RANKL induces organized lymph node growth by stromal cell proliferation

Journal of Immunology

Volumn 188, Issue 3, 2012, Pages 1245-1254

  Hess, Estelle ^a   Duheron, Vincent ^a   Decossas, Marion ^a   Lézot, Frédéric ^b,c   Berdal, Ariane ^b   Chea, Sylvestre ^d   Golub, Rachel ^d   Bosisio, Mattéo R ^e,f   Bridal, S Lori ^e   Choi, Yongwon ^g   Yagita, Hideo ^h   Mueller, Christopher G ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d Cellule Pasteur INSERM U1223   (France)

^e CNRS   (France)

^f Echosens SA   (France)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD31 ANTIGEN; CD45 ANTIGEN; COMPLEMENT COMPONENT C3B RECEPTOR; CXCL13 CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MUCOSAL ADDRESSIN CELL ADHESION MOLECULE 1; NEUTRALIZING ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PODOPLANIN; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CELL COMPOSITION; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOARCHITECTURE; FOLLICULAR DENDRITIC CELL; GENE EXPRESSION; HAIR FOLLICLE; LYMPH NODE; LYMPH NODE GROWTH; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETICULAR FIBROBLASTIC STROMAL CELL; STROMA CELL; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; CELL PROLIFERATION; CHEMOKINE CCL19; CHEMOKINE CXCL13; HAIR FOLLICLE; HOMEOSTASIS; IMMUNE SYSTEM; LYMPH NODES; MICE; MICE, TRANSGENIC; RANK LIGAND; STROMAL CELLS;

EID: 84856576861     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101513     Document Type: Article

References (78)

1. Junt, T., E. Scandella, and B. Ludewig. 2008. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 8: 764-775.
2. Mueller, S. N., and R. N. Germain. 2009. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat. Rev. Immunol. 9: 618-629.
3. Lämmermann, T., and M. Sixt. 2008. The microanatomy of T-cell responses. Immunol. Rev. 221: 26-43. (Pubitemid 351230118)
4. Roozendaal, R., and R. E. Mebius. 2011. Stromal cell-immune cell interactions. Annu. Rev. Immunol. 29: 23-43.
5. Fletcher, A. L., D. Malhotra, and S. J. Turley. 2011. Lymph node stroma broaden the peripheral tolerance paradigm. Trends Immunol. 32: 12-18.
6. Luther, S. A., T. K. Vogt, and S. Siegert. 2011. Guiding blind T cells and dendritic cells: A closer look at fibroblastic reticular cells found within lymph node T zones. Immunol. Lett. 138: 9-11.
7. Katakai, T., H. Suto, M. Sugai, H. Gonda, A. Togawa, S. Suematsu, Y. Ebisuno, K. Katagiri, T.Kinashi, and A. Shimizu. 2008. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J. Immunol. 181: 6189-6200.
8. Palframan, R. T., S. Jung, G. Cheng, W. Weninger, Y. Luo, M. Dorf, D. R. Littman, B. J. Rollins, H. Zweerink, A. Rot, and U. H. von Andrian. 2001. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 194: 1361-1373. (Pubitemid 33055053)
9. Browning, J. L., N. Allaire, A. Ngam-Ek, E. Notidis, J. Hunt, S. Perrin, and R. A. Fava. 2005. Lymphotoxin-beta receptor signaling is required for the homeostatic control of HEV differentiation and function. Immunity 23: 539-550. (Pubitemid 41587893)
10. Pham, T. H., P. Baluk, Y. Xu, I. Grigorova, A. J. Bankovich, R. Pappu, S. R. Coughlin, D. M. McDonald, S. R. Schwab, and J. G. Cyster. 2010. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207: 17-27.
11. Schwab, S. R., and J. G. Cyster. 2007. Finding a way out: lymphocyte egress from lymphoid organs. Nat. Immunol. 8: 1295-1301. (Pubitemid 350131168)
12. Link, A., T. K. Vogt, S. Favre, M. R. Britschgi, H. Acha-Orbea, B. Hinz, J. G. Cyster, and S. A. Luther. 2007. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8: 1255-1265. (Pubitemid 350011765)
13. Kosco, M. H., E. Pflugfelder, and D. Gray. 1992. Follicular dendritic cell-dependent adhesion and proliferation of B cells in vitro. J. Immunol. 148: 2331-2339.
