Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 6189-6200

  Katakai, Tomoya ^a,c,f   Suto, Hidenori ^a,b   Sugai, Manabu ^a,c   Gonda, Hiroyuki ^a,c   Togawa, Atsushi ^d   Suematsu, Sachiko ^e   Ebisuno, Yukihiko ^f   Katagiri, Koko ^f   Kinashi, Tatsuo ^f   Shimizu, Akira ^a,b,c  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY HOSPITAL   (Japan)

^d RIKEN Center for Biosystems Dynamics Research   (Japan)

^e NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^f KANSAI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL13 CHEMOKINE; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOTOXIN BETA RECEPTOR; MUCOSAL ADDRESSIN CELL ADHESION MOLECULE 1; RAG2 PROTEIN; SECONDARY LYMPHOID TISSUE CHEMOKINE; VASCULAR CELL ADHESION MOLECULE 1; NF KAPPA B KINASE; NF-KAPPA B KINASE; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL COMPOSITION; CELL FUNCTION; CELL LINE; CELL MATURATION; CELL MIGRATION; CELL POPULATION; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IN VITRO STUDY; LYMPH NODE; LYMPHOID ORGAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETICULUM CELL; STROMA CELL; AGING; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL MOTION; CYTOLOGY; FIBROBLAST; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOID TISSUE; MESODERM; METABOLISM; MOUSE MUTANT; NEWBORN; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

AGING; ANIMALS; ANIMALS, NEWBORN; B-LYMPHOCYTES; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL13; FIBROBLASTS; HUMANS; LYMPHOID TISSUE; LYMPHOTOXIN BETA RECEPTOR; MESODERM; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STROMAL CELLS;

EID: 58749101541     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.6189     Document Type: Article

References (57)

