TRAIL+ monocytes and monocyte-related cells cause lung damage and thereby increase susceptibility to influenza-Streptococcus pneumoniae coinfection

EMBO Reports

Volumn 16, Issue 9, 2015, Pages 1203-1218

  Ellis, Gregory T ^a   Davidson, Sophia ^a   Crotta, Stefania ^a   Branzk, Nora ^a   Papayannopoulos, Venizelos ^a   Wack, Andreas ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

C C chemokine receptor type (CCR) 2; influenza; neutrophil; Streptococcus pneumoniae; TNF related apoptosis inducing ligand (TRAIL)

Indexed keywords

CHEMOKINE RECEPTOR CCR2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; CCR2 PROTEIN, MOUSE; CYTOKINE; TNFSF10 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INVASION; BACTERIAL LOAD; BACTERIAL OUTGROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; CELL DAMAGE; CELL INFILTRATION; CELL POPULATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DISEASE PREDISPOSITION; EPITHELIUM CELL; IMMUNE RESPONSE; INFECTION CONTROL; INFLAMMATORY CELL; INFLUENZA; LUNG INJURY; MIXED INFECTION; MONOCYTE; MONOCYTE DERIVED CELL; MORTALITY; MOUSE; MOUSE MODEL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIA; SURVIVAL; WILD TYPE; ANIMAL; C57BL MOUSE; COMPLICATION; DEFICIENCY; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS (H3N2); LUNG; METABOLISM; MICROBIOLOGY; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY; PATHOPHYSIOLOGY; PNEUMOCOCCAL INFECTION; STREPTOCOCCUS PNEUMONIAE; VIROLOGY;

ANIMALS; COINFECTION; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; LUNG; MICE; MICE, INBRED C57BL; MONOCYTES; NEUTROPHILS; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMOCOCCAL INFECTIONS; RECEPTORS, CCR2; STREPTOCOCCUS PNEUMONIAE; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84940797003     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201540473     Document Type: Article

References (55)