14. Kumar, V., E. Scandella, R. Danuser, L. Onder, M. Nitschké, Y. Fukui, C. Halin, B. Ludewig, and J. V. Stein. 2010. Global lymphoid tissue remodeling during a viral infection is orchestrated by a B cell-lymphotoxin- dependent pathway. Blood 115: 4725-4733.
15. Cupedo, T., and R. E. Mebius. 2005. Cellular interactions in lymph node development. J. Immunol. 174: 21-25. (Pubitemid 40007386)
16. 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)
17. 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)
18. White, A., D. Carragher, S. Parnell, A. Msaki, N. Perkins, P. Lane, E. Jenkinson, G. Anderson, and J. H. Caamaño. 2007. Lymphotoxin a-dependent and -independent signals regulate stromal organizer cell homeostasis during lymph node organogenesis. Blood 110: 1950-1959. (Pubitemid 47443909)
19. Coles, M. C., H. Veiga-Fernandes, K. E. Foster, T. Norton, S. N. Pagakis, B. Seddon, and D. Kioussis. 2006. Role of T and NK cells and IL7/IL7r interactions during neonatal maturation of lymph nodes. Proc. Natl. Acad. Sci. USA 103: 13457-13462. (Pubitemid 44380129)
20. Tumanov, A. V., D. V. Kuprash, and S. A. Nedospasov. 2003. The role of lymphotoxin in development and maintenance of secondary lymphoid tissues. Cytokine Growth Factor Rev. 14: 275-288. (Pubitemid 36693147)
21. Browning, J. L. 2008. Inhibition of the lymphotoxin pathway as a therapy for autoimmune disease. Immunol. Rev. 223: 202-220. (Pubitemid 351986178)
22. Wada, T., T. Nakashima, N. Hiroshi, and J. M. Penninger. 2006. RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol. Med. 12: 17-25. (Pubitemid 43089652)
23. Dejardin, E., N. M. Droin, M. Delhase, E. Haas, Y. Cao, C. Makris, Z. W. Li, M. Karin, C. F. Ware, and D. R. Green. 2002. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity 17: 525-535. (Pubitemid 35223540)
24. Walsh, M. C., and Y. Choi. 2003. Biology of the TRANCE axis. Cytokine Growth Factor Rev. 14: 251-263. (Pubitemid 36693145)
25. 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.
26. 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. (Pubitemid 29453612)
27. 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.
28. 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-alphabeta on IL-7 receptor-alpha cells that differentially engender lymph nodes and Peyer's patches. Immunity 17: 823-833. (Pubitemid 35477800)
29. Knoop, K. A., N. Kumar, B. R. Butler, S. K. Sakthivel, R. T. Taylor, T. Nochi, H. Akiba, H. Yagita, H. Kiyono, and I. R. Williams. 2009. RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J. Immunol. 183: 5738-5747.
30. Schneider, M. R., R. Schmidt-Ullrich, and R. Paus. 2009. The hair follicle as a dynamic miniorgan. Curr. Biol. 19: R132-R142.
31. Paus, R., B. J. Nickoloff, and T. Ito. 2005. A 'hairy' privilege. Trends Immunol. 26: 32-40. (Pubitemid 40051990)
32. Rossi, S. W., M. Y. Kim, A. Leibbrandt, S. M. Parnell, W. E. Jenkinson, S. H. Glanville, F. M. McConnell, H. S. Scott, J. M. Penninger, E. J. Jenkinson, et al. 2007. RANK signals from CD4(+)3(-) inducer cells regulate development of Aire-expressing epithelial cells in the thymic medulla. J. Exp. Med. 204: 1267-1272. (Pubitemid 46919863)
33. Akiyama, T., Y. Shimo, H. Yanai, J. Qin, D. Ohshima, Y. Maruyama, Y. Asaumi, J. Kitazawa, H. Takayanagi, J. M. Penninger, et al. 2008. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and self-tolerance. Immunity 29: 423-437.
34. White, A. J., D. R. Withers, S. M. Parnell, H. S. Scott, D. Finke, P. J. Lane, E. J. Jenkinson, and G. Anderson. 2008. Sequential phases in the development of Aire-expressing medullary thymic epithelial cells involve distinct cellular input. Eur. J. Immunol. 38: 942-947.
