The Multifaceted Influence of the Mucosal Microflora on Mucosal Dendritic Cell Responses

Immunity

Volumn 31, Issue 3, 2009, Pages 377-388

  Strober, Warren ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD4 ANTIGEN; CYTOKINE; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; STAT3 PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

BACTEROIDES FRAGILIS; BACTEROIDETES; CD4+ T LYMPHOCYTE; CELL CONTACT; CELL FUNCTION; COMMENSAL; CROHN DISEASE; CYTOKINE PRODUCTION; CYTOPHAGA; DENDRITIC CELL; EPITHELIUM CELL; FLAVOBACTERIA; HOMEOSTASIS; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; INTESTINE EPITHELIUM; INTESTINE FLORA; LAMINA PROPRIA; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CYTOKINES; DENDRITIC CELLS; HOMEOSTASIS; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; SIGNAL TRANSDUCTION;

EID: 70049090007     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2009.09.001     Document Type: Review

References (83)

1. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., Yagita H., Ishii N., Evans R., Honda K., and Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature 455 (2008) 808-812
2. Baker K., Qiao S.W., Kuo T., Kobayashi K., Yoshida M., Lencer W.I., and Blumberg R.S. Immune and non-immune functions of the (not so) neonatal Fc receptor, FcRn. Semin Immunopathol. (2009) 10.1007/s00281-009-0160-9 in press. Published online June 3, 2009
3. Barnich N., Aguirre J.E., Reinecker H.C., Xavier R., and Podolsky D.K. Membrane recruitment of NOD2 in intestinal epithelial cells is essential for nuclear factor-κB activation in muramyl dipeptide recognition. J. Cell Biol. 170 (2005) 21-26
4. Barnich N., and Darfeuille-Michaud A. Adherent-invasive Escherichia coli and Crohn's disease. Curr. Opin. Gastroenterol. 23 (2007) 16-20
5. Becker C., Wirtz S., Blessing M., Pirhonen J., Strand D., Bechtold O., Frick J., Galle P.R., Autenrieth I., and Neurath M.F. Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells. J. Clin. Invest. 112 (2003) 693-706
6. Becker C., Fantini M.C., Schramm C., Lehr H.A., Wirtz S., Nikolaev A., Burg J., Strand S., Klessich R., Huber S., et al. TGF-β suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling. Immunity 21 (2004) 491-501
7. Beckwith J., Cong Y., Sundberg J.P., Elson C.O., and Leiter E.H. Cdcs1, a major colitogenic locus in mice, regulates innate and adaptive immune response to enteric bacterial antigens. Gastroenterology 129 (2005) 1473-1484
8. Bogunovic M., Ginhoux F., Helft J., Shang L., Hashimoto D., Greter M., Liu K., Jakubzick C., Ingersoll M.A., Leboeuf M., et al. Origin of the Lamina Propria Dendritic Cell Network. Immunity 31 (2009) 513-525 this issue
9. Boirivant M., Pallone F., Di Giacinto C., Fina D., Monteleone I., Marinaro M., Caruso R., Colantoni A., Palmieri C., Sanchez M., Strober W., MacDonald T.T., and Monteleone G. Inhibition of Smad7 with a specific antisense oligonucleotide facilitates TGF-beta1-induced suppression of colitis. Gastroenterology 131 (2006) 1786-1798
10. Boirivant M., Amendola A., Butera A., Sanchez M., Xu L., Marinaro M., Kitani A., Di Giacinto C., Strober W., and Fuss I.J. A transient breach in the epithelial barrier leads to regulatory T-cell generation and resistance to experimental colitis. Gastroenterology 135 (2008) 1612-1623
11. Bouma G., and Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3 (2003) 521-533
12. Brandwein S.L., McCabe R.P., Cong Y., Waites K.B., Ridwan B.U., Dean P.A., Ohkusa T., Birkenmeier E.H., Sundberg J.P., and Elson C.O. Spontaneous colitic C3H/HeJBir mice demonstrate selective antibody reactivity to antigens of the enteric bacterial flora. J. Immunol. 159 (1997) 44-52
13. Bringer M.A., Glasser A.L., Tung C.H., Méresse S., and Darfeuile-Michaud A. The Crohn's disease-associated adherent-invasive Escherischia coli strain LF82 replicates in mature phagolysosomes within J774 macrophages. Cell. Microbiol. 8 (2006) 471-484
14. Cario E., Gerken G., and Podolsky D.K. Toll-like receptor 2 controls mucosal inflammation by regulating epithelial barrier function. Gastroenterology 132 (2007) 1359-1374
15. Chieppa M., Rescigno M., Huang A.Y., and Germain R.N. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203 (2006) 2841-2852
