The IL-23/Th17 axis is involved in the adaptive immune response to Bacillus anthracis in humans

European Journal of Immunology

Volumn 44, Issue 3, 2014, Pages 752-762

  Harris, Kristina M ^a,c   Ramachandran, Girish ^a,b   Basu, Subhendu ^a,b,d   Rollins, Sandra ^a   Mann, Dean ^a   Cross, Alan S ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b University of Maryland School of Medicine Center for Vaccine Development   (United States)

^c Immune Tolerance Network   (United States)

^d Emergent Biosolutions   (United States)

Author keywords

Bacillus anthracis spores; Human dendritic cells; IL 1 ; IL 23; Th17

Indexed keywords

INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6;

ADAPTIVE IMMUNITY; ANTHRAX; ANTIGEN SPECIFICITY; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL CLEARANCE; BACTERICIDAL ACTIVITY; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; DENDRITIC CELL; HUMAN; HUMAN CELL; INFLAMMATION; MONOCYTE; NONHUMAN; NORMAL HUMAN; PRIORITY JOURNAL; SPORE GERMINATION; TH1 CELL; TH17 CELL;

BACILLUS ANTHRACIS SPORES; HUMAN DENDRITIC CELLS; IL-1Β; IL-23; TH17;

ADAPTIVE IMMUNITY; ANTHRAX; ANTIGENS, BACTERIAL; BACILLUS ANTHRACIS; CYTOKINES; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; HUMANS; INTERLEUKIN-23; PHAGOCYTOSIS; SPORES, BACTERIAL; TH1 CELLS; TH17 CELLS;

EID: 84896041603     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343784     Document Type: Article

References (54)

