Stromal cell regulation of homeostatic and inflammatory lymphoid organogenesis

Immunology

Volumn 140, Issue 1, 2013, Pages 12-21

  Kain, Matthew J W ^a,b   Owens, Benjamin M J ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NEW COLLEGE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cytokines; Inflammation; Mucosal associated lymphoid tissue; Spleen lymph nodes

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANTIBODY CONJUGATE; CELL SURFACE MARKER; CHEMOKINE; CHEMOKINE RECEPTOR CXCR5; COLLAGEN; COMPLEMENT RECEPTOR; CXCL13 CHEMOKINE; CYTOKINE; CYTOKINE ANTIBODY; DESMIN; EPITHELIAL CELL ADHESION MOLECULE; FIBRILLIN; FIBRONECTIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 5; INTERLEUKIN 7; LAMININ; LYMPHOTOXIN ALPHA BETA; LYMPHOTOXIN BETA RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULAR ENDOTHELIAL CADHERIN;

AUTOIMMUNE DISEASE; AUTOINFLAMMATORY DISEASE; B LYMPHOCYTE; BACTERIAL INFECTION; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL INTERACTION; CELL STRUCTURE; CYTOKINE PRODUCTION; HOMEOSTASIS; HUMAN; INFECTION; INFLAMMATION; LYMPH FOLLICLE; LYMPH NODE; LYMPHOID ORGAN; LYMPHOID TISSUE; MESENCHYMAL STROMA CELL; NONHUMAN; ORGANOGENESIS; POSITIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; SECONDARY LYMPHOID ORGAN; STROMA CELL; T LYMPHOCYTE; TERTIARY LYMPHOID ORGAN; VIRUS INFECTION;

CYTOKINES; INFLAMMATION; MUCOSAL ASSOCIATED LYMPHOID TISSUE; SPLEEN/LYMPH NODES;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGEN-PRESENTING CELLS; HOMEOSTASIS; HUMANS; INFLAMMATION; LYMPHOID TISSUE; MODELS, IMMUNOLOGICAL; ORGANOGENESIS; STROMAL CELLS;

EID: 84883207256     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12119     Document Type: Review

References (128)

1. Rennert PD, Browning JL, Mebius R, Mackay F, Hochman PS. Surface lymphotoxin α/β complex is required for the development of peripheral lymphoid organs. J Exp Med 1996; 184:1999-2006.
2. Roozendaal R, Mebius RE. Stromal cell-immune cell interactions. Annu Rev Immunol 2011; 29:23-43.
3. van de Pavert SA, Olivier BJ, Goverse G et al. Chemokine CXCL13 is essential for lymph node initiation and is induced by retinoic acid and neuronal stimulation. Nat Immunol 2009; 10:1193-9.
4. Eberl G, Marmon S, Sunshine MJ, Rennert PD, Choi Y, Littman DR. An essential function for the nuclear receptor RORγ(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol 2004; 5:64-73.
5. - cells, as well as macrophages. J Immunol 2001; 166:6593-601.
6. Drayton DL, Ying X, Lee J, Lesslauer W, Ruddle NH. Ectopic LT αβ directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J Exp Med 2003; 197:1153-63.
7. Banks TA, Rouse BT, Kerley MK et al. Lymphotoxin-alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J Immunol 1995; 155:1685-93.
8. Boulianne B, Porfilio EA, Pikor N, Gommerman JL. Lymphotoxin-sensitive microenvironments in homeostasis and inflammation. Front Immunol 2012; 3:243.
9. Vondenhoff MF, Greuter M, Goverse G et al. LTβR signaling induces cytokine expression and up-regulates lymphangiogenic factors in lymph node anlagen. J Immunol 2009; 182:5439-45.
10. Kim D, Mebius RE, MacMicking JD et al. Regulation of peripheral lymph node genesis by the tumor necrosis factor family member TRANCE. J Exp Med 2000; 192:1467-78.
11. Bénézech C, White A, Mader E et al. Ontogeny of stromal organizer cells during lymph node development. J Immunol 2010; 184:4521-30.
12. van de Pavert SA, Mebius RE. New insights into the development of lymphoid tissues. Nat Rev Immunol 2010; 10:664-664.