35. Hikosaka, Y., T. Nitta, I. Ohigashi, K. Yano, N. Ishimaru, Y. Hayashi, M. Matsumoto, K. Matsuo, J. M. Penninger, H. Takayanagi, et al. 2008. The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity 29: 438-450.
36. Mouri, Y., M. Yano, M. Shinzawa, Y. Shimo, F. Hirota, Y. Nishikawa, T. Nii, H. Kiyonari, T. Abe, H. Uehara, et al. 2011. Lymphotoxin signal promotes thymic organogenesis by eliciting RANK expression in the embryonic thymic stroma. J. Immunol. 186: 5047-5057.
37. Duheron, V., E. Hess, M. Duval, M. Decossas, B. Castaneda, J. E. Klöpper, L. Amoasii, J. B. Barbaroux, I. R. Williams, H. Yagita, et al. 2011. Receptor activator of NF-kappaB (RANK) stimulates the proliferation of epithelial cells of the epidermo-pilosebaceous unit. Proc. Natl. Acad. Sci. USA 108: 5342-5347.
38. Lagasse, E., and I. L. Weissman. 1997. Enforced expression of Bcl-2 in monocytes rescues macrophages and partially reverses osteopetrosis in op/op mice. Cell 89: 1021-1031. (Pubitemid 127678736)
39. Bosisio, M. R., C. Maisonneuve, S. Gregoire, A. Kettaneh, C. G. Mueller, and S. L. Bridal. 2009. Ultrasound biomicroscopy: a powerful tool probing murine lymph node size in vivo. Ultrasound Med. Biol. 35: 1209-1216.
40. Kamijo, S., A. Nakajima, K. Ikeda, K. Aoki, K. Ohya, H. Akiba, H. Yagita, and K. Okumura. 2006. Amelioration of bone loss in collagen-induced arthritis by neutralizing anti-RANKL monoclonal antibody. Biochem. Biophys. Res. Commun. 347: 124-132. (Pubitemid 44026486)
41. Ruedl, C., P. Koebel, M. Bachmann, M. Hess, and K. Karjalainen. 2000. Anatomical origin of dendritic cells determines their life span in peripheral lymph nodes. J. Immunol. 165: 4910-4916.
42. -/- transgenic mice develop compound amelogenesis imperfecta, dentinogenesis imperfecta and periodental osteopetrosis. Bone 41: 851-859.
43. Matsumoto, M., S. F. Lo, C. J. Carruthers, J. Min, S. Mariathasan, G. Huang, D. R. Plas, S. M. Martin, R. S. Geha, M. H. Nahm, and D. D. Chaplin. 1996. Affinity maturation without germinal centres in lymphotoxin-alpha- deficient mice. Nature 382: 462-466. (Pubitemid 26264864)
44. Castaneda, B., Y. Simon, J. Jacques, E. Hess, Y. W. Choi, C. Blin-Wakkach, C. Mueller, A. Berdal, and F. Lézot. 2011. Bone resorption control of tooth eruption and root morphogenesis: Involvement of the receptor activator of NκB (RANK). J. Cell. Physiol. 226: 74-85.
45. Lagasse, E., and I. L. Weissman. 1992. Mouse MRP8 and MRP14, two intracellular calcium-binding proteins associated with the development of the myeloid lineage. Blood 79: 1907-1915.
46. Jakubzick, C., M. Bogunovic, A. J. Bonito, E. L. Kuan, M. Merad, and G. J. Randolph. 2008. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J. Exp. Med. 205: 2839-2850.
47. Gardner, J. M., J. J. Devoss, R. S. Friedman, D. J. Wong, Y. X. Tan, X. Zhou, K. P. Johannes, M. A. Su, H. Y. Chang, M. F. Krummel, and M. S. Anderson. 2008. Deletional tolerance mediated by extrathymic Aire-expressing cells. Science 321: 843-847.
48. Cohen, J. N., C. J. Guidi, E. F. Tewalt, H. Qiao, S. J. Rouhani, A. Ruddell, A. G. Farr, K. S. Tung, and V. H. Engelhard. 2010. Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J. Exp. Med. 207: 681-688.
49. Fletcher, A. L., V. Lukacs-Kornek, E. D. Reynoso, S. E. Pinner, A. Bellemare-Pelletier, M. S. Curry, A. R. Collier, R. L. Boyd, and S. J. Turley. 2010. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J. Exp. Med. 207: 689-697.
