MyD88-dependent TLR1/2 signals educate dendritic cells with gut-specific imprinting properties

Journal of Immunology

Volumn 187, Issue 1, 2011, Pages 141-150

  Wang, Sen ^a   Villablanca, Eduardo J ^a   De Calisto, Jaime ^a   Gomes, Daniel C O ^a,b   Nguyen, Deanna D ^a   Mizoguchi, Emiko ^a   Kagan, Jonathan C ^c   Reinecker, Hans Christian ^a   Hacohen, Nir ^a   Nagler, Cathryn ^d   Xavier, Ramnik J ^a   Rossi Bergmann, Bartira ^b   Chen, Yi Bin ^a   Blomhoff, Rune ^e   Snapper, Scott B ^a   Mora, J Rodrigo ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; OXIDOREDUCTASE; RETINA DEHYDROGENASE; RETINOIC ACID; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME INDUCTION; IMMUNIZATION; IN VIVO STUDY; INTESTINE; LYMPHOCYTE HOMING; LYMPHOCYTOPOIESIS; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; TISSUE SPECIFICITY;

ANIMALS; BONE MARROW CELLS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DENDRITIC CELLS; GENOMIC IMPRINTING; INTESTINAL MUCOSA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELOID DIFFERENTIATION FACTOR 88; RADIATION CHIMERA; RECEPTORS, LYMPHOCYTE HOMING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2;

EID: 79960400021     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003740     Document Type: Article

References (64)

