TLR2-dependent modulation of dendritic cells by LT-IIa-B 5, a novel mucosal adjuvant derived from a type II heat-labile enterotoxin

Journal of Leukocyte Biology

Volumn 90, Issue 5, 2011, Pages 911-921

  Lee, Chang Hoon ^a   Masso Welch, Patricia ^a   Hajishengallis, George ^b   Connell, Terry D ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

Antigen; CCR7; CD4 +; DO11.10 mice; Lymph node; Migration; T cell

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; ESCHERICHIA COLI ENTEROTOXIN; HEAT LABILE ENTEROTOXIN 2A; HEAT LABILE ENTEROTOXIN 2A B 5; IMMUNOGLOBULIN A; IMMUNOLOGICAL ADJUVANT; OVALBUMIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELL ASSAY; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IMMUNE RESPONSE; IMMUNOMODULATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGENS, CD40; ANTIGENS, CD80; ANTIGENS, CD86; BACTERIAL TOXINS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DENDRITIC CELLS; ENTEROTOXINS; ESCHERICHIA COLI PROTEINS; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; NASAL MUCOSA; OVALBUMIN; TOLL-LIKE RECEPTOR 2;

MUS;

EID: 80055096366     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0511236     Document Type: Article

References (50)

1. Holmgren, J., Czerkinsky, C. (2005) Mucosal immunity and vaccines. Nat. Med. 11, S45-S53.
2. Mestecky, J., Ogra, P. L., McGhee, J. R., Lambrecht, B. N., Strober, W. (2005) Mucosal Immunology, 3rd ed., Academic Press, San Diego, CA, USA.
3. Matzinger, P. (1994) Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991-1045.
4. Connell, T. D., Metzger, D., Sfintescu, C., Evans, R. T. (1998) Immunostimulatory activity of LT-IIa, a type II heat-labile enterotoxin of Escherichia coli. Immunol. Lett. 62, 117-120.
5. Wu, H. Y., Russell, M. W. (1997) Nasal lymphoid tissue, intranasal immunization, and compartmentalization of the common mucosal immune system. Immunol. Res. 16, 187-201.
6. Wiley, J. A., Tighe, M. P., Harmsen, A. G. (2005) Upper respiratory tract resistance to influenza infection is not prevented by the absence of either nasal-associated lymphoid tissue or cervical lymph nodes. J. Immunol. 175, 3186-3196.
7. Park, H. S., Francis, K. P., Yu, J., Cleary, P. P. (2003) Membranous cells in nasal-associated lymphoid tissue: a portal of entry for the respiratory mucosal pathogen group A streptococcus. J. Immunol. 171, 2532-2537.
8. Kiyono, H., Fukuyama, S. (2004) NALT-versus Peyer's-patch-mediated mucosal immunity. Nat. Rev. Immunol. 4, 699-710.
9. Iwasaki, A. (2007) Mucosal dendritic cells. Annu. Rev. Immunol. 25, 381-418.
10. Liang, B., Hyland, L., Hou, S. (2001) Nasal-associated lymphoid tissue is a site of long-term virus-specific antibody production following respiratory virus infection of mice. J. Virol. 75, 5416-5420.
11. Wu, H. Y., Nikolova, E. B., Beagley, K. W., Eldridge, J. H., Russell, M. W. (1997) Development of antibody-secreting cells and antigen-specific T cells in cervical lymph nodes after intranasal immunization. Infect. Immun. 65, 227-235.
12. Tilney, N. L. (1971) Patterns of lymphatic drainage in the adult laboratory rat. J. Anat. 109, 369-383.
13. Drakes, M. L., Czinn, S. J., Blanchard, T. G. (2006) Regulation of murine dendritic cell immune responses by Helicobacter felis antigen. Infect. Immun. 74, 4624-4633.
14. Hajishengallis, G., Arce, S., Gockel, C. M., Connell, T. D., Russell, M. W. (2005) Immunomodulation with enterotoxins for the generation of secretory immunity or tolerance: applications for oral infections. J. Dent. Res. 84, 1104-1116.
15. Connell, T. D. (2007) Cholera toxin, LT-I, LT-IIa and LT-IIb: the critical role of ganglioside binding in immunomodulation by type I and type II heat-labile enterotoxins. Expert Rev. Vaccines 6, 821-834.