50. Ma, L., J. Liu, T. Wu, M. Plikus, T. X. Jiang, Q. Bi, Y. H. Liu, S. Müller-Röver, H. Peters, J. P. Sundberg, et al. 2003. 'Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation. Development 130: 379-389. (Pubitemid 36175934)
51. 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.
52. Roozendaal, R., T. R. Mempel, L. A. Pitcher, S. F. Gonzalez, A. Verschoor, R. E. Mebius, U. H. von Andrian, and M. C. Carroll. 2009. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 30: 264-276.
53. Schmutz, S., N. Bosco, S. Chappaz, O. Boyman, H. Acha-Orbea, R. Ceredig, A. G. Rolink, and D. Finke. 2009. Cutting edge: IL-7 regulates the peripheral pool of adult ROR gamma+ lymphoid tissue inducer cells. J. Immunol. 183: 2217-2221.
54. Meier, D., C. Bornmann, S. Chappaz, S. Schmutz, L. A. Otten, R. Ceredig, H. Acha-Orbea, and D. Finke. 2007. Ectopic lymphoid-organ development occurs through interleukin 7-mediated enhanced survival of lymphoid-tissue-inducer cells. Immunity 26: 643-654. (Pubitemid 46756355)
55. Mebius, R. E. 2003. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3: 292-303. (Pubitemid 37328682)
56. Anderson, D. M., E. Maraskovsky, W. L. Billingsley, W. C. Dougall, M. E. Tometsko, E. R. Roux, M. C. Teepe, R. F. DuBose, D. Cosman, and L. Galibert. 1997. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature 390: 175-179. (Pubitemid 27507987)
57. Wong, B. R., R. Josien, S. Y. Lee, B. Sauter, H. L. Li, R. M. Steinman, and Y. Choi. 1997. TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J. Exp. Med. 186: 2075-2080. (Pubitemid 28013694)
58. Cremer, I., M. C. Dieu-Nosjean, S. Maréchal, C. Dezutter-Dambuyant, S. Goddard, D. Adams, N. Winter, C. Menetrier-Caux, C. Sautès-Fridman, W. H. Fridman, and C. G. Mueller. 2002. Long-lived immature dendritic cells mediated by TRANCE-RANK interaction. Blood 100: 3646-3655. (Pubitemid 35303935)
59. Yun, T. J., M. D. Tallquist, A. Aicher, K. L. Rafferty, A. J. Marshall, J. J. Moon, M. E. Ewings, M. Mohaupt, S. W. Herring, and E. A. Clark. 2001. Osteoprotegerin, a crucial regulator of bone metabolism, also regulates B cell development and function. J. Immunol. 166: 1482-1491. (Pubitemid 32114626)
60. Willerford, D. M., J. Chen, J. A. Ferry, L. Davidson, A. Ma, and F. W. Alt. 1995. Interleukin-2 receptor alpha chain regulates the size and content of the peripheral lymphoid compartment. Immunity 3: 521-530.
61. Lee, J. W., M. Epardaud, J. Sun, J. E. Becker, A. C. Cheng, A. R. Yonekura, J. K. Heath, and S. J. Turley. 2007. Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat. Immunol. 8: 181-190. (Pubitemid 46152649)
62. Shamoto, M., M. Shinzato, B. Qian, S. Hosokawa, and M. Ishibashi. 1999. Paracortical hyperplasia of superficial lymph nodes in a new mutant strain of hairless rats (ISh): a lesion similar to human dermatopathic lymphadenopathy. Pathol. Int. 49: 305-309. (Pubitemid 29230794)
63. Kollet, O., A. Dar, S. Shivtiel, A. Kalinkovich, K. Lapid, Y. Sztainberg, M. Tesio, R. M. Samstein, P. Goichberg, A. Spiegel, et al. 2006. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat. Med. 12: 657-664. (Pubitemid 43865234)
64. Loser, K., A. Mehling, S. Loeser, J. Apelt, A. Kuhn, S. Grabbe, T. Schwarz, J. M. Penninger, and S. Beissert. 2006. Epidermal RANKL controls regulatory Tcell numbers via activation of dendritic cells. Nat. Med. 12: 1372-1379. (Pubitemid 44924495)
65. Collin-Osdoby, P., L. Rothe, F. Anderson, M. Nelson, W. Maloney, and P. Osdoby. 2001. Receptor activator of NF-kappa B and osteoprotegerin expression by human microvascular endothelial cells, regulation by inflammatory cytokines, and role in human osteoclastogenesis. J. Biol. Chem. 276: 20659-20672.
