Intradermal immunization in the ear with cholera toxin and its non-toxic β subunit promotes efficient Th1 and Th17 differentiation dependent on migrating DCs

European Journal of Immunology

Volumn 41, Issue 10, 2011, Pages 2894-2904

  Meza Sánchez, David ^a,b   Pérez Montesinos, Gibrán ^a   Sánchez García, Javier ^b   Moreno, José ^c   Bonifaz, Laura C ^a  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

Author keywords

DCs; Migrating DCs; Skin immunization

Indexed keywords

CHOLERA TOXIN; CHOLERA TOXIN B SUBUNIT; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; LYSOZYME;

ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; EAR; IMMUNIZATION; INJECTION SITE; INTERFERON PRODUCTION; LEUKOCYTE MIGRATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE TRANSFER; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH17 CELL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGEN PRESENTATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CHOLERA TOXIN; DENDRITIC CELLS; EAR; HYPERSENSITIVITY, DELAYED; IMMUNIZATION; INJECTIONS, INTRADERMAL; INTERFERON-GAMMA; INTERLEUKIN-1; INTERLEUKIN-17; INTERLEUKIN-5; LYMPHOCYTE ACTIVATION; LYMPHOPOIESIS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; TH1 CELLS; TH17 CELLS;

EID: 80053165004     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040997     Document Type: Article

References (32)

