Unique transcompartmental bridge: Antigen-presenting cells sampling across endothelial and mucosal barriers

Frontiers in Immunology

Volumn 7, Issue JUN, 2016, Pages

  Allen, Frederick ^a   Tong, Alexander A ^a   Huang, Alex Y ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Antigen capture; Antigen presentation; Antigen presenting cell; Cell migration; Dendritic cell; Mucosal immunity; T cell activation; Transcompartment

Indexed keywords

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; BEHAVIOR; CELL MIGRATION; DENDRITIC CELL; GASTROINTESTINAL TRACT; HUMAN; HUMAN TISSUE; IMAGING; IMMUNOSURVEILLANCE; INNATE IMMUNITY; MUCOSAL IMMUNITY; RESPIRATORY TRACT MUCOSA; SAMPLING; SKIN; T LYMPHOCYTE ACTIVATION;

EID: 84977562474     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00231     Document Type: Review

References (60)

1. 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) 22:19-29. doi:10.1016/j.immuni.2004.11.013
2. Cyster JG, Ansel KM, Reif K, Ekland EH, Hyman PL, Tang HL, et al. Follicular stromal cells and lymphocyte homing to follicles. Immunol Rev (2000) 176:181-93. doi:10.1034/j.1600-065X.2000.00618.x
3. Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu Rev Immunol (2001) 19:47-64. doi:10.1146/annurev.immunol.19.1.47
4. Neutra MR, Pringault E, Kraehenbuhl JP. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol (1996) 14:275-300. doi:10.1146/annurev.immunol.14.1.275
5. Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A. Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol (2013) 6:666-77. doi:10.1038/mi.2013.30
6. Mowat AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol (2003) 3:331-41. doi:10.1038/nri1057
7. Jaensson E, Uronen-Hansson H, Pabst O, Eksteen B, Tian J, Coombes JL, et al. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med (2008) 205:2139-49. doi:10.1084/jem.20080414
8. Bogunovic M, Ginhoux F, Helft J, Shang L, Hashimoto D, Greter M, et al. Origin of the lamina propria dendritic cell network. Immunity (2009) 31:513-25. doi:10.1016/j.immuni.2009.08.010
9. Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity (2009) 31:502-12. doi:10.1016/j.immuni.2009.06.025
10. Persson EK, Jaensson E, Agace WW. The diverse ontogeny and function of murine small intestinal dendritic cell/macrophage subsets. Immunobiology (2010) 215:692-7. doi:10.1016/j.imbio.2010.05.013
11. Varol C, Zigmond E, Jung S. Securing the immune tightrope: mononuclear phagocytes in the intestinal lamina propria. Nat Rev Immunol (2010) 10:415-26. doi:10.1038/nri2778
12. Gross M, Salame T-M, Jung S. Guardians of the gut-murine intestinal macrophages and dendritic cells. Front Immunol (2015) 6:254. doi:10.3389/fimmu.2015.00254
13. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol (2001) 2:361-7. doi:10.1038/86373
14. Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science (2005) 307:254-8. doi:10.1126/science.1102901
15. Chieppa M, Rescigno M, Huang AYC, Germain RN. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med (2006) 203:2841-52. doi:10.1084/jem.20061884
16. Arques JL, Hautefort I, Ivory K, Bertelli E, Regoli M, Clare S, et al. Salmonella induces flagellin-and MyD88-dependent migration of bacteria-capturing dendritic cells into the gut lumen. Gastroenterology (2009) 137:579-87.e1-2. doi:10.1053/j.gastro.2009.04.010
17. Hapfelmeier S, Müller AJ, Stecher B, Kaiser P, Barthel M, Endt K, et al. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. J Exp Med (2008) 205:437-50. doi:10.1084/jem.20070633
18. Lelouard H, Fallet M, Bovis B, de Méresse S, Gorvel J-P. Peyer's patch dendritic cells sample antigens by extending dendrites through M cell-specific transcellular pores. Gastroenterology (2012) 142:592-601.e3. doi:10.1053/j.gastro.2011.11.039
19. McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature (2012) 483:345-9. doi:10.1038/nature10863
20. Xu C, Shen Y, Littman DR, Dustin ML, Velázquez P. Visualization of mucosal homeostasis via single-and multiphoton intravital fluorescence microscopy. J Leukoc Biol (2012) 92:413-9. doi:10.1189/jlb.0711344
21. Farache J, Koren I, Milo I, Gurevich I, Kim KW, Zigmond E, et al. Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity (2013) 38:581-95. doi:10.1016/j.immuni.2013.01.009
22. Vallon-Eberhard A, Landsman L, Yogev N, Verrier B, Jung S. Transepithelial pathogen uptake into the small intestinal lamina propria. J Immunol (2006) 176:2465-9. doi:10.4049/jimmunol.176.4.2465
23. Schulz O, Jaensson E, Persson EK, Liu X, Worbs T, Agace WW, et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med (2009) 206:3101-14. doi:10.1084/jem.20091925
24. Chang S-Y, Song JH, Guleng B, Cotoner CA, Arihiro S, Zhao Y, et al. Circulatory antigen processing by mucosal dendritic cells controls CD8+ T cell activation. Immunity (2013) 38:153-65. doi:10.1016/j.immuni.2012.09.018
25. Mazzini E, Massimiliano L, Penna G, Rescigno M. Oral tolerance can be established via gap junction transfer of fed antigens from CX3CR1+ macrophages to CD103+ dendritic cells. Immunity (2014) 40:248-61. doi:10.1016/j.immuni.2013.12.012
26. Nossal G, Ada GL, Austin CM, Pye J. Antigens in immunity: VIII. Localization of 125I-labelled antigens in the secondary response. Immunology (1965) 9(4):349-57.
27. Anderson AO, Anderson ND. Studies on the structure and permeability of the microvasculature in normal rat lymph nodes. Am J Pathol (1975) 80:387-418.
28. Ansel KM, Ngo VN, Hyman PL, Luther SA, Förster R, Sedgwick JD, et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature (2000) 406:309-14. doi:10.1038/35018581
29. Nossal GJ, Abbot A, Mitchell J, Lummus Z. Antigens in immunity. XV. Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J Exp Med (1968) 127:277-90. doi:10.1084/jem.127.2.277
30. Allen CDC, Cyster JG. Follicular dendritic cell networks of primary follicles and germinal centers: phenotype and function. Semin Immunol (2008) 20:14-25. doi:10.1016/j.smim.2007.12.001
31. BajénoffM, Germain RN. B-cell follicle development remodels the conduit system and allows soluble antigen delivery to follicular dendritic cells. Blood (2009) 114:4989-97. doi:10.1182/blood-2009-06-229567
32. Hirosue S, Dubrot J. Modes of antigen presentation by lymph node stromal cells and their immunological implications. Front Immunol (2015) 6:446. doi:10.3389/fimmu.2015.00446
33. Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity (2006) 24:19-28. doi:10.1016/j.immuni.2005.11.010
34. Carroll MC. The complement system in regulation of adaptive immunity. Nat Immunol (2004) 5:981-6. doi:10.1038/ni1113
35. Berger M, Fleisher TA. Native C3 does not bind to the C3b receptor (CR1) of human blood B lymphocytes or alter immunoglobulin synthesis. J Immunol (1983) 130:1021-3.
36. Suzuki K, Grigorova I, Phan TG, Kelly LM, Cyster JG. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med (2009) 206:1485-93. doi:10.1084/jem.20090209
37. 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) 8:992-1000. doi:10.1038/ni1494
38. 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) 30:264-76. doi:10.1016/j.immuni.2008.12.014
39. Heesters BA, Myers RC, Carroll MC. Follicular dendritic cells: dynamic antigen libraries. Nat Rev Immunol (2014) 14:495-504. doi:10.1038/nri3689
40. Girard JP, Moussion C, Förster R. HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat Rev Immunol (2012) 12(11):762-73. doi:10.1038/nri3298
