Isolated lymphoid follicles are dynamic reservoirs for the induction of intestinal IgA

Frontiers in Immunology

Volumn 3, Issue MAY, 2012, Pages 1-7

  Knoop, Kathryn A ^a   Newberry, Rodney D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gut associated lymphoid t issue; IgA; Intestine; Isolated lymphoid follicles

Indexed keywords

EID: 84866689362     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00084     Document Type: Article

References (76)

1. Ansel, K. M., Ngo, V. N., Hyman, P. L., Luther, S. A., Forster, R., Sedgwick, J. D., Browning, J. L., Lipp, M., and Cyster, J. G. (2000). A chemokine- driven positive feedback loop orga- nizes lymphoid follicles. Nature 406, 309-314.
2. Bastlein, C., Burlefinger, R., Holzberg, E., Voeth, C., Garbrecht, M., and Ottenjann, R. (1988). Common variable immunode- ficiency syndrome and nodular lymphoid hyperplasia in the small intestine. Endoscopy 20, 272-275.
3. Bellanti, J. A., Zeligs, B. J., Malka-Rais, J., and Sabra, A. (2003). Abnormal- ities of Th1 function in non-IgE food allergy, celiac disease, and ileal lymphonodular hyperplasia: a new relationship? Ann. Allergy Asthma Immunol. 90, 84-89.
4. Bergqvist, P., Gardby, E., Stensson, A., Bemark, M., and Lycke, N. Y. (2006). Gut IgA class switch recombination in the absence of CD40 does not occur in the lamina propria and is independent of germinal centers. J. Immunol. 177, 7772-7783.
5. 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.
6. Bouskra, D., Brezillon, C., Berard, M., Werts, C., Varona, R., Boneca, I. G., and Eberl, G. (2008). Lymphoid tissue genesis induced by com- mensals through NOD1 regulates intestinal homeostasis. Nature 456, 507-510.
7. Carroccio, A., Iacono, G., Di Prima, L., Ravelli, A., Pirrone, G., Cefalù, A. B., Florena, A. M., Rini, G. B., and Di Fede, G. (2009). Food hypersensitiv- ity as a cause of rectal bleeding in adults. Clin. Gastroenterol. Hepatol. 7, 120-122.
8. Castigli, E., Scott, S., Dedeoglu, F., Bryce, P., Jabara, H., Bhan, A. K., Mizoguchi, E., and Geha, R. S. (2004). Impaired IgA class switching in APRIL-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 101, 3903-3908.
9. Cerutti, A., and Rescigno, M. (2008). The biology of intesti- nal immunoglobulin A responses. Immunity 28, 740-750.
10. Coffman, R. L., Lebman, D. A., and Shrader, B. (1989). Transforming growth factor beta specifically enhances IgA production by lipopolysaccharide-stimulated
11. Conte, M. P., Schippa, S., Zamboni, I., Penta, M., Chiarini, F., Seganti, L., Osborn, J., Falconieri, P., Bor- relli, O., and Cucchiara, S. (2006). Gut-associated bacterial microbiota in paediatric patients with inflam- matory bowel disease. Gut 55, 1760-1767.
12. Cupedo, T., Vondenhoff, M. F., Heere- grave, E. J., De Weerd, A. E., Jansen, W., Jackson, D. G., Kraal, G., and Mebius, R. E. (2004). Presumptive lymph node organiz- ers are differentially represented in developing mesenteric and peripheral nodes. J. Immunol. 173, 2968-2975.
13. DeTogni, P., Goellner, J., Ruddle, N. H., Streeter, P. R., Fick, A., Mariathasan, S., Smith, S. C., Carlson, R., Shornick, L. P., Strauss-Schoenberger, J., Russell, J. H., Karr, R., and Chap- lin, D. D. (1994). Abnormal develop- ment of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264, 703-707.
14. Fagarasan, S. (2006). Intestinal IgA syn- thesis: a primitive form of adaptive immunity that regulates microbial communities in the gut. Curr. Top. Microbiol. Immunol. 308, 137-153.
