IL-10 restrains il-17 to limit lung pathology characteristics following pulmonary infection with francisella tularensis live vaccine strain

American Journal of Pathology

Volumn 183, Issue 5, 2013, Pages 1397-1404

  Slight, Samantha R ^a   Monin, Leticia ^a   Gopal, Radha ^a   Avery, Lyndsay ^a   Davis, Marci ^a   Cleveland, Hillary ^a   Oury, Tim D ^b   Rangel Moreno, Javier ^c   Khader, Shabaana A ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FRANCISELLA TULARENSIS; IMMUNE RESPONSE; INFECTION SENSITIVITY; LUNG INFECTION; MORTALITY; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; TULAREMIA;

ANIMALS; BACTERIAL VACCINES; DISEASE SUSCEPTIBILITY; FRANCISELLA TULARENSIS; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-17; LUNG; MICE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; RESPIRATORY TRACT INFECTIONS; TH1 CELLS; TH17 CELLS; TULAREMIA;

EID: 84886708386     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.07.008     Document Type: Article

References (38)

1. D.T. Dennis, T.V. Inglesby, D.A. Henderson, J.G. Bartlett, M.S. Ascher, E. Eitzen, A.D. Fine, A.M. Friedlander, J. Hauer, M. Layton, S.R. Lillibridge, J.E. McDade, M.T. Osterholm, T. O'Toole, G. Parker, T.M. Perl, P.K. Russell, and K. Tonat Tularemia as a biological weapon: medical and public health management JAMA 285 2001 2763 2773
2. J.W. Conlan Vaccines against Francisella tularensis-past, present and future Expert Rev Vaccines 3 2004 307 314
3. L.S. Anthony, E. Ghadirian, F.P. Nestel, and P.A. Kongshavn The requirement for gamma interferon in resistance of mice to experimental tularemia Microb Pathog 7 1989 421 428
4. K.L. Elkins, A. Cooper, S.M. Colombini, S.C. Cowley, and T.L. Kieffer In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70 Infect Immun 70 2002 1936 1948
5. N.S. Duckett, S. Olmos, D.M. Durrant, and D.W. Metzger Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain Infect Immun 73 2005 2306 2311
6. J.K. Kolls, and S.A. Khader The role of Th17 cytokines in primary mucosal immunity Cytokine Growth Factor Rev 21 2010 443 448
7. Y. Lin, S. Ritchea, A. Logar, S. Slight, M. Messmer, J. Rangel-Moreno, L. Guglani, J.F. Alcorn, H. Strawbridge, S.M. Park, R. Onishi, N. Nyugen, M.J. Walter, D. Pociask, T.D. Randall, S.L. Gaffen, Y. Iwakura, J.K. Kolls, and S.A. Khader Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis Immunity 31 2009 799 810
8. S.C. Cowley, A.I. Meierovics, J.A. Frelinger, Y. Iwakura, and K.L. Elkins Lung CD4- CD8- double-negative T cells are prominent producers of IL-17A and IFN-gamma during primary respiratory murine infection with Francisella tularensis live vaccine strain J Immunol 184 2010 5791 5801
9. G. Markel, E. Bar-Haim, E. Zahavy, H. Cohen, O. Cohen, A. Shafferman, and B. Velan The involvement of IL-17A in the murine response to sub-lethal inhalational infection with Francisella tularensis PLoS One 5 2010 e11176
10. J.W. Conlan, R. KuoLee, H. Shen, and A. Webb Different host defences are required to protect mice from primary systemic vs pulmonary infection with the facultative intracellular bacterial pathogen, Francisella tularensis LVS Microb Pathog 32 2002 127 134
11. M. Saraiva, and A. O'Garra The regulation of IL-10 production by immune cells Nat Rev Immunol 10 2010 170 181
12. P.S. Redford, A. Boonstra, S. Read, J. Pitt, C. Graham, E. Stavropoulos, G.J. Bancroft, and A. O'Garra Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung Eur J Immunol 40 2010 2200 2210
13. W.J. Dai, G. Kohler, and F. Brombacher Both innate and acquired immunity to Listeria monocytogenes infection are increased in IL-10-deficient mice J Immunol 158 1997 2259 2267
14. D.W. Metzger, S.L. Salmon, and G. Kirimanjeswara Differing effects of interleukin-10 on cutaneous and pulmonary Francisella tularensis live vaccine strain infection Infect Immun 81 2013 2022 2027
15. S. Nakae, Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses Immunity 17 2002 375 387
16. D.D. Kang, Y. Lin, J.R. Moreno, T.D. Randall, and S.A. Khader Profiling early lung immune responses in the mouse model of tuberculosis PLoS One 6 2011 e16161
17. M.L. Manni, M.W. Epperly, W. Han, T.S. Blackwell, S.R. Duncan, J.D. Piganelli, and T.D. Oury Leukocyte-derived extracellular superoxide dismutase does not contribute to airspace EC-SOD after interstitial pulmonary injury Am J Physiol Lung Cell Mol Physiol 302 2012 L160 L166
18. S.A. Khader, S. Partida-Sanchez, G. Bell, D.M. Jelley-Gibbs, S. Swain, J.E. Pearl, N. Ghilardi, F.J. Desauvage, F.E. Lund, and A.M. Cooper Interleukin 12p40 is required for dendritic cell migration and T cell priming after Mycobacterium tuberculosis infection J Exp Med 203 2006 1805 1815