66. Kim, H. H., H. S. Shin, H. J. Kwak, K. Y. Ahn, J. H. Kim, H. J. Lee, M. S. Lee, Z. H. Lee, and G. Y. Koh. 2003. RANKL regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. FASEB J. 17: 2163-2165.
67. Min, J. K., Y. M. Kim, Y. M. Kim, E. C. Kim, Y. S. Gho, I. J. Kang, S. Y. Lee, Y. Y. Kong, and Y. G. Kwon. 2003. Vascular endothelial growth factor upregulates expression of receptor activator of NF-kappa B (RANK) in endothelial cells. Concomitant increase of angiogenic responses to RANK ligand. J. Biol. Chem. 278: 39548-39557.
68. Rifas, L., S. Arackal, and M. N. Weitzmann. 2003. Inflammatory T cells rapidly induce differentiation of human bone marrow stromal cells into mature osteoblasts. J. Cell. Biochem. 88: 650-659. (Pubitemid 36258815)
69. Wilke, G., G. Steinhauser, J. Grün, and C. Berek. 2010. In silico subtraction approach reveals a close lineage relationship between follicular dendritic cells and BP3(hi) stromal cells isolated from SCID mice. Eur. J. Immunol. 40: 2165-2173.
70. Min, J. K., Y. M. Kim, S. W. Kim, M. C. Kwon, Y. Y. Kong, I. K. Hwang, M. H. Won, J. Rho, and Y. G. Kwon. 2005. TNF-related activation-induced cytokine enhances leukocyte adhesiveness: induction of ICAM-1 and VCAM-1 via TNF receptor-associated factor and protein kinase C-dependent NF-kappaB activation in endothelial cells. J. Immunol. 175: 531-540. (Pubitemid 40884359)
71. Tomei, A. A., S. Siegert, M. R. Britschgi, S. A. Luther, and M. A. Swartz. 2009. Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J. Immunol. 183: 4273-4283.
72. Gommerman, J. L., and J. L. Browning. 2003. Lymphotoxin/light, lymphoid microenvironments and autoimmune disease. Nat. Rev. Immunol. 3: 642-655. (Pubitemid 37328667)
73. Endres, R., M. B. Alimzhanov, T. Plitz, A. Fütterer, M. H. Kosco-Vilbois, S. A. Nedospasov, K. Rajewsky, and K. Pfeffer. 1999. Mature follicular dendritic cell networks depend on expression of lymphotoxin beta receptor by radio-resistant stromal cells and of lymphotoxin beta and tumor necrosis factor by B cells. J. Exp. Med. 189: 159-168.
74. Vondenhoff, M. F., M. Greuter, G. Goverse, D. Elewaut, P. Dewint, C. F. Ware, K. Hoorweg, G. Kraal, and R. E. Mebius. 2009. LTbetaR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J. Immunol. 182: 5439-5445.
75. Wong, B. R., J. Rho, J. Arron, E. Robinson, J. Orlinick, M. Chao, S. Kalachikov, E. Cayani, F. S. Bartlett, III, W. N. Frankel, et al. 1997. TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N-terminal kinase in T cells. J. Biol. Chem. 272: 25190-25194. (Pubitemid 27415705)
76. Takayanagi, H., K. Ogasawara, S. Hida, T. Chiba, S. Murata, K. Sato, A. Takaoka, T. Yokochi, H. Oda, K. Tanaka, et al. 2000. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 408: 600-605.
77. Yun, T. J., P. M. Chaudhary, G. L. Shu, J. K. Frazer, M. K. Ewings, S. M. Schwartz, V. Pascual, L. E. Hood, and E. A. Clark. 1998. OPG/FDCR-1, a TNF receptor family member, is expressed in lymphoid cells and is upregulated by ligating CD40. J. Immunol. 161: 6113-6121. (Pubitemid 28535982)
78. Matzinger, P., and T. Kamala. 2011. Tissue-based class control: the other side of tolerance. Nat. Rev. Immunol. 11: 221-230.