Viral-bacterial interactions in the respiratory tract

Journal of General Virology

Volumn 97, Issue 12, 2016, Pages 3089-3102

  Bellinghausen, Carla ^a   Rohde, Gernot G U ^a   Savelkoul, Paul H M ^a,b   Wouters, Emiel F M ^a   Stassen, Frank R M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Co infections; Microbial interaction; Respiratory pathogens

Indexed keywords

CYTOKINE; POLYPEPTIDE ANTIBIOTIC AGENT; VIRAL PROTEIN;

AIRWAY EPITHELIAL CELL; BACTERIAL INFECTION; BACTERIUM; CELL FUNCTION; DENDRITIC CELL; HOST CELL; HUMAN; INNATE IMMUNITY; LOWER RESPIRATORY TRACT INFECTION; LUNG ALVEOLUS MACROPHAGE; MICROBIOME; MIXED INFECTION; MUCOCILIARY CLEARANCE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYSTEM; REVIEW; VIRUS; VIRUS INFECTION; VIRUS PATHOGENESIS; ANIMAL; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; RESPIRATORY TRACT INFECTION; VIROLOGY;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; HUMANS; RESPIRATORY TRACT INFECTIONS; VIRUS DISEASES; VIRUSES;

EID: 85007153135     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000627     Document Type: Review

References (152)

1. Arnold, R., König, B., Werchau, H. & König, W. (2004). Respiratory syncytial virus deficient in soluble G protein induced an increased proinflammatory response in human lung epithelial cells. Virology 330, 384-397.
2. Arrevillaga, G., Gaona, J., Sanchez, C., Rosales, V. & Gómez, B. (2012). Respiratory syncytial virus persistence in macrophages downregulates intercellular adhesion molecule-1 expression and reduces adhesion of non-typeable Haemophilus influenzae. Intervirology 55, 442-450.
3. Avadhanula, V., Rodriguez, C. A., Devincenzo, J. P., Wang, Y., Webby, R. J., Ulett, G. C. & Adderson, E. E. (2006). Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral speciesand cell type-dependent manner. J Virol 80, 1629-1636.
4. Avadhanula, V., Wang, Y., Portner, A. & Adderson, E. (2007). Nontypeable Haemophilus influenzae and Streptococcus pneumoniae bind respiratory syncytial virus glycoprotein. J Med Microbiol 56, 1133-1137.
5. Bafadhel, M., McKenna, S., Terry, S., Mistry, V., Reid, C., Haldar, P., McCormick, M., Haldar, K., Kebadze, T. & other authors (2011). Acute exacerbations of chronic obstructive pulmonary disease: identification of biologic clusters and their biomarkers. Am J Respir Crit Care Med 184, 662-671.
6. Beiter, K., Wartha, F., Albiger, B., Normark, S., Zychlinsky, A. & Henriques-Normark, B. (2006). An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16, 401-407.
7. Bellinghausen, C., Gulraiz, F., Heinzmann, A. C., Dentener, M. A., Savelkoul, P. H., Wouters, E. F., Rohde, G. G. & Stassen, F. R. (2016). Exposure to common respiratory bacteria alters the airway epithelial response to subsequent viral infection. Respir Res 17, 68.
8. Bello, S., Minchole, E., Fandos, S., Lasierra, A. B., Ruiz, M. A., Simon, A. L., Panadero, C., Lapresta, C., Menendez, R. & Torres, A. (2014). Inflammatory response in mixed viral-bacterial communityacquired pneumonia. BMC Pulm Med 14, 123.
9. Berends, E. T., Horswill, A. R., Haste, N. M., Monestier, M., Nizet, V. & von Köckritz-Blickwede, M. (2010). Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2, 576-586.
10. Biesbroek, G., Wang, X., Keijser, B. J., Eijkemans, R. M., Trzcinski, K., Rots, N. Y., Veenhoven, R. H., Sanders, E. A. & Bogaert, D. (2014). Seven-valent pneumococcal conjugate vaccine and nasopharyngeal microbiota in healthy children. Emerg Infect Dis 20, 201-210.
