Intestinal dendritic cells: Their role in bacterial recognition, lymphocyte homing, and intestinal inflammation

Inflammatory Bowel Diseases

Volumn 16, Issue 10, 2010, Pages 1787-1807

  Ng, S C ^a   Kamm, M A ^a,b   Stagg, A J ^c   Knight, S C ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ST VINCENT S HOSPITAL   (Australia)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Bacterial recognition; Epithelial cells; Immune tolerance; Inflammation; Inflammatory bowel disease; Intestinal dendritic cells; Lymphocyte homing

Indexed keywords

BACTERIAL ANTIGEN;

ANTIGEN RECOGNITION; BACTERIAL CELL; BACTERIUM IDENTIFICATION; CELL FUNCTION; CELL INTERACTION; DENDRITIC CELL; DISEASE CONTROL; ENTERITIS; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL TOLERANCE; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; LYMPHOCYTE HOMING; MOLECULAR IMPRINTING; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TARGET CELL;

ANIMALS; BACTERIA; DENDRITIC CELLS; HUMANS; INFLAMMATION; INTESTINES;

EID: 78649233878     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21247     Document Type: Review

References (256)

1. Banchereau J, Briere F, Caux C, et al. Immunobiology of dendritic cells. Annu Rev Immunol. 2000; 18: 767-811.
2. Randolph GJ, Angeli V, Swartz MA,. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol. 2005; 5: 617-628.
3. Randolph GJ, Ochando J, Partida-Sanchez S,. Migration of dendritic cell subsets and their precursors. Annu Rev Immunol. 2008; 26: 293-316.
4. Steinman RM,. The control of immunity and tolerance by dendritic cell. Pathol Biol (Paris). 2003; 51: 59-60.
5. Kelsall B,. Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol. 2008; 1: 460-469.
6. Wynn TA,. Basophils trump dendritic cells as APCs for T(H)2 responses. Nat Immunol. 2009; 10: 679-681.
7. Sokol CL, Chu NQ, Yu S, et al. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat Immunol. 2009; 10: 713-720.
8. + T cell interactions promote T(H)2 cytokine-dependent immunity. Nat Immunol. 2009; 10: 697-705.
9. + T cells. Nat Immunol. 2009; 10: 706-712.
10. Mora JR,. Homing imprinting and immunomodulation in the gut: role of dendritic cells and retinoids. Inflamm Bowel Dis. 2008; 14: 275-289.
11. Dudziak D, Kamphorst AO, Heidkamp GF, et al. Differential antigen processing by dendritic cell subsets in vivo. Science. 2007; 315: 107-111.
12. Steinman RM, Banchereau J,. Taking dendritic cells into medicine. Nature. 2007; 449: 419-426.
13. Denning TL, Wang YC, Patel SR, et al. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol. 2007; 8: 1086-1094.
14. +, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med. 2009; 206: 3101-3114.
15. Hume DA,. Differentiation and heterogeneity in the mononuclear phagocyte system. Mucosal Immunol. 2008; 1: 432-441.
16. Shortman K, Liu YJ,. Mouse and human dendritic cell subtypes. Nat Rev Immunol. 2002; 2: 151-161.
17. Schakel K,. Dendritic cellsâwhy can they help and hurt us. Exp Dermatol. 2009; 18: 264-273.
18. Liu K, Victora GD, Schwickert TA, et al. In vivo analysis of dendritic cell development and homeostasis. Science. 2009; 324: 392-397.
19. Ueno H, Klechevsky E, Morita R, et al. Dendritic cell subsets in health and disease. Immunol Rev. 2007; 219: 118-142.
20. Sathe P, Shortman K,. The steady-state development of splenic dendritic cells. Mucosal Immunol. 2008; 1: 425-431.
21. Westcott E, Windsor A, Mattacks C, et al. Fatty acid compositions of lipids in mesenteric adipose tissue and lymphoid cells in patients with and without Crohn's disease and their therapeutic implications. Inflamm Bowel Dis. 2005; 11: 820-827.
22. +, and double-negative Peyer's patch dendritic cells. J Immunol. 2001; 166: 4884-4890.
23. Maric I, Holt PG, Perdue MH, et al. Class II MHC antigen (Ia)-bearing dendritic cells in the epithelium of the rat intestine. J Immunol. 1996; 156: 1408-1414.
24. Flores-Langarica A, Meza-Perez S, Calderon-Amador J, et al. Network of dendritic cells within the muscular layer of the mouse intestine. Proc Natl Acad Sci U S A. 2005; 102: 19039-19044.
25. Allenspach EJ, Lemos MP, Porrett PM, et al. Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity. 2008; 29: 795-806.
26. Iwasaki A, Kelsall BL,. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J Exp Med. 2000; 191: 1381-1394.
27. Iwasaki A, Kelsall BL,. 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.
28. Varol C, Vallon-Eberhard A, Elinav E, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity. 2009; 31: 502-512.
29. Bogunovic M, Ginhoux F, Helft J, et al. Origin of the lamina propria dendritic cell network. Immunity. 2009; 31: 513-525.