13. Schmutz S, Bosco N, Chappaz S, Boyman O, Acha-Orbea H, Ceredig R, Rolink AG, Finke D. Cutting edge: IL-7 regulates the peripheral pool of adult rorγ+ lymphoid tissue inducer cells. J Immunol 2009; 183:2217-21.
14. Luther SA, Ansel KM, Cyster JG. Overlapping roles of CXCL13, interleukin 7 receptorα, and CCR7 ligands in lymph node development. J Exp Med 2003; 197:1191-8.
15. Ansel KM, Ngo VN, Hyman PL et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 2000; 406:309-14.
16. Cupedo T, Lund FE, Ngo VN et al. 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 2004; 173:4889-96.
17. Onder L, Danuser R, Scandella E, Firner S, Chai Q, Hehlgans T, Stein JV, Ludewig B. Endothelial cell-specific lymphotoxin-β receptor signaling is critical for lymph node high endothelial venule formation. J Exp Med, 2013; 210:465-73.
18. Veiga-Fernandes H, Coles MC, Foster KE et al. Tyrosine kinase receptor RET is a key regulator of Peyer's patch organogenesis. Nature 2007; 446:547-51.
19. Ferreira M, Domingues RG, Veiga-Fernandes H. Stroma cell priming in enteric lymphoid organ morphogenesis. Front Immunol 2012; 3:219.
20. Carragher DM, Rangel-Moreno J, Randall TD. Ectopic lymphoid tissues and local immunity. Semin Immunol 2008; 20:26-42.
21. Brendolan A, Caamano JH. Mesenchymal cell differentiation during lymph node organogenesis. Front Immunol 2012; 3:381.
22. Koning JJ, Mebius RE. Interdependence of stromal and immune cells for lymph node function. Trends Immunol 2012; 33:264-70.
23. Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 2007; 8:1255-65.
24. Malhotra D, Fletcher AL, Astarita J et al. Transcriptional profiling of stroma from inflamed resting lymph nodes defines immunological hallmarks. Nat Immunol 2012; 13:499-510.
25. Bajenoff M. Stromal cells control soluble material and cellular transport in lymph nodes. Front Immunol 2012; 3:304.
26. Mueller SN, Germain RN. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol 2009; 9:618-29.
27. Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, Mebius RE, von AU, Carroll MC. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009; 30:264-76.
28. Katakai T. Marginal reticular cells: a stromal subset directly descended from the lymphoid tissue organizer. Front Immunol 2012; 3:200.
29. Bajenoff M, Glaichenhaus N, Germain RN. Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J Immunol 2008; 181:3947-54.
30. Nakano H, Mori S, Yonekawa H, Nariuchi H, Matsuzawa A, Kakiuchi T. A novel mutant gene involved in T-lymphocyte-specific homing into peripheral lymphoid organs on mouse chromosome 4. Blood 1998; 91:2886-95.
31. Gunn MD, Ngo VN, Ansel KM, Ekland EH, Cyster JG, Williams LT. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 1998; 391:799-803.
32. Katakai T, Suto H, Sugai M et al. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J Immunol 2008; 181:6189-200.
33. Vinuesa CG, Tangye SG, Moser B, Mackay CR. Follicular B helper T cells in antibody responses and autoimmunity. Nat Rev Immunol 2005; 5:853-65.
34. + T helper 1 cell differentiation. Immunity 2012; 37:1091-103.
35. Onder L, Narang P, Scandella E et al. IL-7-producing stromal cells are critical for lymph node remodeling. Blood 2012; 120:4675-83.
36. Woodland RT, Schmidt MR, Thompson CB. BLyS and B cell homeostasis. Semin Immunol 2006; 18:318-26.
37. Cyster JG, Schwab SR. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 2012; 30:69-94.
38. Schwab SR, Pereira JP, Matloubian M, Xu Y, Huang Y, Cyster JG. Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 2005; 309:1735-9.
39. Schwab SR, Cyster JG. Finding a way out: lymphocyte egress from lymphoid organs. Nat Immunol 2007; 8:1295-301.
40. Yi T, Wang X, Kelly LM et al. Oxysterol gradient generation by lymphoid stromal cells guides activated B cell movement during humoral responses. Immunity 2012; 37:535-48.
41. Katakai T, Hara T, Sugai M, Gonda H, Shimizu A. Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med 2004; 200:783-95.
