Antigen-presenting cells and antigen presentation in tertiary lymphoid organs

Frontiers in Immunology

Volumn 7, Issue NOV, 2016, Pages

  Hughes, Catherine E ^a   Benson, Robert A ^a   Bedaj, Marija ^a,b   Maffia, Pasquale ^a,c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Antigen presentation; Antigen presenting cells; B cells; Dendritic cells; Follicular dendritic cells; Macrophages; Tertiary lymphoid organs

Indexed keywords

ANTIGEN PRESENTATION; B LYMPHOCYTE; FOLLICULAR DENDRITIC CELL; LYMPHOID ORGAN; MACROPHAGE;

EID: 85006127997     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00481     Document Type: Short Survey

References (90)

1. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol (2006) 6(3):205-17. doi:10.1038/nri1786
2. Halle S, Dujardin HC, Bakocevic N, Fleige H, Danzer H, Willenzon S, et al. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J Exp Med (2009) 206(12):2593-601. doi:10.1084/jem.20091472
3. GeurtsvanKessel CH, Willart MA, Bergen IM, van Rijt LS, Muskens F, Elewaut D, 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(11):2339-49. doi:10.1084/jem.20090410
4. Jupelli M, Shimada K, Chiba N, Slepenkin A, Alsabeh R, Jones HD, et al. Chlamydia pneumoniae infection in mice induces chronic lung inflammation, iBALT formation, and fibrosis. PLoS One (2013) 8(10):e77447. doi:10.1371/journal.pone.0077447
5. Grabner R, Lotzer K, Dopping S, Hildner M, Radke D, Beer M, et al. Lymphotoxin beta receptor signaling promotes tertiary lymphoid organogenesis in the aorta adventitia of aged ApoE-/-mice. J Exp Med (2009) 206(1):233-48. doi:10.1084/jem.20080752
6. Yin C, Mohanta SK, Srikakulapu P, Weber C, Habenicht AJR. Artery tertiary lymphoid organs: powerhouses of atherosclerosis immunity. Front Immunol (2016) 7:387. doi:10.3389/fimmu.2016.00387
7. Hiraoka N, Ino Y, Yamazaki-Itoh R. Tertiary lymphoid organs in cancer tissues. Front Immunol (2016) 7:244. doi:10.3389/fimmu.2016.00244
8. Sautès-Fridman C, Lawand M, Giraldo NA, Kaplon H, Germain C, Fridman WH, et al. Tertiary lymphoid structures in cancers: prognostic value, regulation, and manipulation for therapeutic intervention. Front Immunol (2016) 7:407. doi:10.3389/fimmu.2016.00407
9. Pitzalis C, Jones GW, Bombardieri M, Jones SA. Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nat Rev Immunol (2014) 14(7):447-62. doi:10.1038/nri3700
10. Weyand CM, Goronzy JJ. Ectopic germinal center formation in rheumatoid synovitis. Ann N Y Acad Sci (2003) 987:140-9. doi:10.1111/j.1749-6632.2003.tb06042.x
11. Bombardieri M, Pitzalis C. Ectopic lymphoid neogenesis and lymphoid chemokines in Sjogren's syndrome: at the interplay between chronic inflammation, autoimmunity and lymphomagenesis. Curr Pharm Biotechnol (2012) 13(10):1989-96. doi:10.2174/138920112802273209
12. Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Aloisi F. Detection of ectopic B-cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol (2004) 14(2):164-74. doi:10.1111/j.1750-3639.2004.tb00049.x
13. Tumanov A, Kuprash D, Lagarkova M, Grivennikov S, Abe K, Shakhov A, et al. Distinct role of surface lymphotoxin expressed by B cells in the organization of secondary lymphoid tissues. Immunity (2002) 17(3):239-50. doi:10.1016/S1074-7613(02)00397-7
14. Kratz A, Campos-Neto A, Hanson MS, Ruddle NH. Chronic inflammation caused by lymphotoxin is lymphoid neogenesis. J Exp Med (1996) 183(4):1461-72. doi:10.1084/jem.183.4.1461
