Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement

Journal of Experimental Medicine

Volumn 203, Issue 13, 2006, Pages 2841-2852

  Chieppa, Marcello ^a   Rescigno, Maria ^b   Huang, Alex Y C ^a,c   Germain, Ronald N ^a  

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

^b EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11 ANTIGEN; ENHANCED GREEN FLUORESCENT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; EPITHELIUM CELL; HEMATOPOIETIC CELL; ILEUM; IMMUNOHISTOCHEMISTRY; JEJUNUM; LAMINA PROPRIA; MOUSE; NONHUMAN; PHOTON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SALMONELLA; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD11C; CELL SURFACE EXTENSIONS; CHEMOKINES, CC; DENDRITIC CELLS; EPITHELIAL CELLS; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTESTINE, SMALL; LASER SCANNING CYTOMETRY; MACROPHAGE INFLAMMATORY PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUCOUS MEMBRANE; MYELOID DIFFERENTIATION FACTOR 88; OLIGODEOXYRIBONUCLEOTIDES; POLYSACCHARIDES, BACTERIAL; RECEPTORS, CHEMOKINE; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 33845910419     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061884     Document Type: Article

References (58)

1. Pasare, C., and R. Medzhitov. 2003. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science. 299:1033-1036.
2. 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.
3. Ganz, T. 2003. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3:710-720.
4. Lamm, M.E. 1997. Interaction of antigens and antibodies at mucosal surfaces. Annu. Rev. Microbiol. 51:311-340.
5. Macpherson, A.J., D. Gatto, E. Sainsbury, G.R. Harriman, H. Hengartner, and R.M. Zinkernagel. 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science. 288:2222-2226.
6. Wykes, M., A. Pombo, C. Jenkins, and G.G. MacPherson. 1998. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161:1313-1319.
7. MacPherson, G., N. Kushnir, and M. Wykes. 1999. Dendritic cells, B cells and the regulation of antibody synthesis. Immunol. Rev. 172:325-334.
8. Macpherson, A.J., and T. Uhr. 2004. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science. 303:1662-1665.
9. Qi, H., J.G. Egen, A.Y. Huang, and R.N. Germain. 2006. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science. 312:1672-1676.
10. Neutra, M.R., N.J. Mantis, A. Frey, and P.J. Giannasca. 1999. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Semin. Immunol. 11:171-181.
11. Iwasaki, A., and B.L. Kelsall. 2001. Unique functions of CD11b+, CD8 alpha+, and double-negative Peyer's patch dendritic cells. J. Immunol. 166:4884-4890.
12. Jang, D.H., J.H. Han, S.H. Lee, Y.S. Lee, H. Park, S.H. Lee, H. Kim, and B.K. Kaang. 2005. Cofilin expression induces cofilin-actin rod formation and disrupts synaptic structure and function in Aplysia synapses. Proc. Natl. Acad. Sci. USA. 102:16072-16077.
13. Vallon-Eberhard, A., L. Landsman, N. Yogev, B. Verrier, and S. Jung. 2006. Transepithelial pathogen uptake into the small intestinal lamina propria. J. Immunol. 176:2465-2469.
14. Strober, W., B. Kelsall, I. Fuss, T. Marth, B. Ludviksson, R. Ehrhardt, and M. Neurath. 1997. Reciprocal IFN-gamma and TGF-beta responses regulate the occurrence of mucosal inflammation. Immunol. Today. 18:61-64.
15. + T cells. J. Exp. Med. 183:2669-2674.
16. Rimoldi, M., M. Chieppa, P. Larghi, M. Vulcano, P. Allavena, and M. Rescigno. 2005. Monocyte-derived dendritic cells activated by bacteria or by bacteria-stimulated epithelial cells are functionally different. Blood. 106:2818-2826.
17. 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.
18. Rescigno, M., G. Rotta, B. Valzasina, and P. Ricciardi-Castagnoli. 2001. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 204:572-581.
19. 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.
20. Boes, M., J. Cerny, R. Massol, M. Op den Brouw, T. Kirchhausen, J. Chen, and H.L. Ploegh. 2002. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature. 418:983-988.
21. Jung, S., D. Unutmaz, P. Wong, G. Sano, K. De los Santos, T. Sparwasser, S. Wu, S. Vuthoori, K. Ko, F. Zavala, et al. 2002. In vivo depletion of CD11c(+) dendritic cells abrogates priming of CD8(+) T cells by exogenous cell-associated antigens. Immunity. 17:211-220.
22. Ruedl, C., C. Rieser, G. Bock, G. Wick, and H. Wolf. 1996. Phenotypic and functional characterization of CD11c+ dendritic cell population in mouse Peyer's patches. Eur. J. Immunol. 26:1801-1806.
23. Cario, E. 2005. Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut. 54:1182-1193.
24. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature. 408:740-745.
25. Alexopoulou, L., A.C. Holt, R. Medzhitov, and R.A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 413:732-738.
26. Hayashi, F., K.D. Smith, A. Ozinsky, T.R. Hawn, E.C. Yi, D.R. Goodlett, J.K. Eng, S. Akira, D.M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 410:1099-1103.
27. 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.
28. Ortega-Cava, C.F., S. Ishihara, M.A. Rumi, M.M. Aziz, H. Kazumori, T. Yuki, Y. Mishima, I. Moriyama, C. Kadota, N. Oshima, et al. 2006. Epithelial toll-like receptor 5 is constitutively localized in the mouse cecum and exhibits distinctive down-regulation during experimental colitis. Clin. Vaccine Immunol. 13:132-138.