16. Cong Y., Weaver C.T., Lazenby A., and Elson C.O. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J. Immunol. 169 (2002) 6112-6119
17. Cong Y., Brandwein S.L., McCabe R.P., Lazenby A., Birkenmeier E.H., Sundberg J.P., and Elson C.O. CD4+ T cells reactive to enteric bacterial antigens in spontaneous colitic C3H/HeJBir mice increased T helper cell type 1 response and ability to transfer disease. J. Exp. Med. 187 (1998) 855-864
18. Coombes J.L., Siddiqui K.R., Arancibia-Cárcamo C.V., Hall J., Sun C.M., Belkaid Y., and Powrie F. A functionally specialized population of mucosal CD103+ DCs induce Foxp3+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204 (2007) 1757-1764
19. Coombes J.L., and Powrie F. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8 (2008) 435-446
20. Corr S.C., Gahan C.C., and Hill C. M-cells: Origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunol. Med. Microbiol. 52 (2008) 2-12
21. Darfeuille-Michaud A., Boudeau J., Bulois P., Neut C., Glasser A.L., Barnich N., Bringer M.A., Swidsinski A., Beaugerie L., and Columbel J.F. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127 (2004) 412-421
22. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., and Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8 (2007) 1086-1094
23. Depaolo R.W., Tang F., Kim I., Han M., Levin N., Ciletti N., Lin A., Anderson D., Scheewind O., and Jabri B. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 6 (2008) 350-361
24. De Winter H., Elewaut D., Turovskaya O., Huflejt M., Shimeld C., Hagenbaugh A., Binder S., Takahashi T., Kronenberg M., and Cheroutre H. Regulation of mucosal immune responses by recombinent interleukine 10 produced by intestinal epithelial cells. Gastroenterology 122 (2002) 1829-1841
25. Elson C.O., Cong Y., McCracken V.J., Dimmitt R.A., Lorenz R.G., and Weaver C.T. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol. Rev. 206 (2005) 260-276
26. Fan H., and Cook J.A. Molecular mechanisms of endotoxin tolerance. J. Endotoxin Res. 10 (2004) 71-84
27. Frank D.N., St. Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., and Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104 (2007) 13780-13785
28. Garrett W.S., Lord G.M., Punit S., Lugo-Villarino G., Mazmanian S.K., Ito S., Glickman J.N., and Glimcher L.H. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 131 (2007) 33-45
29. Girardin S.E., Boneca I.G., Viale J., Chamallard M., Labigne A., Thomas G., Philpott D.J., and Sansonetti P.J. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 278 (2003) 8869-8872
30. Grivennikov S., Karin E., Terzic J., Mucida D., Yu G.Y., Vallabhapurapu S., Scheller J., Rose-John S., Cheroutre H., Eckman L., and Karin M. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 15 (2009) 103-113
31. Groschwitz K.R., and Hogan S.P. Intestinal barrier function: Molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 124 (2009) 21-22
32. Hedl M., Li J., Cho J.H., and Abraham C. Chronic stimulation of Nod2 mediates tolerance to bacterial products. Proc. Natl. Acad. Sci. USA 104 (2007) 19440-19445
33. Hermiston M.L., and Gordon J.I. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science 270 (1995) 1203-1207
34. Iliev I.D., Matteoli G., and Rescigno M. The yin and yang of intestinal epithelial cells in controlling dendritic cell function. J. Exp. Med. 204 (2007) 2253-2257
35. Iliev I.D., Spadoni I., Mileti E., Matteoli G., Sonzogni A., Sampietro G.M., Foschi D., Caprioli F., Viale G., and Rescigno M. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut (2009) 10.1136/gut.2008.175166 in press. Published online June 30, 2009
36. Iliev I.D., Mileti E., Matteloi G., Chieppa M., and Rescigno M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2 (2009) 340-350
37. Ivanov I.I., Frutos R.L., Manel N., Yosinaga K., Rifkin D.B., Sartor R.B., Finlay B.B., and Litman D.R. Specific microbiota directs the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4 (2008) 337-349
38. Iwamoto S., Iwai S., Tsjiyama K., Kurahashi C., Takeshita K., Naoe M., Masunaga A., Ogawa Y., Oguchi K., and Miyazaki A. TNF-α drives human CD14+ monocytes to differentiate into CD70+ dendritic cells evoking Th1 and Th17 responses. J. Immunol. 179 (2007) 1449-1457