1. Mora, J. R. 2008. Homing imprinting and immunomodulation in the gut: role of dendritic cells and retinoids. Inflamm. Bowel Dis. 14: 275-289.
2. Mora, J. R., M. R. Bono, N. Manjunath, W. Weninger, L. L. Cavanagh, M. Rosemblatt, and U. H. Von Andrian. 2003. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424: 88-93.
3. Eksteen, B., J. R. Mora, E. L. Haughton, N. C. Henderson, L. Lee-Turner, E. J. Villablanca, S. M. Curbishley, A. I. Aspinall, U. H. von Andrian, and D. H. Adams. 2009. Gut homing receptors on CD8 T cells are retinoic acid dependent and not maintained by liver dendritic or stellate cells. Gastroenterology 137: 320-329.
4. Johansson-Lindbom, B., M. Svensson, M. A. Wurbel, B. Malissen, G. Márquez, and W. Agace. 2003. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J. Exp. Med. 198: 963-969.
5. Mora, J. R., M. Iwata, B. Eksteen, S. Y. Song, T. Junt, B. Senman, K. L. Otipoby, A. Yokota, H. Takeuchi, P. Ricciardi-Castagnoli, et al. 2006. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314: 1157-1160. (Pubitemid 44789048)
6. Iwata, M., A. Hirakiyama, Y. Eshima, H. Kagechika, C. Kato, and S. Y. Song. 2004. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21: 527-538.
7. Mucida, D., Y. Park, G. Kim, O. Turovskaya, I. Scott, M. Kronenberg, and H. Cheroutre. 2007. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317: 256-260. (Pubitemid 47076203)
8. Sun, C. M., J. A. Hall, R. B. Blank, N. Bouladoux, M. Oukka, J. R. Mora, and Y. Belkaid. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204: 1775-1785.
9. Coombes, J. L., K. R. Siddiqui, C. V. Arancibia-Cárcamo, J. Hall, C. M. Sun, Y. Belkaid, and F. Powrie. 2007. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 204: 1757-1764.
10. Kawai, T., and S. Akira. 2008. Toll-like receptor and RIG-I-like receptor signaling. Ann. N. Y. Acad. Sci. 1143: 1-20.
11. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
12. Napolitani, G., A. Rinaldi, F. Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6: 769-776.
13. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150. (Pubitemid 28361303)
14. Enzler, T., S. Gillessen, J. P. Manis, D. Ferguson, J. Fleming, F. W. Alt, M. Mihm, and G. Dranoff. 2003. Deficiencies of GM-CSF and interferon gamma link inflammation and cancer. J. Exp. Med. 197: 1213-1219.
15. Svensson, M., B. Johansson-Lindbom, F. Zapata, E. Jaensson, L. M. Austenaa, R. Blomhoff, andW. W. Agace. 2008. Retinoic acid receptor signaling levels and antigen dose regulate gut homing receptor expression on CD8+ T cells. Mucosal Immunol. 1: 38-48.
16. Denning, T. L., Y. C. Wang, S. R. Patel, I. R. Williams, and B. Pulendran. 2007. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8: 1086-1094.
17. Klein, C., D. Nguyen, C. H. Liu, A. Mizoguchi, A. K. Bhan, H. Miki, T. Takenawa, F. S. Rosen, F. W. Alt, R. C. Mulligan, and S. B. Snapper. 2003. Gene therapy for Wiskott-Aldrich syndrome: rescue of T-cell signaling and amelioration of colitis upon transplantation of retrovirally transduced hematopoietic stem cells in mice. Blood 101: 2159-2166.
18. Klonowski, K. D., K. J. Williams, A. L. Marzo, D. A. Blair, E. G. Lingenheld, and L. Lefrançois. 2004. Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 20: 551-562. (Pubitemid 38638125)
19. Svensson, M., J. Marsal, A. Ericsson, L. Carramolino, T. Brodén, G. Márquez, and W. W. Agace. 2002. CCL25 mediates the localization of recently activated CD8alphabeta(+) lymphocytes to the small-intestinal mucosa. J. Clin. Invest. 110: 1113-1121.
20. Kool, M., T. Soullié, M. van Nimwegen, M. A. Willart, F. Muskens, S. Jung, H. C. Hoogsteden, H. Hammad, and B. N. Lambrecht. 2008. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J. Exp. Med. 205: 869-882.
21. Zhu, Q., C. Egelston, A. Vivekanandhan, S. Uematsu, S. Akira, D. M. Klinman, I. M. Belyakov, and J. A. Berzofsky. 2008. Toll-like receptor ligands synergize through distinct dendritic cell pathways to induce T cell responses: implications for vaccines. Proc. Natl. Acad. Sci. USA 105: 16260-16265.
22. Guarda, G., C. Dostert, F. Staehli, K. Cabalzar, R. Castillo, A. Tardivel, P. Schneider, and J. Tschopp. 2009. T cells dampen innate immune responses through inhibition of NLRP1 and NLRP3 inflammasomes. Nature 460: 269-273.