15. Fagarasan, S., Kawamoto, S., Kanagawa, O., and Suzuki, K. (2010). Adaptive immune regulation in the gut: T cell- dependent and T cell-independent IgA synthesis. Annu. Rev. Immunol. 28, 243-273.
16. 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.
17. Fink, L. N., and Frøkiær, H. (2008). Dendritic cells from Peyer's patches and mesenteric lymph nodes differ from spleen dendritic cells in their response to commensal gut bacteria. Scand. J. Immunol. 68, 270-279.
18. Garside,P.,Millington,O.,and Smith,K. M. (2004). The anatomy of mucosal immune responses. Ann. N. Y. Acad. Sci. 1029, 9-15.
19. Gebert, A., Rothkotter, H. J., and Pabst, R. (1996). M cells in Peyer's patches of the intestine. Int. Rev. Cytol. 167, 91-159.
20. Gunn, M. D., Ngo, V. N., Ansel, K. M., Ekland, E. H., Cyster, J. G., and Williams, L. T. (1998). A B- cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 391, 799-803.
21. 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 folli- cles on the antimesenteric wall of the mouse small intestine. J. Immunol. 168, 57-64.
22. Hamilton, S. R., Keren, D. F., Yardley, J. H., and Brown, G. (1981). No impairment of local intesti- nal immune response to keyhole limpet haemocyanin in the absence of Peyer's patches. Immunology 42, 431-435.
23. Hashizume, T., Momoi, F., Kurita-Ochiai, T., Kaminogawa, S., Hosono, A., Kataoka, K., Shinozaki- Kuwahara, N., Kweon, M. N., and Yamamoto, M. (2007). Isolated lym- phoid follicles are not IgA inductive sites for recombinant Salmonella. Biochem. Biophys. Res. Commun. 360, 388-393.
24. Hashizume, T., Togawa, A., Nochi, T., Igarashi, O., Kweon, M. N., Kiyono, H., and Yamamoto, M. (2008). Peyer's patches are required for intestinal immunoglobulin A responses to Salmonella. Infect. Immun. 76, 927-934.
25. Honda, K., Nakano, H., Yoshida, H., Nishikawa, S., Rennert, P. D., Ikuta, K., Tamechika, M., Yamaguchi, K., Fukumoto, T., Chiba, T., and Nishikawa, S. I. (2001). Molecular basis for hematopoi- etic/mesenchymal interaction dur- ing initiation of peyer's patch organogenesis. J. Exp. Med. 193, 621-630.
26. Hu, S., Yang, K., Yang, J., Li, M., and Xiong, N. (2011). Critical roles of chemokine receptor CCR10 in regulating memory IgA responses in intestines. Proc. Natl. Acad. Sci. U.S.A. 108, E1035-E1044.
27. 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.
28. Iwasaki, A., and Kelsall, B. L. (2000). Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and sec- ondary lymphoid organ chemokine. J. Exp. Med. 191, 1381-1394.
29. Kanamori, Y., Ishimaru, K., Nanno, M., Maki, K., Ikuta, K., Nariuchi, H., and Ishikawa, H. (1996). Iden- tification of novel lymphoid tis- sues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic prog- enitors develop. J. Exp. Med. 184, 1449-1459.
30. Kiss, E. A., Vonarbourg, C., Kopfmann, S., Hobeika, E., Finke, D., Esser, C., and Diefenbach, A. (2011). Natural aryl hydrocarbon receptor ligands control organogenesis of intesti- nal lymphoid follicles. Science 334, 1561-1565.
31. Knoop, K. A., Butler, B. R., Kumar, N., Newberry, R. D., and Williams, I. R. (2011). Distinct developmental requirements for isolated lymphoid follicle formation in the small and large intestine RANKL is essential only in the small intestine. Am. J. Pathol. 179, 1861-1871.
