Intestinal dendritic cells: Their role in intestinal inflammation, manipulation by the gut microbiota and differences between mice and men

Immunology Letters

Volumn 150, Issue 1-2, 2013, Pages 30-40

  Mann, Elizabeth R ^a   Landy, Jonathan D ^a,b   Bernardo, David ^a   Peake, Simon T C ^a,b   Hart, Ailsa L ^a,b   Al Hassi, Hafid Omar ^a   Knight, Stella C ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ST MARK S HOSPITAL   (United Kingdom)

Author keywords

Dendritic cells; Mucosal immunology; T cell homing; Tolerance

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CX3CR1; GLYCOPROTEIN P 15095; PROBIOTIC AGENT; RETINOIC ACID; TOLL LIKE RECEPTOR 4; VSL3;

BACTERIAL COLONIZATION; BIFIDOBACTERIUM; CELL FUNCTION; CELLULAR IMMUNITY; COLITIS; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG MECHANISM; ENTERITIS; FAECALIBACTERIUM PRAUSNITZII; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; INTESTINAL DENDRITIC CELL; INTESTINE FLORA; LACTOBACILLUS ACIDOPHILUS; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; MACROPHAGE; MOLECULAR IMPRINTING; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE; TISSUE SPECIFICITY; ULCERATIVE COLITIS;

ANIMALS; DENDRITIC CELLS; HUMANS; IMMUNE TOLERANCE; INFLAMMATION; INTESTINES; METAGENOME; MICE; ORGAN SPECIFICITY;

EID: 84874410778     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2013.01.007     Document Type: Review

References (170)

1. Steinman R.M. Dendritic cells: understanding immunogenicity. Eur J Immunol 2007, 37(Suppl. 1):S53-S60.
2. Steinman R.M. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012, 30:1-22.
3. Stagg A.J., Kamm M.A., Knight S.C. Intestinal dendritic cells increase T cell expression of α4β7 integrin. Eur J Immunol 2002, 32:1445-1454.
4. Mora J.R., Bono M.R., Manjunath N., Weninger W., Cavanagh L.L., Rosemblatt M., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 2003, 424:88-93.
5. Johansson-Lindbom B., Svensson M., Wurbel M.A., Malissen B., Marquez G., Agace W. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med 2003, 198:963-969.
6. + T cells activated in cutaneous or mucosal lymphoid tissues. J Exp Med 2002, 195:135-141.
7. Von Andrian U.H., Mackay C.R. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000, 343:1020-1034.
8. Masopust D., Vezys V., Marzo A.L., Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001, 291:2413-2417.
9. Mowat A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 2003, 3:331-341.
10. Chirdo F.G., Millington O.R., Beacock-Sharp H., Mowat A.M. Immunomodulatory dendritic cells in intestinal lamina propria. Eur J Immunol 2005, 35:1831-1840.
11. Hart A.L., Al-Hassi H.O., Rigby R.J., Bell S.J., Emmanuel A.V., Knight S.C., et al. Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology 2005, 129:50-65.
12. Strober W., Fuss I., Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest 2007, 117:514-521.
13. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007, 449:819-826.
14. Konstantinov S.R., Smidt H., de Vos W.M., Bruijns S.C., Singh S.K., Valence F., et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci USA 2008, 105:19474-19479.
15. Foligne B., Zoumpopoulou G., Dewulf J., Ben Y.A., Chareyre F., Sirard J.C., et al. A key role of dendritic cells in probiotic functionality. PLoS ONE 2007, 2:e313.
16. Persson E.K., Jaensson E., Agace W.W. The diverse ontogeny and function of murine small intestinal dendritic cell/macrophage subsets. Immunobiology 2010, 215:692-697.
17. Varol C., Zigmond E., Jung S. Securing the immune tightrope: mononuclear phagocytes in the intestinal lamina propria. Nat Rev Immunol 2010, 10:415-426.
18. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005, 307:254-258.
19. Rescigno M. Before they were gut dendritic cells. Immunity 2009, 31:454-456.
20. 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, 31:502-512.
21. Bogunovic M., Ginhoux F., Helft J., Shang L., Hashimoto D., Greter M., et al. Origin of the lamina propria dendritic cell network. Immunity 2009, 31:513-525.
22. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 2009, 206:3101-3114.
23. + regulatory T cells in the lamina propria. Immunity 2011, 34:237-246.
24. + dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J Immunol 2010, 184:2026-2037.
25. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 2007, 8:1086-1094.
26. Tamoutounour S., Henri S., Lelouard H., de B.B., de H.C., van der Woude C.J., et al. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur J Immunol 2012, 42(12):3150-3166.
27. hi monocyte precursors. Mucosal Immunol 2012, 10.1038/mi.2012.89.
28. Coombes J.L., Powrie F. Dendritic cells in intestinal immune regulation. Nat Rev Immunol 2008, 8:435-446.
29. Coombes J.L., Maloy K.J. Control of intestinal homeostasis by regulatory T cells and dendritic cells. Semin Immunol 2007, 19:116-126.
30. Laffont S., Powrie F. Immunology dendritic-cell genealogy. Nature 2009, 462:732-733.
31. Geissmann F., Gordon S., Hume D.A., Mowat A.M., Randolph G.J. Unravelling mononuclear phagocyte heterogeneity. Nat Rev Immunol 2010, 10:453-460.
32. Agace W.W., Higgins J.M., Sadasivan B., Brenner M.B., Parker C.M. T-lymphocyte-epithelial-cell interactions: integrin αE(CD103)β7, LEEP-CAM and chemokines. Curr Opin Cell Biol 2000, 12:563-568.
33. + regulatory T cells. Mucosal Immunol 2008, 1(Suppl. 1):S34-S38.
34. Schlickum S., Sennefelder H., Friedrich M., Harms G., Lohse M.J., Kilshaw P., et al. Integrin αE(CD103)β7 influences cellular shape and motility in a ligand-dependent fashion. Blood 2008, 112:619-625.
35. + dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 2005, 202:1063-1073.
36. - dendritic cells. J Exp Med 2009, 206:1995-2011.
37. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J Exp Med 2007, 204:1757-1764.
38. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3T reg cells via retinoic acid. J Exp Med 2007, 204:1775-1785.
39. Annacker O., Coombes J.L., Malmstrom V., Uhlig H.H., Bourne T., Johansson-Lindbom B., et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med 2005, 202:1051-1061.
40. Benson M.J., Pino-Lagos K., Rosemblatt M., Noelle R.J. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J Exp Med 2007, 204:1765-1774.
41. Mucida D., Park Y., Kim G., Turovskaya O., Scott I., Kronenberg M., et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007, 317:256-260.
42. - dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol 2013, 6:104-113.
43. + regulatory T cells. J Immunol 2007, 179:3724-3733.
44. + Treg cell conversion of naive T cells. Immunity 2009, 30:471-472.
45. hi Cells. Immunity 2008, 29:758-770.
46. Maynard C.L., Hatton R.D., Helms W.S., Oliver J.R., Stephensen C.B., Weaver C.T. Contrasting roles for all-trans retinoic acid in TGF-β-mediated induction of Foxp3 and IL10 genes in developing regulatory T cells. J Exp Med 2009, 206:343-357.
47. Uematsu S., Fujimoto K., Jang M.H., Yang B.G., Jung Y.J., Nishiyama M., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 2008, 9:769-776.
48. Bedford P.A., Knight S.C. The effect of retinoids on dendritic cell function. Clin Exp Immunol 1989, 75:481-486.
49. Spadoni I., Iliev I.D., Rossi G., Rescigno M. Dendritic cells produce TSLP that limits the differentiation of Th17 cells, fosters Treg development, and protects against colitis. Mucosal Immunol 2012, 5:184-193.
50. Rimoldi M., Chieppa M., Salucci V., Avogadri F., Sonzogni A., Sampietro G.M., et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 2005, 6:507-514.
51. Iliev I.D., Mileti E., Matteoli G., Chieppa M., Rescigno M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol 2009, 2:340-350.
52. + regulatory T cells in human thymus. J Immunol 2010, 184:2999-3007.
53. Reardon C., Lechmann M., Brustle A., Gareau M.G., Shuman N., Philpott D., et al. Thymic stromal lymphopoetin-induced expression of the endogenous inhibitory enzyme SLPI mediates recovery from colonic inflammation. Immunity 2011, 35:223-235.
54. + dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med 2008, 205:2139-2149.
55. Iliev I.D., Spadoni I., Mileti E., Matteoli G., Sonzogni A., Sampietro G.M., et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 2009, 58:1481-1489.
56. + dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction. Gut 2010, 59:595-604.
57. + dendritic cells decreases in the coeliac lesion. Scand J Immunol 2011, 74:186-194.
58. + T cells by small-intestinal dendritic cells in patients with type 1 diabetes. Diabetes 2011, 60:2120-2124.
59. Bell S.J., Rigby R., English N., Mann S.D., Knight S.C., Kamm M.A., et al. Migration and maturation of human colonic dendritic cells. J Immunol 2001, 166:4958-4967.
60. +) colonic lamina propria cells is associated with inflammation in ulcerative colitis. Clin Exp Immunol 2009, 158:205-218.
61. O'Garra A., Barrat F.J., Castro A.G., Vicari A., Hawrylowicz C. Strategies for use of IL-10 or its antagonists in human disease. Immunol Rev 2008, 223:114-131.
62. Saraiva M., O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010, 10:170-181.
63. Iwasaki A., Kelsall B.L. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 1999, 190:229-239.
64. Iwasaki A., Kelsall B.L. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J Exp Med 2000, 191:1381-1394.
65. +, and double-negative Peyer's patch dendritic cells. J Immunol 2001, 166:4884-4890.
66. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 2003, 21:685-711.
67. Cruickshank S.M., English N.R., Felsburg P.J., Carding S.R. Characterization of colonic dendritic cells in normal and colitic mice. World J Gastroenterol 2005, 11:6338-6347.
68. Chow J.C., Young D.W., Golenbock D.T., Christ W.J., Gusovsky F. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 1999, 274:10689-10692.
69. Michelsen K.S., Aicher A., Mohaupt M., Hartung T., Dimmeler S., Kirschning C.J., et al. The role of Toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCS). Peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J Biol Chem 2001, 276:25680-25686.
70. Morath S., Stadelmaier A., Geyer A., Schmidt R.R., Hartung T. Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J Exp Med 2002, 195:1635-1640.
71. Schwandner R., Dziarski R., Wesche H., Rothe M., Kirschning C.J. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J Biol Chem 1999, 274:17406-17409.
72. Takeuchi O., Hoshino K., Akira S. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J Immunol 2000, 165:5392-5396.
73. Yoshimura A., Lien E., Ingalls R.R., Tuomanen E., Dziarski R., Golenbock D. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J Immunol 1999, 163:1-5.
74. Kaisho T., Akira S. Regulation of dendritic cell function through Toll-like receptors. Curr Mol Med 2003, 3:759-771.
75. Takenaka S., Safroneeva E., Xing Z., Gauldie J. Dendritic cells derived from murine colonic mucosa have unique functional and phenotypic characteristics. J Immunol 2007, 178:7984-7993.
76. Duchmann R., Kaiser I., Hermann E., Mayet W., Ewe K., Meyer zum Buschenfelde K.H. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 1995, 102:448-455.
77. Duchmann R., Neurath M.F., Meyer zum Buschenfelde K.H. Responses to self and non-self intestinal microflora in health and inflammatory bowel disease. Res Immunol 1997, 148:589-594.
78. Karlis J., Penttila I., Tran T.B., Jones B., Nobbs S., Zola H., et al. Characterization of colonic and mesenteric lymph node dendritic cell subpopulations in a murine adoptive transfer model of inflammatory bowel disease. Inflamm Bowel Dis 2004, 10:834-847.
79. Niess J.H. Role of mucosal dendritic cells in inflammatory bowel disease. World J Gastroenterol 2008, 14:5138-5148.
80. + T cells. Am J Pathol 1996, 148:1503-1515.
81. Strober W., Fuss I.J., Blumberg R.S. The immunology of mucosal models of inflammation. Annu Rev Immunol 2002, 20:495-549.
82. + T cell-induced colitis. Eur J Immunol 2003, 33:1073-1083.
83. hi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J Exp Med 2012, 209:139-155.
84. Abe K., Nguyen K.P., Fine S.D., Mo J.H., Shen C., Shenouda S., et al. Conventional dendritic cells regulate the outcome of colonic inflammation independently of T cells. Proc Natl Acad Sci USA 2007, 104:17022-17027.