30. Bell SJ, Rigby R, English N, et al. Migration and maturation of human colonic dendritic cells. J Immunol. 2001; 166: 4958-4967.
31. Hart AL, Al Hassi HO, Rigby RJ, et al. Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology. 2005; 129: 50-65.
32. Shale M, Ghosh S,. How intestinal epithelial cells tolerise dendritic cells and its relevance to inflammatory bowel disease. Gut. 2009; 58: 1291-1299.
33. Chabot S, Wagner JS, Farrant S, et al. TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium. J Immunol. 2006; 176: 4275-4283.
34. + dendritic cells. J Immunol. 2003; 171: 2797-2803.
35. Rimoldi M, Chieppa M, Salucci V, et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol. 2005; 6: 507-514.
36. Zaph C, Troy AE, Taylor BC, et al. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature. 2007; 446: 552-556.
37. Liu LM, MacPherson GG,. Lymph-borne (veiled) dendritic cells can acquire and present intestinally administered antigens. Immunology. 1991; 73: 281-286.
38. Liu LM, MacPherson GG,. Antigen acquisition by dendritic cells: intestinal dendritic cells acquire antigen administered orally and can prime naive T cells in vivo. J Exp Med. 1993; 177: 1299-1307.
39. Iwasaki A,. Mucosal dendritic cells. Annu Rev Immunol. 2007; 25: 381-418.
40. Corr SC, Gahan CC, Hill C,. M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunol Med Microbiol. 2008; 52: 2-12.
41. Jang MH, Kweon MN, Iwatani K, et al. Intestinal villous M cells: an antigen entry site in the mucosal epithelium. Proc Natl Acad Sci U S A. 2004; 101: 6110-6115.
42. Hopkins SA, Niedergang F, Corthesy-Theulaz IE, et al. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol. 2000; 2: 59-68.
43. Hopkins SA, Kraehenbuhl JP,. Dendritic cells of the murine Peyer's patches colocalize with Salmonella typhimurium avirulent mutants in the subepithelial dome. Adv Exp Med Biol. 1997; 417: 105-109.
44. Shreedhar VK, Kelsall BL, Neutra MR,. Cholera toxin induces migration of dendritic cells from the subepithelial dome region to T- and B-cell areas of Peyer's patches. Infect Immun. 2003; 71: 504-509.
45. Macpherson AJ, Uhr T,. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science. 2004; 303: 1662-1665.
46. Weltzin R, Lucia-Jandris P, Michetti P, et al. Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J Cell Biol. 1989; 108: 1673-1685.
47. Neutra MR, Kraehenbuhl JP,. The role of transepithelial transport by M cells in microbial invasion and host defense. J Cell Sci Suppl. 1993; 17: 209-215.
48. Heystek HC, Moulon C, Woltman AM, et al. Human immature dendritic cells efficiently bind and take up secretory IgA without the induction of maturation. J Immunol. 2002; 168: 102-107.
49. Geissmann F, Launay P, Pasquier B, et al. A subset of human dendritic cells expresses IgA Fc receptor (CD89), which mediates internalization and activation upon cross-linking by IgA complexes. J Immunol. 2001; 166: 346-352.
50. Huang FP, Platt N, Wykes M, et al. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med. 2000; 191: 435-444.
51. Van NG, Raposo G, Candalh C, et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology. 2001; 121: 337-349.
52. Karlsson M, Lundin S, Dahlgren U, et al. "Tolerosomes" are produced by intestinal epithelial cells. Eur J Immunol. 2001; 31: 2892-2900.
53. Fleeton MN, Contractor N, Leon F, et al. Peyer's patch dendritic cells process viral antigen from apoptotic epithelial cells in the intestine of reovirus-infected mice. J Exp Med. 2004; 200: 235-245.
54. Rescigno M, Rotta G, Valzasina B, et al. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001; 204: 572-581.
55. Collan Y,. Characteristics of nonepithelial cells in the epithelium of normal rat ileum. Scand J Gastroenterol Suppl. 1972; 18: 1-66.
56. Niess JH, Brand S, Gu X, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science. 2005; 307: 254-258.
57. Chieppa M, Rescigno M, Huang AY, et al. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med. 2006; 203: 2841-2852.
58. Arques JL, Hautefort I, Ivory K, et al. Salmonella induces flagellin- and MyD88-dependent migration of bacteria-capturing dendritic cells into the gut lumen. Gastroenterology. 2009; 137: 579-587.
59. Baker K, Qiao SW, Kuo T, et al. Immune and non-immune functions of the (not so) neonatal Fc receptor, FcRn. Semin Immunopathol. 2009; 31: 223-236.
60. Kobayashi K, Qiao SW, Yoshida M, et al. An FcRn-dependent role for anti-flagellin immunoglobulin G in pathogenesis of colitis in mice. Gastroenterology. 2009; 137: 1746-1756.