23. Hammerschmidt, S. I., M. Ahrendt, U. Bode, B. Wahl, E. Kremmer, R. Förster, and O. Pabst. 2008. Stromal mesenteric lymph node cells are essential for the generation of gut-homing T cells in vivo. J. Exp. Med. 205: 2483-2490.
24. Bennett, B. L., D. T. Sasaki, B. W. Murray, E. C. O'Leary, S. T. Sakata, W. Xu, J. C. Leisten, A. Motiwala, S. Pierce, Y. Satoh, et al. 2001. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98: 13681-13686.
25. Yokota, A., H. Takeuchi, N. Maeda, Y. Ohoka, C. Kato, S. Y. Song, and M. Iwata. 2009. GM-CSF and IL-4 synergistically trigger dendritic cells to acquire retinoic acid-producing capacity. Int. Immunol. 21: 361-377.
26. Harrington, L. E., M. Galvan, L. G. Baum, J. D. Altman, and R. Ahmed. 2000. Differentiating between memory and effector CD8 T cells by altered expression of cell surface O-glycans. J. Exp. Med. 191: 1241-1246.
27. Jaensson, E., H. Uronen-Hansson, O. Pabst, B. Eksteen, J. Tian, J. L. Coombes, P. L. Berg, T. Davidsson, F. Powrie, B. Johansson-Lindbom, and W. W. Agace. 2008. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205: 2139-2149.
28. Wilson, N. S., L. J. Young, F. Kupresanin, S. H. Naik, D. Vremec, W. R. Heath, S. Akira, K. Shortman, J. Boyle, E. Maraskovsky, et al. 2008. Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol. Cell Biol. 86: 200-205.
29. Marrack, P., A. S. McKee, and M. W. Munks. 2009. Towards an understanding of the adjuvant action of aluminium. Nat. Rev. Immunol. 9: 287-293.
30. Edwards, A. D., S. S. Diebold, E. M. Slack, H. Tomizawa, H. Hemmi, T. Kaisho, S. Akira, and C. Reis e Sousa. 2003. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur. J. Immunol. 33: 827-833.
31. Uematsu, S., M. H. Jang, N. Chevrier, Z. Guo, Y. Kumagai, M. Yamamoto, H. Kato, N. Sougawa, H. Matsui, H. Kuwata, et al. 2006. Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat. Immunol. 7: 868-874.
32. Uematsu, S., K. Fujimoto, M. H. Jang, B. G. Yang, Y. J. Jung, M. Nishiyama, S. Sato, T. Tsujimura, M. Yamamoto, Y. Yokota, et al. 2008. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9: 769-776.
33. Rescigno, M., M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J. P. Kraehenbuhl, and P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2: 361-367.
34. Niess, J. H., S. Brand, X. Gu, L. Landsman, S. Jung, B. A. McCormick, J. M. Vyas, M. Boes, H. L. Ploegh, J. G. Fox, et al. 2005. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307: 254-258. (Pubitemid 40116240)
35. Farhat, K., S. Riekenberg, H. Heine, J. Debarry, R. Lang, J. Mages, U. Buwitt- Beckmann, K. Röschmann, G. Jung, K. H. Wiesmüller, and A. J. Ulmer. 2008. Heterodimerization of TLR2 with TLR1 or TLR6 expands the ligand spectrum but does not lead to differential signaling. J. Leukoc. Biol. 83: 692-701.
36. Robichon, C., D. Vidal-Ingigliardi, and A. P. Pugsley. 2005. Depletion of apolipoprotein N-acyltransferase causes mislocalization of outer membrane lipoproteins in Escherichia coli. J. Biol. Chem. 280: 974-983.
37. Dove, W. F., L. Clipson, K. A. Gould, C. Luongo, D. J. Marshall, A. R. Moser, M. A. Newton, and R. F. Jacoby. 1997. Intestinal neoplasia in the ApcMin mouse: independence from the microbial and natural killer (beige locus) status. Cancer Res. 57: 812-814.
38. Dillon, S., A. Agrawal, T. Van Dyke, G. Landreth, L. McCauley, A. Koh, C. Maliszewski, S. Akira, and B. Pulendran. 2004. A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells. J. Immunol. 172: 4733-4743. (Pubitemid 38456394)
39. Agrawal, S., A. Agrawal, B. Doughty, A. Gerwitz, J. Blenis, T. Van Dyke, and B. Pulendran. 2003. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171: 4984-4989. (Pubitemid 37432777)
40. Adhikary, G., Y. Sun, and E. Pearlman. 2008. C-Jun NH2 terminal kinase (JNK) is an essential mediator of Toll-like receptor 2-induced corneal inflammation. J. Leukoc. Biol. 83: 991-997.
41. Berndt, B. E., M. Zhang, G. H. Chen, G. B. Huffnagle, and J. Y. Kao. 2007. The role of dendritic cells in the development of acute dextran sulfate sodium colitis. J. Immunol. 179: 6255-6262.
42. Nagamine, C. M., J. J. Sohn, B. H. Rickman, A. B. Rogers, J. G. Fox, and D. B. Schauer. 2008. Helicobacter hepaticus infection promotes colon tumorigenesis in the BALB/c-Rag2(-/-) Apc(Min/+) mouse. Infect. Immun. 76: 2758-2766.
43. Arend, W. P., G. Palmer, and C. Gabay. 2008. IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 223: 20-38.
