Plasmacytoid dendritic cell-derived IFNα modulates Th17 differentiation during early Bordetella pertussis infection in mice

Mucosal Immunology

Volumn 9, Issue 3, 2016, Pages 777-786

  Wu, V ^a   Smith, A A ^a   You, H ^a   Nguyen, T A ^a,b   Ferguson, R ^a   Taylor, M ^a   Park, J E ^a   Llontop, P ^a   Youngman, K R ^a   Abramson, T ^a  

^a SAN JOSE STATE UNIVERSITY   (United States)

^b BD BIOSCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BLOCKING ANTIBODY;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; BACTERIAL STRAIN; BORDETELLA PERTUSSIS; CELL ISOLATION; CONTROLLED STUDY; COUGHING; FEMALE; FLOW CYTOMETRY; HISTOLOGY; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE; LUNG PARENCHYMA; LYMPH NODE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MONONUCLEAR CELL; MOUSE; NONHUMAN; PERTUSSIS; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE ACTIVATION; TH17 CELL; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL DIFFERENTIATION; COCULTURE; DENDRITIC CELL; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; LUNG; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY;

ANIMALS; ANTIBODIES, BLOCKING; BACTERIAL LOAD; BORDETELLA PERTUSSIS; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; FEMALE; HUMANS; IMMUNOMODULATION; INTERFERON-ALPHA; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; TH17 CELLS; WHOOPING COUGH;

EID: 84964951649     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.101     Document Type: Article

References (50)