61. Morelli AE,. The immune regulatory effect of apoptotic cells and exosomes on dendritic cells: its impact on transplantation. Am J Transplant. 2006; 6: 254-261.
62. Cario E, Rosenberg IM, Brandwein SL, et al. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol. 2000; 164: 966-972.
63. Hisamatsu T, Suzuki M, Reinecker HC, et al. CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology. 2003; 124: 993-1000.
64. Inohara N, Ogura Y, Chen FF, et al. Human Nod1 confers responsiveness to bacterial lipopolysaccharides. J Biol Chem. 2001; 276: 2551-2554.
65. Macpherson AJ, Smith K,. Mesenteric lymph nodes at the center of immune anatomy. J Exp Med. 2006; 203: 497-500.
66. Viney JL, Mowat AM, O'Malley JM, et al. Expanding dendritic cells in vivo enhances the induction of oral tolerance. J Immunol. 1998; 160: 5815-5825.
67. Macpherson AJ, Uhr T,. Compartmentalization of the mucosal immune responses to commensal intestinal bacteria. Ann N Y Acad Sci. 2004; 1029: 36-43.
68. Macpherson AJ, Slack E,. The functional interactions of commensal bacteria with intestinal secretory IgA. Curr Opin Gastroenterol. 2007; 23: 673-678.
69. Jang MH, Sougawa N, Tanaka T, et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J Immunol. 2006; 176: 803-810.
70. Worbs T, Bode U, Yan S, et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med. 2006; 203: 519-527.
71. Bimczok D, Sowa EN, Faber-Zuschratter H, et al. Site-specific expression of CD11b and SIRPalpha (CD172a) on dendritic cells: implications for their migration patterns in the gut immune system. Eur J Immunol. 2005; 35: 1418-1427.
72. Turnbull EL, Yrlid U, Jenkins CD, et al. Intestinal dendritic cell subsets: differential effects of systemic TLR4 stimulation on migratory fate and activation in vivo. J Immunol. 2005; 174: 1374-1384.
73. Pugh CW, Macpherson GG, Steer HW,. Characterization of nonlymphoid cells derived from rat peripheral lymph. J Exp Med. 1983; 157: 1758-1779.
74. Wilson NS, Young LJ, Kupresanin F, et al. Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol Cell Biol. 2008; 86: 200-205.
75. Stagg AJ, Norin KE, Midtvedt T, et al. Mesenteric dendritic cells from germ-free mice cause less T-cell stimulation but still induce α4β7 integrin. Microbial Ecology on Health and Disease 2007; 171-183.
76. Wendland M, Czeloth N, Mach N, et al. CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine. Proc Natl Acad Sci U S A. 2007; 104: 6347-6352.
77. Cerovic V, McDonald V, Nassar MA, et al. New insights into the roles of dendritic cells in intestinal immunity and tolerance. Int Rev Cell Mol Biol. 2009; 272: 33-105.
78. Steinman RM, Hawiger D, Nussenzweig MC,. Tolerogenic dendritic cells. Annu Rev Immunol. 2003; 21: 685-711.
79. + Treg using monoclonal antibodies to CD200R. Transplantation. 2005; 79: 488-491. (Pubitemid 40280183)
80. +) T cells. Int Immunol. 2000; 12: 177-185.
81. + regulatory T cells from human peripheral blood. J Immunol. 2001; 166: 7282-7289.
82. Levings MK, Sangregorio R, Galbiati F, et al. IFN-alpha and IL-10 induce the differentiation of human type 1 T regulatory cells. J Immunol. 2001; 166: 5530-5539.
83. + T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. J Exp Med. 2002; 196: 1335-1346.
84. + subset. J Immunol. 2000; 165: 1357-1363.
85. Rimoldi M, Chieppa M, Larghi P, et al. Monocyte-derived dendritic cells activated by bacteria or by bacteria-stimulated epithelial cells are functionally different. Blood. 2005; 106: 2818-2826.
86. + T cells to rapidly secrete IL-4 in BALB/c mice infected with Leishmania major. J Immunol. 2000; 165: 5637-5645.
87. O'Boyle CJ, MacFie J, Mitchell CJ, et al. Microbiology of bacterial translocation in humans. Gut. 1998; 42: 29-35.
88. + regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med. 2007; 204: 1757-1764.
89. Sun CM, Hall JA, Blank RB, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med. 2007; 204: 1775-1785.
90. + regulatory T cells. J Immunol. 2007; 179: 3724-3733.
91. + regulatory T cells: more of the same or a division of labor? Immunity. 2009; 30: 626-635.
92. Hori S, Nomura T, Sakaguchi S,. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003; 299: 1057-1061.
93. Coombes JL, Powrie F,. Dendritic cells in intestinal immune regulation. Nat Rev Immunol. 2008; 8: 435-446.
94. Zhou X, Bailey-Bucktrout SL, Jeker LT, et al. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol. 2009; 10: 1000-1007.
