Location, location, location: Tissue-specific regulation of immune responses

Journal of Leukocyte Biology

Volumn 94, Issue 3, 2013, Pages 409-421

  Hu, Wei ^a   Pasare, Chandrashekhar ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Dendritic cell; Microbiota; Microenvironment

Indexed keywords

BETA CATENIN; CD103 ANTIGEN; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; INTERLEUKIN 6; INTERLEUKIN 8; LANGERIN; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; AUTOIMMUNITY; B LYMPHOCYTE; CANDIDA ALBICANS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; COMMENSAL; CONTACT ALLERGY; CYTOKINE PRODUCTION; DENDRITIC CELL; GERMINAL CENTER; HUMAN; IMMUNOREGULATION; INTESTINE MUCOSA; MACROPHAGE; MEMORY T LYMPHOCYTE; MICROENVIRONMENT; MICROFLORA; MICROORGANISM DETECTION; MUCOSAL IMMUNITY; NONHUMAN; PHENOTYPE; POSITIVE FEEDBACK; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SKIN LEISHMANIASIS; STROMA CELL; TISSUE SPECIFICITY;

DENDRITIC CELL; MICROBIOTA; MICROENVIRONMENT;

ANIMALS; B-LYMPHOCYTES; CELLULAR MICROENVIRONMENT; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; MACROPHAGES; ORGAN SPECIFICITY; T-LYMPHOCYTES;

EID: 84883217531     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0413207     Document Type: Review

References (165)

1. Iwasaki, A. (2007) Mucosal dendritic cells. Annu. Rev. Immunol. 25, 381-418.
2. Steinman, R. M. (2012) Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30, 1-22.
3. Cerutti, A., Puga, I., Cols, M. (2012) New helping friends for B cells. Eur. J. Immunol. 42, 1956-1968.
4. Itano, A. A., Jenkins, M. K. (2003) Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 4, 733-739.
5. Geissmann, F., Manz, M. G., Jung, S., Sieweke, M. H., Merad, M., Ley, K. (2010) Development of monocytes, macrophages, and dendritic cells. Science 327, 656-661.
6. Murray, P. J., Wynn, T. A. (2011) Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737.
7. McGaha, T. L., Chen, Y., Ravishankar, B., van Rooijen, N., Karlsson, M. C. (2011) Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 117, 5403-5412.
8. Junt, T., Moseman, E. A., Iannacone, M., Massberg, S., Lang, P. A., Boes, M., Fink, K., Henrickson, S. E., Shayakhmetov, D. M., Di Paolo, N. C., van Rooijen, N., Mempel, T. R., Whelan, S. P., von Andrian, U. H. (2007) Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450, 110-114.
9. Shortman, K., Liu, Y. J. (2002) Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2, 151-161.
10. Henri, S., Vremec, D., Kamath, A., Waithman, J., Williams, S., Benoist, C., Burnham, K., Saeland, S., Handman, E., Shortman, K. (2001) The dendritic cell populations of mouse lymph nodes. J. Immunol. 167, 741-748.
11. Villadangos, J. A., Schnorrer, P. (2007) Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 7, 543-555.
12. Kamath, A. T., Henri, S., Battye, F., Tough, D. F., Shortman, K. (2002) Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 100, 1734-1741.
13. Geissmann, F., Dieu-Nosjean, M. C., Dezutter, C., Valladeau, J., Kayal, S., Leborgne, M., Brousse, N., Saeland, S., Davoust, J. (2002) Accumulation of immature Langerhans cells in human lymph nodes draining chronically inflamed skin. J. Exp. Med. 196, 417-430.
14. De Heusch, M., Blocklet, D., Egrise, D., Hauquier, B., Vermeersch, M., Goldman, S., Moser, M. (2007) Bidirectional MHC molecule exchange between migratory and resident dendritic cells. J. Leukoc. Biol. 82, 861-868.
15. Nestle, F. O., Di Meglio, P., Qin, J. Z., Nickoloff, B. J. (2009) Skin immune sentinels in health and disease. Nat. Rev. Immunol. 9, 679-691.
16. Allan, R. S., Smith, C. M., Belz, G. T., van Lint, A. L., Wakim, L. M., Heath, W. R., Carbone, F. R. (2003) Epidermal viral immunity induced by CD8α+ dendritic cells but not by Langerhans cells. Science 301, 1925-1928.
17. Ritter, U., Meissner, A., Scheidig, C., Korner, H. (2004) CD8 α-and Langerin-negative dendritic cells, but not Langerhans cells, act as principal antigen-presenting cells in leishmaniasis. Eur. J. Immunol. 34, 1542-1550.
18. Brewig, N., Kissenpfennig, A., Malissen, B., Veit, A., Bickert, T., Fleischer, B., Mostbock, S., Ritter, U. (2009) Priming of CD8+ and CD4+ T cells in experimental leishmaniasis is initiated by different dendritic cell subtypes. J. Immunol. 182, 774-783.