1. Higgs, R., Higgins, S.C., Ross, P.J. & Mills, K.H. Immunity to the respiratory pathogen Bordetella pertussis. Mucosal Immunol. 5, 485-500 (2012).
2. Warfel, J.M. & Merkel, T.J. Bordetella pertussis infection induces amucosal IL-17 response and long-lived Th17 and Th1 immune memory cells in nonhuman primates. Mucosal Immunol. 6, 787-796 (2013).
3. Warfel, J.M., Zimmerman, L.I. & Merkel, T.J. Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proc. Natl Acad. Sci. USA 111, 787-792 (2014).
4. Fedele, G. et al. Bordetella pertussis commits human dendritic cells to promote a Th1/Th17 response through the activity of adenylate cyclase toxin and MAPK-pathways. PLoS One 5, e8734 (2010).
5. Adkins, I. et al. Bordetella adenylate cyclase toxin differentially modulates toll-like receptor-stimulated activation, migration and T cell stimulatory capacity of dendritic cells. PLoS One 9, e104064 (2014).
6. Dunne, A. et al. Inflammasome activation by adenylate cyclase toxin directs Th17 responses and protection against Bordetella pertussis. J. Immunol. 185, 1711-1719 (2010).
7. Fedele, G. et al. Lipopolysaccharides from Bordetella pertussis and Bordetella parapertussis differently modulate human dendritic cell functions resulting in divergent prevalence of Th17-polarized responses. J Immunol. 181, 208-216 (2008).
8. Stenger, R.M. et al. Immunodominance in mouse and human CD4+ T-cell responses specific for the Bordetella pertussis virulence factor P.69 pertactin. Infect. Immun. 77, 896-903 (2009).
9. Scanlon, K.M. et al. Epithelial anion transporter pendrin contributes to inflammatory lung pathology in mouse models of Bordetella pertussis infection. Infect. Immun. 82, 4212-4221 (2014).
10. Andreasen, C., Powell, D.A. & Carbonetti, N.H. Pertussis toxin stimulates IL-17 production in response to Bordetella pertussis infection in mice. PLoS One 4, e7079 (2009).
11. Andreasen, C. & Carbonetti, N.H. Role of neutrophils in response to Bordetella pertussis infection in mice. Infect. Immun. 77, 1182-1188 (2009).
12. Higgins, S.C., Jarnicki, A.G., Lavelle, E.C. & Mills, K.H. TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177, 7980-7989 (2006).
13. Henderson, M.W. et al. Contribution of Bordetella filamentous hemagglutinin and adenylate cyclase toxin to suppression and evasion of IL-17-mediated inflammation. Infect. Immun. 80, 2061-2075 (2012).
14. Dubin, P.J. & Kolls, J.K. Th17 cytokines and mucosal immunity. Immunol. Rev. 226, 160-171 (2008).
15. Colonna, M., Trinchieri, G. & Liu, Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5, 1219-1226 (2004).
16. Asselin-Paturel, C. & Trinchieri, G. Production of type I interferons: plasmacytoid dendritic cells and beyond. J. Exp. Med. 202, 461-465 (2005).
17. Parker, D. & Prince, A. Type I interferon response to extracellular bacteria in the airway epithelium. Trends Immunol. 32, 582-588 (2011).
18. Henry, T. et al. Type I IFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J. Immunol. 184, 3755-3767 (2010).
19. Nikolaus, S. et al. Interferon beta-1a in ulcerative colitis: A placebo controlled, randomised, dose escalating study. Gut 52, 1286-1290 (2003).
20. Tilg, H. et al. A randomised placebo controlled trial of pegylated interferon alpha in active ulcerative colitis. Gut 52, 1728-1733 (2003).
21. Zhang, L., Yuan, S., Cheng, G. & Guo, B. Type I IFN promotes IL-10 production from T cells to suppress Th17 cells and Th17-associated autoimmune inflammation. PLoS One 6, e28432 (2011).
22. Dieterich, C. & Relman, D.A. Modulation of the host interferon response and ISGylation pathway by B. pertussis filamentous hemagglutinin. PLoS One 6, e27535 (2011).
23. Nguyen, T.M. et al. Differential expression of alpha 4 integrins on effector memory T helper cells during Bordetella infections. Delayed responses in Bordetella pertussis. PLoS One 7, e52903 (2012).
24. Penna, G., Sozzani, S. & Adorini, L. Cutting edge: selective usage of chemokine receptors by plasmacytoid dendritic cells. J. Immunol. 167, 1862-1866 (2001).
25. Yoneyama, H. et al. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int. Immunol. 16, 915-928 (2004).
26. Eppert, B.L., Motz, G.T., Wortham,B.W., Flury, J.L. & Borchers, M.T.CCR7 deficiency leads to leukocyte activation and increased clearance in response to pulmonary Pseudomonas aeruginosa infection. Infect. Immun. 78, 2099-2107 (2010).
27. Umemoto, E. et al. Constitutive plasmacytoid dendritic cell migration to the splenic white pulp is cooperatively regulated by CCR7-and CXCR4-mediated signaling. J. Immunol. 189, 191-199 (2012).
28. Blasius, A.L. & Colonna, M. Sampling and signaling in plasmacytoid dendritic cells: The potential roles of Siglec-H. Trends Immunol. 27, 255-260 (2006).
29. Blasius, A.L., Giurisato, E., Cella, M., Schreiber, R.D., Shaw, A.S. & Colonna,M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 177, 3260-3265 (2006).
30. Sheehan, K.C. et al. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interferon Cytokine Res. 26, 804-819 (2006).
31. Ross, P.J. et al. Relative contribution of Th1 and Th17 cells in adaptive immunity to Bordetella pertussis: towards the rational design of an improved acellular pertussis vaccine. PLoS Pathog. 9, e1003264 (2013).
32. Kolls, J.K. & Khader, S.A. The role of Th17 cytokines in primary mucosal immunity. Cytokine Growth Factor Rev. 21, 443-448 (2010).
33. Ye, P. et al. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25, 335-340 (2001).
34. Hernandez-Santos, N., Huppler, A.R., Peterson, A.C., Khader, S.A., McKenna, K.C. & Gaffen, S.L. Th17 cells confer long-term adaptive immunity to oral mucosal Candida albicans infections. Mucosal Immunol. 6, 900-910 (2013).
35. Huang, W., Na, L., Fidel, P.L. & Schwarzenberger, P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190, 624-631 (2004).
36. Ewanowich, C.A., Melton, A.R., Weiss, A.A., Sherburne, R.K. & Peppler, M.S. Invasion of HeLa 229 cells by virulent Bordetella pertussis. Infect. Immun. 57, 2698-2704 (1989).
37. Friedman, R.L., Nordensson, K.,Wilson, L., Akporiaye, E.T. & Yocum, D.E. Uptake and intracellular survival of Bordetella pertussis in human macrophages. Infect. Immun. 60, 4578-4585 (1992).
38. Lamberti, Y., Gorgojo, J., Massillo, C. & Rodriguez, M.E. Bordetella pertussis entry into respiratory epithelial cells and intracellular survival. Pathog. Dis. 69, 194-204 (2013).
39. Fennelly, N.K. et al. Bordetella pertussis expresses a functional type III secretion system that subverts protective innate and adaptive immune responses. Infect. Immun. 76, 1257-1266 (2008).
40. Manh, T.P., Alexandre, Y., Baranek, T., Crozat, K. & Dalod, M. Plasmacytoid, conventional, and monocyte-derived dendritic cells undergo a profound and convergent genetic reprogramming during their maturation. Eur. J. Immunol. 43, 1706-1715 (2013).
41. Guo, B., Chang, E.Y. & Cheng, G. The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J. Clin. Invest. 118, 1680-1690 (2008).
42. Diveu, C. et al. IL-27 blocks RORc expression to inhibit lineage commitment of Th17 cells. J. Immunol. 182, 5748-5756 (2009).
43. Amadi-Obi, A. et al. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13, 711-718 (2007).
44. Stumhofer, J.S. et al. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7, 937-945 (2006).
45. Moschen, A.R., Geiger, S., Krehan, I., Kaser, A. & Tilg, H. Interferon-alpha controls IL-17 expression in vitro and in vivo. Immunobiology 213, 779-787 (2008).
46. Dhanani, S.,Huang,M.,Wang, J. & Dubinett, S.M. Interferon-alpha inhibits murine macrophage transforming growth factor-beta mRNA expression. Inflammation 18, 301-309 (1994).
47. Asselin-Paturel, C., Brizard, G., Pin, J.J., Briere, F. & Trinchieri, G. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J. Immunol. 171, 6466-6477 (2003).
48. Boonstra, A. et al. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. J Exp Med 197, 101-109 (2003).
49. Chen, Y.L., Chen, T.T., Pai, L.M., Wesoly, J., Bluyssen, H.A. & Lee, C.K. A type I IFN-Flt3 ligand axis augments plasmacytoid dendritic cell development from common lymphoid progenitors. J. Exp. Med. 210, 2515-2522 (2013).
50. Relman, D.A., Domenighini, M., Tuomanen, E., Rappuoli, R. & Falkow, S. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc. Natl Acad. Sci. USA 86, 2637-2641 (1989).