95. Travis MA, Reizis B, Melton AC, et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature. 2007; 449: 361-365.
96. Lacy-Hulbert A, Smith AM, Tissire H, et al. Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins. Proc Natl Acad Sci U S A. 2007; 104: 15823-15828.
97. Pulendran B,. Modulating TH1/TH2 responses with microbes, dendritic cells, and pathogen recognition receptors. Immunol Res. 2004; 29: 187-196. (Pubitemid 38822408)
98. Akira S,. TLR signaling. Curr Top Microbiol Immunol. 2006; 311: 1-16.
99. Akira S, Uematsu S, Takeuchi O,. Pathogen recognition and innate immunity. Cell. 2006; 124: 783-801.
100. Neish AS,. Microbes in gastrointestinal health and disease. Gastroenterology. 2009; 136: 65-80.
101. Liu YJ,. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 2005; 23: 275-306.
102. Krug A, Rothenfusser S, Hornung V, et al. Identification of CpG oligonucleotide sequences with high induction of IFN-alpha/beta in plasmacytoid dendritic cells. Eur J Immunol. 2001; 31: 2154-2163.
103. Stagg AJ, Hart AL, Knight SC, et al. The dendritic cell: its role in intestinal inflammation and relationship with gut bacteria. Gut. 2003; 52: 1522-1529.
104. Figdor CG, van KY, Adema GJ,. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol. 2002; 2: 77-84.
105. den DJ, Gringhuis SI, Geijtenbeek TB,. Innate signaling by the C-type lectin DC-SIGN dictates immune responses. Cancer Immunol Immunother. 2009; 58: 1149-1157.
106. Konstantinov SR, Smidt H, de Vos WM, et al. S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc Natl Acad Sci U S A. 2008; 105: 19474-19479.
107. Mariathasan S, Monack DM,. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat Rev Immunol. 2007; 7: 31-40.
108. Delbridge LM, O'Riordan MX,. Innate recognition of intracellular bacteria. Curr Opin Immunol. 2007; 19: 10-16.
109. Fritz JH, Girardin SE,. How Toll-like receptors and Nod-like receptors contribute to innate immunity in mammals. J Endotoxin Res. 2005; 11: 390-394.
110. Fritz JH, Ferrero RL, Philpott DJ, et al. Nod-like proteins in immunity, inflammation and disease. Nat Immunol. 2006; 7: 1250-1257.
111. Depaolo RW, Tang F, Kim I, et al. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe. 2008; 4: 350-361.
112. Boirivant M, Amendola A, Butera A, et al. A transient breach in the epithelial barrier leads to regulatory T-cell generation and resistance to experimental colitis. Gastroenterology. 2008; 135: 1612-1623.
113. Kolls JK, Linden A,. Interleukin-17 family members and inflammation. Immunity. 2004; 21: 467-476.
114. Harrington LE, Mangan PR, Weaver CT,. Expanding the effector CD4 T-cell repertoire: the Th17 lineage. Curr Opin Immunol. 2006; 18: 349-356.
115. van Beelen AJ, Zelinkova Z, Taanman-Kueter EW, et al. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity. 2007; 27: 660-669.
116. Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009; 139: 485-498.
117. Wang Q, McLoughlin RM, Cobb BA, et al. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J Exp Med. 2006; 203: 2853-2863.
118. Pulendran B, Kumar P, Cutler CW, et al. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J Immunol. 2001; 167: 5067-5076.
119. - dendritic cells. J Immunol. 2003; 171: 1156-1163.
120. Boonstra A, sselin-Paturel C, Gilliet M, et al. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J Exp Med. 2003; 197: 101-109.
121. Uematsu S, Fujimoto K, Jang MH, 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.
122. Manicassamy S, Ravindran R, Deng J, et al. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat Med. 2009; 15: 401-409.
123. Monteleone I, Platt AM, Jaensson E, et al. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur J Immunol. 2008; 38: 1533-1547.
124. Magalhaes JG, Tattoli I, Girardin SE,. The intestinal epithelial barrier: how to distinguish between the microbial flora and pathogens. Semin Immunol. 2007; 19: 106-115.
125. Kapsenberg ML,. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol. 2003; 3: 984-993.
126. Chen CC, Louie S, McCormick BA, et al. Helminth-primed dendritic cells alter the host response to enteric bacterial infection. J Immunol. 2006; 176: 472-483.
127. +) T helper-1 type responses to commensal bacteria in normal human intestinal lamina propria. Clin Immunol. 2009; 131: 317-332.
128. Hayashi F, Smith KD, Ozinsky A, et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 2001; 410: 1099-1103.
129. + lamina propria cells. Nat Immunol. 2006; 7: 868-874.
130. Maloy KJ, Kullberg MC,. IL-23 and Th17 cytokines in intestinal homeostasis. Mucosal Immunol. 2008; 1: 339-349.
131. Smits HH, van Beelen AJ, Hessle C, et al. Commensal Gram-negative bacteria prime human dendritic cells for enhanced IL-23 and IL-27 expression and enhanced Th1 development. Eur J Immunol. 2004; 34: 1371-1380.