15. Barone F, Nayar S, Campos J, Cloake T, Withers DR, Toellner KM, et al. IL-22 regulates lymphoid chemokine production and assembly of tertiary lymphoid organs. Proc Natl Acad Sci U S A (2015) 112(35):11024-9. doi:10.1073/pnas.1503315112
16. Marinkovic T, Garin A, Yokota Y, Fu YX, Ruddle NH, Furtado GC, et al. Interaction of mature CD3+CD4+ T cells with dendritic cells triggers the development of tertiary lymphoid structures in the thyroid. J Clin Invest (2006) 116(10):2622-32. doi:10.1172/jci28993
17. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K, Hartson L, Sprague F, Goodrich S, et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat Med (2004) 10(9):927-34. doi:10.1038/nm1091
18. 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(12):3183-94. doi:10.1172/jci28756
19. Jones GW, Hill DG, Jones SA. Understanding immune cells in tertiary lymphoid organ development: it is all starting to come together. Front Immunol (2016) 7:401. doi:10.3389/fimmu.2016.00401
20. Guedj K, Khallou-Laschet J, Clement M, Morvan M, Gaston AT, Fornasa G, et al. M1 macrophages act as LTβR-independent lymphoid tissue inducer cells during atherosclerosis-related lymphoid neogenesis. Cardiovasc Res (2014) 101(3):434-43. doi:10.1093/cvr/cvt263
21. 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(9):5720-8. doi:10.4049/jimmunol.174.9.5720
22. Ruddle NH. Lymphatic vessels and tertiary lymphoid organs. J Clin Invest (2014) 124(3):953-9. doi:10.1172/jci71611
23. Kambayashi T, Laufer TM. Atypical MHC class II-expressing antigen-presenting cells: can anything replace a dendritic cell? Nat Rev Immunol (2014) 14(11):719-30. doi:10.1038/nri3754
24. Muniz LR, Pacer ME, Lira SA, Furtado GC. A critical role for dendritic cells in the formation of lymphatic vessels within tertiary lymphoid structures. J Immunol (2011) 187(2):828-34. doi:10.4049/jimmunol.1004233
25. Browning JL, Allaire N, Ngam-Ek A, Notidis E, Hunt J, Perrin S, et al. Lymphotoxin-beta receptor signaling is required for the homeostatic control of HEV differentiation and function. Immunity (2005) 23(5):539-50. doi:10.1016/j.immuni.2005.10.002
26. Ludewig B, Odermatt B, Landmann S, Hengartner H, Zinkernagel RM. Dendritic cells induce autoimmune diabetes and maintain disease via de novo formation of local lymphoid tissue. J Exp Med (1998) 188(8):1493-501. doi:10.1084/jem.188.8.1493
27. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol (2008) 26(27):4410-7. doi:10.1200/JCO.2007.15.0284
28. Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med (2014) 189(7):832-44. doi:10.1164/rccm.201309-1611OC
29. Cho HJ, Shashkin P, Gleissner CA, Dunson D, Jain N, Lee JK, et al. Induction of dendritic cell-like phenotype in macrophages during foam cell formation. Physiol Genomics (2007) 29(2):149-60. doi:10.1152/physiolgenomics.00051.2006
30. Chen X, Jensen PE. The role of B lymphocytes as antigen-presenting cells. Arch Immunol Ther Exp (2008) 56(2):77-83. doi:10.1007/s00005-008-0014-5
31. Srikakulapu P, Hu D, Yin C, Mohanta SK, Bontha SV, Peng L, et al. Artery tertiary lymphoid organs control multilayered territorialized atherosclerosis B-cell responses in aged ApoE-/-mice. Arterioscler Thromb Vasc Biol (2016) 36(6):1174-85. doi:10.1161/ATVBAHA.115.306983
32. Germain C, Gnjatic S, Dieu-Nosjean MC. Tertiary lymphoid structure-associated B cells are key players in anti-tumor immunity. Front Immunol (2015) 6:67. doi:10.3389/fimmu.2015.00067
33. Jones GW, Jones SA. Ectopic lymphoid follicles: inducible centres for generating antigen-specific immune responses within tissues. Immunology (2016) 147(2):141-51. doi:10.1111/imm.12554