19. Bedoui, S., Whitney, P. G., Waithman, J., Eidsmo, L., Wakim, L., Caminschi, I., Allan, R. S., Wojtasiak, M., Shortman, K., Carbone, F. R., Brooks, A. G., Heath, W. R. (2009) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10, 488-495.
20. Igyarto, B. Z., Haley, K., Ortner, D., Bobr, A., Gerami-Nejad, M., Edelson, B. T., Zurawski, S. M., Malissen, B., Zurawski, G., Berman, J., Kaplan, D. H. (2011) Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35, 260-272.
21. Henri, S., Poulin, L. F., Tamoutounour, S., Ardouin, L., Guilliams, M., de Bovis, B., Devilard, E., Viret, C., Azukizawa, H., Kissenpfennig, A., Malissen, B. (2010) CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207, 189-206.
22. Romani, N., Brunner, P. M., Stingl, G. (2012) Changing views of the role of Langerhans cells. J. Invest. Dermatol. 132, 872-881.
23. Honda, T., Nakajima, S., Egawa, G., Ogasawara, K., Malissen, B., Miyachi, Y., Kabashima, K. (2010) Compensatory role of Langerhans cells and langerin-positive dermal dendritic cells in the sensitization phase of murine contact hypersensitivity. J. Allergy Clin. Immunol. 125, 1154. e2-1156. e2.
24. Noordegraaf, M., Flacher, V., Stoitzner, P., Clausen, B. E. (2010) Functional redundancy of Langerhans cells and Langerin+ dermal dendritic cells in contact hypersensitivity. J. Invest. Dermatol. 130, 2752-2759.
25. Mayerova, D., Parke, E. A., Bursch, L. S., Odumade, O. A., Hogquist, K. A. (2004) Langerhans cells activate naive self-antigen-specific CD8 T cells in the steady state. Immunity 21, 391-400.
26. Kautz-Neu, K., Noordegraaf, M., Dinges, S., Bennett, C. L., John, D., Clausen, B. E., von Stebut, E. (2011) Langerhans cells are negative regulators of the anti-Leishmania response. J. Exp. Med. 208, 885-891.
27. Kaplan, D. H., Jenison, M. C., Saeland, S., Shlomchik, W. D., Shlomchik, M. J. (2005) Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23, 611-620.
28. Shklovskaya, E., O'Sullivan, B. J., Ng, L. G., Roediger, B., Thomas, R., Weninger, W., Fazekas de St Groth, B. (2011) Langerhans cells are precommitted to immune tolerance induction. Proc. Natl. Acad. Sci. USA 108, 18049-18054.
29. Schwarz, A., Noordegraaf, M., Maeda, A., Torii, K., Clausen, B. E., Schwarz, T. (2010) Langerhans cells are required for UVR-induced immunosuppression. J. Invest. Dermatol. 130, 1419-1427.
30. Rescigno, M. (2010) Intestinal dendritic cells. Adv. Immunol. 107, 109-138.
31. Coombes, J. L., Powrie, F. (2008) Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8, 435-446.
32. Flores-Langarica, A., Meza-Perez, S., Calderon-Amador, J., Estrada-Garcia, T., Macpherson, G., Lebecque, S., Saeland, S., Steinman, R. M., Flores-Romo, L. (2005) Network of dendritic cells within the muscular layer of the mouse intestine. Proc. Natl. Acad. Sci. USA 102, 19039-19044.
33. Monteleone, I., Platt, A. M., Jaensson, E., Agace, W. W., Mowat, A. M. (2008) IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur. J. Immunol. 38, 1533-1547.
34. Iwasaki, A., Kelsall, B. L. (2001) Unique functions of CD11b+, CD8 +, and double-negative Peyer's patch dendritic cells. J. Immunol. 166, 4884-4890.
35. Johansson-Lindbom, B., Svensson, M., Wurbel, M. A., Malissen, B., Marquez, G., Agace, W. (2003) Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J. Exp. Med. 198, 963-969.
36. Bogunovic, M., Ginhoux, F., Helft, J., Shang, L., Hashimoto, D., Greter, M., Liu, K., Jakubzick, C., Ingersoll, M. A., Leboeuf, M., Stanley, E. R., Nussenzweig, M., Lira, S. A., Randolph, G. J., Merad, M. (2009) Origin of the lamina propria dendritic cell network. Immunity 31, 513-525.
37. Johansson-Lindbom, B., Svensson, M., Pabst, O., Palmqvist, C., Marquez, G., Forster, R., Agace, W. W. (2005) Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 202, 1063-1073.
38. Jaensson, E., Uronen-Hansson, H., Pabst, O., Eksteen, B., Tian, J., Coombes, J. L., Berg, P. L., Davidsson, T., Powrie, F., Johansson-Lindbom, B., Agace, W. W. (2008) Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205, 2139-2149.
39. Svensson, M., Johansson-Lindbom, B., Zapata, F., Jaensson, E., Austenaa, L. M., Blomhoff, R., Agace, W. W. (2008) Retinoic acid receptor signaling levels and antigen dose regulate gut homing receptor expression on CD8+ T cells. Mucosal Immunol. 1, 38-48.