39. Jaensson E., Uronen-Hansson H., Pabst O., Eksteen B., Tian J., Coombes J.L., Berg P.L., Davidsson T., Powrie F., Johansson-Lindbom B., and Agace W.W. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205 (2008) 2139-2149
40. Jarry A., Bossard C., Bou-Hanna C., Masson D., Espaze E., Denis M.G., and Laboisse C.L. Mucosal IL-10 and TGF-β play crucial roles in preventing LPS-driven, IFN-γ-mediated epithelial damage in human colon explants. J. Clin. Invest. 118 (2008) 1132-1142
41. Kleessen B., Kroesen A.J., Buhr H.J., and Blaut M. Mucosa and invading bacteria in patients with inflammatory bowel disease compared with controls. Scand. J. Gastroenterol. 37 (2002) 1034-1041
42. Kobayashi K., Qiao S.W., Yoshida M., Baker K., Lencer W.I., and Blumberg R.S. An FcRn-dependent role for anti-flagellin in pathogenesis of immunoglobulin G-mediated colitis in mice. Gastroenterology (2009) 10.1053/j.gastro.2009.07.059 in press. Published online August 6, 2009
43. Kobayashi K., Hernandez L.D., Galán J.E., Janeway Jr. C.A., Medzhitov R., and Flavell R.A. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110 (2002) 191-202
44. Kobayashi K.S., Chamallard M., Ogura Y., Hengariu O., Inohara N., Nuñez G., and Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 307 (2005) 731-734
45. Kramer M., Netea M.G., de Jong D.J., Kulberg B.J., and Adema G.J. Impaired dendritic cell function in Crohn's disease patients with NOD2 3020insC mutation. J. Leukoc. Biol. 79 (2006) 860-866
46. Kyd J.M., and Cripps A.W. Functional differences between M cells and enterocytes in sampling luminal antigens. Vaccine 26 (2008) 6221-6224
47. Liew F.Y., Xu D., Brint E.K., and O'Neill L.A. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5 (2005) 446-458
48. Liu H., Komai-Koma M., Xu D., and Liew F.Y. Toll-like receptor 2 signaling modulates the functions of CD4CD25 regulatory cells. Proc. Natl. Acad. Sci. USA 103 (2006) 7048-7053
49. Lodes M.J., Cong Y., Elson C.O., Mohameth R., Landers C.J., Targan S.R., Fort M., and Hershberg R.M. Bacterial flagellin is a dominant antigen in Crohn's disease. J. Clin. Invest. 113 (2004) 1296-1306
50. Manocha M., Svend R., Laouar A., Liao G., Bhan A., Borst J., Terhorst C., and Manjunath N. Blocking CD27-CD70 costimulates pathway suppresses experimental colitis. J. Immunol. 183 (2009) 270-276
51. Mazmanian S.K., Round J.L., and Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453 (2008) 620-625
52. McCole D.F., and Barrett K.E. Varied role of the gut epithelium in mucosal homeostasis. Curr. Opin. Gastroenterol. 23 (2007) 647-654
53. 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., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307 (2005) 254-258
54. Niess J.H. The commensal gut flora drives the accumulation of CX3CR1 DCs responsible for the induction of Th17 responses in the large intestine. Mucosal Immunol. 2 Suppl. 1 (2009) 81
55. Ogura Y., Lala S., Xin W., Smith E., Dowds T.A., Chen F.F., Zimmermann E., Tretlakova M., Cho J.H., Greenson J.K., et al. Expression of NOD2 in Paneth cells; a possible link to Crohn's ileitis. Gut 52 (2003) 1591-1597
56. Ouellette A.J. Paneth cell alpha defensin synthesis and function. Curr. Top. Microbiol. Immunol. 306 (2006) 1-25
57. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004) 229-241
58. Rescigno M., Rotta G., Valzasina B., and Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 204 (2001) 572-581
59. Rimoldi M., Chieppa M., Salucci V., Avogadri F., Sonzogni A., Sampietro G.M., Nespoli A., Viale G., Allavene P., and Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 6 (2005) 507-514
60. Roesler J., Thürigen A., Sun L., Koch R., Winkler U., Laass M.W., Gahr M., Rösen-Wolff A., and Henker J. Influence of CARD15 mutations on disease activity and response to therapy in 65 pediatric Crohn patients from Saxony, Germany. J. Pediatr. Gastroenterol. Nutr. 41 (2005) 27-32
61. Salzman N.H., Underwood M.A., and Bevins C.L. Paneth cells, defensins, and the commensal microbiota: A hypothesis on intimate interplay at the intestinal mucosa. Semin. Immunol. 19 (2007) 70-83
62. Shen C., Landers C.J., Derkowski C., Elson C.O., and Targan S.R. Enhanced CBirt-specific innate and adaptive immune responses in Crohn's disease. Inflamm. Bowel Dis. 14 (2008) 1641-1651