132. Ng SC, Benjamin JL, Koutsoumpas A, et al. Altered intestinal dendritic function in patients with active Crohn's disease is associated with an imbalance in pro- and anti-inflammatory faecal microbiota. Gut. 2009; 58 (suppl 2): P1005.
133. Mata-Haro V, Cekic C, Martin M, et al. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science. 2007; 316: 1628-1632.
134. Fitzgerald KA, Golenbock DT,. Immunology. The shape of things to come. Science. 2007; 316: 1574-1576.
135. d'Ostiani CF, Del SG, Bacci A, et al. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J Exp Med. 2000; 191: 1661-1674.
136. Huang Q, Liu D, Majewski P, et al. The plasticity of dendritic cell responses to pathogens and their components. Science. 2001; 294: 870-875.
137. Joffre O, Nolte MA, Sporri R, et al. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev. 2009; 227: 234-247.
138. Duchmann R, Neurath MF, Meyer zum Buschenfelde KH,. Responses to self and non-self intestinal microflora in health and inflammatory bowel disease. Res Immunol. 1997; 148: 589-594.
139. Duchmann R, Kaiser I, Hermann E, et al. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol. 1995; 102: 448-455.
140. Karlis J, Penttila I, Tran TB, 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.
141. Niess JH,. Role of mucosal dendritic cells in inflammatory bowel disease. World J Gastroenterol. 2008; 14: 5138-5148.
142. + T cells. Am J Pathol. 1996; 148: 1503-1515.
143. Strober W, Fuss IJ, Blumberg RS,. The immunology of mucosal models of inflammation. Annu Rev Immunol. 2002; 20: 495-549.
144. + T cell-induced colitis. Eur J Immunol. 2003; 33: 1073-1083.
145. Malmstrom V, Shipton D, Singh B, 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.
146. +) T cells to subepithelial dendritic cell aggregates precedes the development of colitis in a murine adoptive transfer model. Lab Invest. 2001; 81: 1339-1349.
147. + regulatory T cells. J Immunol. 2003; 170: 3939-3943.
148. Becker C, Wirtz S, Blessing M, et al. Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells. J Clin Invest. 2003; 112: 693-706.
149. + dendritic cells. Inflamm Bowel Dis. 2009; 15: 236-247.
150. Cua DJ, Sherlock J, Chen Y, et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 2003; 421: 744-748.
151. Murphy CA, Langrish CL, Chen Y, et al. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med. 2003; 198: 1951-1957.
152. Hue S, Ahern P, Buonocore S, et al. Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J Exp Med. 2006; 203: 2473-2483.
153. Weaver CT, Hatton RD, Mangan PR, et al. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol. 2007; 25: 821-852.
154. Bettelli E, Korn T, Oukka M, et al. Induction and effector functions of T(H)17 cells. Nature. 2008; 453: 1051-1057.
155. Langrish CL, McKenzie BS, Wilson NJ, et al. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev. 2004; 202: 96-105.
156. Garrett WS, Lord GM, Punit S, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007; 131: 33-45.
157. Alcaide P, Jones TG, Lord GM, et al. Dendritic cell expression of the transcription factor T-bet regulates mast cell progenitor homing to mucosal tissue. J Exp Med. 2007; 204: 431-439.
158. Silva MA,. Intestinal dendritic cells and epithelial barrier dysfunction in Crohn's disease. Inflamm Bowel Dis. 2009; 15: 436-453.
159. Kaser A, Ludwiczek O, Holzmann S, et al. Increased expression of CCL20 in human inflammatory bowel disease. J Clin Immunol. 2004; 24: 74-85. (Pubitemid 38375798)
160. - dendritic cell populations in the colonic mucosa of patients with Crohn's disease. Eur J Immunol. 2003; 33: 143-151.
161. de BA, Mende I, Baretton G, et al. A subset of human dendritic cells in the T cell area of mucosa-associated lymphoid tissue with a high potential to produce TNF-alpha. J Immunol. 2003; 170: 5089-5094.
162. - dendritic cells accumulate in the subepithelial dome and internalize translocated Escherichia coli HB101 in the Peyer's patches of ileal Crohn's disease. Am J Pathol. 2009; 174: 82-90.
163. Vuckovic S, Florin TH, Khalil D, et al. CD40 and CD86 upregulation with divergent CMRF44 expression on blood dendritic cells in inflammatory bowel diseases. Am J Gastroenterol. 2001; 96: 2946-2956.
164. Baumgart DC, Metzke D, Schmitz J, et al. Patients with active inflammatory bowel disease lack immature peripheral blood plasmacytoid and myeloid dendritic cells. Gut. 2005; 54: 228-236.
165. Murakami H, Akbar SM, Matsui H, et al. Macrophage migration inhibitory factor activates antigen-presenting dendritic cells and induces inflammatory cytokines in ulcerative colitis. Clin Exp Immunol. 2002; 128: 504-510.