11. Blevins, L. K., Wren, J. T., Holbrook, B. C., Hayward, S. L., Swords, W. E., Parks, G. D. & Alexander-Miller, M. A. (2014). Coinfection with Streptococcus pneumoniae negatively modulates the size and composition of the ongoing influenza-specific CD8+ T cell response. J Immunol 193, 5076-5087.
12. Brown, T. I., Collie, D. S., Shaw, D. J., Rzechorzek, N. M. & Sallenave, J. M. (2014). Sheep lung segmental delivery strategy demonstrates adenovirus priming of local lung responses to bacterial LPS and the role of elafin as a response modulator. PLoS One 9, e107590.
13. Cabello, H., Torres, A., Celis, R., El-Ebiary, M., Puig de la Bellacasa, J., Xaubet, A., Gonzalez, J., Agustí, C. & Soler, N. (1997). Bacterial colonization of distal airways in healthy subjects and chronic lung disease: a bronchoscopic study. Eur Respir J 10, 1137-1144.
14. Casalegno, J. S., Ottmann, M., Duchamp, M. B., Escuret, V., Billaud, G., Frobert, E., Morfin, F. & Lina, B. (2010). Rhinoviruses delayed the circulation of the pandemic influenza A (H1N1) 2009 virus in France. Clin Microbiol Infect 16, 326-329.
15. Charlson, E. S., Bittinger, K., Haas, A. R., Fitzgerald, A. S., Frank, I., Yadav, A., Bushman, F. D. & Collman, R. G. (2011). Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 184, 957-963.
16. Chattoraj, S. S., Ganesan, S., Faris, A., Comstock, A., Lee, W. M. & Sajjan, U. S. (2011a). Pseudomonas aeruginosa suppresses interferon response to rhinovirus infection in cystic fibrosis but not in normal bronchial epithelial cells. Infect Immun 79, 4131-4145.
17. Chattoraj, S. S., Ganesan, S., Jones, A. M., Helm, J. M., Comstock, A. T., Bright-Thomas, R., LiPuma, J. J., Hershenson, M. B. & Sajjan, U. S. (2011b). Rhinovirus infection liberates planktonic bacteria from biofilm and increases chemokine responses in cystic fibrosis airway epithelial cells. Thorax 66, 333-339.
18. Chilvers, M. A., McKean, M., Rutman, A., Myint, B. S., Silverman, M. & O’Callaghan, C. (2001). The effects of coronavirus on human nasal ciliated respiratory epithelium. Eur Respir J 18, 965-970.
19. Chiu, C. & Openshaw, P. J. (2015). Antiviral B cell and T cell immunity in the lungs. Nat Immunol 16, 18-26.
20. Colamussi, M. L., White, M. R., Crouch, E. & Hartshorn, K. L. (1999). Influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood 93, 2395-2403.
21. Cortjens, B., de Boer, O. J., de Jong, R., Antonis, A. F., Sabogal Piñeros, Y. S., Lutter, R., van Woensel, J. B. & Bem, R. A. (2016). Neutrophil extracellular traps cause airway obstruction during respiratory syncytial virus disease. J Pathol 238, 401-411.
22. de Graaff, P. M., de Jong, E. C., van Capel, T. M., van Dijk, M. E., Roholl, P. J., Boes, J., Luytjes, W., Kimpen, J. L. & van Bleek, G. M. (2005). Respiratory syncytial virus infection of monocyte-derived dendritic cells decreases their capacity to activate CD4 T cells. J Immunol 175, 5904-5911.
23. de Steenhuijsen Piters, W. A., Heinonen, S., Hasrat, R., Bunsow, E., Smith, B., Suarez-Arrabal, M. C., Chaussabel, D., Cohen, D. M., Sanders, E. A. & other authors (2016). Nasopharyngeal microbiota, host transcriptome, and disease severity in children with respiratory syncytial virus infection. Am J Respir Crit Care Med 194, 1104-1115.