29. Vogel, S.N., C.T. Hansen, and D.L. Rosenstreich. 1979. Characterization of a congenitally LPS-resistant, athymic mouse strain. J. Immunol. 122:619-622.
30. Beutler, B., X. Du, and A. Poltorak. 2001. Identification of Toll-like receptor 4 (Tlr4) as the sole conduit for LPS signal transduction: genetic and evolutionary studies. J. Endotoxin Res. 7:277-280.
31. Wooten, R.M., Y. Ma, R.A. Yoder, J.P. Brown, J.H. Weis, J.F. Zachary, C.J. Kirschning, and J.J. Weis. 2002. Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J. Immunol. 168:348-355.
32. 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.
33. Janssens, S., K. Burns, J. Tschopp, and R. Beyaert. 2002. Regulation of interleukin-1- and lipopolysaccharide-induced NF-kappaB activation by alternative splicing of MyD88. Curr. Biol. 12:467-471.
34. Burns, K., S. Janssens, B. Brissoni, N. Olivos, R. Beyaert, and J. Tschopp. 2003. Inhibition of interleukin 1 receptor/Toll-like receptor signaling through the alternatively spliced, short form of MyD88 is due to its failure to recruit IRAK-4. J. Exp. Med. 197:263-268.
35. Izadpanah, A., M.B. Dwinell, L. Eckmann, N.M. Varki, and M.F. Kagnoff. 2001. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G710-G719.
36. Galan, J.E., and R. Curtiss III. 1989. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA. 86:6383-6387.
37. Shea, J.E., C.R. Beuzon, C. Gleeson, R. Mundy, and D.W. Holden. 1999. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect. Immun. 67:213-219.
38. Jung, S., J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20:4106-4114.
39. Fong, A.M., L.A. Robinson, D.A. Steeber, T.F. Tedder, O. Yoshie, T. Imai, and D.D. Patel. 1998. Fractalkine and CX3CR1 mediate a novel mechanism of leukocyte capture, firm adhesion, and activation under physiologic flow. J. Exp. Med. 188:1413-1419.
40. Ayabe, T., T. Ashida, Y. Kohgo, and T. Kono. 2004. The role of Paneth cells and their antimicrobial peptides in innate host defense. Trends Microbiol. 12:394-398.
41. Chabot, S., J.S. Wagner, S. Farrant, and M.R. Neutra. 2006. TLRs regulate the gatekeeping functions of the intestinal follicle-associated epithelium. J. Immunol. 176:4275-4283.
42. Sanders, C.J., Y. Yu, D.A. Moore III, I.R. Williams, and A.T. Gewirtz. 2006. Humoral immune response to flagellin requires T cells and activation of innate immunity. J. Immunol. 177:2810-2818.
43. Allavena, P., M. Chieppa, P. Monti, and L. Piemonti. 2004. From pattern recognition receptor to regulator of homeostasis: the double-faced macrophage mannose receptor. Crit. Rev. Immunol. 24:179-192.
44. Huang, F.P., N. Platt, M. Wykes, J.R. Major, T.J. Powell, C.D. Jenkins, and G.G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191:435-444.
45. Iwasaki, A., and B.L. Kelsall. 1999. 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. 190:229-239.
46. Kelsall, B.L., and M. Rescigno. 2004. Mucosal dendritic cells in immunity and inflammation. Nat. Immunol. 5:1091-1095.
47. Alpan, O., E. Bachelder, E. Isil, H. Arnheiter, and P. Matzinger. 2004. 'Educated' dendritic cells act as messengers from memory to naive T helper cells. Nat. Immunol. 5:615-622.
48. Alpan, O., G. Rudomen, and P. Matzinger. 2001. The role of dendritic cells, B cells, and M cells in gut-oriented immune responses. J. Immunol. 166:4843-4852.
49. Larson, D.R., W.R. Zipfel, R.M. Williams, S.W. Clark, M.P. Bruchez, F.W. Wise, and W.W. Webb. 2003. Water-soluble quantum dots for multiphoton fluorescence imaging in vivo. Science. 300:1434-1436.
50. von Andrian, U.H., and T.R. Mempel. 2003. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3:867-878.
51. Cahalan, M.D., I. Parker, S.H. Wei, and M.J. Miller. 2002. Two-photon tissue imaging: seeing the immune system in a fresh light. Nat. Rev. Immunol. 2:872-880.
52. Huang, A.Y., H. Qi, and R.N. Germain. 2004. Illuminating the landscape of in vivo immunity: insights from dynamic in situ imaging of secondary lymphoid tissues. Immunity. 21:331-339.
53. Germain, R.N., F. Castellino, M. Chieppa, J.G. Egen, A.Y. Huang, L.Y. Koo, and H. Qi. 2005. An extended vision for dynamic high-resolution intravital immune imaging. Semin. Immunol. 17:431-441.
54. Bousso, P., and E.A. Robey. 2004. Dynamic behavior of T cells and thymocytes in lymphoid organs as revealed by two-photon microscopy. Immunity. 21:349-355.
55. Germain, R.N., M.J. Miller, M.L. Dustin, and M.C. Nussenzweig. 2006. Dynamic imaging of the immune system: progress, pitfalls and promise. Nat. Rev. Immunol. 6:497-507.
56. Klinman, D.M. 2004. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat. Rev. Immunol. 4:249-258.
57. Gots, R.E., S.B. Formal, and R.A. Giannella. 1974. Indomethacin inhibition of Salmonella typhimurium, Shigella flexneri, and cholera-mediated rabbit ileal secretion. J. Infect. Dis. 130:280-284.
58. Avogadri, F., C. Martinoli, L. Petrovska, C. Chiodoni, P. Transidico, V. Bronte, R. Longhi, M.P. Colombo, G. Dougan, and M. Rescigno. 2005. Cancer immunotherapy based on killing of Salmonella-infected tumor cells. Cancer Res. 65:3920-3927.