1. Palese P, (2004) Influenza: old and new threats. Nat Med 10: S82-S87
2. McCullers JA, (2014) The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol 12: 252-262
3. Robinson KM, Kolls JK, Alcorn JF, (2015) The immunology of influenza virus-associated bacterial pneumonia. Curr Opin Immunol 34C: 59-67
4. Kadioglu A, Weiser JN, Paton JC, Andrew PW, (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6: 288-301
5. Morens DM, Taubenberger JK, Fauci AS, (2008) Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 198: 962-970
6. Cilloniz C, Ewig S, Menendez R, Ferrer M, Polverino E, Reyes S, Gabarrus A, Marcos MA, Cordoba J, Mensa J, et al, (2012) Bacterial co-infection with H1N1 infection in patients admitted with community acquired pneumonia. J Infect 65: 223-230
7. Fleming-Dutra KE, Taylor T, Link-Gelles R, Garg S, Jhung MA, Finelli L, Jain S, Shay D, Chaves SS, Baumbach J, et al, (2013) Effect of the 2009 influenza A(H1N1) pandemic on invasive pneumococcal pneumonia. J Infect Dis 207: 1135-1143
8. Shrestha S, Foxman B, Weinberger DM, Steiner C, Viboud C, Rohani P, (2013) Identifying the interaction between influenza and pneumococcal pneumonia using incidence data. Sci Transl Med 5: 191ra84
9. Metzger DW, Sun K, (2013) Immune dysfunction and bacterial coinfections following influenza. J Immunol 191: 2047-2052
10. Goulding J, Godlee A, Vekaria S, Hilty M, Snelgrove R, Hussell T, (2011) Lowering the threshold of lung innate immune cell activation alters susceptibility to secondary bacterial superinfection. J Infect Dis 204: 1086-1094
11. Smith MW, Schmidt JE, Rehg JE, Orihuela CJ, McCullers JA, (2007) Induction of pro- and anti-inflammatory molecules in a mouse model of pneumococcal pneumonia after influenza. Comp Med 57: 82-89
12. Smith AM, Adler FR, Ribeiro RM, Gutenkunst RN, McAuley JL, McCullers JA, Perelson AS, (2013) Kinetics of coinfection with influenza A virus and Streptococcus pneumoniae. PLoS Pathog 9: e1003238
13. Sun K, Metzger DW, (2008) Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med 14: 558-564
14. Shahangian A, Chow EK, Tian X, Kang JR, Ghaffari A, Liu SY, Belperio JA, Cheng G, Deng JC, (2009) Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 119: 1910-1920
15. Li W, Moltedo B, Moran TM, (2012) Type I interferon induction during influenza virus infection increases susceptibility to secondary Streptococcus pneumoniae infection by negative regulation of gammadelta T cells. J Virol 86: 12304-12312
16. Cao J, Wang D, Xu F, Gong Y, Wang H, Song Z, Li D, Zhang H, Zhang L, Xia Y, et al, (2014) Activation of IL-27 signalling promotes development of postinfluenza pneumococcal pneumonia. EMBO Mol Med 6: 120-140
17. Ivanov S, Renneson J, Fontaine J, Barthelemy A, Paget C, Fernandez EM, Blanc F, De Trez C, Van Maele L, Dumoutier L, et al, (2013) Interleukin-22 reduces lung inflammation during influenza A virus infection and protects against secondary bacterial infection. J Virol 87: 6911-6924
18. Ghoneim HE, Thomas PG, McCullers JA, (2013) Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 191: 1250-1259
19. McAuley JL, Hornung F, Boyd KL, Smith AM, McKeon R, Bennink J, Yewdell JW, McCullers JA, (2007) Expression of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host Microbe 2: 240-249
20. Pittet LA, Hall-Stoodley L, Rutkowski MR, Harmsen AG, (2010) Influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am J Respir Cell Mol Biol 42: 450-460
21. Siegel SJ, Roche AM, Weiser JN, (2014) Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe 16: 55-67
22. Serbina NV, Pamer EG, (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7: 311-317
23. Davis KM, Nakamura S, Weiser JN, (2011) Nod2 sensing of lysozyme-digested peptidoglycan promotes macrophage recruitment and clearance of S. pneumoniae colonization in mice. J Clin Invest 121: 3666-3676
24. Winter C, Taut K, Srivastava M, Langer F, Mack M, Briles DE, Paton JC, Maus R, Welte T, Gunn MD, et al, (2007) Lung-specific overexpression of CC chemokine ligand (CCL) 2 enhances the host defense to Streptococcus pneumoniae infection in mice: role of the CCL2-CCR2 axis. J Immunol 178: 5828-5838
25. Herold S, Steinmueller M, von Wulffen W, Cakarova L, Pinto R, Pleschka S, Mack M, Kuziel WA, Corazza N, Brunner T, et al, (2008) Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 205: 3065-3077
26. Lin KL, Suzuki Y, Nakano H, Ramsburg E, Gunn MD, (2008) CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J Immunol 180: 2562-2572
27. Aldridge JR Jr, Moseley CE, Boltz DA, Negovetich NJ, Reynolds C, Franks J, Brown SA, Doherty PC, Webster RG, Thomas PG, (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci USA 106: 5306-5311
28. Schaefer U, Voloshanenko O, Willen D, Walczak H, (2007) TRAIL: a multifunctional cytokine. Front Biosci 12: 3813-3824
29. Steinwede K, Henken S, Bohling J, Maus R, Ueberberg B, Brumshagen C, Brincks EL, Griffith TS, Welte T, Maus UA, (2012) TNF-related apoptosis-inducing ligand (TRAIL) exerts therapeutic efficacy for the treatment of pneumococcal pneumonia in mice. J Exp Med 209: 1937-1952
30. Davidson S, Crotta S, McCabe TM, Wack A, (2014) Pathogenic potential of interferon alphabeta in acute influenza infection. Nat Commun 5: 3864