24. de Vos, A. F., Pater, J. M., van den Pangaart, P. S., de Kruif, M. D., van’t Veer, C. & van der Poll, T. (2009). In vivo lipopolysaccharide exposure of human blood leukocytes induces cross-tolerance to multiple TLR ligands. J Immunol 183, 533-542.
25. Didierlaurent, A., Goulding, J., Patel, S., Snelgrove, R., Low, L., Bebien, M., Lawrence, T., van Rijt, L. S., Lambrecht, B. N. & other authors (2008). Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med 205, 323-329.
26. Drake, M. G., Evans, S. E., Dickey, B. F., Fryer, A. D. & Jacoby, D. B. (2013). Toll-like receptor-2/6 and Toll-like receptor-9 agonists suppress viral replication but not airway hyperreactivity in guinea pigs. Am J Respir Cell Mol Biol 48, 790-796.
27. Elhaik-Goldman, S., Kafka, D., Yossef, R., Hadad, U., Elkabets, M., Vallon-Eberhard, A., Hulihel, L., Jung, S., Ghadially, H. & other authors (2011). The natural cytotoxicity receptor 1 contribution to early clearance of Streptococcus pneumoniae and to natural killer-macrophage cross talk. PLoS One 6, e23472.
28. Engelich, G., White, M. & Hartshorn, K. L. (2001). Neutrophil survival is markedly reduced by incubation with influenza virus and Streptococcus pneumoniae: role of respiratory burst. J Leukoc Biol 69, 50-56.
29. Erb-Downward, J. R., Thompson, D. L., Han, M. K., Freeman, C. M., McCloskey, L., Schmidt, L. A., Young, V. B., Toews, G. B., Curtis, J. L. & other authors (2011). Analysis of the lung microbiome in the "healthy" smoker and in COPD. PLoS One 6, e16384.
30. Faris, A. N., Ganesan, S., Chattoraj, A., Chattoraj, S. S., Comstock, A. T., Unger, B. L., Hershenson, M. B. & Sajjan, U. S. (2016). Rhinovirus delays cell repolarization in a model of injured/regenerating human airway epithelium. Am J Respir Cell Mol Biol 55, 487-499.
31. Fernandez-Sesma, A., Marukian, S., Ebersole, B. J., Kaminski, D., Park, M. S., Yuen, T., Sealfon, S. C., García-Sastre, A. & Moran, T. M. (2006). Influenza virus evades innate and adaptive immunity via the NS1 protein. J Virol 80, 6295-6304.
32. Flórido, M., Grima, M. A., Gillis, C. M., Xia, Y., Turner, S. J., Triccas, J. A., Stambas, J. & Britton, W. J. (2013). Influenza A virus infection impairs mycobacteria-specific T cell responses and mycobacterial clearance in the lung during pulmonary coinfection. J Immunol 191, 302-311.
33. Franke-Ullmann, G., Pförtner, C., Walter, P., Steinmüller, C., Lohmann-Matthes, M. L., Kobzik, L. & Freihorst, J. (1995). Alteration of pulmonary macrophage function by respiratory syncytial virus infection in vitro. J Immunol 154, 268-280.
34. Garcia-Nuñez, M., Millares, L., Pomares, X., Ferrari, R., PerezBrocal, V., Gallego, M., Espasa, M., Moya, A. & Monsó, E. (2014). Severity-related changes of bronchial microbiome in chronic obstructive pulmonary disease. J Clin Microbiol 52, 4217-4223.
35. Gern, J. E., Dick, E. C., Lee, W. M., Murray, S., Meyer, K., Handzel, Z. T. & Busse, W. W. (1996). Rhinovirus enters but does not replicate inside monocytes and airway macrophages. J Immunol 156, 621-627.
36. Ghoneim, H. E., Thomas, P. G. & McCullers, J. A. (2013). Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 191, 1250-1259.