42. Kumar V, Scandella E, Danuser R et al. Global lymphoid tissue remodeling during a viral infection is orchestrated by a B cell-lymphotoxin-dependent pathway. Blood 2010; 115:4725-33.
43. Mueller SN, Hosiawa-Meagher KA, Konieczny BT, Sullivan BM, Bachmann MF, Locksley RM, Ahmed R, Matloubian M. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 2007; 317:670-4.
44. Soderberg KA, Payne GW, Sato A, Medzhitov R, Segal SS, Iwasaki A. Innate control of adaptive immunity via remodeling of lymph node feed arteriole. Proc Natl Acad Sci U S A 2005; 102:16315-20.
45. Chyou S, Ekland EH, Carpenter AC, Tzeng TC, Tian S, Michaud M, Madri JA, Lu TT. Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J Immunol 2008; 181:3887-96.
46. Dalton JE, Maroof A, Owens BM et al. Inhibition of receptor tyrosine kinases restores immunocompetence and improves immune-dependent chemotherapy against experimental leishmaniasis in mice. J Clin Invest 2010; 120:1204-16.
47. Hamada H, Hiroi T, Nishiyama Y et al. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J Immunol 2002; 168:57-64.
48. + lympho-hemopoietic progenitors develop. J Exp Med 1996; 184:1449-59.
49. Lügering A, Ross M, Sieker M, Heidemann J, Williams IR, Domschke W, Kucharzik T. CCR6 identifies lymphoid tissue inducer cells within cryptopatches. Clin Exp Immunol 2010; 160:440-9.
50. Tsuji M, Suzuki K, Kitamura H et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 2008; 29:261-71.
51. Lorenz RG, Chaplin DD, McDonald KG, McDonough JS, Newberry RD. Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin-sufficient B lymphocytes, lymphotoxin β receptor, and TNF receptor I function. J Immunol 2003; 170:5475-82.
52. McDonald KG, McDonough JS, Newberry RD. 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 2005; 174:5720-8.
53. Ota N, Wong K, Valdez PA, Zheng Y, Crellin NK, Diehl L, Ouyang W. IL-22 bridges the lymphotoxin pathway with the maintenance of colonic lymphoid structures during infection with Citrobacter rodentium. Nat Immunol 2011; 12:941-8.
54. Halle S, Bumann D, Herbrand H, Willer Y, Dähne S, Förster R, Pabst O. Solitary intestinal lymphoid tissue provides a productive port of entry for Salmonella enterica serovar Typhimurium. Infect Immun 2007; 75:1577-85.
55. Bouskra D, Brézillon C, Bérard M, Werts C, Varona R, Boneca IG, Eberl G. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008; 456:507-10.
56. Neyt K, Perros F, GeurtsvanKessel CH, Hammad H, Lambrecht BN. Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol 2012; 33:297-305.
57. Genta RM, Hamner HW, Graham DY. Gastric lymphoid follicles in Helicobacter pylori infection: frequency, distribution, and response to triple therapy. Hum Pathol 1993; 24:577-83.
58. Drayton DL, Liao S, Mounzer RH, Ruddle NH. Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol 2006; 7:344-53.
59. Stranford S, Ruddle NH. Follicular dendritic cells, conduits, lymphatic vessels, and high endothelial venules in tertiary lymphoid organs: parallels with lymph node stroma. Front Immunol 2012; 3:350.
60. Cupedo T, Jansen W, Kraal G, Mebius RE. Induction of secondary and tertiary lymphoid structures in the skin. Immunity 2004; 21:655-67.
61. Suematsu S, Watanabe T. Generation of a synthetic lymphoid tissue-like organoid in mice. Nat Biotechnol 2004; 22:1539-45.
62. Meier D, Bornmann C, Chappaz S, Schmutz S, Otten LA, Ceredig R, Acha-Orbea H, Finke D. Ectopic lymphoid-organ development occurs through interleukin 7-mediated enhanced survival of lymphoid-tissue-inducer cells. Immunity 2007; 26:643-54.
63. + T cells with dendritic cells triggers the development of tertiary lymphoid structures in the thyroid. J Clin Invest 2006; 116:2622-32.