32. Knoop, K. A., Kumar, N., Butler, B. R., Sakthivel, S. K., Taylor, R. T., Nochi, T., Akiba, H., Yagita, H., Kiyono, H., and Williams, I. R. (2009). RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J. Immunol. 183, 5738-5747.
33. Kokkonen, J., Holm, K., Karttunen, T. J., and Maki, M. (2000). Children with untreated food allergy express a rela- tive increment in the density of duo- denal gammadelta+ T cells. Scand. J. Gastroenterol. 35, 1137-1142.
34. Kokkonen, J., Karttunen, T. J., and Niinimaki, A. (1999). Lymphonodular hyperplasia as a sign of food allergy in children. J. Pediatr. Gastroenterol. Nutr. 29, 57-62.
35. Kokkonen, J., Tikkanen, S., Karttunen, T. J., and Savilahti, E. (2002). A similar high level of immunoglobu- lin A and immunoglobulin G class milk antibodies and increment of local lymphoid tissue on the duo- denal mucosa in subjects with cow's milk allergy and recurrent abdomi- nal pains. Pediatr. Allergy Immunol. 13, 129-136.
36. Krauss, E., Konturek, P., Maiss, J., Kressel, J., Schulz, U., Hahn, E. G., Neurath, M. F., and Raithel, M. (2010). Clinical significance of lym- phoid hyperplasia of the lower gas- trointestinal tract. Endoscopy 42, 334-337.
37. Laufer, I., and deSa, D. (1978). Lym- phoid follicular pattern: a normal feature of the pediatric colon. AJR Am.J.Roentgenol.130, 51-55.
38. Lee, J. S., Cella, M., Mcdonald, K. G., Garlanda, C., Kennedy, G. D., Nukaya, M., Mantovani, A., Kopan, R., Bradfield, C. A., Newberry, R. D., and Colonna,M. (2011). AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and inde- pendent of Notch. Nat. Immunol. 13, 144-151.
39. Longerich, S., Basu, U.,Alt, F., and Storb, U. (2006). AID in somatic hyper- mutation and class switch recom- bination. Curr. Opin. Immunol. 18, 164-174.
40. Lorenz, R. G., Chaplin, D. D., Mcdonald, K. G., Mcdonough, J. S., and Newberry, R. D. (2003). Isolated lym- phoid follicle formation is inducible and dependent upon lymphotoxin- sufficient B lymphocytes, lympho- toxin ß receptor, and TNF recep- tor I function. J. Immunol. 170, 5475-5482.
41. Lorenz, R. G., and Newberry, R. D. (2004). Isolated lymphoid follicles can function as sites for induction of mucosal immune responses. Ann. N. Y. Acad. Sci. 1029, 44-57.
42. MacLennan, I. C. (1994). Germinal centers. Annu. Rev. Immunol. 12, 117-139.
43. Macpherson, A. J. (2006). IgA adap- tation to the presence of com- mensal bacteria in the intestine. Curr. Top. Microbiol. Immunol. 308, 117-136.
44. Macpherson, A. J., Gatto, D., Sainsbury, E., Harriman, G. R., Hengartner, H., and Zinkernagel, R. M. (2000). A primitive T cell-independent mech- anism of intestinal mucosal IgA responses to commensal bacteria. Science 288, 2222-2226.
45. Macpherson, A. J., Mccoy, K. D., Johansen, F. E., and Brandtzaeg, P. (2008). The immune geography of IgA induction and function. Mucosal Immunol. 1, 11-22.
46. Macpherson, A. J., and Uhr, T. (2004). Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303, 1662-1665.
47. Maczulak,A. E.,Wolin, M. J., and Miller, T. L. (1989). Increase in colonic methanogens and total anaerobes in aging rats. Appl. Environ. Microbiol. 55, 2468-2473.