37. Golda, A., Malek, N., Dudek, B., Zeglen, S., Wojarski, J., Ochman, M., Kucewicz, E., Zembala, M., Potempa, J. & Pyrc, K. (2011). Infection with human coronavirus NL63 enhances Streptococcal adherence to epithelial cells. J Gen Virol 92, 1358-1368.
38. Guilliams, M., Lambrecht, B. N. & Hammad, H. (2013). Division of labor between lung dendritic cells and macrophages in the defense against pulmonary infections. Mucosal Immunol 6, 464-473.
39. Gulraiz, F., Bellinghausen, C., Bruggeman, C. A. & Stassen, F. R. (2015). Haemophilus influenzae increases the susceptibility and inflammatory response of airway epithelial cells to viral infections. FASEB J 29, 849-858.
40. Hafez, M. M., Abdel-Wahab, K. S. & El-Fouhil, D. F. (2010). Augmented adherence and internalization of group A Streptococcus pyogenes to influenza A virus infected MDCK cells. J Basic Microbiol 50, S46-57.
41. Hakansson, A., Kidd, A., Wadell, G., Sabharwal, H. & Svanborg, C. (1994). Adenovirus infection enhances in vitro adherence of Streptococcus pneumoniae. Infect Immun 62, 2707-2714.
42. Hament, J. M., Aerts, P. C., Fleer, A., Van Dijk, H., Harmsen, T., Kimpen, J. L. & Wolfs, T. F. (2004). Enhanced adherence of Streptococcus pneumoniae to human epithelial cells infected with respiratory syncytial virus. Pediatr Res 55, 972-978.
43. Hament, J. M., Aerts, P. C., Fleer, A., van Dijk, H., Harmsen, T., Kimpen, J. L. & Wolfs, T. F. (2005). Direct binding of respiratory syncytial virus to pneumococci: a phenomenon that enhances both pneumococcal adherence to human epithelial cells and pneumococcal invasiveness in a murine model. Pediatr Res 58, 1198-1203.
44. Hasenberg, M., Stegemann-Koniszewski, S. & Gunzer, M. (2013). Cellular immune reactions in the lung. Immunol Rev 251, 189-214.
45. Hector, A., Kirn, T., Ralhan, A., Graepler-Mainka, U., Berenbrinker, S., Riethmueller, J., Hogardt, M., Wagner, M., Pfleger, A. & other authors (2016). Microbial colonization and lung function in adolescents with cystic fibrosis. J Cyst Fibros 15, 340-349.
46. Heinrich, A., Haarmann, H., Zahradnik, S., Frenzel, K., Schreiber, F., Klassert, T. E., Heyl, K. A., Endres, A. S., Schmidtke, M. & other authors (2016). Moraxella catarrhalis decreases antiviral innate immune responses by down-regulation of TLR3 via inhibition of p53 in human bronchial epithelial cells. FASEB J 30. 10.1096/fj.201500172R.
47. Hendricks, M. R., Lashua, L. P., Fischer, D. K., Flitter, B. A., Eichinger, K. M., Durbin, J. E., Sarkar, S. N., Coyne, C. B., Empey, K. M. & Bomberger, J. M. (2016). Respiratory syncytial virus infection enhances Pseudomonas aeruginosa biofilm growth through dysregulation of nutritional immunity. Proc Natl Acad Sci U S A 113, 1642-1647.
48. Herold, S., Steinmueller, M., von Wulffen, W., Cakarova, L., Pinto, R., Pleschka, S., Mack, M., Kuziel, W. A., Corazza, N. & other authors (2008). Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J Exp Med 205, 3065-3077.
49. Hesker, P. R. & Krupnick, A. S. (2013). The role of natural killer cells in pulmonary immunosurveillance. Front Biosci 5, 575-587.
50. Hinojosa, E., Boyd, A. R. & Orihuela, C. J. (2009). Age-associated inflammation and Toll-like receptor dysfunction prime the lungs for pneumococcal pneumonia. J Infect Dis 200, 546-554.
