaacson, and N. A. Wright (Oxford, New York, Tokyo: Oxford University Press).
96. Wotherspoon, A. C., Doglioni, C., Diss, T. C., Pan, L., Moschini, A., de Boni, M., and Isaacson, P. G. (1993). Regression of primary lowgrade B-cell gastric lymphoma of mucosaassociated lymphoid tissue type after eradication of Helicobacter pylori. Lancet 342, 575-577.
97. Wotherspoon, A. C., Ortiz-Hidalgo, C., Falzon, M. R., and Isaacson, P. G. (1991). Helicobacter pyloriassociated gastritis and primary B-cell gastric lymphoma. Lancet 338, 1175-1176.
98. Xu, W., Santini, P. A., Matthews, A. J., Chiu, A., Plebani, A., He, B., Chen, K., and Cerutti, A. (2008). Viral doublestranded RNA triggers Ig class switching by activating upper respiratory mucosa B cells through an innate TLR3 pathway involving BAFF. J. Immunol. 181, 276-287.
99. Yuvaraj, S., Dijkstra, G., Burgerhof, J. G., Dammers, P. M., Stoel, M., Visser, A., Kroese, F. G., and Bos, N. A. (2009). Evidence for local expansion of IgA plasma cell precursors in human ileum. J. Immunol. 183, 4871-4878.
100. 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-beta: evidence for TGF-beta but not IL-10-dependent direct S mu→S alpha and sequential S mu→S gamma, S gamma→S alpha DNA recombination. J. Immunol. 161, 5217-5225.