34. MacLennan IC. Germinal centers. Annu Rev Immunol (1994) 12:117-39. doi:10.1146/annurev.iy.12.040194.001001
35. Fu YX, Huang G, Wang Y, Chaplin DD. B lymphocytes induce the formation of follicular dendritic cell clusters in a lymphotoxin alpha-dependent fashion. J Exp Med (1998) 187(7):1009-18. doi:10.1084/jem.187.7.1009
36. Allen CD, Cyster JG. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol (2008) 20(1):14-25. doi:10.1016/j.smim.2007.12.001
37. Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R, Sedgwick JD, et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature (2000) 406(6793):309-14. doi:10.1038/35018581
38. Le Pottier L, Devauchelle V, Fautrel A, Daridon C, Saraux A, Youinou P, et al. Ectopic germinal centers are rare in Sjogren's syndrome salivary glands and do not exclude autoreactive B cells. J Immunol (2009) 182(6):3540-7. doi:10.4049/jimmunol.0803588
39. Heesters BA, Myers RC, Carroll MC. Follicular dendritic cells: dynamic antigen libraries. Nat Rev Immunol (2014) 14(7):495-504. doi:10.1038/nri3689
40. Kranich J, Krautler NJ. How follicular dendritic cells shape the B-cell antigenome. Front Immunol (2016) 7:225. doi:10.3389/fimmu.2016.00225
41. Victoratos P, Kollias G. Induction of autoantibody-mediated spontaneous arthritis critically depends on follicular dendritic cells. Immunity (2009) 30(1):130-42. doi:10.1016/j.immuni.2008.10.019
42. Drayton DL, Ying X, Lee J, Lesslauer W, Ruddle NH. Ectopic LT alpha beta directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J Exp Med (2003) 197(9):1153-63. doi:10.1084/jem.20021761
43. Moser B, Schaerli P, Loetscher P. CXCR5(+) T cells: follicular homing takes center stage in T-helper-cell responses. Trends Immunol (2002) 23(5):250-4. doi:10.1016/S1471-4906(02)02218-4
44. Barone F, Bombardieri M, Manzo A, Blades MC, Morgan PR, Challacombe SJ, et al. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjogren's syndrome. Arthritis Rheum (2005) 52(6):1773-84. doi:10.1002/art.21062
45. 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. doi:10.3389/fimmu.2012.00350
46. Fleige H, Ravens S, Moschovakis GL, Bölter J, Willenzon S, Sutter G, et al. IL-17-induced CXCL12 recruits B cells and induces follicle formation in BALT in the absence of differentiated FDCs. J Exp Med (2014) 211(4):643-51. doi:10.1084/jem.20131737
47. El Shikh ME, Pitzalis C. Follicular dendritic cells in health and disease. Front Immunol (2012) 3:292. doi:10.3389/fimmu.2012.00292
48. Ishimaru N, Arakaki R, Yoshida S, Yamada A, Noji S, Hayashi Y. Expression of the retinoblastoma protein RbAp48 in exocrine glands leads to Sjogren's syndrome-like autoimmune exocrinopathy. J Exp Med (2008) 205(12):2915-27. doi:10.1084/jem.20080174
49. Kapsogeorgou EK, Moutsopoulos HM, Manoussakis MN. Functional expression of a costimulatory B7.2 (CD86) protein on human salivary gland epithelial cells that interacts with the CD28 receptor, but has reduced binding to CTLA4. J Immunol (2001) 166(5):3107-13. doi:10.4049/jimmunol.166.5.3107
50. Dimitriou ID, Kapsogeorgou EK, Moutsopoulos HM, Manoussakis MN. CD40 on salivary gland epithelial cells: high constitutive expression by cultured cells from Sjogren's syndrome patients indicating their intrinsic activation. Clin Exp Immunol (2002) 127(2):386-92. doi:10.1046/j.1365-2249.2002.01752.x
51. Tsunawaki S, Nakamura S, Ohyama Y, Sasaki M, Ikebe-Hiroki A, Hiraki A, et al. Possible function of salivary gland epithelial cells as nonprofessional antigen-presenting cells in the development of Sjogren's syndrome. J Rheumatol (2002) 29(9):1884-96.