85. + T cells to subepithelial dendritic cell aggregates precedes the development of colitis in a murine adoptive transfer model. Lab Invest 2001, 81:1339-1349.
86. Malmstrom V., Shipton D., Singh B., Al-Shamkhani A., Puklavec M.J., Barclay A.N., et al. CD134L expression on dendritic cells in the mesenteric lymph nodes drives colitis in T cell-restored SCID mice. J Immunol 2001, 166:6972-6981.
87. + regulatory T cells. J Immunol 2003, 170:3939-3943.
88. Silva M.A. Intestinal dendritic cells and epithelial barrier dysfunction in Crohn's disease. Inflamm Bowel Dis 2009, 15:436-453.
89. Verstege M.I., ten Kate F.J., Reinartz S.M., van Drunen C.M., Slors F.J., Bemelman W.A., et al. Dendritic cell populations in colon and mesenteric lymph nodes of patients with Crohn's disease. J Histochem Cytochem 2008, 56:233-241.
90. Kaser A., Ludwiczek O., Holzmann S., Moschen A.R., Weiss G., Enrich B., et al. Increased expression of CCL20 in human inflammatory bowel disease. J Clin Immunol 2004, 24:74-85.
91. - dendritic cell populations in the colonic mucosa of patients with Crohn's disease. Eur J Immunol 2003, 33:143-151.
92. + intestinal dendritic cells during colonic inflammation. World J Gastroenterol 2010, 16:21-29.
93. Sansonetti P.J. War and peace at mucosal surfaces. Nat Rev Immunol 2004, 4:953-964.
94. Jang M.H., Kweon M.N., Iwatani K., Yamamoto M., Terahara K., Sasakawa C., et al. Intestinal villous M cells: an antigen entry site in the mucosal epithelium. Proc Natl Acad Sci USA 2004, 101:6110-6115.
95. Neutra M.R. M cells in antigen sampling in mucosal tissues. Curr Top Microbiol Immunol 1999, 236:17-32.
96. Lavelle E.C., Murphy C., O'Neill L.A., Creagh E.M. The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol 2010, 3:17-28.
97. Figdor C.G., van K.Y., Adema G.J. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol 2002, 2:77-84.
98. Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol Rev 2004, 199:227-250.
99. Pulendran B., Kumar P., Cutler C.W., Mohamadzadeh M., Van D.T., Banchereau J. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J Immunol 2001, 167:5067-5076.
100. Rescigno M. Intestinal dendritic cells. Adv Immunol 2010, 107:109-138.
101. Rescigno M., Di S.A. Dendritic cells in intestinal homeostasis and disease. J Clin Invest 2009, 119:2441-2450.
102. Zeuthen L.H., Fink L.N., Frokiaer H. Epithelial cells prime the immune response to an array of gut-derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor-β. Immunology 2008, 123:197-208.
103. Mileti E., Matteoli G., Iliev I.D., Rescigno M. Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS ONE 2009, 4:e7056.
104. Guarner F., Bourdet-Sicard R., Brandtzaeg P., Gill H.S., McGuirk P., van Eden W., et al. Mechanisms of disease: the hygiene hypothesis revisited. Nat Clin Pract Gastroenterol Hepatol 2006, 3:275-284.
105. Asquith M., Powrie F. An innately dangerous balancing act: intestinal homeostasis, inflammation, and colitis-associated cancer. J Exp Med 2010, 207:1573-1577.
106. Sellon R.K., Tonkonogy S., Schultz M., Dieleman L.A., Grenther W., Balish E., et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 1998, 66:5224-5231.
107. Chichlowski M., Sharp J.M., Vanderford D.A., Myles M.H., Hale L.P. Helicobacter typhlonius and Helicobacter rodentium differentially affect the severity of colon inflammation and inflammation-associated neoplasia in IL10-deficient mice. Comp Med 2008, 58:534-541.
108. Grassl G.A., Valdez Y., Bergstrom K.S., Vallance B.A., Finlay B.B. Chronic enteric salmonella infection in mice leads to severe and persistent intestinal fibrosis. Gastroenterology 2008, 134:768-780.