40. Coombes, J. L., Siddiqui, K. R., Arancibia-Carcamo, C. V., Hall, J., Sun, C. M., Belkaid, Y., Powrie, F. (2007) A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764.
41. Schulz, O., Jaensson, E., Persson, E. K., Liu, X., Worbs, T., Agace, W. W., Pabst, O. (2009) Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 206, 3101-3114.
42. Niess, J. H., Brand, S., Gu, X., Landsman, L., Jung, S., McCormick, B. A., Vyas, J. M., Boes, M., Ploegh, H. L., Fox, J. G., Littman, D. R., Reinecker, H. C. (2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307, 254-258.
43. Farache, J., Koren, I., Milo, I., Gurevich, I., Kim, K. W., Zigmond, E., Furtado, G. C., Lira, S. A., Shakhar, G. (2013) Luminal bacteria recruit CD103(+) dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 38, 581-595.
44. Niess, J. H., Adler, G. (2010) Enteric flora expands gut lamina propria CX3CR1+ dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J. Immunol. 184, 2026-2037.
45. Smith, P. D., Smythies, L. E., Shen, R., Greenwell-Wild, T., Gliozzi, M., Wahl, S. M. (2011) Intestinal macrophages and response to microbial encroachment. Mucosal Immunol. 4, 31-42.
46. Smythies, L. E., Sellers, M., Clements, R. H., Mosteller-Barnum, M., Meng, G., Benjamin, W. H., Orenstein, J. M., Smith, P. D. (2005) Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115, 66-75.
47. Smith, P. D., Smythies, L. E., Mosteller-Barnum, M., Sibley, D. A., Russell, M. W., Merger, M., Sellers, M. T., Orenstein, J. M., Shimada, T., Graham, M. F., Kubagawa, H. (2001) Intestinal macrophages lack CD14 and CD89 and consequently are down-regulated for LPS-and IgA-mediated activities. J. Immunol. 167, 2651-2656.
48. Smythies, L. E., Shen, R., Bimczok, D., Novak, L., Clements, R. H., Eckhoff, D. E., Bouchard, P., George, M. D., Hu, W. K., Dandekar, S., Smith, P. D. (2010) Inflammation anergy in human intestinal macrophages is due to Smad-induced IκBα expression and NF-κB inactivation. J. Biol. Chem. 285, 19593-19604.
49. Plantinga, M., Hammad, H., Lambrecht, B. N. (2010) Origin and functional specializations of DC subsets in the lung. Eur. J. Immunol. 40, 2112-2118.
50. GeurtsvanKessel, C. H., Willart, M. A., van Rijt, L. S., Muskens, F., Kool, M., Baas, C., Thielemans, K., Bennett, C., Clausen, B. E., Hoogsteden, H. C., Osterhaus, A. D., Rimmelzwaan, G. F., Lambrecht, B. N. (2008) Clearance of influenza virus from the lung depends on migratory langerin+CD11b-but not plasmacytoid dendritic cells. J. Exp. Med. 205, 1621-1634.
51. Desch, A. N., Randolph, G. J., Murphy, K., Gautier, E. L., Kedl, R. M., Lahoud, M. H., Caminschi, I., Shortman, K., Henson, P. M., Jakubzick, C. V. (2011) CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J. Exp. Med. 208, 1789-1797.
52. Beaty, S. R., Rose C. E., Jr., Sung, S. S. (2007) Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 178, 1882-1895.
53. Del Rio, M. L., Rodriguez-Barbosa, J. I., Kremmer, E., Forster, R. (2007) CD103+ and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J. Immunol. 178, 6861-6866.
54. Rimoldi, M., Chieppa, M., Salucci, V., Avogadri, F., Sonzogni, A., Sampietro, G. M., Nespoli, A., Viale, G., Allavena, P., Rescigno, M. (2005) Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6, 507-514.
55. Smythies, L. E., Maheshwari, A., Clements, R., Eckhoff, D., Novak, L., Vu, H. L., Mosteller-Barnum, L. M., Sellers, M., Smith, P. D. (2006) Mucosal IL-8 and TGF-β recruit blood monocytes: evidence for crosstalk between the lamina propria stroma and myeloid cells. J. Leukoc. Biol. 80, 492-499.
56. Contractor, N., Louten, J., Kim, L., Biron, C. A., Kelsall, B. L. (2007) Cutting edge: Peyer's patch plasmacytoid dendritic cells (pDCs) produce low levels of type I interferons: possible role for IL-10, TGFβ, and prostaglandin E2 in conditioning a unique mucosal pDC phenotype. J. Immunol. 179, 2690-2694.
57. Zaph, C., Troy, A. E., Taylor, B. C., Berman-Booty, L. D., Guild, K. J., Du, Y., Yost, E. A., Gruber, A. D., May, M. J., Greten, F. R., Eckmann, L., Karin, M., Artis, D. (2007) Epithelial-cell-intrinsic IKK-β expression regulates intestinal immune homeostasis. Nature 446, 552-556.