52. Londei M, Lamb JR, Bottazzo GF, Feldmann M. Epithelial cells expressing aberrant MHC class II determinants can present antigen to cloned human T cells. Nature (1984) 312(5995):639-41. doi:10.1038/312639a0
53. Cohen JN, Guidi CJ, Tewalt EF, Qiao H, Rouhani SJ, Ruddell A, et al. Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J Exp Med (2010) 207(4):681-8. doi:10.1084/jem.20092465
54. Gardner JM, Devoss JJ, Friedman RS, Wong DJ, Tan YX, Zhou X, et al. Deletional tolerance mediated by extrathymic Aire-expressing cells. Science (2008) 321(5890):843-7. doi:10.1126/science.1159407
55. van Delft MA, Huitema LF, Tas SW. The contribution of NF-κB signalling to immune regulation and tolerance. Eur J Clin Invest (2015) 45(5):529-39. doi:10.1111/eci.12430
56. Fletcher AL, Lukacs-Kornek V, Reynoso ED, Pinner SE, Bellemare-Pelletier A, Curry MS, et al. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J Exp Med (2010) 207(4):689-97. doi:10.1084/jem.20092642
57. Link A, Hardie DL, Favre S, Britschgi MR, Adams DH, Sixt M, et al. Association of T-zone reticular networks and conduits with ectopic lymphoid tissues in mice and humans. Am J Pathol (2011) 178(4):1662-75. doi:10.1016/j.ajpath.2010.12.039
58. Bajenoff M, Granjeaud S, Guerder S. The strategy of T cell antigen-presenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J Exp Med (2003) 198(5):715-24. doi:10.1084/jem.20030167
59. Sixt M, Kanazawa N, Selg M, Samson T, Roos G, Reinhardt DP, et al. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity (2005) 22(1):19-29. doi:10.1016/j.immuni.2004.11.013
60. Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, Mebius RE, et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity (2009) 30(2):264-76. doi:10.1016/j.immuni.2008.12.014
61. Bajenoff M, Germain RN. B-cell follicle development remodels the conduit system and allows soluble antigen delivery to follicular dendritic cells. Blood (2009) 114(24):4989-97. doi:10.1182/blood-2009-06-229567
62. Clark SL Jr. The reticulum of lymph nodes in mice studied with the electron microscope. Am J Anat (1962) 110:217-57. doi:10.1002/aja.1001100303
63. Pape KA, Catron DM, Itano AA, Jenkins MK. The humoral immune response is initiated in lymph nodes by B cells that acquire soluble antigen directly in the follicles. Immunity (2007) 26(4):491-502. doi:10.1016/j.immuni.2007.02.011
64. Carrasco YR, Batista FD. 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 (2007) 27(1):160-71. doi:10.1016/j.immuni.2007.06.007
65. Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, Boes M, et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature (2007) 450(7166):110-4. doi:10.1038/nature06287
66. Phan TG, Grigorova I, Okada T, Cyster JG. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat Immunol (2007) 8(9):992-1000. doi:10.1038/ni1494
67. Qi H, Egen JG, Huang AY, Germain RN. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science (2006) 312(5780):1672-6. doi:10.1126/science.1125703
68. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science (2005) 307(5715):1630-4. doi:10.1126/science.1108003
69. Penaranda C, Tang Q, Ruddle NH, Bluestone JA. Prevention of diabetes by FTY720-mediated stabilization of peri-islet tertiary lymphoid organs. Diabetes (2010) 59(6):1461-8. doi:10.2337/db09-1129
70. Kraal G. Cells in the marginal zone of the spleen. Int Rev Cytol (1992) 132:31-74. doi:10.1016/S0074-7696(08)62453-5
71. Nolte MA, Belien JA, Schadee-Eestermans I, Jansen W, Unger WW, van Rooijen N, et al. A conduit system distributes chemokines and small blood-borne molecules through the splenic white pulp. J Exp Med (2003) 198(3):505-12. doi:10.1084/jem.20021801
72. Hu D, Mohanta SK, Yin C, Peng L, Ma Z, Srikakulapu P, et al. Artery tertiary lymphoid organs control aorta immunity and protect against atherosclerosis via vascular smooth muscle cell lymphotoxin beta receptors. Immunity (2015) 42(6):1100-15. doi:10.1016/j.immuni.2015.05.015