44. Sutterwala, F. S., Y. Ogura, M. Szczepanik, M. Lara-Tejero, G. S. Lichtenberger, E. P. Grant, J. Bertin, A. J. Coyle, J. E. Galán, P. W. Askenase, and R. A. Flavell. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
45. Martinon, F., A. Mayor, and J. Tschopp. 2009. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27: 229-265.
46. Dudda, J. C., A. Lembo, E. Bachtanian, J. Huehn, C. Siewert, A. Hamann, E. Kremmer, R. Förster, and S. F. Martin. 2005. Dendritic cells govern induction and reprogramming of polarized tissue-selective homing receptor patterns of T cells: important roles for soluble factors and tissue microenvironments. Eur. J. Immunol. 35: 1056-1065.
47. Hou, B., B. Reizis, and A. L. DeFranco. 2008. Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and -extrinsic mechanisms. Immunity 29: 272-282.
48. Gasse, P., C. Mary, I. Guenon, N. Noulin, S. Charron, S. Schnyder-Candrian, B. Schnyder, S. Akira, V. F. Quesniaux, V. Lagente, et al. 2007. IL-1R1/MyD88 signaling and the inflammasome are essential in pulmonary inflammation and fibrosis in mice. J. Clin. Invest. 117: 3786-3799.
49. Sanders, C. J., D. A. Moore, III, I. R. Williams, and A. T. Gewirtz. 2008. Both radioresistant and hemopoietic cells promote innate and adaptive immune responses to flagellin. J. Immunol. 180: 7184-7192.
50. Edele, F., R. Molenaar, D. Gütle, J. C. Dudda, T. Jakob, B. Homey, R. Mebius, M. Hornef, and S. F. Martin. 2008. Cutting edge: instructive role of peripheral tissue cells in the imprinting ofTcell homing receptor patterns. J. Immunol. 181: 3745-3749.
51. Iliev, I. D., E. Mileti, G. Matteoli, M. Chieppa, and M. Rescigno. 2009. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2: 340-350.
52. Monteleone, I., A. M. Platt, E. Jaensson, W. W. Agace, and A. M. Mowat. 2008. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur. J. Immunol. 38: 1533-1547.
53. Lavelle, E. C., C. Murphy, L. A. O'Neill, and E. M. Creagh. 2009. The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol. 3: 17-28.
54. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241. (Pubitemid 38962578)
55. Schoonjans, K., L. Dubuquoy, J. Mebis, E. Fayard, O. Wendling, C. Haby, K. Geboes, and J. Auwerx. 2005. Liver receptor homolog 1 contributes to intestinal tumor formation through effects on cell cycle and inflammation. Proc. Natl. Acad. Sci. USA 102: 2058-2062.
56. Chae, W. J., T. F. Gibson, D. Zelterman, L. Hao, O. Henegariu, and A. L. Bothwell. 2010. Ablation of IL-17A abrogates progression of spontaneous intestinal tumorigenesis. Proc. Natl. Acad. Sci. USA 107: 5540-5544.
57. Barton, G. M., and J. C. Kagan. 2009. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9: 535-542.
58. Chandran, S. S., D. Verhoeven, J. R. Teijaro, M. J. Fenton, and D. L. Farber. 2009. TLR2 engagement on dendritic cells promotes high frequency effector and memory CD4 T cell responses. J. Immunol. 183: 7832-7841.
59. Ahrendt, M., S. I. Hammerschmidt, O. Pabst, R. Pabst, and U. Bode. 2008. Stromal cells confer lymph node-specific properties by shaping a unique microenvironment influencing local immune responses. J. Immunol. 181: 1898-1907.
60. Mora, J. R., G. Cheng, D. Picarella, M. Briskin, N. Buchanan, and U. H. von Andrian. 2005. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201: 303-316.
61. Iiyama, R., T. Kanai, K. Uraushihara, T. Ishikura, S. Makita, T. Totsuka, M. Yamazaki, T. Nakamura, T. Miyata, H. Yoshida, et al. 2003. Normal development of the gut-associated lymphoid tissue except Peyer's patch in MyD88-deficient mice. Scand. J. Immunol. 58: 620-627.
62. Wurbel, M. A., M. Malissen, D. Guy-Grand, E. Meffre, M. C. Nussenzweig, M. Richelme, A. Carrier, and B. Malissen. 2001. Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gammadelta(+) gut intraepithelial lymphocytes. Blood 98: 2626-2632.
63. Wurbel, M. A., M. Malissen, D. Guy-Grand, B. Malissen, and J. J. Campbell. 2007. Impaired accumulation of antigen-specific CD8 lymphocytes in chemokine CCL25-deficient intestinal epithelium and lamina propria. J. Immunol. 178: 7598-7606.
64. Manicassamy, S., R. Ravindran, J. Deng, H. Oluoch, T. L. Denning, S. P. Kasturi, K. M. Rosenthal, B. D. Evavold, and B. Pulendran. 2009. Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat. Med. 15: 401-409.