58. Lee, S. W., Park, Y., Eun, S. Y., Madireddi, S., Cheroutre, H., Croft, M. (2012) Cutting edge: 4-1BB controls regulatory activity in dendritic cells through promoting optimal expression of retinal dehydrogenase. J. Immunol. 189, 2697-2701.
59. Manicassamy, S., Reizis, B., Ravindran, R., Nakaya, H., Salazar-Gonzalez, R. M., Wang, Y. C., Pulendran, B. (2010) Activation of β-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329, 849-853.
60. Hayashi, T., Beck, L., Rossetto, C., Gong, X., Takikawa, O., Takabayashi, K., Broide, D. H., Carson, D. A., Raz, E. (2004) Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J. Clin. Invest. 114, 270-279.
61. Snelgrove, R. J., Goulding, J., Didierlaurent, A. M., Lyonga, D., Vekaria, S., Edwards, L., Gwyer, E., Sedgwick, J. D., Barclay, A. N., Hussell, T. (2008) A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat. Immunol. 9, 1074-1083.
62. Forster, R., Davalos-Misslitz, A. C., Rot, A. (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 8, 362-371.
63. Lanzavecchia, A. (1999) Three signals and a master switch in the regulation of T-cell immunity. Cold Spring Harb. Symp. Quant. Biol. 64, 253-257.
64. Sigmundsdottir, H., Butcher, E. C. (2008) Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 9, 981-987.
65. Kronenberg, M., Gapin, L. (2002) The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2, 557-568.
66. Kaufmann, S. H. (1996) γ/δ and other unconventional T lymphocytes: what do they see and what do they do? Proc. Natl. Acad. Sci. USA 93, 2272-2279.
67. Sonnenberg, G. F., Artis, D. (2012) Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease. Immunity 37, 601-610.
68. Guy-Grand, D., Cerf-Bensussan, N., Malissen, B., Malassis-Seris, M., Briottet, C., Vassalli, P. (1991) Two gut intraepithelial CD8+ lymphocyte populations with different T cell receptors: a role for the gut epithelium in T cell differentiation. J. Exp. Med. 173, 471-481.
69. Rocha, B., von Boehmer, H., Guy-Grand, D. (1992) Selection of intraepithelial lymphocytes with CD8 α/α co-receptors by self-antigen in the murine gut. Proc. Natl. Acad. Sci. USA 89, 5336-5340.
70. Cruz, D., Sydora, B. C., Hetzel, K., Yakoub, G., Kronenberg, M., Cheroutre, H. (1998) An opposite pattern of selection of a single T cell antigen receptor in the thymus and among intraepithelial lymphocytes. J. Exp. Med. 188, 255-265.
71. Leishman, A. J., Gapin, L., Capone, M., Palmer, E., MacDonald, H. R., Kronenberg, M., Cheroutre, H. (2002) Precursors of functional MHC class I-or class II-restricted CD8αα(+) T cells are positively selected in the thymus by agonist self-peptides. Immunity 16, 355-364.
72. Leishman, A. J., Naidenko, O. V., Attinger, A., Koning, F., Lena, C. J., Xiong, Y., Chang, H. C., Reinherz, E., Kronenberg, M., Cheroutre, H. (2001) T cell responses modulated through interaction between CD8αα and the nonclassical MHC class I molecule, TL. Science 294, 1936-1939.
73. Masopust, D., Jiang, J., Shen, H., Lefrancois, L. (2001) Direct analysis of the dynamics of the intestinal mucosa CD8 T cell response to systemic virus infection. J. Immunol. 166, 2348-2356.
74. Kim, S. K., Reed, D. S., Heath, W. R., Carbone, F., Lefrancois, L. (1997) Activation and migration of CD8 T cells in the intestinal mucosa. J. Immunol. 159, 4295-4306.
75. Kim, S. K., Schluns, K. S., Lefrancois, L. (1999) Induction and visualization of mucosal memory CD8 T cells following systemic virus infection. J. Immunol. 163, 4125-4132.
76. Kaech, S. M., Wherry, E. J., Ahmed, R. (2002) Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2, 251-262.
77. Gupta, S., Gollapudi, S. (2007) Effector memory CD8+ T cells are resistant to apoptosis. Ann. N. Y. Acad. Sci. 1109, 145-150.
78. Grayson, J. M., Harrington, L. E., Lanier, J. G., Wherry, E. J., Ahmed, R. (2002) Differential sensitivity of naive and memory CD8+ T cells to apoptosis in vivo. J. Immunol. 169, 3760-3770.
79. Croft, M., Bradley, L. M., Swain, S. L. (1994) Naive versus memory CD4 T cell response to antigen. Memory cells are less dependent on accessory cell costimulation and can respond to many antigen-presenting cell types including resting B cells. J. Immunol. 152, 2675-2685.
80. Berg, R. E., Crossley, E., Murray, S., Forman, J. (2003) Memory CD8+ T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J. Exp. Med. 198, 1583-1593.