16. Nawar, H. F., Arce, S., Russell, M. W., Connell, T. D. (2005) Mucosal adjuvant properties of mutant LT-IIa and LT-IIb enterotoxins that exhibit altered ganglioside-binding activities. Infect. Immun. 73, 1330-1342.
17. Nawar, H. F., King-Lyons, N. D., Hu, J. C., Pasek, R. C., Connell, T. D. (2010) LT-IIc, a new member of the type II heat-labile enterotoxin family encoded by an Escherichia coli strain obtained from a nonmammalian host. Infect. Immun. 78, 4705-4713.
18. Russell, M. W., Bergmeier, L. A., Zanders, E. D., Lehner, T. (1980) Protein antigens of Streptococcus mutans: purification and properties of a double antigen and its protease-resistant component. Infect. Immun. 28, 486-493.
19. Nawar, H. F., Arce, S., Russell, M. W., Connell, T. D. (2007) Mutants of type II heat-labile enterotoxin LT-IIa with altered ganglioside-binding activities and diminished toxicity are potent mucosal adjuvants. Infect. Immun. 75, 621-633.
20. Martin, M., Metzger, D. J., Michalek, S. M., Connell, T. D., Russell, M. W. (2000) Comparative analysis of the mucosal adjuvanticity of the type II heat-labile enterotoxins LT-IIa and LT-IIb. Infect. Immun. 68, 281-287.
21. Hajishengallis, G., Tapping, R. I., Martin, M. H., Nawar, H., Lyle, E. A., Russell, M. W., Connell, T. D. (2005) Toll-like receptor 2 mediates cellular activation by the B subunits of type II heat-labile enterotoxins. Infect. Immun. 73, 1343-1349.
22. Liang, S., Hosur, K. B., Lu, S., Nawar, H. F., Weber, B. R., Tapping, R. I., Connell, T. D., Hajishengallis, G. (2009) Mapping of a microbial protein domain involved in binding and activation of the TLR2/TLR1 heterodimer. J. Immunol. 182, 2978-2985.
23. Wooten, R. M., Ma, Y., Yoder, R. A., Brown, J. P., Weis, J. H., Zachary, J. F., Kirschning, C. J., Weis, J. J. (2002) Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J. Immunol. 168, 348-355.
24. Murphy, K. M., Heimberger, A. B., Loh, D. Y. (1990) Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 250, 1720-1723.
25. Hajishengallis, G., Nawar, H., Tapping, R. I., Russell, M. W., Connell, T. D. (2004) The type II heat-labile enterotoxins LT-IIa and LT-IIb and their respective B pentamers differentially induce and regulate cytokine production in human monocytic cells. Infect. Immun. 72, 6351-6358.
26. Liang, S., Wang, M., Triantafilou, K., Triantafilou, M., Nawar, H. F., Russell, M. W., Connell, T. D., Hajishengallis, G. (2007) The A subunit of type IIb enterotoxin (LT-IIb) suppresses the proinflammatory potential of the B subunit and its ability to recruit and interact with TLR2. J. Immunol. 178, 4811-4819.
27. Song, J. H., Kim, J. I., Kwon, H. J., Shim, D. H., Parajuli, N., Cuburu, N., Czerkinsky, C., Kweon, M. N. (2009) CCR7-CCL19/CCL21-regulated dendritic cells are responsible for effectiveness of sublingual vaccination. J. Immunol. 182, 6851-6860.
28. Villablanca, E. J., Mora, J. R. (2008) A two-step model for Langerhans cell migration to skin-draining LN. Eur. J. Immunol. 38, 2975-2980.
29. Bromley, S. K., Thomas, S. Y., Luster, A. D. (2005) Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat. Immunol. 6, 895-901.
30. Fainaru, O., Shseyov, D., Hantisteanu, S., Groner, Y. (2005) Accelerated chemokine receptor 7-mediated dendritic cell migration in Runx3 knockout mice and the spontaneous development of asthma-like disease. Proc. Natl. Acad. Sci. USA 102, 10598-10603.
31. Niess, J. H., Reinecker, H. C. (2006) Dendritic cells in the recognition of intestinal microbiota. Cell. Microbiol. 8, 558-564.
32. West, M. A., Wallin, R. P., Matthews, S. P., Svensson, H. G., Zaru, R., Ljunggren, H. G., Prescott, A. R., Watts, C. (2004) Enhanced dendritic cell antigen capture via Toll-like receptor-induced actin remodeling. Science 305, 1153-1157.
33. Liang, S., Wang, M., Tapping, R. I., Stepensky, V., Nawar, H. F., Triantafilou, M., Triantafilou, K., Connell, T. D., Hajishengallis, G. (2007) Ganglioside GD1a is an essential coreceptor for Toll-like receptor 2 signaling in response to the B subunit of type IIb enterotoxin. J. Biol. Chem. 282, 7532-7542.