1. Agrawal, A., Lingappa, J., Leppla, S. H., Agrawal, S., Jabbar, A., Quinn, C. and Pulendran, B., Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature 2003. 424: 329-334.
2. Kang, T. J., Basu, S., Zhang, L., Thomas, K. E., Vogel, S. N., Baillie, L. and Cross, A. S., Bacillus anthracis spores and lethal toxin induce IL-1beta via functionally distinct signaling pathways. Eur. J. Immunol. 2008. 38: 1574-1584.
3. Kang, T. J., Fenton, M. J., Weiner, M. A., Hibbs, S., Basu, S., Baillie, L. and Cross, A. S., Murine macrophages kill the vegetative form of Bacillus anthracis. Infect. Immun. 2005. 73: 7495-7501.
4. Acosta-Rodriguez, E. V., Napolitani, G., Lanzavecchia, A. and Sallusto, F., Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007. 8: 942-949.
5. Chung, Y., Chang, S. H., Martinez, G. J., Yang, X. O., Nurieva, R., Kang, H. S., Ma, L. et al., Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 2009. 30: 576-587.
6. Volpe, E., Servant, N., Zollinger, R., Bogiatzi, S. I., Hupe, P., Barillot, E. and Soumelis, V., A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat. Immunol. 2008. 9: 650-657.
7. McGeachy, M. J., Chen, Y., Tato, C. M., Laurence, A., Joyce-Shaikh, B., Blumenschein, W. M., McClanahan, T. K. et al., The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 2009. 10: 314-324.
8. Iwakura, Y. and Ishigame, H., The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 2006. 116: 1218-1222.
9. Ishigame, H., Nakajima, A., Saijo, S., Komiyama, Y., Nambu, A., Matsuki, T., Nakae, S. et al., The role of TNFalpha and IL-17 in the development of excess IL-1 signaling-induced inflammatory diseases in IL-1 receptor antagonist-deficient mice. Ernst Schering Res. Found. Workshop 2006. 56: 129-153.
10. Bettelli, E., Korn, T., Oukka, M. and Kuchroo, V. K., Induction and effector functions of T(H)17 cells. Nature 2008. 453: 1051-1057.
11. Jaffar, Z., Ferrini, M. E., Girtsman, T. A. and Roberts, K., Antigen-specific Treg regulate Th17-mediated lung neutrophilic inflammation, B-cell recruitment and polymeric IgA and IgM levels in the airways. Eur. J. Immunol. 2009. 39: 3307-3314.
12. Liang, S. C., Tan, X. Y., Luxenberg, D. P., Karim, R., Dunussi-Joannopoulos, K., Collins, M. and Fouser, L. A., Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 2006. 203: 2271-2279.
13. Ouyang, W., Kolls, J. K. and Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008. 28: 454-467.
14. Zelante, T., De, L. A., D'Angelo, C., Moretti, S. and Romani, L., IL-17/Th17 in anti-fungal immunity: what's new? Eur. J. Immunol. 2009. 39: 645-648.
15. Zhang, Z., Clarke, T. B. and Weiser, J. N., Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J. Clin. Invest 2009. 119: 1899-1909.
16. Khader, S. A., Bell, G. K., Pearl, J. E., Fountain, J. J., Rangel-Moreno, J., Cilley, G. E., Shen, F. et al., IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 2007. 8: 369-377.
17. Henry, C. J., Grayson, J. M., Brzoza-Lewis, K. L., Mitchell, L. M., Westcott, M. M., Cook, A. S. and Hiltbold, E. M., The roles of IL-12 and IL-23 in CD8+ T cell-mediated immunity against Listeria monocytogenes: insights from a DC vaccination model. Cell. Immunol. 2010. 264: 23-31.
18. Pickering, A. K., Osorio, M., Lee, G. M., Grippe, V. K., Bray, M. and Merkel, T. J., Cytokine response to infection with Bacillus anthracis spores. Infect. Immun. 2004. 72: 6382-6389.
19. Brittingham, K. C., Ruthel, G., Panchal, R. G., Fuller, C. L., Ribot, W. J., Hoover, T. A., Young, H. A. et al., Dendritic cells endocytose Bacillus anthracis spores: implications for anthrax pathogenesis. J. Immunol. 2005. 174: 5545-5552.
20. Hahn, A. C., Lyons, C. R. and Lipscomb, M. F., Effect of Bacillus anthracis virulence factors on human dendritic cell activation. Hum. Immunol. 2008. 69: 552-561.
21. Gervassi, A., Alderson, M. R., Suchland, R., Maisonneuve, J. F., Grabstein, K. H. and Probst, P., Differential regulation of inflammatory cytokine secretion by human dendritic cells upon Chlamydia trachomatis infection. Infect. Immun. 2004. 72: 7231-7239.
22. Gerosa, F., Baldani-Guerra, B., Lyakh, L. A., Batoni, G., Esin, S., Winkler-Pickett, R. T., Consolaro, M. R. et al., Differential regulation of interleukin 12 and interleukin 23 production in human dendritic cells. J. Exp. Med. 2008. 205: 1447-1461.
23. Giacomini, E., Iona, E., Ferroni, L., Miettinen, M., Fattorini, L., Orefici, G., Julkunen, I. et al., Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 2001. 166: 7033-7041.
24. Roses, R. E., Xu, S., Xu, M., Koldovsky, U., Koski, G. and Czerniecki, B. J., Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists. J. Immunol. 2008. 181: 5120-5127.
25. Harris, K. M., Monocytes differentiated with GM-CSF and IL-15 initiate Th17 and Th1 responses that are contact-dependent and mediated by IL-15. J. Leukoc. Biol. 2011. 90: 727-734.
26. Harris, K. M., Fasano, A. and Mann, D. L., Cutting edge: IL-1 controls the IL-23 response induced by gliadin, the etiologic agent in celiac disease. J. Immunol. 2008. 181: 4457-4460.
27. Romani, L., Immunity to fungal infections. Nat. Rev. Immunol. 2011. 11: 275-288.
28. Ma, C. S., Chew, G. Y., Simpson, N., Priyadarshi, A., Wong, M., Grimbacher, B., Fulcher, D. A. et al., Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 2008. 205: 1551-1557.
29. Puel, A., Cypowyj, S., Bustamante, J., Wright, J. F., Liu, L., Lim, H. K., Migaud, M. et al., Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011. 332: 65-68.