81. Soudja, S. M., Ruiz, A. L., Marie, J. C., Lauvau, G. (2012) Inflammatory monocytes activate memory CD8(+) T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion. Immunity 37, 549-562.
82. Sallusto, F., Geginat, J., Lanzavecchia, A. (2004) Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763.
83. Sallusto, F., Lenig, D., Forster, R., Lipp, M., Lanzavecchia, A. (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708-712.
84. Pepper, M., Jenkins, M. K. (2011) Origins of CD4(+) effector and central memory T cells. Nat. Immunol. 12, 467-471.
85. Ariotti, S., Haanen, J. B., Schumacher, T. N. (2012) Behavior and function of tissue-resident memory T cells. Adv. Immunol. 114, 203-216.
86. Gebhardt, T., Wakim, L. M., Eidsmo, L., Reading, P. C., Heath, W. R., Carbone, F. R. (2009) Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524-530.
87. Wakim, L. M., Woodward-Davis, A., Bevan, M. J. (2010) Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc. Natl. Acad. Sci. USA 107, 17872-17879.
88. Teijaro, J. R., Turner, D., Pham, Q., Wherry, E. J., Lefrancois, L., Farber, D. L. (2011) Cutting edge: tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J. Immunol. 187, 5510-5514.
89. Wakim, L. M., Gupta, N., Mintern, J. D., Villadangos, J. A. (2013) Enhanced survival of lung tissue-resident memory CD8(+) T cells during infection with influenza virus due to selective expression of IFITM3. Nat. Immunol. 14, 238-245.
90. Purwar, R., Campbell, J., Murphy, G., Richards, W. G., Clark, R. A., Kupper, T. S. (2011) Resident memory T cells (T(RM) are abundant in human lung: diversity, function, and antigen specificity. PLoS One 6, e16245.
91. Hofmann, M., Pircher, H. (2011) E-Cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands. Proc. Natl. Acad. Sci. USA 108, 16741-16746.
92. Masopust, D., Choo, D., Vezys, V., Wherry, E. J., Duraiswamy, J., Akondy, R., Wang, J., Casey, K. A., Barber, D. L., Kawamura, K. S., Fraser, K. A., Webby, R. J., Brinkmann, V., Butcher, E. C., Newell, K. A., Ahmed, R. (2010) Dynamic T cell migration program provides resident memory within intestinal epithelium. J. Exp. Med. 207, 553-564.
93. Wakim, L. M., Woodward-Davis, A., Liu, R., Hu, Y., Villadangos, J., Smyth, G., Bevan, M. J. (2012) The molecular signature of tissue resident memory CD8 T cells isolated from the brain. J. Immunol. 189, 3462-3471.
94. Gebhardt, T., Whitney, P. G., Zaid, A., Mackay, L. K., Brooks, A. G., Heath, W. R., Carbone, F. R., Mueller, S. N. (2011) Different patterns of peripheral migration by memory CD4+ and CD8+ T cells. Nature 477, 216-219.
95. Shin, H., Iwasaki, A. (2012) A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491, 463-467.
96. Anacker, R. L., Barclay, W. R., Brehmer, W., Goode, G., List, R. H., Ribi, E., Tarmina, D. F. (1969) Effectiveness of cell walls of Mycobacterium bovis strain BCG administered by various routes and in different adjuvants in protecting mice against airborne infection with Mycobacterium tuberculosis strain H37Rv. Am. Rev. Respir. Dis. 99, 242-248.
97. Larson, C. L., Wicht, W. C. (1962) Studies of resistance to experimental tuberculosis in mice vaccinated with living attenuated tubercle bacilli and challenged with virulent organisms. Am. Rev. Respir. Dis. 85, 833-846.
98. Lefford, M. J., Warner, S., Amell, L. (1979) Listeria pneumonitis: influence of route of immunization on resistance to airborne infection. Infect. Immun. 25, 672-679.
99. Pepper, M., Linehan, J. L., Pagan, A. J., Zell, T., Dileepan, T., Cleary, P. P., Jenkins, M. K. (2010) Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 11, 83-89.
100. Dileepan, T., Linehan, J. L., Moon, J. J., Pepper, M., Jenkins, M. K., Cleary, P. P. (2011) Robust antigen specific Th17 T cell response to group A Streptococcus is dependent on IL-6 and intranasal route of infection. PLoS Pathog. 7, e1002252.
101. Hue, S., Ahern, P., Buonocore, S., Kullberg, M. C., Cua, D. J., McKenzie, B. S., Powrie, F., Maloy, K. J. (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473-2483.
102. Woolard, M. D., Hensley, L. L., Kawula, T. H., Frelinger, J. A. (2008) Respiratory Francisella tularensis live vaccine strain infection induces Th17 cells and prostaglandin E2, which inhibits generation of γ interferon-positive T cells. Infect. Immun. 76, 2651-2659.
103. DePaolo, R. W., Kamdar, K., Khakpour, S., Sugiura, Y., Wang, W., Jabri, B. (2012) A specific role for TLR1 in protective T(H)17 immunity during mucosal infection. J. Exp. Med. 209, 1437-1444.