1. Moser, M. and Murphy, K. M., Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 2000. 1: 199-205.
2. + T cells by exogenous cell-associated antigens. Immunity 2002. 17: 211-220.
3. Wilson, N. S. and Villadangos, J. A., Lymphoid organ dendritic cells: beyond the Langerhans cells paradigm. Immunol. Cell Biol. 2004. 82: 91-98.
4. Bennett, C. L., van Rijn, E., Jung, S., Inaba, K., Steinman, R. M., Kapsenberg, M. L. and Clausen, B. E., Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol. 2005. 169: 569-576.
5. Kaplan, D. H., Jenison, M. C., Saeland, S., Shlomchik, W. D. and Shlomchik, M. J., Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 2005. 23: 611-620.
6. Kissenpfennig, A., Henri, S., Dubois, B., Laplace-Builhe, C., Perrin, P., Romani, N., Tripp, C. H. et al., Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005. 22: 643-654.
7. Sen, D., Forrest, L., Kepler, T. B., Parker, I. and Cahalan, M. D., Selective and site-specific mobilization of dermal dendritic cells and Langerhans cells by Th1- and Th2-polarizing adjuvants. Proc. Natl. Acad. Sci. USA 2010. 107: 8334-8339.
8. Zhao, X., Deak, E., Soderberg, K., Linehan, M., Spezzano, D., Zhu, J., Knipe, D. M. and Iwasaki, A., Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J. Exp. Med. 2003. 197: 153-162.
9. Nagao, K., Ginhoux, F., Leitner, W. W., Motegi, S., Bennett, C. L., Clausen, B. E., Merad, M. and Udey, M. C., Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc. Natl. Acad. Sci. USA 2009. 106: 3312-3317.
10. Strid, J., Hourihane, J., Kimber, I., Callard, R. and Strobel, S., Disruption of the stratum corneum allows potent epicutaneous immunization with protein antigens resulting in a dominant systemic Th2 response. Eur. J. Immunol. 2004. 34: 2100-2109.
11. Hammond, S. A., Walwender, D., Alving, C. R. and Glenn, G. M., Transcutaneous immunization: T cell responses and boosting of existing immunity. Vaccine 2001. 19: 2701-2707.
12. El-Ghorr, A. A., Williams, R. M., Heap, C. and Norval, M., Transcutaneous immunisation with herpes simplex virus stimulates immunity in mice. FEMS Immunol. Med. Microbiol. 2000. 29: 255-261.
13. King, I. L., Kroenke, M. A. and Segal, B. M., GM-CSF-dependent, CD103+dermal dendritic cells play a critical role in Th effector cell differentiation after subcutaneous immunization. J. Exp. Med. 2010. 207: 953-961.
14. He, R., Oyoshi, M. K., Jin, H. and Geha, R. S., Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc. Natl. Acad. Sci. USA 2007. 104: 15817-15822.
15. Williams, N. A., Hirst, T. R. and Nashar, T. O., Immune modulation by the cholera-like enterotoxins: from adjuvant to therapeutic. Immunol. Today 1999. 20: 95-101.
16. Simecka, J. W., Jackson, R. J., Kiyono, H. and McGhee, J. R., Mucosally induced immunoglobulin E-associated inflammation in the respiratory tract. Infect. Immun. 2000. 68: 672-679.
17. Yamamoto, S., Kiyono, H., Yamamoto, M., Imaoka, K., Fujihashi, K., Van Ginkel, F. W., Noda, M. et al., A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc. Natl. Acad. Sci. USA 1997. 94: 5267-5272.
18. Schaffeler, M. P., Brokenshire, J. S. and Snider, D. P., Detection of precursor Th cells in mesenteric lymph nodes after oral immunization with protein antigen and cholera toxin. Int. Immunol. 1997. 9: 1555-1562.
19. Lee, J. B., Jang, J. E., Song, M. K. and Chang, J., Intranasal delivery of cholera toxin induces th17-dominated T-cell response to bystander antigens. PLoS One 2009. 4: e5190.
20. Datta, S. K., Sabet, M., Nguyen, K. P., Valdez, P. A., Gonzalez-Navajas, J. M., Islam, S., Mihajlov, I. et al., Mucosal adjuvant activity of cholera toxin requires Th17 cells and protects against inhalation anthrax. Proc. Natl. Acad. Sci. USA 2010. 107: 10638-10643.
21. Grdic, D., Ekman, L., Schon, K., Lindgren, K., Mattsson, J., Magnusson, K. E., Ricciardi-Castagnoli, P. and Lycke, N., Splenic marginal zone dendritic cells mediate the cholera toxin adjuvant effect: dependence on the ADP-ribosyltransferase activity of the holotoxin. J. Immunol. 2005. 175: 5192-5202.
22. Allenspach, E. J., Lemos, M. P., Porrett, P. M., Turka, L. A. and Laufer, T. M., Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity 2008. 29: 795-806.
23. Itano, A. A., McSorley, S. J., Reinhardt, R. L., Ehst, B. D., Ingulli, E., Rudensky, A. Y. and Jenkins, M. K., Distinct dendritic cell populations sequentially present antigen to CD4T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003. 19: 47-57.
24. Anjuere, F., George-Chandy, A., Audant, F., Rousseau, D., Holmgren, J. and Czerkinsky, C., Transcutaneous immunization with cholera toxin B subunit adjuvant suppresses IgE antibody responses via selective induction of Th1 immune responses. J. Immunol. 2003. 170: 1586-1592.
25. Sixt, M., Kanazawa, N., Selg, M., Samson, T., Roos, G., Reinhardt, D. P., Pabst, R. et al., The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005. 22: 19-29.
26. Kawamura, Y. I., Kawashima, R., Shirai, Y., Kato, R., Hamabata, T., Yamamoto, M., Furukawa, K. et al., Cholera toxin activates dendritic cells through dependence on GM1-ganglioside which is mediated by NF-kappaB translocation. Eur. J. Immunol. 2003. 33: 3205-3212.
27. Eriksson, K., Fredriksson, M., Nordstrom, I. and Holmgren, J., Cholera toxin and its B subunit promote dendritic cell vaccination with different influences on Th1 and Th2 development. Infect. Immun. 2003. 71: 1740-1747.
28. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D. et al., Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006. 441: 231-234.
29. Su, S. B., Silver, P. B., Wang, P., Chan, C. C. and Caspi, R. R., Cholera toxin prevents Th1-mediated autoimmune disease by inducing immune deviation. J. Immunol. 2004. 173: 755-761.
30. Areas, A. P., Oliveira, M. L., Miyaji, E. N., Leite, L. C. and Ho, P. L., Intradermal immunization of mice with cholera toxin B-pneumococcal surface protein A fusion protein is protective against intraperitoneal challenge with Streptococcus pneumoniae. Infect. Immun. 2005. 73: 3810-3813.
31. He, D., Wu, L., Kim, H. K., Li, H., Elmets, C. A. and Xu, H., IL-17 and IFN-gamma mediate the elicitation of contact hypersensitivity responses by different mechanisms and both are required for optimal responses. J. Immunol. 2009. 183: 1463-1470.
32. Obst, R., van Santen, H. M., Melamed, R., Kamphorst, A. O., Benoist, C. and Mathis, D., Sustained antigen presentation can promote an immunogenic T cell response, like dendritic cell activation. Proc. Natl. Acad. Sci. USA 2007. 104: 15460-15465.