1. Fu, Y. X., and D. D. Chaplin. 1999. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17: 399-433. (Pubitemid 29241130)
2. Gretz, J. E., A. O. Anderson, and S. Shaw. 1997. Cords, channels, corridors, and conduits: critical architectural elements facilitating cell interactions in the lymph node cortex. Immunol. Rev. 156: 11-24.
3. Katakai, T., T. Hara, J. H. Lee, H. Gonda, M. Sugai, and A. Shimizu. 2004. A novel reticular stromal structure in lymph node cortex: an immuno-platform for interactions among dendritic cells, T cells, and B cells. Int. Immunol. 16: 1133-1142. (Pubitemid 39136730)
4. Katakai, T., T. Hara, M. Sugai, H. Gonda, and A. Shimizu. 2004. Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J. Exp. Med. 200: 783-795. (Pubitemid 39299464)
5. Gretz, J. E., C. C. Norbury, A. O. Anderson, A. E. Proudfoot, and S. Shaw. 2000. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J. Exp. Med. 192: 1425-1440.
6. Sixt, M., N. Kanazawa, M. Selg, T. Samson, G. Roos, D. P. Reinhardt, R. Pabst, M. B. Lutz, and L. Sorokin. 2005. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 22: 19-29. (Pubitemid 40143448)
7. Cyster, J. G. 1999. Chemokines and cell migration in secondary lymphoid organs. Science 286: 2098-2102. (Pubitemid 129516279)
8. Cyster, J. G., K. M. Ansel, K. Reif, E. H. Ekland, P. L. Hyman, H. L. Tang, S. A. Luther, and V. N. Ngo. 2000. Follicular stromal cells and lymphocyte homing to follicles. Immunol. Rev. 176: 181-193.
9. Luther, S. A., H. L. Tang, P. L. Hyman, A. G. Farr, and J. G. Cyster. 2000. Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc. Natl. Acad. Sci. USA 97: 12694-12699.
10. Nishikawa, S., K. Honda, P. Vieira, and H. Yoshida. 2003. Organogenesis of peripheral lymphoid organs. Immunol. Rev. 195: 72-80.
11. Mebius, R. E. 2003. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3: 292-303.
12. Kiyono, H., and S. Fukuyama. 2004. NALT- versus Peyer's-patch-mediated mucosal immunity. Nat. Rev. Immunol. 4: 699-710. (Pubitemid 39223076)
13. Eberl, G. 2005. Inducible lymphoid tissues in the adult gut: recapitulation of a fetal developmental pathway? Nat. Rev. Immunol. 5: 413-420. (Pubitemid 40685990)
14. Mebius, R. E., and G. Kraal. 2005. Structure and function of the spleen. Nat. Rev. Immunol. 5: 606-616.
15. + cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 7: 493-504.
16. - cells in the embryonic intestine induces the organizing center of Peyer's patches. Int. Immunol. 11: 643-655.
17. Honda, K., H. Nakano, H. Yoshida, S. Nishikawa, P. Rennert, K. Ikuta, M. Tamechika, K. Yamaguchi, T. Fukumoto, T. Chiba, and S. I. Nishikawa. 2001. Molecular basis for hematopoietic/mesenchymal interaction during initiation of Peyer's patch organogenesis. J. Exp. Med. 193: 621-630. (Pubitemid 32539558)
18. 1 integrin activation by CXCR5. Immunity 17: 363-373.
19. Weih, F., and J. Caamano. 2003. Regulation of secondary lymphoid organ development by the nuclear factor-κB signal transduction pathway. Immunol. Rev. 195: 91-105. (Pubitemid 37153456)
20. Yokota, Y., A. Mansouri, S. Mori, S. Sugawara, S. Adachi, S. Nishikawa, and P. Gruss. 1999. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397: 702-706. (Pubitemid 29108390)
21. Sun, Z., D. Unutmaz, Y. R. Zou, M. J. Sunshine, A. Pierani, S. Brenner-Morton, R. E. Mebius, and D. R. Littman. 2000. Requirement for RORγ in thymocyte survival and lymphoid organ development. Science 288: 2369-2373. (Pubitemid 30448162)
22. Eberl, G., S. Marmon, M. J. Sunshine, P. D. Rennert, Y. Choi, and D. R. Littman. 2004. An essential function for the nuclear receptor RORγt in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5: 64-73. (Pubitemid 38081470)
23. Kim, D., R. E. Mebius, J. D. MacMicking, S. Jung, T. Cupedo, Y. Castellanos, J. Rho, B. R. Wong, R. Josien, N. Kim, et al. 2000. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J. Exp. Med. 192: 1467-1478. (Pubitemid 30953884)
24. Kong, Y. Y., H. Yoshida, I. Sarosi, H. L. Tan, E. Timms, C. Capparelli, S. Morony, A. J. Oliveira-dos-Santos, G. Van, A. Itie, et al. 1999. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397: 315-323. (Pubitemid 29061638)
25. Dougall, W. C., M. Glaccum, K. Charrier, K. Rohrbach, K. Brasel, T. De Smedt, E. Daro, J. Smith, M. E. Tometsko, C. R. Maliszewski, et al. 1999. RANK is essential for osteoclast and lymph node development. Genes Dev. 13: 2412-2424.
26. Yoshida, H., A. Naito, J. Inoue, M. Satoh, S. M. Santee-Cooper, C. F. Ware, A. Togawa, S. Nishikawa, and S. Nishikawa. 2002. Different cytokines induce surface lymphotoxin-αβ on IL-7 receptor-α cells that differentially engender lymph nodes and Peyer's patches. Immunity 17: 823-833. (Pubitemid 35477800)
27. Farr, A. G., M. L. Berry, A. Kim, A. J. Nelson, M. P. Welch, and A. Aruffo. 1992. Characterization and cloning of a novel glycoprotein expressed by stromal cells in T-dependent areas of peripheral lymphoid tissues. J. Exp. Med. 176: 1477-1482.
28. Berney, C., S. Herren, C. A. Power, S. Gordon, L. Martinez-Pomares, and M. H. Kosco-Vilbois. 1999. A member of the dendritic cell family that enters B cell follicles and stimulates primary antibody responses identified by a mannose receptor fusion protein. J. Exp. Med. 190: 851-860. (Pubitemid 29451630)