63. Simms L.A., Doecke J.D., Walsh M.D., Huang N., Fowler E.V., and Radford-Smith G.L. Reduced alpha-defensin expression is associated with inflammation and not NOD2 mutation status in ileal Crohn's disease. Gut 57 (2008) 903-910
64. Strober W., Murray P.J., Kitani A., and Watanabe T. Signalling pathways and molecular interactions of NOD1 and NOD2. Nat. Rev. Immunol. 6 (2006) 9-20
65. Strober W. The fundamental basis of inflammatory bowel disease. J. Clin. Invest. 117 (2007) 514-521
66. Strober W. The molecular basis of NOD2 susceptibility mutations in Crohn's disease. Mucosal Immunol. 1 Suppl. 1 (2008) S5-S9
67. Sundberg J.P., Elson C.O., Bedigian H., and Birkenmeier E.H. Spontaneous, heritable colitis in a new substrain of C3H/HeJ mice. Gastroenterology 107 (1994) 1726-1735
68. Sutmuller R.P., Morgan M.E., Netea M.G., Grauer O., and Adema G.J. Toll-like receptors on regulatory T cells: Expanding immune regulation. Trends Immunol. 27 (2006) 387-393
69. Swidsinski A., Ladhoff A., Pernthaler A., Swidsinski S., Loening-Baucke V., Ortner M., Weber J., Hoffmann U., Schreiber S., Dietel M., and Lochs H. Mucosal flora in inflammatory bowel disease. Gastroenterology 122 (2002) 44-54
70. Targan S.R., Landers C.J., Yang H., Lodes M.J., Cong Y., Papadakis K.A., Vasilauskas E., Elson C.O., and Hershberg R.M. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease. Gastroenterology 128 (2005) 2020-2028
71. Uematsu S., Fujimoto K., Jang M.H., Yang B.G., Jung Y.J., Nishikyama M., Sato S., Tsujimura T., Yamamoto M., Yokota Y., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9 (2008) 769-776
72. Varol C., Vallon-Eberhard A., Elinav E., Aychek T., Shapira Y., Luche H., Fehling H.J., Hardt W.-D., Shakhar G., and Jung S. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31 (2009) 502-512 this issue
73. Vijay-Kumar M., Sanders C.J., Taylor R.T., Kumar A., Aitken J.D., Sitaraman S.V., Neish A.S., Uematsu S., Akira S., Williams T.R., and Gewirtz A.T. Deletion of TLR5 results in spontaneous colitis in mice. J. Clin. Invest. 117 (2007) 3909-3921
74. Wang Q., McLoughlin R.M., Cobb B.A., Charrel-Dennis M., Zaleski K.J., Golenbock D., Tzianabos A.O., and Kasper D.L. A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 203 (2006) 2853-2863
75. Wang Y.H., and Liu Y.J. Thymic stromal lymphopoietin, OX40-ligand, and interleukin-25 in allergic responses. Clin. Exp. Allergy 39 (2009) 798-806
76. Watanabe T., Kitani A., Murray P.J., and Strober W. NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses. Nat. Immunol. 5 (2004) 800-808
77. Watanabe T., Kitani A., Murray P.J., Wakatsuki Y., Fuss I.J., and Strober W. Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis. Immunity 25 (2006) 473-485
78. Watanabe T., Asano N., Murray P.J., Ozato K., Tailor P., Fuss I.J., Kitani A., and Strober W. Muramyl dipeptide activation of nucleotide-binding oligomerization domain 2 protects mice from experimental colitis. J. Clin. Invest. 118 (2008) 545-559
79. Wehkamp J., Salzman N.H., Porter E., Nuding S., Weichenthal M., Petras R.E., Shen B., Scheffeler E., Schwab M., Linzmeier R., et al. Reduced Paneth cell alpha-defensin in ileal Crohn's disease. Proc. Natl. Acad. Sci. USA 102 (2005) 18129-18134
80. Wu S., Rhee K.J., Albesiano E., Rabizadeh S., Wu X., Yen H.-R., Huso D.L., Brancati F.L., Wick E., McAllister F., et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med. (2009) 10.1038/nm.2015 in press. Published online August 23, 2009
81. Yang Z., Fuss I.J., Watanabe T., Asano N., Davey M.P., Rosenbaum J.T., Strober W., and Kitani A. NOD2 transgenic mice exhibit enhanced MDP-mediated down-regulation of TLR2 responses and resistance to colitis induction. Gastroenterology 133 (2007) 1510-1521
82. Yoshida M., Claypool S.M., Wanger J.S., Mizoguchi E., Mizoguchi A., Roopenian D.C., Lencer W.I., and Blumberg R.S. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20 (2004) 769-783
83. Yoshida M., Kobayashi K., Kuo T.T., Bry L., Glickman J.N., Claypool S.M., Kaser A., Nagaishi T., Higgins D.E., Mizoguchi E., et al. Neonatal Fc receptor for IgG regulates mucosal immune responses to luminal bacteria. J. Clin. Invest. 116 (2006) 2142-2151