109. Sitaraman S.V., Klapproth J.M., Moore D.A., Landers C., Targan S., Williams I.R., et al. Elevated flagellin-specific immunoglobulins in Crohn's disease. Am J Physiol Gastrointest Liver Physiol 2005, 288:G403-G406.
110. Ott S.J., Musfeldt M., Wenderoth D.F., Hampe J., Brant O., Folsch U.R., et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004, 53:685-693.
111. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007, 104:13780-13785.
112. Lepage P., Hasler R., Spehlmann M.E., Rehman A., Zvirbliene A., Begun A., et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 2011, 141:227-236.
113. Manichanh C., Rigottier-Gois L., Bonnaud E., Gloux K., Pelletier E., Frangeul L., et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006, 55:205-211.
114. Kang S., Denman S.E., Morrison M., Yu Z., Dore J., Leclerc M., et al. Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray. Inflamm Bowel Dis 2010, 16:2034-2042.
115. McLaughlin S.D., Walker A.W., Churcher C., Clark S.K., Tekkis P.P., Johnson M.W., et al. The bacteriology of pouchitis: a molecular phylogenetic analysis using 16S rRNA gene cloning and sequencing. Ann Surg 2010, 252:90-98.
116. Ng S.C., Benjamin J.L., McCarthy N.E., Hedin C.R., Koutsoumpas A., Plamondon S., et al. Relationship between human intestinal dendritic cells, gut microbiota, and disease activity in Crohn's disease. Inflamm Bowel Dis 2011, 17:2027-2037.
117. Lefrancois L., Parker C.M., Olson S., Muller W., Wagner N., Schon M.P., et al. The role of β7 integrins in CD8 T cell trafficking during an antiviral immune response. J Exp Med 1999, 189:1631-1638.
118. Berlin C., Berg E.L., Briskin M.J., Andrew D.P., Kilshaw P.J., Holzmann B., et al. α4β7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell 1993, 74:185-195.
119. Berg E.L., McEvoy L.M., Berlin C., Bargatze R.F., Butcher E.C. L-selectin-mediated lymphocyte rolling on MAdCAM-1. Nature 1993, 366:695-698.
120. Zabel B.A., Agace W.W., Campbell J.J., Heath H.M., Parent D., Roberts A.I., et al. Human G protein-coupled receptor GPR-9-6/CC chemokine receptor 9 is selectively expressed on intestinal homing T lymphocytes, mucosal lymphocytes, and thymocytes and is required for thymus-expressed chemokine-mediated chemotaxis. J Exp Med 1999, 190:1241-1256.
121. Wurbel M.A., Philippe J.M., Nguyen C., Victorero G., Freeman T., Wooding P., et al. The chemokine TECK is expressed by thymic and intestinal epithelial cells and attracts double- and single-positive thymocytes expressing the TECK receptor CCR9. Eur J Immunol 2000, 30:262-271.
122. Pan J., Kunkel E.J., Gosslar U., Lazarus N., Langdon P., Broadwell K., et al. A novel chemokine ligand for CCR10 and CCR3 expressed by epithelial cells in mucosal tissues. J Immunol 2000, 165:2943-2949.
123. Mann E.R., Bernardo D., Al-Hassi H.O., English N.R., Clark S.K., McCarthy N.E., et al. Human gut-specific homeostatic dendritic cells are generated from blood precursors by the gut microenvironment. Inflamm Bowel Dis 2012, 18:1275-1286.
124. Wendland M., Czeloth N., Mach N., Malissen B., Kremmer E., Pabst O., et al. CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine. Proc Natl Acad Sci USA 2007, 104:6347-6352.
125. + plasmacytoid dendritic cells in the small intestine suppress development of intestinal inflammation in mice. Immunol Lett 2012, 146:64-69.
126. Drakes M.L., Stiff P.J., Blanchard T.G. Inverse relationship between dendritic cell CCR9 expression and maturation state. Immunology 2009, 127:466-476.
127. Dandie G.W., Watkins F.Y., Ragg S.J., Holloway P.E., Muller H.K. The migration of Langerhans' cells into and out of lymph nodes draining normal, carcinogen and antigen-treated sheep skin. Immunol Cell Biol 1994, 72:79-86.
128. Mora J.R., Cheng G., Picarella D., Briskin M., Buchanan N., Von Andrian U.H. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J Exp Med 2005, 201:303-316.
