The role of IL-27 in susceptibility to post-influenza Staphylococcus aureus pneumonia

Respiratory Research

Volumn 16, Issue 1, 2015, Pages

  Robinson, Keven M ^a,c   Lee, Benjamin ^a   Scheller, Erich V ^a   Mandalapu, Sivanarayana ^a   Enelow, Richard I ^b   Kolls, Jay K ^a   Alcorn, John F ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

IL 27; Influenza; Staphylococcus aureus; Type 17 immunity

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 27; INTERLEUKIN 27 RECEPTOR; INTERLEUKIN 6; INTERLEUKIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE RECEPTOR; IL10 PROTEIN, MOUSE; IL27 PROTEIN, MOUSE; IL27RA PROTEIN, MOUSE; INTERLEUKIN DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; C57BL 6 MOUSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; HISTOLOGY; INFECTION SENSITIVITY; INFLAMMATORY CELL; INFLUENZA A; INFLUENZA VIRUS A H1N1; MALE; MIXED INFECTION; MORBIDITY; MOUSE; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; STAPHYLOCOCCAL PNEUMONIA; STAPHYLOCOCCUS AUREUS; TH17 CELL; VIRUS LOAD; WILD TYPE; ANIMAL; C57BL MOUSE; CELLULAR IMMUNITY; DEFICIENCY; DISEASE MODEL; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); KNOCKOUT MOUSE; LUNG; MICROBIOLOGY; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; TIME FACTOR; VIROLOGY;

ANIMALS; BACTERIAL LOAD; COINFECTION; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; IMMUNITY, CELLULAR; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKINS; LUNG; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA, STAPHYLOCOCCAL; RECEPTORS, CYTOKINE; STAPHYLOCOCCUS AUREUS; TH17 CELLS; TIME FACTORS; VIRAL LOAD;

EID: 84923268193     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/s12931-015-0168-8     Document Type: Article

References (32)