30. Chung, Y. and Dong, C., Don't leave home without it: the IL-23 visa to T(H)-17 cells. Nat. Immunol. 2009. 10: 236-238.
31. Manetti, R., Gerosa, F., Giudizi, M. G., Biagiotti, R., Parronchi, P., Piccinni, M. P., Sampognaro, S. et al., Interleukin 12 induces stable priming for interferon gamma (IFN-gamma) production during differentiation of human T helper (Th) cells and transient IFN-gamma production in established Th2 cell clones. J. Exp. Med. 1994. 179: 1273-1283.
32. Kwok, W. W., Yang, J., James, E., Bui, J., Huston, L., Wiesen, A. R. and Roti, M., The anthrax vaccine adsorbed vaccine generates protective antigen (PA)-Specific CD4+ T cells with a phenotype distinct from that of naive PA T cells. Infect. Immun. 2008. 76: 4538-4545.
33. Laughlin, E. M., Miller, J. D., James, E., Fillos, D., Ibegbu, C. C., Mittler, R. S., Akondy, R. et al., Antigen-specific CD4+ T cells recognize epitopes of protective antigen following vaccination with an anthrax vaccine. Infect. Immun. 2007. 75: 1852-1860.
34. Ingram, R. J., Metan, G., Maillere, B., Doganay, M., Ozkul, Y., Kim, L. U., Baillie, L. et al., Natural exposure to cutaneous anthrax gives long-lasting T cell immunity encompassing infection-specific epitopes. J. Immunol. 2010. 184: 3814-3821.
35. Boniface, K., Blumenschein, W. M., Brovont-Porth, K., McGeachy, M. J., Basham, B., Desai, B., Pierce, R. et al., Human Th17 cells comprise heterogeneous subsets including IFN-gamma-producing cells with distinct properties from the Th1 lineage. J. Immunol. 2010. 185: 679-687.
36. Zielinski, C. E., Mele, F., Aschenbrenner, D., Jarrossay, D., Ronchi, F., Gattorno, M., Monticelli, S. et al., Pathogen-induced human TH17 cells produce IFN-gamma or IL-10 and are regulated by IL-1beta. Nature 2012. 484: 514-518.
37. Sallusto, F., Zielinski, C. E. and Lanzavecchia, A., Human Th17 subsets. Eur. J. Immunol. 2012. 42: 2215-2220.
38. Cleret, A., Quesnel-Hellmann, A., Vallon-Eberhard, A., Verrier, B., Jung, S., Vidal, D., Mathieu, J. et al., Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J. Immunol. 2007. 178: 7994-8001.
39. Shetron-Rama, L. M., Herring-Palmer, A. C., Huffnagle, G. B. and Hanna, P., Transport of Bacillus anthracis from the lungs to the draining lymph nodes is a rapid process facilitated by CD11c +cells. Microb. Pathog. 2010. 49: 38-46.
40. Alileche, A., Serfass, E. R., Muehlbauer, S. M., Porcelli, S. A. and Brojatsch, J., Anthrax lethal toxin-mediated killing of human and murine dendritic cells impairs the adaptive immune response. PLoS Pathog. 2005. 1: e19.
41. Cleret-Buhot, A., Mathieu, J., Tournier, J. N. and Quesnel-Hellmann, A., Both lethal and edema toxins of Bacillus anthracis disrupt the human dendritic cell chemokine network. PLoS. ONE 2012. 7: e43266.
42. Cleret, A., Quesnel-Hellmann, A., Mathieu, J., Vidal, D. and Tournier, J. N., Resident CD11c+ lung cells are impaired by anthrax toxins after spore infection. J. Infect. Dis. 2006. 194: 86-94.
43. Paccani, S. R., Benagiano, M., Savino, M. T., Finetti, F., Tonello, F., D'Elios, M. M. and Baldari, C. T., The adenylate cyclase toxin of Bacillus anthracis is a potent promoter of T(H)17 cell development. J. Allergy Clin. Immunol. 2011. 127: 1635-1637.
44. Glomski, I. J., Corre, J. P., Mock, M. and Goossens, P. L., Cutting Edge: IFN-gamma-producing CD4 T lymphocytes mediate spore-induced immunity to capsulated Bacillus anthracis. J. Immunol. 2007. 178: 2646-2650.
45. 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.
46. Garraud, K., Cleret, A., Mathieu, J., Fiole, D., Gauthier, Y., Quesnel-Hellmann, A. and Tournier, J. N., Differential role of the interleukin-17 axis and neutrophils in resolution of inhalational anthrax. Infect. Immun. 2012. 80: 131-142.
47. Shinn, A. H., Bravo, N. C., Maecker, H. T. and Smith, J. W., TNF-alpha detection using a flow cytometric assay to determine cellular responses to anthrax vaccine. J. Immunol. Methods 2003. 282: 169-174.
48. Dheda, K., Chang, J. S., Lala, S., Huggett, J. F., Zumla, A. and Rook, G. A., Gene expression of IL17 and IL23 in the lungs of patients with active tuberculosis. Thorax 2008. 63: 566-568.
49. Scriba, T. J., Kalsdorf, B., Abrahams, D. A., Isaacs, F., Hofmeister, J., Black, G., Hassan, H. Y. et al., Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J. Immunol. 2008. 180: 1962-1970.
50. Loving, C. L., Osorio, M., Kim, Y. G., Nunez, G., Hughes, M. A. and Merkel, T. J., Nod1/Nod2-mediated recognition plays a critical role in induction of adaptive immunity to anthrax after aerosol exposure. Infect. Immun. 2009. 77: 4529-4537.
51. Sander, L. E., Davis, M. J., Boekschoten, M. V., Amsen, D., Dascher, C. C., Ryffel, B., Swanson, J. A. et al., Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 2011. 474: 385-389.
52. Sauer, J. D., Sotelo-Troha, K., von, M. J., Monroe, K. M., Rae, C. S., Brubaker, S. W., Hyodo, M. et al., The N-ethyl-N-nitrosourea-induced Goldenticket mouse mutant reveals an essential function of Sting in the in vivo interferon response to Listeria monocytogenes and cyclic dinucleotides. Infect. Immun. 2011. 79: 688-694.
53. Blander, J. M. and Sander, L. E., Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 2012. 12: 215-225.
54. Schlienger, K., Craighead, N., Lee, K. P., Levine, B. L. and June, C. H., Efficient priming of protein antigen-specific human CD4(+) T cells by monocyte-derived dendritic cells. Blood 2000. 96: 3490-3498.