129. Mora J.R. Homing imprinting and immunomodulation in the gut: role of dendritic cells and retinoids. Inflamm Bowel Dis 2008, 14:275-289.
130. Iwata M. Retinoic acid production by intestinal dendritic cells and its role in T-cell trafficking. Semin Immunol 2009, 21:8-13.
131. Manicassamy S., Pulendran B. Retinoic acid-dependent regulation of immune responses by dendritic cells and macrophages. Semin Immunol 2009, 21:22-27.
132. Iwata M., Hirakiyama A., Eshima Y., Kagechika H., Kato C., Song S.Y. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004, 21:527-538.
133. Cassani B., Villablanca E.J., Quintana F.J., Love P.E., Lacy-Hulbert A., Blaner W.S., et al. Gut-tropic T cells that express integrin α4β7 and CCR9 are required for induction of oral immune tolerance in mice. Gastroenterology 2011, 141:2109-2118.
134. Ohmori K., Fukui F., Kiso M., Imai T., Yoshie O., Hasegawa H., et al. Identification of cutaneous lymphocyte-associated antigen as sialyl 6-sulfo Lewis X, a selectin ligand expressed on a subset of skin-homing helper memory T cells. Blood 2006, 107:3197-3204.
135. Saurer L., McCullough K.C., Summerfield A. In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J Immunol 2007, 179:3504-3514.
136. Hammerschmidt S.I., Ahrendt M., Bode U., Wahl B., Kremmer E., Forster R., et al. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J Exp Med 2008, 205:2483-2490.
137. Lampen A., Meyer S., Arnhold T., Nau H. Metabolism of vitamin A and its active metabolite all-trans-retinoic acid in small intestinal enterocytes. J Pharmacol Exp Ther 2000, 295:979-985.
138. + antigen-presenting cells control the proliferation and differentiation of T cells in the intestinal mucosa. Nat Immunol 2005, 6:698-706.
139. Farkas S., Hornung M., Sattler C., Edtinger K., Steinbauer M., Anthuber M., et al. Blocking MAdCAM-1 in vivo reduces leukocyte extravasation and reverses chronic inflammation in experimental colitis. Int J Colorectal Dis 2006, 21:71-78.
140. Goto A., Arimura Y., Shinomura Y., Imai K., Hinoda Y. Antisense therapy of MAdCAM-1 for trinitrobenzenesulfonic acid-induced murine colitis. Inflamm Bowel Dis 2006, 12:758-765.
141. Kato S., Hokari R., Matsuzaki K., Iwai A., Kawaguchi A., Nagao S., et al. Amelioration of murine experimental colitis by inhibition of mucosal addressin cell adhesion molecule-1. J Pharmacol Exp Ther 2000, 295:183-189.
142. Matsuzaki K., Tsuzuki Y., Matsunaga H., Inoue T., Miyazaki J., Hokari R., et al. In vivo demonstration of T lymphocyte migration and amelioration of ileitis in intestinal mucosa of SAMP1/Yit mice by the inhibition of MAdCAM-1. Clin Exp Immunol 2005, 140:22-31.
143. + T cells. J Immunol 1997, 158:2099-2106.
144. Arihiro S., Ohtani H., Suzuki M., Murata M., Ejima C., Oki M., et al. Differential expression of mucosal addressin cell adhesion molecule-1 (MAdCAM-1) in ulcerative colitis and Crohn's disease. Pathol Int 2002, 52:367-374.
145. Souza H.S., Elia C.C., Spencer J., MacDonald T.T. Expression of lymphocyte-endothelial receptor-ligand pairs, α4β7/MAdCAM-1 and OX40/OX40 ligand in the colon and jejunum of patients with inflammatory bowel disease. Gut 1999, 45:856-863.
146. Hart A.L., Kamm M.A., Knight S.C., Stagg A.J. Quantitative and functional characteristics of intestinal-homing memory T cells: analysis of Crohn's disease patients and healthy controls. Clin Exp Immunol 2004, 135:137-145.
147. Dudda J.C., Lembo A., Bachtanian E., Huehn J., Siewert C., Hamann A., et al. 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 2005, 35:1056-1065.
148. Wang S., Villablanca E.J., De C.J., Gomes D.C., Nguyen D.D., Mizoguchi E., et al. MyD88-dependent TLR1/2 signals educate dendritic cells with gut-specific imprinting properties. J Immunol 2011, 187:141-150.