48. Marchesi, F., Martin, A. P., Thirunarayanan, N., Devany, E., Mayer, L., Grisotto, M. G., Furtado, G. C., and Lira, S. A. (2009). CXCL13 expression in the gut promotes accumulation of IL-22-producing lymphoid tissue- inducer cells, and formation of isolated lymphoid follicles. Mucosal Immunol. 2, 486-494.
49. Massacand, J. C., Kaiser, P., Ernst, B., Tardivel, A., Burki, K., Schneider, P., and Harris, N. L. (2008). Intesti- nal bacteria condition dendritic cells to promote IgA production. PLoS ONE 3, e2588. doi:10.1371/jour- nal.pone.0002588
50. McDonald, K. G., Leach, M. R., Huang, C., Wang, C., and Newberry, R. D. (2011). Aging impacts isolated lymphoid follicle development and function. Immun. Ageing 8, 1.
51. McDonald, K. G., Mcdonough, J. S., Dieckgraefe, B. K., and Newberry, R. D. (2010). Dendritic cells pro- duce CXCL13 and participate in the development of murine small intes- tine lymphoid tissues. Am. J. Pathol. 176, 2367-2377.
52. Misra, S. P., Misra, V., Dwivedi, M., and Singh, P. A. (1998). CASE REPORT: Helicobacter pyloriinduced lymphonodular hyperplasia: a new cause of gastric outlet obstruction. J. Gastroenterol. Hepatol. 13, 1191-1194.
53. 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.
54. Ohashi, Y., Hiraguchi, M., Sunaba, C., Tanaka, C., Fujisawa, T., and Ushida, K. (2010). Colonization of seg- mented filamentous bacteria and its interaction with the luminal IgA level in conventional mice. Anaerobe 16, 543-546.
55. O'Leary, A. D., and Sweeney, E. C. (1986). Lymphoglandular com- plexes of the colon: structure and distribution. Histopathology 10, 267-283.
56. Owen, R. L., Piazza, A. J., and Ermak, T. H. (1991). Ultrastructural and cytoarchitectural features of lym- phoreticular organs in the colon and rectum of adult BALB/c mice. Am. J. Anat. 190, 10-18.
57. Pabst, O., Herbrand, H., Friedrichsen, M., Velaga, S., Dorsch, M., Berhardt, G., Worbs, T., Macpherson, A. J., and Forster, R. (2006). Adaptation of solitary intestinal lymphoid tis- sue in response to microbiota and chemokine receptor CCR7 signal- ing. J. Immunol. 177, 6824-6832.
58. Rennert, P. D., Browning, J. L., Mebius, R., Mackay, F., and Hochman, P. S. (1996). Surface lymphotoxin a/ß complex is required for the development of peripheral lym- phoid organs. J. Exp. Med. 184, 1999-2006.
59. Scharenberg, A. M., Hannibal, M. C., Torgerson,T., Ochs, H.D., and Rawl- ings, D. J. (1993). "Common vari- able immune deficiency overview," in GeneReviews™ [Internet], eds R. A. Pagon, T. D. Bird, C. R. Dolan, K. Stephens, and N. P. Adam (Seattle: University of Washington).
60. Schmucker, D. L., and Daniels, C. K. (1986). Aging, gastrointestinal infec- tions, and mucosal immunity. J. Am. Geriatr. Soc. 34, 377-384.
61. Schmucker, D. L., Heyworth, M. F., Owen, R. L., and Daniels, C. K. (1996). Impact of aging on gastrointestinal mucosal immunity. Dig. Dis. Sci. 41, 1183-1193.
62. Schuurman, H. J., Kuper, C. F., and Vos, J. G. (1994). Histopathology of the immune system as a tool to assess immunotoxicity. Toxicology 86, 187-212.
63. Shaoul, R., Eliakim, R., Tamir, A., and Karban, A. (2006). Ileal lymphon- odular hyperplasia is not associ- ated with NOD2/CARD15 muta- tions. J. Pediatr. Gastroenterol. Nutr. 43, 30-34.