73. Macritchie N, Grassia G, Sabir SR, Maddaluno M, Welsh P, Sattar N, et al. Plasmacytoid dendritic cells play a key role in promoting atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol (2012) 32(11):2569-79. doi:10.1161/ATVBAHA.112.251314
74. Sage AP, Murphy D, Maffia P, Masters LM, Sabir SR, Baker LL, et al. MHC Class II-restricted antigen presentation by plasmacytoid dendritic cells drives proatherogenic T cell immunity. Circulation (2014) 130(16):1363-73. doi:10.1161/CIRCULATIONAHA.114.011090
75. Maddaluno M, MacRitchie N, Grassia G, Ialenti A, Butcher JP, Garside P, et al. Murine aortic smooth muscle cells acquire, though fail to present exogenous protein antigens on major histocompatibility complex class II molecules. Biomed Res Int (2014) 2014:949845. doi:10.1155/2014/949845
76. Obst R, van Santen HM, Melamed R, Kamphorst AO, Benoist C, Mathis D. Sustained antigen presentation can promote an immunogenic T cell response, like dendritic cell activation. Proc Natl Acad Sci U S A (2007) 104(39):15460-5. doi:10.1073/pnas.0707331104
77. Celli S, Lemaitre F, Bousso P. Real-time manipulation of T cell-dendritic cell interactions in vivo reveals the importance of prolonged contacts for CD4+ T cell activation. Immunity (2007) 27(4):625-34. doi:10.1016/j.immuni.2007.08.018
78. Baumjohann D, Preite S, Reboldi A, Ronchi F, Ansel KM, Lanzavecchia A, et al. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity (2013) 38(3):596-605. doi:10.1016/j.immuni.2012.11.020
79. Henrickson SE, Perro M, Loughhead SM, Senman B, Stutte S, Quigley M, et al. Antigen availability determines CD8(+) T cell-dendritic cell interaction kinetics and memory fate decisions. Immunity (2013) 39(3):496-507. doi:10.1016/j.immuni.2013.08.034
80. Rabenstein H, Behrendt AC, Ellwart JW, Naumann R, Horsch M, Beckers J, et al. Differential kinetics of antigen dependency of CD4+ and CD8+ T cells. J Immunol (2014) 192(8):3507-17. doi:10.4049/jimmunol.1302725
81. Benson RA, MacLeod MK, Hale BG, Patakas A, Garside P, Brewer JM. Antigen presentation kinetics control T cell/dendritic cell interactions and follicular helper T cell generation in vivo. Elife (2015) 4. doi:10.7554/eLife.06994
82. Joshi NS, Akama-Garren EH, Lu Y, Lee DY, Chang GP, Li A, et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity (2015) 43(3):579-90. doi:10.1016/j.immuni.2015.08.006
83. Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature (2004) 427(6970):154-9. doi:10.1038/nature02238
84. Zinselmeyer BH, Dempster J, Gurney AM, Wokosin D, Miller M, Ho H, et al. In situ characterization of CD4+ T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J Exp Med (2005) 201(11):1815-23. doi:10.1084/jem.20050203
85. Nasr IW, Reel M, Oberbarnscheidt MH, Mounzer RH, Baddoura FK, Ruddle NH, et al. Tertiary lymphoid tissues generate effector and memory T cells that lead to allograft rejection. Am J Transplant (2007) 7(5):1071-9. doi:10.1111/j.1600-6143.2007.01756.x
86. Itano AA, Jenkins MK. Antigen presentation to naive CD4 T cells in the lymph node. Nat Immunol (2003) 4(8):733-9. doi:10.1038/ni957
87. Cyster JG. B cell follicles and antigen encounters of the third kind. Nat Immunol (2010) 11(11):989-96. doi:10.1038/ni.1946
88. Germain RN, Robey EA, Cahalan MD. A decade of imaging cellular motility and interaction dynamics in the immune system. Science (2012) 336(6089):1676-81. doi:10.1126/science.1221063
89. Robins H. Immunosequencing: applications of immune repertoire deep sequencing. Curr Opin Immunol (2013) 25(5):646-52. doi:10.1016/j.coi.2013.09.017
90. Calis JJ, Rosenberg BR. Characterizing immune repertoires by high throughput sequencing: strategies and applications. Trends Immunol (2014) 35(12):581-90. doi:10.1016/j.it.2014.09.004