51. Hinshaw, V. S., Olsen, C. W., Dybdahl-Sissoko, N. & Evans, D. (1994). Apoptosis: a mechanism of cell killing by influenza A and B viruses. J Virol 68, 3667-3673.
52. Ichinohe, T., Pang, I. K., Kumamoto, Y., Peaper, D. R., Ho, J. H., Murray, T. S. & Iwasaki, A. (2011). Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 108, 5354-5359.
53. Ishizuka, S., Yamaya, M., Suzuki, T., Takahashi, H., Ida, S., Sasaki, T., Inoue, D., Sekizawa, K., Nishimura, H. & Sasaki, H. (2003). Effects of rhinovirus infection on the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells. J Infect Dis 188, 1928-1939.
54. Iverson, A. R., Boyd, K. L., McAuley, J. L., Plano, L. R., Hart, M. E. & McCullers, J. A. (2011). Influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis 203, 880-888.
55. Jakab, G. J., Warr, G. A. & Sannes, P. L. (1980). Alveolar macrophage ingestion and phagosome-lysosome fusion defect associated with virus pneumonia. Infect Immun 27, 960-968.
56. Jamieson, A. M., Yu, S., Annicelli, C. H. & Medzhitov, R. (2010). Influenza virus-induced glucocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe 7, 103-114.
57. Jiang, Z., Nagata, N., Molina, E., Bakaletz, L. O., Hawkins, H. & Patel, J. A. (1999). Fimbria-mediated enhanced attachment of nontypeable Haemophilus influenzae to respiratory syncytial virus-infected respiratory epithelial cells. Infect Immun 67, 187-192.
58. Jounai, K., Sugimura, T., Ohshio, K. & Fujiwara, D. (2015). Oral administration of Lactococcus lactis subsp. lactis JCM5805 enhances lung immune response resulting in protection from murine Parainfluenza virus infection. PLoS One 10, e0119055.
59. Kamada, N., Seo, S. U., Chen, G. Y. & Núñez, G. (2013). Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 13, 321-335.
60. Kaplan, M. J. & Radic, M. (2012). Neutrophil extracellular traps: doubleedged swords of innate immunity. J Immunol 189, 2689-2695.
61. Kash, J. C., Walters, K. A., Davis, A. S., Sandouk, A., Schwartzman, L. M., Jagger, B. W., Chertow, D. S., Li, Q., Kuestner, R. E. & other authors (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
62. Kawai, T. & Akira, S. (2011). Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650
63. Kilani, M. M., Mohammed, K. A., Nasreen, N., Hardwick, J. A., Kaplan, M. H., Tepper, R. S. & Antony, V. B. (2004). Respiratory syncytial virus causes increased bronchial epithelial permeability. Chest 126, 186-191
64. Kudva, A., Scheller, E. V., Robinson, K. M., Crowe, C. R., Choi, S. M., Slight, S. R., Khader, S. A., Dubin, P. J., Enelow, R. I. & other authors (2011). Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J Immunol 186, 1666-1674.
65. Laurie, K. L., Guarnaccia, T. A., Carolan, L. A., Yan, A. W., Aban, M., Petrie, S., Cao, P., Heffernan, J. M., McVernon, J. & other authors (2015). Interval between infections and viral hierarchy are determinants of viral interference following influenza virus infection in a ferret model. J Infect Dis 212, 1701-1710.
66. Lecaille, F., Lalmanach, G. & Andrault, P. M. (2016). Antimicrobial proteins and peptides in human lung diseases: a friend and foe partnership with host proteases. Biochimie 122, 151-168.
67. Lee, B., Robinson, K. M., McHugh, K. J., Scheller, E. V., Mandalapu, S., Chen, C., Di, Y. P., Clay, M. E., Enelow, R. I. & other authors (2015). Influenza-induced type I interferon enhances susceptibility to gram-negative and gram-positive bacterial pneumonia in mice. Am J Physiol Lung Cell Mol Physiol 309, L158-167.