149. Kunii J., Takahashi K., Kasakura K., Tsuda M., Nakano K., Hosono A., et al. Commensal bacteria promote migration of mast cells into the intestine. Immunobiology 2011, 216:692-697.
150. Bernardo D., Sanchez B., Al-Hassi H.O., Mann E.R., Urdaci M.C., Knight S.C., et al. Microbiota/host crosstalk biomarkers: regulatory response of human intestinal dendritic cells exposed to Lactobacillus extracellular encrypted peptide. PLoS ONE 2012, 7:e36262.
151. Radhakrishnan S., Iijima K., Kobayashi T., Kita H., Pease L.R. Dendritic cells activated by cross-linking B7-DC (PD-L2) block inflammatory airway disease. J Allergy Clin Immunol 2005, 116:668-674.
152. Trucco M., Giannoukakis N. Immunoregulatory dendritic cells to prevent and reverse new-onset Type 1 diabetes mellitus. Expert Opin Biol Ther 2007, 7:951-963.
153. Lebre M.C., Tak P.P. Dendritic cells in rheumatoid arthritis: which subset should be used as a tool to induce tolerance. Hum Immunol 2009, 70:321-324.
154. Mora J.R., Iwata M., Eksteen B., Song S.Y., Junt T., Senman B., et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006, 314:1157-1160.
155. Strober W. Vitamin A rewrites the ABCs of oral tolerance. Mucosal Immunol 2008, 1:92-95.
156. Belardelli F., Ferrantini M. Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol 2002, 23:201-208.
157. Ueno H., Klechevsky E., Morita R., Aspord C., Cao T., Matsui T., et al. Dendritic cell subsets in health and disease. Immunol Rev 2007, 219:118-142.
158. Ng S.C., Kamm M.A., Stagg A.J., Knight S.C. Intestinal dendritic cells: their role in bacterial recognition, lymphocyte homing, and intestinal inflammation. Inflamm Bowel Dis 2010, 16:1787-1807.
159. Hart A.L., Lammers K., Brigidi P., Vitali B., Rizzello F., Gionchetti P., et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 2004, 53:1602-1609.
160. Ng S.C., Plamondon S., Kamm M.A., Hart A.L., Al-Hassi H.O., Guenther T., et al. Immunosuppressive effects via human intestinal dendritic cells of probiotic bacteria and steroids in the treatment of acute ulcerative colitis. Inflamm Bowel Dis 2010, 16:1286-1298.
161. Wang X., O'Gorman M.R., Bu H.F., Koti V., Zuo X.L., Tan X.D. Probiotic preparation VSL#3 alters the distribution and phenotypes of dendritic cells within the intestinal mucosa in C57BL/10 J mice. J Nutr 2009, 139:1595-1602.
162. Shida K., Nanno M., Nagata S. Flexible cytokine production by macrophages and T cells in response to probiotic bacteria: a possible mechanism by which probiotics exert multifunctional immune regulatory activities. Gut Microbes 2011, 2:109-114.
163. Vanderpool C., Yan F., Polk D.B. Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm Bowel Dis 2008, 14:1585-1596.
164. Isaacs K., Herfarth H. Role of probiotic therapy in IBD. Inflamm Bowel Dis 2008, 14:1597-1605.
165. WHO Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food 2002.
166. Besselink M.G., van Santvoort H.C., Buskens E., Boermeester M.A., van G.H., Timmerman H.M., et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 2008, 371:651-659.
167. Tsilingiri K., Barbosa T., Penna G., Caprioli F., Sonzogni A., Viale G., et al. Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex-vivo organ culture model. Gut 2012, 61:1007-1015.
168. Salim S.Y., Soderholm J.D. Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm Bowel Dis 2011, 17:362-381.
169. Vetrano S., Rescigno M., Cera M.R., Correale C., Rumio C., Doni A., et al. Unique role of junctional adhesion molecule-a in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 2008, 135:173-184.
170. Hoarau C., Martin L., Faugaret D., Baron C., Dauba A., Aubert-Jacquin C., et al. Supernatant from bifidobacterium differentially modulates transduction signaling pathways for biological functions of human dendritic cells. PLoS ONE 2008, 3:e2753.