41. Manickasingham SP, Reise Sousa C. Mature T cell seeks antigen for meaningful relationship in lymph node. Immunology (2001) 102:381-6. doi:10.1046/j.1365-2567.2001.01219.x
42. Manickasingham S, Sousa CE. Microbial and T cell-derived stimuli regulate antigen presentation by dendritic cells in vivo. J Immunol (2000) 165:5027-34. doi:10.4049/jimmunol.165.9.5027
43. Itano AA, McSorley SJ, Reinhardt RL, Ehst BD, Ingulli E, Rudensky AY, et al. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity (2003) 19:47-57. doi:10.1016/S1074-7613(03)00175-4
44. Gray EE, Cyster JG. Lymph node macrophages. J Innate Immun (2012) 4:424-36. doi:10.1159/000337007
45. Mebius RE, Streeter PR, Brevé J, Duijvestijn AM, Kraal G. The influence of afferent lymphatic vessel interruption on vascular addressin expression. J Cell Biol (1991) 115:85-95. doi:10.1083/jcb.115.1.85
46. 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) 27:160-71. doi:10.1016/j.immuni.2007.06.007
47. Szakal AK, Holmes KL, Tew JG. Transport of immune complexes from the subcapsular sinus to lymph node follicles on the surface of nonphagocytic cells, including cells with dendritic morphology. J Immunol (1983) 131:1714-27.
48. Förster R, Braun A, Worbs T. Lymph node homing of T cells and dendritic cells via afferent lymphatics. Trends Immunol (2012) 33(6):271-80. doi:10.1016/j.it.2012.02.007
49. Braun A, Worbs T, Moschovakis GL, Halle S, Hoffmann K, Bölter J, et al. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat Immunol (2011) 12:879-87. doi:10.1038/ni.2085
50. Gerner MY, Torabi-Parizi P, Germain RN. Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens. Immunity (2015) 42:172-85. doi:10.1016/j.immuni.2014.12.024
51. Sung S, Fu SM, Rose CE, Gaskin F. A major lung CD103 (aE)-ß7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol (2006) 176(4):2161-72. doi:10.4049/jimmunol.176.4.2161
52. Jahnsen FL, Strickland DH, Thomas JA, Tobagus IT, Napoli S, Zosky GR, et al. Accelerated antigen sampling and transport by airway mucosal dendritic cells following inhalation of a bacterial stimulus. J Immunol (2006) 177(9):5861-7. doi:10.4049/jimmunol.177.9.5861
53. Hammad H, Lambrecht BN. Dendritic cells and epithelial cells: linking innate and adaptive immunity in asthma. Nat Rev Immunol (2008) 8:193-204. doi:10.1038/nri2275
54. Zoltán Veres T, Voedisch S, Spies E, Tschernig T, Braun A. Spatiotemporal and functional behavior of airway dendritic cells visualized by two-photon microscopy. Am J Pathol (2011) 179:603-9. doi:10.1016/j.ajpath.2011.04.039
55. Thornton EE, Looney MR, Bose O, Sen D, Sheppard D, Locksley R, et al. Spatiotemporally separated antigen uptake by alveolar dendritic cells and airway presentation to T cells in the lung. J Exp Med (2012) 209:1183-99. doi:10.1084/jem.20112667
56. Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med (2009) 15:410-6. doi:10.1038/nm.1946
57. Nimmerjahn A, KirchhoffF, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science (2005) 308:1314-8. doi:10.1126/science.1110647
58. Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol (2004) 75:388-97. doi:10.1189/jlb.0303114
59. Barkauskas DS, Evans TA, Myers J, Petrosiute A, Silver J, Huang AY. Extravascular CX3CR1+ cells extend intravascular dendritic processes into intact central nervous system vessel lumen. Microsc Microanal (2013) 19:778-90. doi:10.1017/S1431927613000482
60. Hammad H, Lambrecht BN. Dendritic cells and airway epithelial cells at the interface between innate and adaptive immune responses. Allergy (2011) 66:579-87. doi:10.1111/j.1398-9995.2010.02528.x