34. Wooten, R. M., Ma, Y., Yoder, R. A., Brown, J. P., Weis, J. H., Zachary, J. F., Kirschning, C. J., Weis, J. J. (2002) Toll-like receptor 2 plays a pivotal role in host defense and inflammatory response to Borrelia burgdorferi. Vector Borne Zoonotic Dis. 2, 275-278.
35. Sekine, S., Kataoka, K., Fukuyama, Y., Adachi, Y., Davydova, J., Yamamoto, M., Kobayashi, R., Fujihashi, K., Suzuki, H., Curiel, D. T., Shizukuishi, S., McGhee, J. R., Fujihashi, K. (2008) A novel adenovirus expressing Flt3 ligand enhances mucosal immunity by inducing mature nasopharyngeal-associated lymphoreticular tissue dendritic cell migration. J. Immunol. 180, 8126-8134.
36. Enioutina, E. Y., Bareyan, D., Daynes, R. A. (2008) TLR ligands that stimulate the metabolism of vitamin D3 in activated murine dendritic cells can function as effective mucosal adjuvants to subcutaneously administered vaccines. Vaccine 26, 601-613.
37. Schumann, K., Lammermann, T., Bruckner, M., Legler, D. F., Polleux, J., Spatz, J. P., Schuler, G., Forster, R., Lutz, M. B., Sorokin, L., Sixt, M. (2010) Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 32, 703-713.
38. Yen, J. H., Kong, W., Ganea, D. (2010) IFN-β inhibits dendritic cell migration through STAT-1-mediated transcriptional suppression of CCR7 and matrix metalloproteinase 9. J. Immunol. 184, 3478-3486.
39. Lapteva, N., Seethammagari, M. R., Hanks, B. A., Jiang, J., Levitt, J. M., Slawin, K. M., Spencer, D. M. (2007) Enhanced activation of human dendritic cells by inducible CD40 and Toll-like receptor-4 ligation. Cancer Res. 67, 10528-10537.
40. Cyster, J. G. (1999) Chemokines and cell migration in secondary lymphoid organs. Science 286, 2098-2102.
41. Leitner, J., Grabmeier-Pfistershammer, K., Steinberger, P. (2010) Receptors and ligands implicated in human T cell costimulatory processes. Immunol. Lett. 128, 89-97.
42. Huang, X., Reynolds, A. D., Mosley, R. L., Gendelman, H. E. (2009) CD 4+ T cells in the pathobiology of neurodegenerative disorders. J. Neuroimmunol. 211, 3-15.
43. Kapsenberg, M. L. (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3, 984-993.
44. Berenson, C. S., Nawar, H. F., Yohe, H. C., Castle, S. A., Ashline, D. J., Reinhold, V. N., Hajishengallis, G., Connell, T. D. (2010) Mammalian cell ganglioside-binding specificities of E. coli enterotoxins LT-IIb and variant LT-IIb(T13I). Glycobiology 20, 41-54.
45. Nawar, H. F., Greene, C. J., Lee, C. H., Mandell, L. M., Hajishengallis, G., Connell, T. D. (2011) LT-IIc, a new member of the type II heat-labile enterotoxin family, exhibits potent immunomodulatory properties that are different from those induced by LT-IIa or LT-IIb. Vaccine 29, 721-727.
46. Caux, C., Ait-Yahia, S., Chemin, K., de Bouteiller, O., Dieu-Nosjean, M. C., Homey, B., Massacrier, C., Vanbervliet, B., Zlotnik, A., Vicari, A. (2000) Dendritic cell biology and regulation of dendritic cell trafficking by chemokines. Springer Semin. Immunopathol. 22, 345-369.
47. Le Borgne, M., Dubois, B., Kaiserlian, D. (2007) Dendritic cells of mucosa and skin: "recruited for vaccination". Med. Sci. (Paris) 23, 819-825.
48. Dieu-Nosjean, M. C., Vicari, A., Lebecque, S., Caux, C. (1999) Regulation of dendritic cell trafficking: a process that involves the participation of selective chemokines. J. Leukoc. Biol. 66, 252-262.
49. Xin, H. M., Peng, Y. Z., Yuan, Z. Q., Guo, H. (2009) In vitro maturation and migration of immature dendritic cells after chemokine receptor 7 transfection. Can. J. Microbiol. 55, 859-866.
50. Caux, C., Vanbervliet, B., Massacrier, C., Ait-Yahia, S., Vaure, C., Chemin, K., Dieu-Nosjean And, M. C., Vicari, A. (2002) Regulation of dendritic cell recruitment by chemokines. Transplantation 73, S7-S11.