1. Hoyert DL, Xu J. Deaths: preliminary data for 2011. Natl Vital Stat Rep 2012, 61:1-51. 24984457.
2. Rubinstein E, Kollef MH, Nathwani D. Pneumonia caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 2008, 46(Suppl 5):S378-385. 10.1086/533594, 18462093.
3. Williams DJ, Hall M, Brogan TV, Farris RW, Myers AL, Newland JG, Shah SS. Influenza coinfection and outcomes in children with complicated pneumonia. Arch Pediatr Adolesc Med 2011, 165:506-512. 10.1001/archpediatrics.2010.295, 21300649.
4. Finelli L, Fiore A, Dhara R, Brammer L, Shay DK, Kamimoto L, Fry A, Hageman J, Gorwitz R, Bresee J, Uyeki T. Influenza-associated pediatric mortality in the United States: increase of Staphylococcus aureus coinfection. Pediatrics 2008, 122:805-811. 10.1542/peds.2008-1336, 18829805.
5. Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008, 198:962-970. 10.1086/591708, 18710327.
6. Hunter CA, Kastelein R. Interleukin-27: balancing protective and pathological immunity. Immunity 2012, 37:960-969. 10.1016/j.immuni.2012.11.003, 23244718.
7. Khader SA, Gaffen SL, Kolls JK. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol 2009, 2:403-411. 10.1038/mi.2009.100, 19587639.
8. Diveu C, McGeachy MJ, Boniface K, Stumhofer JS, Sathe M, Joyce-Shaikh B, Chen Y, Tato CM, McClanahan TK, de Waal MR, et al. IL-27 blocks RORc expression to inhibit lineage commitment of Th17 cells. J Immunol 2009, 182:5748-5756. 10.4049/jimmunol.0801162, 19380822.
9. Saraiva M, O'Garra A. The regulation of IL-10 production by immune cells. Nat Rev Immunol 2010, 10:170-181. 10.1038/nri2711, 20154735.
10. Redford PS, Murray PJ, O'Garra A. The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 2011, 4:261-270. 10.1038/mi.2011.7, 21451501.
11. Arimori Y, Nakamura R, Yamada H, Shibata K, Maeda N, Kase T, Yoshikai Y. Type I interferon limits influenza virus-induced acute lung injury by regulation of excessive inflammation in mice. Antiviral Res 2013, 99:230-237. 10.1016/j.antiviral.2013.05.007, 23721943.
12. van der Sluijs KF, van Elden LJ, Nijhuis M, Schuurman R, Pater JM, Florquin S, Goldman M, Jansen HM, Lutter R, van der Poll T. IL-10 is an important mediator of the enhanced susceptibility to pneumococcal pneumonia after influenza infection. J Immunol 2004, 172:7603-7609. 10.4049/jimmunol.172.12.7603, 15187140.
13. Greenberger MJ, Strieter RM, Kunkel SL, Danforth JM, Goodman RE, Standiford TJ. Neutralization of IL-10 increases survival in a murine model of Klebsiella pneumonia. J Immunol 1995, 155:722-729. 7608550.
14. Steinhauser ML, Hogaboam CM, Kunkel SL, Lukacs NW, Strieter RM, Standiford TJ. IL-10 is a major mediator of sepsis-induced impairment in lung antibacterial host defense. J Immunol 1999, 162:392-399. 9886412.
15. Kudva A, Scheller EV, Robinson KM, Crowe CR, Choi SM, Slight SR, Khader SA, Dubin PJ, Enelow RI, Kolls JK, Alcorn JF. Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 2011, 186:1666-1674. 10.4049/jimmunol.1002194, 21178015.
16. Robinson KM, Choi SM, McHugh KJ, Mandalapu S, Scheller EV, Enelow RI, Chan YR, Kolls JK, Alcorn JF. Influenza A Exacerbates Staphylococcus aureus Pneumonia by Attenuating IL-1b Production in Mice. J Immunol 2013, 191:5153-9. 10.4049/jimmunol.1301237, 24089191.
17. Cox JH, Kljavin NM, Ramamoorthi N, Diehl L, Batten M, Ghilardi N. IL-27 promotes T cell-dependent colitis through multiple mechanisms. J Exp Med 2011, 208:115-123. 10.1084/jem.20100410, 21173106.
18. Braciale TJ. Immunologic recognition of influenza virus-infected cells. I. Generation of a virus-strain specific and a cross-reactive subpopulation of cytotoxic T cells in the response to type A influenza viruses of different subtypes. Cell Immunol 1977, 33:423-436. 10.1016/0008-8749(77)90170-8, 303150.
19. Robinson KM, McHugh KJ, Mandalapu S, Clay ME, Lee B, Scheller EV, Enelow RI, Chan YR, Kolls JK, Alcorn JF. Influenza A virus exacerbates Staphylococcus aureus pneumonia in mice by attenuating antimicrobial peptide production. J Infect Dis 2014, 209:865-875. 10.1093/infdis/jit527, 24072844.
20. Zhou L, Ivanov II, Spolski R, Min R, Shenderov K, Egawa T, Levy DE, Leonard WJ, Littman DR. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007, 8:967-974. 10.1038/ni1488, 17581537.
21. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, Dong C. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 2007, 282:9358-9363. 10.1074/jbc.C600321200, 17277312.
22. Crowe CR, Chen K, Pociask DA, Alcorn JF, Krivich C, Enelow RI, Ross TM, Witztum JL, Kolls JK. Critical role of IL-17RA in immunopathology of influenza infection. J Immunol 2009, 183:5301-5310. 10.4049/jimmunol.0900995, 19783685.
23. Liu FD, Kenngott EE, Schroter MF, Kuhl A, Jennrich S, Watzlawick R, Hoffmann U, Wolff T, Norley S, Scheffold A, et al. Timed Action of IL-27 Protects from Immunopathology while Preserving Defense in Influenza. PLoS Pathog 2014, 10:e1004110. 10.1371/journal.ppat.1004110, 24809349.
24. Sun J, Dodd H, Moser EK, Sharma R, Braciale TJ. CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nat Immunol 2011, 12:327-334. 10.1038/ni.1996, 21297642.
25. Perona-Wright G, Kohlmeier JE, Bassity E, Freitas TC, Mohrs K, Cookenham T, Situ H, Pearce EJ, Woodland DL, Mohrs M. Persistent loss of IL-27 responsiveness in CD8+ memory T cells abrogates IL-10 expression in a recall response. Proc Natl Acad Sci U S A 2012, 109:18535-18540. 10.1073/pnas.1119133109, 23091017.
26. Sun J, Madan R, Karp CL, Braciale TJ. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat Med 2009, 15:277-284. 10.1038/nm.1929, 19234462.
27. McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, Huston G, Tighe M, Hamada H, Sell S, Dutton RW, Swain SL. IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J Immunol 2009, 182:7353-7363. 10.4049/jimmunol.0900657, 19494257.
28. Mayer KD, Mohrs K, Reiley W, Wittmer S, Kohlmeier JE, Pearl JE, Cooper AM, Johnson LL, Woodland DL, Mohrs M. Cutting edge: T-bet and IL-27R are critical for in vivo IFN-gamma production by CD8 T cells during infection. J Immunol 2008, 180:693-697. 10.4049/jimmunol.180.2.693, 18178806.
29. Morandi F, Prigione I, Airoldi I. Human TCRgammadelta + T cells represent a novel target for IL-27 activity. Eur J Immunol 2012, 42:1547-1552. 10.1002/eji.201142241, 22678908.
30. Cao J, Wang D, Xu F, Gong Y, Wang H, Song Z, Li D, Zhang H, Zhang L, Xia Y, et al. Activation of IL-27 signalling promotes development of postinfluenza pneumococcal pneumonia. EMBO Mol Med 2014, 6:120-140. 10.1002/emmm.201302890, 24408967.
31. Shahangian A, Chow EK, Tian X, Kang JR, Ghaffari A, Liu SY, Belperio JA, Cheng G, Deng JC. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 2009, 119:1910-1920. 10.1172/JCI35412, 19487810.
32. Sun K, Metzger DW. Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med 2008, 14:558-564. 10.1038/nm1765, 18438414.