166. Yeung MM, Melgar S, Baranov V, et al. Characterisation of mucosal lymphoid aggregates in ulcerative colitis: immune cell phenotype and TcR-gammadelta expression. Gut. 2000; 47: 215-227.
167. Ikeda Y, Akbar F, Matsui H, et al. Characterization of antigen-presenting dendritic cells in the peripheral blood and colonic mucosa of patients with ulcerative colitis. Eur J Gastroenterol Hepatol. 2001; 13: 841-850.
168. Christ AD, Stevens AC, Koeppen H, et al. An interleukin 12-related cytokine is up-regulated in ulcerative colitis but not in Crohn's disease. Gastroenterology. 1998; 115: 307-313.
169. Fuss IJ, Heller F, Boirivant M, et al. Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest. 2004; 113: 1490-1497.
170. + colonic lamina propria cells is associated with inflammation in ulcerative colitis. Clin Exp Immunol. 2009; 158: 205-218.
171. Sakuraba A, Sato T, Kamada N, et al. Th1/Th17 Immune response is induced by mesenteric lymph node dendritic cells in Crohn's disease. Gastroenterology. 2009; 137: 1736-1745.
172. Hornef MW, Frisan T, Vandewalle A, et al. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med. 2002; 195: 559-570.
173. Hisamatsu T, Ogata H, Hibi T,. Innate immunity in inflammatory bowel disease: state of the art. Curr Opin Gastroenterol. 2008; 24: 448-454.
174. Iliev ID, Spadoni I, Mileti E, et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut. 2009; 58: 1481-1489.
175. + dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med. 2005; 202: 1063-1073.
176. + dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med. 2008; 205: 2139-2149.
177. Iliev ID, Mileti E, Matteoli G, et al. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2009; 2: 340-350.
178. + regulatory T cell expansion induced by antigen-driven interaction with intestinal epithelial cells independent of local dendritic cells. Gut. 2009; 58: 211-219.
179. Butler M, Ng CY, van Heel DA, et al. Modulation of dendritic cell phenotype and function in an in vitro model of the intestinal epithelium. Eur J Immunol. 2006; 36: 864-874.
180. Sigmundsdottir H, Butcher EC,. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat Immunol. 2008; 9: 981-987.
181. Johansson-Lindbom B, Agace WW,. Generation of gut-homing T cells and their localization to the small intestinal mucosa. Immunol Rev. 2007; 215: 226-242.
182. Butcher EC, Williams M, Youngman K, et al. Lymphocyte trafficking and regional immunity. Adv Immunol. 1999; 72: 209-253.
183. Zabel BA, Agace WW, Campbell JJ, 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.
184. Ohmori K, Fukui F, Kiso M, 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.
185. + T cells are resident in normal skin. J Immunol. 2006; 176: 4431-4439.
186. Campbell JJ, Haraldsen G, Pan J, et al. The chemokine receptor CCR4 in
187. Campbell JJ, O'Connell DJ, Wurbel MA,. Cutting edge: chemokine receptor CCR4 is necessary for antigen-driven cutaneous accumulation of CD4 T cells under physiological conditions. J Immunol. 2007; 178: 3358-3362.
188. Schaerli P, Ebert L, Willimann K, et al. A skin-selective homing mechanism for human immune surveillance T cells. J Exp Med. 2004; 199: 1265-1275.
189. Mora JR, Bono MR, Manjunath N, et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature. 2003; 424: 88-93.
190. Stagg AJ, Kamm MA, Knight SC,. Intestinal dendritic cells increase T cell expression of alpha4beta7 integrin. Eur J Immunol. 2002; 32: 1445-1454.
191. Johansson-Lindbom B, Svensson M, Wurbel MA, et al. 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.
192. Mora JR, Cheng G, Picarella D, et al. 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.
193. Annacker O, Coombes JL, Malmstrom V, et al. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med. 2005; 202: 1051-1061.
194. Hammerschmidt SI, Ahrendt M, Bode U, 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.
195. Iwata M,. Retinoic acid production by intestinal dendritic cells and its role in T-cell trafficking. Semin Immunol. 2009; 21: 8-13.
196. Manicassamy S, Pulendran B,. Retinoic acid-dependent regulation of immune responses by dendritic cells and macrophages. Semin Immunol. 2009; 21: 22-27.
197. Iwata M, Hirakiyama A, Eshima Y, et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 2004; 21: 527-538.
198. Blomhoff R, Blomhoff HK,. Overview of retinoid metabolism and function. J Neurobiol. 2006; 66: 606-630.
199. + T-cell subsets and effectively control intestinal inflammation. Gastroenterology. 2009; 137: 1391-1402.
200. Saurer L, McCullough KC, Summerfield A,. In vitro induction of mucosa-type dendritic cells by all-trans retinoic acid. J Immunol. 2007; 179: 3504-3514.