104. Campbell, D. J., Butcher, E. C. (2002) Rapid acquisition of tissue-specific homing phenotypes by CD4(+) T cells activated in cutaneous or mucosal lymphoid tissues. J. Exp. Med. 195, 135-141.
105. Berlin, C., Berg, E. L., Briskin, M. J., Andrew, D. P., Kilshaw, P. J., Holzmann, B., Weissman, I. L., Hamann, A., Butcher, E. C. (1993) α 4 β 7 Integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 74, 185-195.
106. Campbell, D. J., Butcher, E. C. (2002) Intestinal attraction: CCL25 functions in effector lymphocyte recruitment to the small intestine. J. Clin. Invest. 110, 1079-1081.
107. Tietz, W., Allemand, Y., Borges, E., von Laer, D., Hallmann, R., Vestweber, D., Hamann, A. (1998) CD4+ T cells migrate into inflamed skin only if they express ligands for E-and P-selectin. J. Immunol. 161, 963-970.
108. Reiss, Y., Proudfoot, A. E., Power, C. A., Campbell, J. J., Butcher, E. C. (2001) CC chemokine receptor (CCR)4 and the CCR10 ligand cutaneous T cell-attracting chemokine (CTACK) in lymphocyte trafficking to inflamed skin. J. Exp. Med. 194, 1541-1547.
109. Stagg, A. J., Kamm, M. A., Knight, S. C. (2002) Intestinal dendritic cells increase T cell expression of α4β7 integrin. Eur. J. Immunol. 32, 1445-1454.
110. Dudda, J. C., Lembo, A., Bachtanian, E., Huehn, J., Siewert, C., Hamann, A., Kremmer, E., Forster, R., Martin, S. F. (2005) Dendritic cells govern induction and reprogramming of polarized tissue-selective homing receptor patterns of T cells: important roles for soluble factors and tissue microenvironments. Eur. J. Immunol. 35, 1056-1065.
111. Mora, J. R., Cheng, G., Picarella, D., Briskin, M., Buchanan, N., von Andrian, U. H. (2005) Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin-and gut-associated lymphoid tissues. J. Exp. Med. 201, 303-316.
112. Iwata, M., Hirakiyama, A., Eshima, Y., Kagechika, H., Kato, C., Song, S. Y. (2004) Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538.
113. Sigmundsdottir, H., Pan, J., Debes, G. F., Alt, C., Habtezion, A., Soler, D., Butcher, E. C. (2007) DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat. Immunol. 8, 285-293.
114. Hu, W., Troutman, T. D., Edukulla, R., Pasare, C. (2011) Priming microenvironments dictate cytokine requirements for T helper 17 cell lineage commitment. Immunity 35, 1010-1022.
115. Picker, L. J., Treer, J. R., Ferguson-Darnell, B., Collins, P. A., Bergstresser, P. R., Terstappen, L. W. (1993) Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyteassociated antigen, a tissue-selective homing receptor for skin-homing T cells. J. Immunol. 150, 1122-1136.
116. Kim, C. H., Nagata, K., Butcher, E. C. (2003) Dendritic cells support sequential reprogramming of chemoattractant receptor profiles during naive to effector T cell differentiation. J. Immunol. 171, 152-158.
117. Kim, C. H., Rott, L., Kunkel, E. J., Genovese, M. C., Andrew, D. P., Wu, L., Butcher, E. C. (2001) Rules of chemokine receptor association with T cell polarization in vivo. J. Clin. Invest. 108, 1331-1339.
118. Horwitz, D. A., Zheng, S. G., Gray, J. D. (2008) Natural and TGF-β-induced Foxp3(+)CD4(+) CD25(+) regulatory T cells are not mirror images of each other. Trends Immunol. 29, 429-435.
119. Denning, T. L., Wang, Y. C., Patel, S. R., Williams, I. R., Pulendran, B. (2007) Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8, 1086-1094.
120. Iliev, I. D., Spadoni, I., Mileti, E., Matteoli, G., Sonzogni, A., Sampietro, G. M., Foschi, D., Caprioli, F., Viale, G., Rescigno, M. (2009) Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 58, 1481-1489.
121. Iliev, I. D., Mileti, E., Matteoli, G., Chieppa, M., Rescigno, M. (2009) Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2, 340-350.
122. Saurer, L., McCullough, K. C., Summerfield, A. (2007) In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J. Immunol. 179, 3504-3514.
123. Lathrop, S. K., Bloom, S. M., Rao, S. M., Nutsch, K., Lio, C. W., Santacruz, N., Peterson, D. A., Stappenbeck, T. S., Hsieh, C. S. (2011) Peripheral education of the immune system by colonic commensal microbiota. Nature 478, 250-254.
124. Bilate, A. M., Lafaille, J. J. (2012) Induced CD4+Foxp3+ regulatory T cells in immune tolerance. Annu. Rev. Immunol. 30, 733-758.