19. + T helper cells mediate protective immunity against tuberculosis J Clin Invest 123 2013 712 726
20. R. Gopal, Y. Lin, N. Obermajer, S. Slight, N. Nuthalapati, M. Ahmed, P. Kalinski, and S.A. Khader IL-23-dependent IL-17 drives Th1-cell responses following Mycobacterium bovis BCG vaccination Eur J Immunol 42 2012 364 373
21. J.W. Heinecke, W. Li, G.A. Francis, and J.A. Goldstein Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative cross-linking of proteins J Clin Invest 91 1993 2866 2872
22. J.M. Daley, A.A. Thomay, M.D. Connolly, J.S. Reichner, and J.E. Albina Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice J Leukoc Biol 83 2008 64 70
23. J.M. Pitt, E. Stavropoulos, P.S. Redford, A.M. Beebe, G.J. Bancroft, D.B. Young, and A. O'Garra Blockade of IL-10 signaling during bacillus Calmette-Guerin vaccination enhances and sustains Th1, Th17, and innate lymphoid IFN-gamma and IL-17 responses and increases protection to Mycobacterium tuberculosis infection J Immunol 189 2012 4079 4087
24. D.J. Berg, N. Davidson, R. Kuhn, W. Muller, S. Menon, G. Holland, L. Thompson-Snipes, M.W. Leach, and D. Rennick Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses J Clin Invest 98 1996 1010 1020
25. N.J. Davidson, M.W. Leach, M.M. Fort, L. Thompson-Snipes, R. Kuhn, W. Muller, D.J. Berg, and D.M. Rennick T helper cell 1-type CD4+ T cells, but not B cells, mediate colitis in interleukin 10-deficient mice J Exp Med 184 1996 241 251
26. D. Yen, J. Cheung, H. Scheerens, F. Poulet, T. McClanahan, B. McKenzie, M.A. Kleinschek, A. Owyang, J. Mattson, W. Blumenschein, E. Murphy, M. Sathe, D.J. Cua, R.A. Kastelein, and D. Rennick IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6 J Clin Invest 116 2006 1310 1316
27. K.K. McKinstry, T.M. Strutt, A. Buck, J.D. Curtis, J.P. Dibble, G. Huston, M. Tighe, H. Hamada, S. Sell, R.W. Dutton, and S.L. Swain IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge J Immunol 182 2009 7353 7363
28. H. Li, S. Nookala, X.R. Bina, J.E. Bina, and F. Re Innate immune response to Francisella tularensis is mediated by TLR2 and caspase-1 activation J Leukoc Biol 80 2006 766 773
29. S. Periasamy, A. Singh, B. Sahay, T. Rahman, P.J. Feustel, G.H. Pham, E.J. Gosselin, and T.J. Sellati Development of tolerogenic dendritic cells and regulatory T cells favors exponential bacterial growth and survival during early respiratory tularemia J Leukoc Biol 90 2011 493 507
30. K.R. Hazlett, S.D. Caldon, D.G. McArthur, K.A. Cirillo, G.S. Kirimanjeswara, M.L. Magguilli, M. Malik, A. Shah, S. Broderick, I. Golovliov, D.W. Metzger, K. Rajan, T.J. Sellati, and D.J. Loegering Adaptation of Francisella tularensis to the mammalian environment is governed by cues which can be mimicked in vitro Infect Immun 76 2008 4479 4488
31. C.A. Albright, R.B. Sartor, and S.L. Tonkonogy Endogenous antigen presenting cell-derived IL-10 inhibits T lymphocyte responses to commensal enteric bacteria Immunol Lett 123 2009 77 87
32. J.P. Butchar, M.V. Rajaram, L.P. Ganesan, K.V. Parsa, C.D. Clay, L.S. Schlesinger, and S. Tridandapani Francisella tularensis induces IL-23 production in human monocytes J Immunol 178 2007 4445 4454
33. M.D. Woolard, L.L. Hensley, T.H. Kawula, and J.A. Frelinger Respiratory Francisella tularensis live vaccine strain infection induces Th17 cells and prostaglandin E2, which inhibits generation of gamma interferon-positive T cells Infect Immun 76 2008 2651 2659
34. H. Shen, G. Harris, W. Chen, A. Sjostedt, P. Ryden, and W. Conlan Molecular immune responses to aerosol challenge with Francisella tularensis in mice inoculated with live vaccine candidates of varying efficacy PLoS One 5 2010 e13349
35. C. Paranavitana, E. Zelazowska, L. DaSilva, P.R. Pittman, and M. Nikolich Th17 cytokines in recall responses against Francisella tularensis in humans J Interferon Cytokine Res 30 2010 471 476
36. T. Khayrullina, J.H. Yen, H. Jing, and D. Ganea In vitro differentiation of dendritic cells in the presence of prostaglandin E2 alters the IL-12/IL-23 balance and promotes differentiation of Th17 cells J Immunol 181 2008 721 735
37. K. Boniface, K.S. Bak-Jensen, Y. Li, W.M. Blumenschein, M.J. McGeachy, T.K. McClanahan, B.S. McKenzie, R.A. Kastelein, D.J. Cua, and R. de Waal Malefyt Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling J Exp Med 206 2009 535 548
38. P. Kalinski, C.M. Hilkens, A. Snijders, F.G. Snijdewint, and M.L. Kapsenberg IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells J Immunol 159 1997 28 35