29. McNagny, K. M., R. P. Bucy, and M. D. Cooper. 1991. Reticular cells in peripheral lymphoid tissues express the phosphatidylinositol-linked BP-3 antigen. Eur. J. Immunol. 21: 509-515.
30. +-ATPase-reactive TCR transgenic mouse. J. Immunol. 177: 7858-7867.
31. Katagiri, K., A. Maeda, M. Shimonaka, and T. Kinashi. 2003. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulator of LFA-1. Nat. Immunol. 4: 741-748. (Pubitemid 36986757)
32. Sukumar, S., A. K. Szakal, and J. G. Tew. 2006. Isolation of functionally active murine follicular dendritic cells. J. Immunol. Methods 313: 81-95.
33. Katakai, T., T. Hara, M. Sugai, H. Gonda, and A. Shimizu. 2003. Th1-biased tertiary lymphoid tissue supported by CXC chemokine ligand 13-producing stromal network in chronic lesions of autoimmune gastritis. J. Immunol. 171: 4359-4368. (Pubitemid 37238714)
34. Cupedo, T., M. F. Vondenhoff, E. J. Heeregrave, A. E. De Weerd, W. Jansen, D. G. Jackson, G. Kraal, and R. E. Mebius. 2004. Presumptive lymph node organizers are differentially represented in developing mesenteric and peripheral nodes. J. Immunol. 173: 2968-2975. (Pubitemid 39142001)
35. Rennert, P. D., J. L. Browning, R. Mebius, F. Mackay, and P. S. Hochman. 1996. Surface lymphotoxin α/β complex is required for the development of peripheral lymphoid organs. J. Exp. Med. 184: 1999-2006.
36. Rennert, P. D., D. James, F. Mackay, J. L. Browning, and P. S. Hochman. 1998. Lymph node genesis is induced by signaling through the lymphotoxin β receptor. Immunity 9: 71-79. (Pubitemid 28361296)
37. Shinkura, R., K. Kitada, F. Matsuda, K. Tashiro, K. Ikuta, M. Suzuki, K. Kogishi, T. Serikawa, and T. Honjo. 1999. Alymphoplasia is caused by a point mutation in the mouse gene encoding NF-κB-inducing kinase. Nat. Genet. 22: 74-77. (Pubitemid 29214808)
38. Koike, R., T. Nishimura, R. Yasumizu, H. Tanaka, Y. Hataba, T. Watanabe, S. Miyawaki, and M. Miyasaka. 1996. The splenic marginal zone is absent in alymphoplastic aly mutant mice. Eur. J. Immunol. 26: 669-675. (Pubitemid 26091398)
39. Bajénoff, M., J. G. Egen, L. Y. Koo, J. P. Laugier, F. Brau, N. Glaichenhaus, and R. N. Germain. 2006. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25: 989-1001. (Pubitemid 44914055)
40. Luther, S. A., T. Lopez, W. Bai, D. Hanahan, and J. G. Cyster. 2000. BLC expression in pancreatic islets cause B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 12: 471-481.
41. Aloisi, F., and R. Pujol-Borrell. 2006. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol. 6: 205-217. (Pubitemid 43290990)
42. Gonzalez, M., F. Mackay, J. L. Browning, M. H. Kosco-Vilbois, and R. J. Noelle. 1998. The sequential role of lymphotoxin and B cells in the development of splenic follicles. J. Exp. Med. 187: 997-1007. (Pubitemid 28176400)
43. Hashi, H., H. Yoshida, K. Honda, S. Fraser, H. Kubo, M. Awane, A. Takabayashi, H. Nakano, Y. Yamaoka, and S. Nishikawa. 2001. Compartmentalization of Peyer's patch anlagen before lymphocyte entry. J. Immunol. 166: 3702-3709. (Pubitemid 32224892)
44. Cupedo, T., F. E. Lund, V. N. Ngo, T. D. Randall, W. Jansen, M. J. Greuter, R. de Waal-Malefyt, G. Kraal, J. G. Cyster, and R. E. Mebius. 2004. Initiation of cellular organization in lymph nodes is regulated by non-B cell-derived signals and is not dependent on CXC chemokine ligand 13. J. Immunol. 173: 4889-4896. (Pubitemid 39387770)
45. Taylor, R. T., S. R. Patel, E. Lin, B. R. Butler, J. G. Lake, R. D. Newberry, and I. R. Williams. 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.
46. + lympho-hemopoietic progenitors develop. J. Exp. Med. 184: 1449-1459.
47. Cupedo, T., and R. E. Mebius. 2005. Cellular interactions in lymph node development. J. Immunol. 174: 21-25. (Pubitemid 40007386)
48. Itano, A. A., and M.K. Jenkins. 2003. Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 4: 733-739.
49. Iwasaki, A., and B. L. Kelsall. 2000. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J. Exp. Med. 191: 1381-1394. (Pubitemid 30227125)
50. Mowat, A. M. 2003. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3: 331-341. (Pubitemid 37328685)
51. Pape, K. A., D. M. Catron, A. A. Itano, and M. K. Jenkins. 2007. The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity 26: 491-502.
52. Carrasco, Y. R., and F. D. Batista. 2007. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 27: 160-171.
53. Phan, T. G., I. Grigorova, T. Okada, and J. G. Cyster. 2007. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 8: 992-1000.
54. Junt, T., E. A. Moseman, M. Iannacone, S. Massberg, P. A. Lang, M. Boes, K. Fink, S. E. Henrickson, D. M. Shayakhmetov, N. C. Di Paolo, et al. 2007. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450: 110-114. (Pubitemid 350070574)
55. Lo, C. G., T. T. Lu, and J. G. Cyster. 2003. Integrin-dependence of lymphocyte entry into the splenic white pulp. J. Exp. Med. 197: 356-361.
56. Woolf, E., I. Grigorova, A. Sagiv, V. Grabovsky, S. W. Feigelson, Z. Shulman, T. Hartmann, M. Sixt, J. G. Cyster, and R. Alon. 2007. Lymph node chemokines promote sustained T lymphocyte motility without triggering stable integrin adhesiveness in the absence of shear forces. Nat. Immunol. 8: 1076-1085. (Pubitemid 47423755)
57. Lämmermann, T., B. L. Bader, S. J. Monkley, T. Worbs, R. Wedlich-Söldner, K. Hirsch, M. Keller, R. Förster, D. R. Critchley, R. Fässler, and M. Sixt. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453: 51-55. (Pubitemid 351630331)