125. Travis, M. A., Reizis, B., Melton, A. C., Masteller, E., Tang, Q., Proctor, J. M., Wang, Y., Bernstein, X., Huang, X., Reichardt, L. F., Bluestone, J. A., Sheppard, D. (2007) Loss of integrin α(v)β8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449, 361-365.
126. Josefowicz, S. Z., Niec, R. E., Kim, H. Y., Treuting, P., Chinen, T., Zheng, Y., Umetsu, D. T., Rudensky, A. Y. (2012) Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 482, 395-399.
127. Taylor, B. C., Zaph, C., Troy, A. E., Du, Y., Guild, K. J., Comeau, M. R., Artis, D. (2009) TSLP regulates intestinal immunity and inflammation in mouse models of helminth infection and colitis. J. Exp. Med. 206, 655-667.
128. Spadoni, I., Iliev, I. D., Rossi, G., Rescigno, M. (2012) Dendritic cells produce TSLP that limits the differentiation of Th17 cells, fosters Treg development, and protects against colitis. Mucosal Immunol. 5, 184-193.
129. Zaph, C., Du, Y., Saenz, S. A., Nair, M. G., Perrigoue, J. G., Taylor, B. C., Troy, A. E., Kobuley, D. E., Kastelein, R. A., Cua, D. J., Yu, Y., Artis, D. (2008) Commensal-dependent expression of IL-25 regulates the IL-23-IL-17 axis in the intestine. J. Exp. Med. 205, 2191-2198.
130. Weber, D. A., Attinger, A., Kemball, C. C., Wigal, J. L., Pohl, J., Xiong, Y., Reinherz, E. L., Cheroutre, H., Kronenberg, M., Jensen, P. E. (2002) Peptide-independent folding and CD8 α α binding by the nonclassical class I molecule, thymic leukemia antigen. J. Immunol. 169, 5708-5714.
131. Siddiqui, K. R., Laffont, S., Powrie, F. (2010) E-Cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated colitis. Immunity 32, 557-567.
132. Laffont, S., Siddiqui, K. R., Powrie, F. (2010) Intestinal inflammation abrogates the tolerogenic properties of MLN CD103+ dendritic cells. Eur. J. Immunol. 40, 1877-1883.
133. DePaolo, R. W., Abadie, V., Tang, F., Fehlner-Peach, H., Hall, J. A., Wang, W., Marietta, E. V., Kasarda, D. D., Waldmann, T. A., Murray, J. A., Semrad, C., Kupfer, S. S., Belkaid, Y., Guandalini, S., Jabri, B. (2011) Co-adjuvant effects of retinoic acid and IL-15 induce inflammatory immunity to dietary antigens. Nature 471, 220-224.
134. De Vries, V. C., Pino-Lagos, K., Nowak, E. C., Bennett, K. A., Oliva, C., Noelle, R. J. (2011) Mast cells condition dendritic cells to mediate allograft tolerance. Immunity 35, 550-561.
135. Griffin, M. D., Lutz, W. H., Phan, V. A., Bachman, L. A., McKean, D. J., Kumar, R. (2000) Potent inhibition of dendritic cell differentiation and maturation by vitamin D analogs. Biochem. Biophys. Res. Commun. 270, 701-708.
136. Piemonti, L., Monti, P., Sironi, M., Fraticelli, P., Leone, B. E., Dal Cin, E., Allavena, P., Di Carlo, V. (2000) Vitamin D3 affects differentiation, maturation, and function of human monocyte-derived dendritic cells. J. Immunol. 164, 4443-4451.
137. Penna, G., Adorini, L. (2000) 1 α,25-Dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J. Immunol. 164, 2405-2411.
138. O'Garra, A., Barrat, F. J., Castro, A. G., Vicari, A., Hawrylowicz, C. (2008) Strategies for use of IL-10 or its antagonists in human disease. Immunol. Rev. 223, 114-131.
139. Diehl, G. E., Longman, R. S., Zhang, J. X., Breart, B., Galan, C., Cuesta, A., Schwab, S. R., Littman, D. R. (2013) Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature 494, 116-120.
140. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., Cheng, G., Yamasaki, S., Saito, T., Ohba, Y., Taniguchi, T., Takeda, K., Hori, S., Ivanov, I. I., Umesaki, Y., Itoh, K., Honda, K. (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331, 337-341.
141. Round, J. L., Lee, S. M., Li, J., Tran, G., Jabri, B., Chatila, T. A., Mazmanian, S. K. (2011) The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 332, 974-977.
142. Mileti, E., Matteoli, G., Iliev, I. D., Rescigno, M. (2009) Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS One 4, e7056.
143. Atarashi, K., Nishimura, J., Shima, T., Umesaki, Y., Yamamoto, M., Onoue, M., Yagita, H., Ishii, N., Evans, R., Honda, K., Takeda, K. (2008) ATP drives lamina propria T(H)17 cell differentiation. Nature 455, 808-812.
144. Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K., Littman, D. R. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498.