68. Lee, L. N., Dias, P., Han, D., Yoon, S., Shea, A., Zakharov, V., Parham, D. & Sarawar, S. R. (2010). A mouse model of lethal synergism between influenza virus and Haemophilus influenzae. Am J Pathol 176, 800-811.
69. LeMessurier, K. S., Hacker, H., Chi, L., Tuomanen, E. & Redecke, V. (2013). Type I interferon protects against pneumococcal invasive disease by inhibiting bacterial transmigration across the lung. PLoS Pathog 9, e1003727.
70. LeVine, A. M., Koeningsknecht, V. & Stark, J. M. (2001). Decreased pulmonary clearance of S. pneumoniae following influenza A infection in mice. J Virol Methods 94, 173-186.
71. Li, N., Ren, A., Wang, X., Fan, X., Zhao, Y., Gao, G. F., Cleary, P. & Wang, B. (2015). Influenza viral neuraminidase primes bacterial coinfection through TGF-b-mediated expression of host cell receptors. Proc Natl Acad Sci U S A 112, 238-243.
72. Li, W., Moltedo, B. & Moran, T. M. (2012). Type I interferon induction during influenza virus infection increases susceptibility to secondary Streptococcus pneumoniae infection by negative regulation of gd T cells. J Virol 86, 12304-12312.
73. Liu, Q., Zhang, Z., Zheng, Z., Zheng, C., Liu, Y., Hu, Q., Ke, X. & Wang, H. (2016). Human bocavirus NS1 and NS1-70 proteins inhibit TNF-a-mediated activation of NF-kB by targeting p65. Sci Rep 6, 28481
74. Ma, Y., Li, X. & Kuang, E. (2016). Viral evasion of natural killer cell activation. Viruses 8, 95.
75. MacDonald, M., Korman, T., King, P., Hamza, K. & Bardin, P. (2013). Exacerbation phenotyping in chronic obstructive pulmonary disease. Respirology 18, 1280-1281.
76. Mallia, P., Footitt, J., Sotero, R., Jepson, A., Contoli, M., Trujillo-Torralbo, M. B., Kebadze, T., Aniscenko, J., Oleszkiewicz, G. & other authors (2012). Rhinovirus infection induces degradation of antimicrobial peptides and secondary bacterial infection in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 186, 1117-1124.
77. Mandelboim, O., Lieberman, N., Lev, M., Paul, L., Arnon, T. I., Bushkin, Y., Davis, D. M., Strominger, J. L., Yewdell, J. W. & Porgador, A. (2001). Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409, 1055-1060.
78. Marks, L. R., Davidson, B. A., Knight, P. R. & Hakansson, A. P. (2013). Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease. MBio 4, e00438-13.
79. Marsland, B. J. & Gollwitzer, E. S. (2014). Host-microorganism interactions in lung diseases. Nat Rev Immunol 14, 827-835.
80. McAuley, J. L., Hornung, F., Boyd, K. L., Smith, A. M., McKeon, R., Bennink, J., Yewdell, J. W. & McCullers, J. A. (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.
81. McCullers, J. A. (2014). The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol 12, 252-262.
82. McCullers, J. A. & Rehg, J. E. (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.
83. McCullers, J. A., Iverson, A. R., McKeon, R. & Murray, P. J. (2008). The platelet activating factor receptor is not required for exacerbation of bacterial pneumonia following influenza. Scand J Infect Dis 40, 11-17.
84. McGillivary, G., Mason, K. M., Jurcisek, J. A., Peeples, M. E. & Bakaletz, L. O. (2009). Respiratory syncytial virus-induced dysregulation of expression of a mucosal beta-defensin augments colonization of the upper airway by non-typeable Haemophilus influenzae. Cell Microbiol 11, 1399-1408.
85. McNamee, L. A. & Harmsen, A. G. (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.
86. Mohan, A. & Sethi, S. (2015). What is bacterial colonisation in COPD? Controversies In COPD. Lausanne, Switzerland: European Respiratory Society.