31. Brincks EL, Gurung P, Langlois RA, Hemann EA, Legge KL, Griffith TS, (2011) The magnitude of the T cell response to a clinically significant dose of influenza virus is regulated by TRAIL. J Immunol 187: 4581-4588
32. Nathan C, (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182
33. McNamee LA, Harmsen AG, (2006) Both influenza-induced neutrophil dysfunction and neutrophil-independent mechanisms contribute to increased susceptibility to a secondary Streptococcus pneumoniae infection. Infect Immun 74: 6707-6721
34. Engelich G, White M, Hartshorn KL, (2001) Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. J Leukoc Biol 69: 50-56
35. Damjanovic D, Lai R, Jeyanathan M, Hogaboam CM, Xing Z, (2013) Marked improvement of severe lung immunopathology by influenza-associated pneumococcal superinfection requires the control of both bacterial replication and host immune responses. Am J Pathol 183: 868-880
36. LeVine AM, Koeningsknecht V, Stark JM, (2001) Decreased pulmonary clearance of S. pneumoniae following influenza A infection in mice. J Virol Methods 94: 173-186
37. Takashima K, Tateda K, Matsumoto T, Iizawa Y, Nakao M, Yamaguchi K, (1997) Role of tumor necrosis factor alpha in pathogenesis of pneumococcal pneumonia in mice. Infect Immun 65: 257-260
38. Belisle SE, Tisoncik JR, Korth MJ, Carter VS, Proll SC, Swayne DE, Pantin-Jackwood M, Tumpey TM, Katze MG, (2010) Genomic profiling of tumor necrosis factor alpha (TNF-alpha) receptor and interleukin-1 receptor knockout mice reveals a link between TNF-alpha signaling and increased severity of 1918 pandemic influenza virus infection. J Virol 84: 12576-12588
39. Hussell T, Pennycook A, Openshaw PJ, (2001) Inhibition of tumor necrosis factor reduces the severity of virus-specific lung immunopathology. Eur J Immunol 31: 2566-2573
40. Damjanovic D, Divangahi M, Kugathasan K, Small CL, Zganiacz A, Brown EG, Hogaboam CM, Gauldie J, Xing Z, (2011) Negative regulation of lung inflammation and immunopathology by TNF-alpha during acute influenza infection. Am J Pathol 179: 2963-2976
41. McCullers JA, Rehg JE, (2002) Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J Infect Dis 186: 341-350
42. Langlet C, Tamoutounour S, Henri S, Luche H, Ardouin L, Gregoire C, Malissen B, Guilliams M, (2012) CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 188: 1751-1760
43. Misharin AV, Morales-Nebreda L, Mutlu GM, Budinger GR, Perlman H, (2013) Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am J Respir Cell Mol Biol 49: 503-510
44. Hogner K, Wolff T, Pleschka S, Plog S, Gruber AD, Kalinke U, Walmrath HD, Bodner J, Gattenlohner S, Lewe-Schlosser P, et al, (2013) Macrophage-expressed IFN-beta contributes to apoptotic alveolar epithelial cell injury in severe influenza virus pneumonia. PLoS Pathog 9: e1003188
45. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE, (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64-70
46. Jamieson AM, Pasman L, Yu S, Gamradt P, Homer RJ, Decker T, Medzhitov R, (2013) Role of tissue protection in lethal respiratory viral-bacterial coinfection. Science 340: 1230-1234
47. Brincks EL, Katewa A, Kucaba TA, Griffith TS, Legge KL, (2008) CD8 T cells utilize TRAIL to control influenza virus infection. J Immunol 181: 4918-4925
48. Lin KL, Sweeney S, Kang BD, Ramsburg E, Gunn MD, (2011) CCR2-antagonist prophylaxis reduces pulmonary immune pathology and markedly improves survival during influenza infection. J Immunol 186: 508-515
49. Subramaniam R, Barnes PF, Fletcher K, Boggaram V, Hillberry Z, Neuenschwander P, Shams H, (2014) Protecting against post-influenza bacterial pneumonia by increasing phagocyte recruitment and ROS production. J Infect Dis 209: 1827-1836
50. Robinson KM, McHugh KJ, Mandalapu S, Clay ME, Lee B, Scheller EV, Enelow RI, Chan YR, Kolls JK, Alcorn JF, (2014) Influenza A virus exacerbates Staphylococcus aureus pneumonia in mice by attenuating anti-microbial peptide production. J Infect Dis 209: 865-875
51. van Kessel KP, Bestebroer J, van Strijp JA, (2014) Neutrophil-mediated phagocytosis of Staphylococcus aureus. Front Immunol 5: 467
52. Lee LN, Dias P, Han D, Yoon S, Shea A, Zakharov V, Parham D, Sarawar SR, (2010) A mouse model of lethal synergism between influenza virus and Haemophilus influenzae. Am J Pathol 176: 800-811
53. Small CL, Shaler CR, McCormick S, Jeyanathan M, Damjanovic D, Brown EG, Arck P, Jordana M, Kaushic C, Ashkar AA, et al, (2010) Influenza infection leads to increased susceptibility to subsequent bacterial superinfection by impairing NK cell responses in the lung. J Immunol 184: 2048-2056
54. Ward CL, Dempsey MH, Ring CJ, Kempson RE, Zhang L, Gor D, Snowden BW, Tisdale M, (2004) Design and performance testing of quantitative real time PCR assays for influenza A and B viral load measurement. J Clin Virol 29: 179-188
55. Kash JC, Walters KA, Davis AS, Sandouk A, Schwartzman LM, Jagger BW, Chertow DS, Li Q, Kuestner RE, Ozinsky A, et al, (2011) Lethal synergism of 2009 pandemic H1N1 influenza virus and Streptococcus pneumoniae coinfection is associated with loss of murine lung repair responses. MBio 2: e00172-11