64. Lochner M. Tertiary lymphoid tissues in the colon: friend and foe. Gut microbes 2011; 2:193-7.
65. Lochner M, Ohnmacht C, Presley L, Bruhns P, Si-Tahar M, Sawa S, Eberl G. Microbiota-induced tertiary lymphoid tissues aggravate inflammatory disease in the absence of RORγt and LTi cells. J Exp Med 2011; 208:125-34.
66. Spits H, Artis D, Colonna M et al. Innate lymphoid cells - a proposal for uniform nomenclature. Nat Rev Immunol 2013; 13:145-9.
67. Bernink JH, Peters CP, Munneke M et al. Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol 2013; 14:221-9.
68. Pearson C, Uhlig HH, Powrie F. Lymphoid microenvironments and innate lymphoid cells in the gut. Trends Immunol 2012; 33:289-96.
69. Ware CF. Network communications: lymphotoxins, LIGHT, and TNF. Annu Rev Immunol 2005; 23:787-819.
70. Peters A, Pitcher LA, Sullivan JM et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 2011; 35:986-96.
71. Grogan JL, Ouyang W. A role for Th17 cells in the regulation of tertiary lymphoid follicles. Eur J Immunol 2012; 42:2255-62.
72. Peduto L, Dulauroy S, Lochner M, Späth GF, Morales MA, Cumano A, Eberl G. Inflammation recapitulates the ontogeny of lymphoid stromal cells. J Immunol 2009; 182:5789-99.
73. + perivascular cells identify a major source of profibrotic cells during acute tissue injury. Nat Med 2012; 18:1262-70.
74. Krautler NJ, Kana V, Kranich J et al. Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 2012; 150:194-206.
75. Benezech C, Mader E, Desanti G et al. Lymphotoxin-β receptor signaling through NF-κB2-RelB pathway reprograms adipocyte precursors as lymph node stromal cells. Immunity 2012; 37:721-34.
76. Sura R, Colombel JF, Van Kruiningen HJ. Lymphatics, tertiary lymphoid organs and the granulomas of Crohn's disease: an immunohistochemical study. Aliment Pharmacol Ther 2011; 33:930-9.
77. Desreumaux P, Ernst O, Geboes K et al. Inflammatory alterations in mesenteric adipose tissue in Crohn's disease. Gastroenterology 1999; 117:73-81.
78. Lindhout E, van EM, van PM, Lindeman J, Dinant HJ, de Groot C. Fibroblast-like synoviocytes from rheumatoid arthritis patients have intrinsic properties of follicular dendritic cells. J Immunol 1999; 162:5949-56.
79. Braun A, Takemura S, Vallejo AN, Goronzy JJ, Weyand CM. Lymphotoxin β-mediated stimulation of synoviocytes in rheumatoid arthritis. Arthritis Rheum 2004; 50:2140-50.
80. Phillips RJ, Burdick MD, Hong K et al. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest 2004; 114:438-46.
81. Reilkoff RA, Bucala R, Herzog EL. Fibrocytes: emerging effector cells in chronic inflammation. Nat Rev Immunol 2011; 11:427-35.
82. Barone F, Nayar S, Buckley CD. The role of non-hematopoietic stromal cells in the persistence of inflammation. Front Immunol 2012; 3:416.
83. Owens BM, Simmons A. Intestinal stromal cells in mucosal immunity and homeostasis. Mucosal Immunol 2013; 6:224-34.
84. Stott DI, Hiepe F, Hummel M, Steinhauser G, Berek C. Antigen-driven clonal proliferation of B cells within the target tissue of an autoimmune disease. The salivary glands of patients with Sjögren's syndrome. J Clin Invest 1998; 102:938-46.
85. Bombardieri M, Barone F, Humby F et al. Activation-induced cytidine deaminase expression in follicular dendritic cell networks and interfollicular large B cells supports functionality of ectopic lymphoid neogenesis in autoimmune sialoadenitis and MALT lymphoma in Sjogren's syndrome. J Immunol 2007; 179:4929-38.
86. Kaiserling E. Newly-formed lymph nodes in the submucosa in chronic inflammatory bowel disease. Lymphology 2001; 34:22-9.