87. Molyneaux, P. L., Mallia, P., Cox, M. J., Footitt, J., Willis-Owen, S. A., Homola, D., Trujillo-Torralbo, M. B., Elkin, S., Kon, O. M. & other authors (2013). Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 188, 1224-1231.
88. Monsó, E., Rosell, A., Bonet, G., Manterola, J., Cardona, P. J., Ruiz, J. & Morera, J. (1999). Risk factors for lower airway bacterial colonization in chronic bronchitis. Eur Respir J 13, 338-342.
89. Morens, D. M., Taubenberger, J. K. & Fauci, A. S. (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.
90. Nahid, M. A., Satoh, M. & Chan, E. K. (2011). Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signaling. J Immunol 186, 1723-1734.
91. Nakamura, S., Davis, K. M. & Weiser, J. N. (2011). Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J Clin Invest 121, 3657-3665.
92. Narasaraju, T., Yang, E., Samy, R. P., Ng, H. H., Poh, W. P., Liew, A. A., Phoon, M. C., van Rooijen, N. & Chow, V. T. (2011). Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am J Pathol 179, 199-210.
93. Narayana Moorthy, A., Narasaraju, T., Rai, P., Perumalsamy, R., Tan, K. B., Wang, S., Engelward, B. & Chow, V. T. (2013). In vivo and in vitro studies on the roles of neutrophil extracellular traps during secondary pneumococcal pneumonia after primary pulmonary influenza infection. Front Immunol 4, 56.
94. Neagos, J., Standiford, T. J., Newstead, M. W., Zeng, X., Huang, S. K. & Ballinger, M. N. (2015). Epigenetic regulation of tolerance to Toll-like receptor ligands in alveolar epithelial cells. Am J Respir Cell Mol Biol 53, 872-881.
95. Netea, M. G., Simon, A., van de Veerdonk, F., Kullberg, B. J., Van der Meer, J. W. & Joosten, L. A. (2010). IL-1beta processing in host defense: beyond the inflammasomes. PLoS Pathog 6, e1000661.
96. Nie, S., Lin, S. J., Kim, S. K., Welsh, R. M. & Selin, L. K. (2010). Pathological features of heterologous immunity are regulated by the private specificities of the immune repertoire. Am J Pathol 176, 2107-2112.
97. Norton, E. B., Clements, J. D., Voss, T. G. & Cardenas-Freytag, L. (2010). Prophylactic administration of bacterially derived immunomodulators improves the outcome of influenza virus infection in a murine model. J Virol 84, 2983-2995.
98. Nugent, K. M. & Pesanti, E. L. (1979). Effect of influenza infection on the phagocytic and bactericidal activities of pulmonary macrophages. Infect Immun 26, 651-657.
99. Nunn, P., Williams, B., Floyd, K., Dye, C., Elzinga, G. & Raviglione, M. (2005). Tuberculosis control in the era of HIV. Nat Rev Immunol 5, 819-826.
100. Okamoto, S., Kawabata, S., Nakagawa, I., Okuno, Y., Goto, T., Sano, K. & Hamada, S. (2003). Influenza A virus-infected hosts boost an invasive type of Streptococcus pyogenes infection in mice. J Virol 77, 4104-4112.
101. Oliver, B. G., Lim, S., Wark, P., Laza-Stanca, V., King, N., Black, J. L., Burgess, J. K., Roth, M. & Johnston, S. L. (2008). Rhinovirus exposure impairs immune responses to bacterial products in human alveolar macrophages. Thorax 63, 519-525.
102. Papi, A., Bellettato, C. M., Braccioni, F., Romagnoli, M., Casolari, P., Caramori, G., Fabbri, L. M. & Johnston, S. L. (2006). Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med 173, 1114-1121.
103. Passariello, C., Schippa, S., Conti, C., Russo, P., Poggiali, F., Garaci, E. & Palamara, A. T. (2006). Rhinoviruses promote internalisation of Staphylococcus aureus into non-fully permissive cultured pneumocytes. Microbes Infect 8, 758-766.