64. Spencer, J., Barone, F., and Dunn- Walters, D. (2009). Generation of Immunoglobulin diversity in human gut-associated lymphoid tis- sue. Semin. Immunol. 21, 139-146.
65. Suzuki, K., Meek, B., Doi, Y., Muramatsu, M., Chiba, T., Honjo, T., and Fagarasan, S. (2004). Aberrant expansion of segmented filamen- tous bacteria in IgA-deficient gut. Proc. Natl. Acad. Sci. U.S.A. 101, 1981-1986.
66. Taylor, R. T., Lugering, A., Newell, K. A., and Williams, I. R. (2004). Intesti- nal cryptopatch formation in mice requires lymphotoxin a and the lym- photoxin ß receptor. J. Immunol. 173, 7183-7189.
67. Taylor, R. T., Patel, S. R., Lin, E., Butler, B. R., Lake, J. G., New- berry, R. D., and Williams, I. R. (2007). Lymphotoxin-independent expression of TNF-related activation-induced cytokine by stromal cells in cryptopatches, isolated lymphoid follicles, and Peyer's patches. J. Immunol. 178, 5659-5667.
68. 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, pro- duction in gnotobiotic Ig allotype chimeric mice. J. Immunol. 170, 4564-4571.
69. Tsuji, M., Suzuki, K., Kitamura, H., Maruya, M., Kinoshita, K., Ivanov, Ii, Itoh, K., Littman, D. R., and Fagarasan, S. (2008). Requirement for lymphoid tissueinducer cells in isolated follicle formation and T cellindependent immunoglobu- linA generation in the gut. Immunity 29, 261-271.
70. van de Pavert, S. A., Olivier, B. J., Goverse, G., Vondenhoff, M. F., Greuter, M., Beke, P., Kusser, K.,Höpken, U. E., Lipp, M., Niederreither, K., Blomhoff, R., Sitnik, K., Agace, W. W., Randall, T. D., De Jonge, W. J., and Mebius, R. E. (2009). Chemokine CXCL13 is essential for lymph node initia- tion and is induced by retinoic acid and neuronal stimulation. Nat. Immunol. 10, 1193-1199.
71. Velaga, S., Herbrand, H., Friedrich- sen, M., Jiong, T., Dorsch, M., Hoffmann, M. W., Forster, R., and Pabst, O. (2009). Chemokine recep- tor CXCR5 supports solitary intesti- nal lymphoid tissue formation,B cell homing, and induction of intesti- nal IgA responses. J. Immunol. 182, 2610-2619.
72. Wang, C., Mcdonald, K. G., Mcdonough, J. S., and Newberry, R. D. (2006). Murine isolated lymphoid follicles contain follicular B lympho- cytes with a mucosal phenotype. Am. J. Physiol. Gastrointest. Liver Physiol. 291, G595-G604.
73. Webster, A. D. (1973). Nodular lym- phoid hyperplasia with hypogam- maglobulinaemia. Proc. R. Soc. Med. 66, 1127-1128.
74. Webster, A. D., Kenwright, S., Ballard, J., Shiner, M., Slavin, G., Levi, A. J., Loewi, G., and Asherson, G. L. (1977). Nodular lymphoid hyperplasia of the bowel in pri- mary hypogammaglobulinaemia: study of in vivo and in vitro lymphocyte function. Gut 18, 364-372.
75. Wei, M., Shinkura, R., Doi, Y., Maruya, M., Fagarasan, S., and Honjo, T. (2011). Mice carrying a knock- in mutation of Aicda resulting inadefectinsomatichyper- mutation have impaired gut homeostasis and compromised mucosal defense. Nat. Immunol. 12, 264-270.
76. Yamamoto, M., Rennert, P., Mcghee, J. R., Kweon, M. N., Yamamoto, S., Dohi, T., Otake, S., Bluethmann, H., Fujihashi, K., and Kiyono, H. (2000). Alternate mucosal immune system: organized Peyer's patches are not required for IgA responses in the gas- trointestinal tract. J. Immunol. 164, 5184-5191.