201. Lampen A, Meyer S, Arnhold T, et al. Metabolism of vitamin A and its active metabolite all-trans-retinoic acid in small intestinal enterocytes. J Pharmacol Exp Ther. 2000; 295: 979-985.
202. + antigen-presenting cells control the proliferation and differentiation of T cells in the intestinal mucosa. Nat Immunol. 2005; 6: 698-706.
203. + T cells. Mucosal Immunol. 2008; 1: 38-48.
204. Dudda JC, Lembo A, Bachtanian E, 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.
205. Sigmundsdottir H, Pan J, Debes GF, et al. DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27. Nat Immunol. 2007; 8: 285-293.
206. Benson MJ, Pino-Lagos K, Rosemblatt M, et al. 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.
207. Mucida D, Park Y, Kim G, et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007; 317: 256-260.
208. +) Treg cell conversion of naive T cells. Immunity. 2009; 30: 471-472.
209. +CD44hi Cells. Immunity. 2008; 29: 758-770.
210. Maynard CL, Hatton RD, Helms WS, et al. Contrasting roles for all-trans retinoic acid in TGF-beta-mediated induction of Foxp3 and Il10 genes in developing regulatory T cells. J Exp Med. 2009; 206: 343-357.
211. O'Connor W Jr, Kamanaka M, Booth CJ, et al. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol. 2009; 10: 603-609.
212. Nenci A, Becker C, Wullaert A, et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature. 2007; 446: 557-561.
213. + DCs. J Exp Med. 2009; 206: 3115-3130.
214. Eksteen B, Liaskou E, Adams DH,. Lymphocyte homing and its role in the pathogenesis of IBD. Inflamm Bowel Dis. 2008; 14: 1298-1312.
215. + T cells. J Immunol. 1997; 158: 2099-2106.
216. Kato S, Hokari R, Matsuzaki K, et al. Amelioration of murine experimental colitis by inhibition of mucosal addressin cell adhesion molecule-1. J Pharmacol Exp Ther. 2000; 295: 183-189.
217. Matsuzaki K, Tsuzuki Y, Matsunaga H, 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.
218. Farkas S, Hornung M, Sattler C, 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.
219. Goto A, Arimura Y, Shinomura Y, et al. Antisense therapy of MAdCAM-1 for trinitrobenzenesulfonic acid-induced murine colitis. Inflamm Bowel Dis. 2006; 12: 758-765.
220. Souza HS, Elia CC, Spencer J, et al. Expression of lymphocyte-endothelial receptor-ligand pairs, alpha4beta7/MAdCAM-1 and OX40/OX40 ligand in the colon and jejunum of patients with inflammatory bowel disease. Gut. 1999; 45: 856-863.
221. Arihiro S, Ohtani H, Suzuki 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.
222. Briskin M, Winsor-Hines D, Shyjan A, et al. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol. 1997; 151: 97-110.
223. Hesterberg PE, Winsor-Hines D, Briskin MJ, et al. Rapid resolution of chronic colitis in the cotton-top tamarin with an antibody to a gut-homing integrin alpha 4 beta 7. Gastroenterology. 1996; 111: 1373-1380.
224. Feagan BG, Greenberg GR, Wild G, et al. Treatment of ulcerative colitis with a humanized antibody to the alpha4beta7 integrin. N Engl J Med. 2005; 352: 2499-2507.
225. Targan SR, Feagan BG, Fedorak RN, et al. Natalizumab for the treatment of active Crohn's disease: results of the ENCORE Trial. Gastroenterology. 2007; 132: 1672-1683.
226. Schreiber S, Reinisch W, Vanasek T, et al. Traficet-EN, an oral CCR-9 specific antagonist, induces high levels of remission in the open-label phase of PROTECT-1 in Crohn's disease. Gut 2008; 57: 002.
227. Ghosh S, Goldin E, Gordon FH, et al. Natalizumab for active Crohn's disease. N Engl J Med. 2003; 348: 24-32.
228. Ng SC, Plamondon S, Kamm MA, et al. Intestinal dendritic cells in ulcerative colitis have altered homing characteristics (CD103-alpha E) expression: a valuable therapeutic target? Gut 2008; 55: OP045.
229. Ardizzone S, Puttini PS, Cassinotti A, et al. Extraintestinal manifestations of inflammatory bowel disease. Dig Liver Dis. 2008; 40 (suppl 2):, S253-S259.
230. + gut-homing lymphocytes to the liver in primary sclerosing cholangitis. J Exp Med. 2004; 200: 1511-1517.
231. Eksteen B, Mora JR, Haughton EL, et al. Gut homing receptors on CD8 T-cells ARE retinoic acid dependent and not maintained by Liver dendritic or stellate cells. Gastroenterology. 2009; 137: 320-329.
232. Lackey DE, Ashley SL, Davis AL, et al. Retinoic acid decreases adherence of murine myeloid dendritic cells and increases production of matrix metalloproteinase-9. J Nutr. 2008; 138: 1512-1519.