87. Paavonen K, Mandelin J, Partanen T, Jussila L, Li TF, Ristimaki A, Alitalo K, Konttinen YT. Vascular endothelial growth factors C and D and their VEGFR-2 and 3 receptors in blood and lymphatic vessels in healthy and arthritic synovium. J Rheumatol 2002; 29:39-45.
88. Rangel-Moreno J, Hartson L, Navarro C, Gaxiola M, Selman M, Randall TD. Inducible bronchus-associated lymphoid tissue (iBALT) in patients with pulmonary complications of rheumatoid arthritis. J Clin Invest 2006; 116:3183-94.
89. Scandella E, Bolinger B, Lattmann E et al. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat Immunol 2008; 9:667-75.
90. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat Med 2004; 10:927-34.
91. Rangel-Moreno J, Moyron-Quiroz JE, Hartson L, Kusser K, Randall TD. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. Proc Natl Acad Sci USA 2007; 104:10577-82.
92. GeurtsvanKessel CH, Willart MA, Bergen IM et al. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J Exp Med 2009; 206:2339-49.
93. Rangel-Moreno J, Carragher DM, De la Luz Garcia-Hernandez M et al. The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat Immunol 2011; 12:639-46.
94. Cupedo T. An unexpected role for IL-17 in lymphoid organogenesis. Nat Immunol 2011; 12:590-2.
95. Fleige H, Haas JD, Stahl FR, Willenzon S, Prinz I, Förster R. Induction of BALT in the absence of IL-17. Nat Immunol 2012; 13:1 author reply 2.
96. Moyron-Quiroz JE, Rangel-Moreno J, Hartson L et al. Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity 2006; 25:643-54.
97. Magliozzi R, Howell O, Vora A, Serafini B, Nicholas R, Puopolo M, Reynolds R, Aloisi F. Meningeal B-cell follicles in secondary progressive multiple sclerosis associate with early onset of disease and severe cortical pathology. Brain 2007; 130:1089-104.
98. Kuerten S, Schickel A, Kerkloh C, Recks MS, Addicks K, Ruddle NH, Lehmann PV. Tertiary lymphoid organ development coincides with determinant spreading of the myelin-specific T cell response. Acta Neuropathol 2012; 124:861-73.
99. Kendall PL, Yu G, Woodward EJ, Thomas JW. Tertiary lymphoid structures in the pancreas promote selection of B lymphocytes in autoimmune diabetes. J Immunol 2007; 178:5643-51.
100. Szodoray P, Jellestad S, Teague MO, Jonsson R. Attenuated apoptosis of B cell activating factor-expressing cells in primary Sjogren's syndrome. Lab Invest 2003; 83:357-65.
101. McNamee EN, Masterson JC, Jedlicka P, Collins CB, Williams IR, Rivera-Nieves J. Ectopic lymphoid tissue alters the chemokine gradient, increases lymphocyte retention and exacerbates murine ileitis. Gut 2013; 62:53-62.
102. Weih F, ner R, Hu D, Beer M, Habenicht AJ. Control of dichotomic innate and adaptive immune responses by artery tertiary lymphoid organs in atherosclerosis. Front Physiol 2012; 3:226.
103. Browning JL. Inhibition of the lymphotoxin pathway as a therapy for autoimmune disease. Immunol Rev 2008; 223:202-20.
104. Columba-Cabezas S, Griguoli M, Rosicarelli B, Magliozzi R, Ria F, Serafini B, Aloisi F. Suppression of established experimental autoimmune encephalomyelitis and formation of meningeal lymphoid follicles by lymphotoxin β receptor-Ig fusion protein. J Neuroimmunol 2006; 179:76-86.
105. Gommerman JL, Browning JL. Lymphotoxin/light, lymphoid microenvironments and autoimmune disease. Nat Rev Immunol 2003; 3:642-55.
106. Wu Q, Salomon B, Chen M, Wang Y, Hoffman LM, Bluestone JA, Fu YX. Reversal of spontaneous autoimmune insulitis in nonobese diabetic mice by soluble lymphotoxin receptor. J Exp Med 2001; 193:1327-32.
107. Fava RA, Kennedy SM, Wood SG et al. Lymphotoxin-β receptor blockade reduces CXCL13 in lacrimal glands and improves corneal integrity in the NOD model of Sjogren's syndrome. Arthritis Res Ther 2011; 13:R182.