145. Hall, J. A., Bouladoux, N., Sun, C. M., Wohlfert, E. A., Blank, R. B., Zhu, Q., Grigg, M. E., Berzofsky, J. A., Belkaid, Y. (2008) Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29, 637-649.
146. Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M. J., Salcedo, R., Kastenmuller, W., Deming, C., Quinones, M., Koo, L., Conlan, S., Spencer, S., Hall, J. A., Dzutsev, A., Kong, H., Campbell, D. J., Trinchieri, G., Segre, J. A., Belkaid, Y. (2012) Compartmentalized control of skin immunity by resident commensals. Science 337, 1115-1119.
147. Gardby, E., Wrammert, J., Schon, K., Ekman, L., Leanderson, T., Lycke, N. (2003) Strong differential regulation of serum and mucosal IgA responses as revealed in CD28-deficient mice using cholera toxin adjuvant. J. Immunol. 170, 55-63.
148. Cebra, J. J., Periwal, S. B., Lee, G., Lee, F., Shroff, K. E. (1998) Development and maintenance of the gut-associated lymphoid tissue (GALT): the roles of enteric bacteria and viruses. Dev. Immunol. 6, 13-18.
149. Sun, C. M., Hall, J. A., Blank, R. B., Bouladoux, N., Oukka, M., Mora, J. R., Belkaid, Y. (2007) Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785.
150. Cazac, B. B., Roes, J. (2000) TGF-β receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 13, 443-451.
151. Defrance, T., Vanbervliet, B., Briere, F., Durand, I., Rousset, F., Banchereau, J. (1992) Interleukin 10 and transforming growth factor β cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J. Exp. Med. 175, 671-682.
152. Tsuji, M., Komatsu, N., Kawamoto, S., Suzuki, K., Kanagawa, O., Honjo, T., Hori, S., Fagarasan, S. (2009) Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 323, 1488-1492.
153. Tezuka, H., Abe, Y., Iwata, M., Takeuchi, H., Ishikawa, H., Matsushita, M., Shiohara, T., Akira, S., Ohteki, T. (2007) Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448, 929-933.
154. Suzuki, K., Maruya, M., Kawamoto, S., Sitnik, K., Kitamura, H., Agace, W. W., Fagarasan, S. (2010) The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 33, 71-83.
155. Tsuji, M., Suzuki, K., Kitamura, H., Maruya, M., Kinoshita, K., Ivanov, I. I., Itoh, K., Littman, D. R., Fagarasan, S. (2008) Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cellindependent immunoglobulin A generation in the gut. Immunity 29, 261-271.
156. Uematsu, S., Fujimoto, K., Jang, M. H., Yang, B. G., Jung, Y. J., Nishiyama, M., Sato, S., Tsujimura, T., Yamamoto, M., Yokota, Y., Kiyono, H., Miyasaka, M., Ishii, K. J., Akira, S. (2008) Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9, 769-776.
157. Bergqvist, P., Stensson, A., Lycke, N. Y., Bemark, M. (2010) T cell-independent IgA class switch recombination is restricted to the GALT and occurs prior to manifest germinal center formation. J. Immunol. 184, 3545-3553.
158. Barone, F., Patel, P., Sanderson, J. D., Spencer, J. (2009) Gut-associated lymphoid tissue contains the molecular machinery to support Tcell-dependent and T-cell-independent class switch recombination. Mucosal Immunol. 2, 495-503.
159. Tezuka, H., Abe, Y., Asano, J., Sato, T., Liu, J., Iwata, M., Ohteki, T. (2011) Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 34, 247-257.
160. He, B., Xu, W., Santini, P. A., Polydorides, A. D., Chiu, A., Estrella, J., Shan, M., Chadburn, A., Villanacci, V., Plebani, A., Knowles, D. M., Rescigno, M., Cerutti, A. (2007) Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelialcell secretion of the cytokine APRIL. Immunity 26, 812-826.
161. Xu, W., He, B., Chiu, A., Chadburn, A., Shan, M., Buldys, M., Ding, A., Knowles, D. M., Santini, P. A., Cerutti, A. (2007) Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat. Immunol. 8, 294-303.
162. Litinskiy, M. B., Nardelli, B., Hilbert, D. M., He, B., Schaffer, A., Casali, P., Cerutti, A. (2002) DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3, 822-829.
163. He, B., Santamaria, R., Xu, W., Cols, M., Chen, K., Puga, I., Shan, M., Xiong, H., Bussel, J. B., Chiu, A., Puel, A., Reichenbach, J., Marodi, L., Doffinger, R., Vasconcelos, J., Issekutz, A., Krause, J., Davies, G., Li, X., Grimbacher, B., Plebani, A., Meffre, E., Picard, C., Cunningham-Rundles, C., Casanova, J. L., Cerutti, A. (2010) The transmembrane activator TACI triggers immunoglobulin class switching by activating B cells through the adaptor MyD88. Nat. Immunol. 11, 836-845.
164. Raz, E. (2007) Organ-specific regulation of innate immunity. Nat. Immunol. 8, 3-4.
165. Blander, J. M., Sander, L. E. (2012) Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 12, 215-225.