233. Szeles L, Keresztes G, Torocsik D, et al. 1,25-dihydroxyvitamin D3 is an autonomous regulator of the transcriptional changes leading to a tolerogenic dendritic cell phenotype. J Immunol. 2009; 182: 2074-2083.
234. Ng SC, Hart AL, Kamm MA, et al. Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis. 2009; 15: 300-310.
235. Mohamadzadeh M, Olson S, Kalina WV, et al. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A. 2005; 102: 2880-2885.
236. Hart AL, Lammers K, Brigidi P, et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut. 2004; 53: 1602-1609.
237. Drakes M, Blanchard T, Czinn S,. Bacterial probiotic modulation of dendritic cells. Infect Immun. 2004; 72: 3299-3309.
238. de Moreno de LA, Dogi CA, Galdeano CM, et al. Effect of the administration of a fermented milk containing Lactobacillus casei DN-114001 on intestinal microbiota and gut associated immune cells of nursing mice and after weaning until immune maturity. BMC Immunol. 2008; 9: 27.
239. Hoarau C, Martin L, Faugaret D, et al. Supernatant from bifidobacterium differentially modulates transduction signaling pathways for biological functions of human dendritic cells. PLoS One. 2008; 3: e2753.
240. Tsai YT, Cheng PC, Fan CK, et al. Time-dependent persistence of enhanced immune response by a potential probiotic strain Lactobacillus paracasei subsp. paracasei NTU 101. Int J Food Microbiol. 2008; 128: 219-225.
241. Wang X, O'Gorman MR, Bu HF, et al. Probiotic preparation VSL#3 alters the distribution and phenotypes of dendritic cells within the intestinal mucosa in C57BL/10J mice. J Nutr. 2009; 139: 1595-1602.
242. Chen CC, Chiu CH, Lin TY, et al. Effect of probiotics Lactobacillus acidophilus on Citrobacter rodentium colitis: the role of dendritic cells. Pediatr Res. 2009; 65: 169-175.
243. Ng SC, Plamondon S, Kamm MA, et al. Immunosuppressive effetcs via human intestinal dendritic cells of probiotic bacteria and steroids in the treatment of acute ulcerative colitis. Inflammatory Bowel Dis. 2010 (in press).
244. Thomas S, Przesdzing I, Metzke D, et al. Saccharomyces boulardii inhibits lipopolysaccharide-induced activation of human dendritic cells and T cell proliferation. Clin Exp Immunol. 2009; 156: 78-87.
245. Kanzato H, Fujiwara S, Ise W, et al. Lactobacillus acidophilus strain L-92 induces apoptosis of antigen-stimulated T cells by modulating dendritic cell function. Immunobiology. 2008; 213: 399-408.
246. Mannon PJ, Leon F, Fuss IJ, et al. Successful granulocyte-colony stimulating factor treatment of Crohn's disease is associated with the appearance of circulating interleukin-10-producing T cells and increased lamina propria plasmacytoid dendritic cells. Clin Exp Immunol. 2009; 155: 447-456.
247. Ng SC, Koutsampous A, Hedin CR,. Production of IL-10 by colonic dendritic cells is associated with higher concentrations of faecal microbiota in patients with active Crohn's disease. Gut. 2008; 377.
248. Lindsay JO, Whelan K, Stagg AJ, et al. Clinical, microbiological, and immunological effects of fructo-oligosaccharide in patients with Crohn's disease. Gut. 2006; 55: 348-355.
249. Piemonti L, Monti P, Allavena P, et al. Glucocorticoids affect human dendritic cell differentiation and maturation. J Immunol. 1999; 162: 6473-6481.
250. Woltman AM, de Fijter JW, Kamerling SW, et al. The effect of calcineurin inhibitors and corticosteroids on the differentiation of human dendritic cells. Eur J Immunol. 2000; 30: 1807-1812.
251. Moser M, De ST, Sornasse T, et al. Glucocorticoids down-regulate dendritic cell function in vitro and in vivo. Eur J Immunol. 1995; 25: 2818-2824.
252. Piemonti L, Monti P, Allavena P, et al. Glucocorticoids increase the endocytic activity of human dendritic cells. Int Immunol. 1999; 11: 1519-1526.
253. Pedersen AE, Schmidt EG, Gad M, et al. Dexamethasone/1alpha-25- dihydroxyvitamin D3-treated dendritic cells suppress colitis in the SCID T-cell transfer model. Immunology. 2009; 127: 354-364.
254. Wada Y, Hisamatsu T, Kamada N, et al. Retinoic acid contributes to the induction of IL-12-hypoproducing dendritic cells. Inflamm Bowel Dis. 2009; 15: 1548-1546.
255. Yokota A, Takeuchi H, Maeda N, et al. GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int Immunol. 2009; 21: 361-377.
256. Palucka AK, Laupeze B, Aspord C, et al. Immunotherapy via dendritic cells. Adv Exp Med Biol. 2005; 560: 105-114.