108. Mackay F, Browning JL, Lawton P et al. Both the lymphotoxin and tumor necrosis factor pathways are involved in experimental murine models of colitis. Gastroenterology 1998; 115:1464-75.
109. Fava RA, Notidis E, Hunt J et al. A role for the lymphotoxin/LIGHT axis in the pathogenesis of murine collagen-induced arthritis. J Immunol 2003; 171:115-26.
110. Finch DK, Ettinger R, Karnell JL, Herbst R, Sleeman MA. Effects of CXCL13 inhibition on lymphoid follicles in models of autoimmune disease. Eur J Clin Invest 2013; 43:501-9.
111. Fletcher AL, Lukacs-Kornek V, Reynoso ED et al. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J Exp Med 2010; 207:689-97.
112. Lukacs-Kornek V, Malhotra D, Fletcher AL, Acton SE, Elpek KG, Tayalia P, Collier AR, Turley SJ. Regulated release of nitric oxide by nonhematopoietic stroma controls expansion of the activated T cell pool in lymph nodes. Nat Immunol 2011; 12:1096-104.
113. Mueller SN, Matloubian M, Clemens DM, Sharpe AH, Freeman GJ, Gangappa S, Larsen CP, Ahmed R. Viral targeting of fibroblastic reticular cells contributes to immunosuppression and persistence during chronic infection. Proc Natl Acad Sci USA 2007; 104:15430-5.
114. Owens BM, Kaye PM. Stromal cell induction of regulatory dendritic cells. Front Immunol 2012; 3:262.
115. Matsumura Y. Cancer stromal targeting (CAST) therapy. Adv Drug Deliv Rev 2012; 64:710-9.
116. Thaunat O, Graff-Dubois S, Brouard S et al. Immune responses elicited in tertiary lymphoid tissues display distinctive features. PLoS ONE 2010; 5:e11398.
117. Onder L, Scandella E, Chai Q et al. A novel bacterial artificial chromosome-transgenic podoplanin-cre mouse targets lymphoid organ stromal cells in vivo. Front Immunol 2011; 2:50.
118. Turley SJ, Fletcher AL, Elpek KG. The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat Rev Immunol 2010; 10:813-25.
119. Mabbott NA, Kenneth BJ, Kobayashi A et al. Expression of mesenchyme-specific gene signatures by follicular dendritic cells: insights from the meta-analysis of microarray data from multiple mouse cell populations. Immunology 2011; 133:482-98.
120. Kratz A, Campos-Neto A, Hanson MS, Ruddle NH. Chronic inflammation caused by lymphotoxin is lymphoid neogenesis. J Exp Med 1996; 183:1461-72.
121. Lee Y, Chin RK, Christiansen P, Sun Y, Tumanov AV, Wang J, Chervonsky AV, Fu YX. Recruitment and activation of naive T cells in the islets by lymphotoxin β receptor-dependent tertiary lymphoid structure. Immunity 2006; 25:499-509.
122. Luther SA, Lopez T, Bai W, Hanahan D, Cyster JG. BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 2000; 12:471-81.
123. Luther SA, Bidgol A, Hargreaves DC, Schmidt A, Xu Y, Paniyadi J, Matloubian M, Cyster JG. Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J Immunol 2002; 169:424-33.
124. Furtado GC, Marinkovic T, Martin AP et al. Lymphotoxin β receptor signaling is required for inflammatory lymphangiogenesis in the thyroid. Proc Natl Acad Sci USA 2007; 104:5026-31.
125. Weninger W, Carlsen HS, Goodarzi M, Moazed F, Crowley MA, Baekkevold ES, Cavanagh LL, von Andrian UH. Naive T cell recruitment to nonlymphoid tissues: a role for endothelium-expressed CC chemokine ligand 21 in autoimmune disease and lymphoid neogenesis. J Immunol 2003; 170:4638-48.
126. Lee JJ, McGarry MP, Farmer SC et al. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J Exp Med 1997; 185:2143-56.
127. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 2006; 6:205-17.
128. Lötzer K, Döpping S, Connert S et al. Mouse aorta smooth muscle cells differentiate into lymphoid tissue organizer-like cells on combined tumor necrosis factor receptor-1/lymphotoxin β-receptor NF-κB signaling. Arterioscler Thromb Vasc Biol 2010; 30:395-402.