104. Pettigrew, M. M., Marks, L. R., Kong, Y., Gent, J. F., RocheHakansson, H. & Hakansson, A. P. (2014). Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection. Infect Immun 82, 4607-4619.
105. Polack, F. P., Irusta, P. M., Hoffman, S. J., Schiatti, M. P., Melendi, G. A., Delgado, M. F., Laham, F. R., Thumar, B., Hendry, R. M. & other authors (2005). The cysteine-rich region of respiratory syncytial virus attachment protein inhibits innate immunity elicited by the virus and endotoxin. Proc Natl Acad Sci U S A 102, 8996-9001.
106. Rameix-Welti, M. A., Zarantonelli, M. L., Giorgini, D., Ruckly, C., Marasescu, M., van der Werf, S., Alonso, J. M., Naffakh, N. & Taha, M. K. (2009). Influenza A virus neuraminidase enhances meningococcal adhesion to epithelial cells through interaction with sialic acid-containing meningococcal capsules. Infect Immun 77, 3588-3595.
107. Ratner, A. J., Lysenko, E. S., Paul, M. N. & Weiser, J. N. (2005). Synergistic proinflammatory responses induced by polymicrobial colonization of epithelial surfaces. Proc Natl Acad Sci U S A 102, 3429-3434.
108. Raza, M. W., Blackwell, C. C., Elton, R. A. & Weir, D. M. (2000). Bactericidal activity of a monocytic cell line (THP-1) against common respiratory tract bacterial pathogens is depressed after infection with respiratory syncytial virus. J Med Microbiol 49, 227-233.
109. Raza, M. W., Ogilvie, M. M., Blackwell, C. C., Stewart, J., Elton, R. A. & Weir, D. M. (1993). Effect of respiratory syncytial virus infection on binding of Neisseria meningitidis and Haemophilus influenzae type b to a human epithelial cell line (HEp-2). Epidemiol Infect 110, 339-347.
110. Robinson, K. M., McHugh, K. J., Mandalapu, S., Clay, M. E., Lee, B., Scheller, E. V., Enelow, R. I., Chan, Y. R., Kolls, J. K. & Alcorn, J. F. (2014). Influenza A virus exacerbates Staphylococcus aureus pneumonia in mice by attenuating antimicrobial peptide production. J Infect Dis 209, 865-875.
111. Sajjan, U. S., Jia, Y., Newcomb, D. C., Bentley, J. K., Lukacs, N. W., LiPuma, J. J. & Hershenson, M. B. (2006). H. influenzae potentiates airway epithelial cell responses to rhinovirus by increasing ICAM-1 and TLR3 expression. FASEB J 20, 2121-2123.
112. Sajjan, U., Wang, Q., Zhao, Y., Gruenert, D. C. & Hershenson, M. B. (2008). Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 178, 1271-1281.
113. Sanford, B. A. & Ramsay, M. A. (1987). Bacterial adherence to the upper respiratory tract of ferrets infected with influenza A virus. Proc Soc Exp Biol Med 185, 120-128.
114. Sanford, B. A., Davison, V. E. & Ramsay, M. A. (1982). Fibrinogen-mediated adherence of group A Streptococcus to influenza A virus-infected cell cultures. Infect Immun 38, 513-520.
115. Scheer, S., Krempl, C., Kallfass, C., Frey, S., Jakob, T., Mouahid, G., Mone, H., Schmitt-Graff, A., Staeheli, P. & Lamers, M. C. (2014). S. Mansoni bolsters anti-viral immunity in the murine respiratory tract. PLoS One 9, e112469.
116. Schultz-Cherry, S., Dybdahl-Sissoko, N., Neumann, G., Kawaoka, Y. & Hinshaw, V. S. (2001). Influenza virus ns1 protein induces apoptosis in cultured cells. J Virol 75, 7875-7881.
117. Shahangian, A., Chow, E. K., Tian, X., Kang, J. R., Ghaffari, A., Liu, S. Y., Belperio, J. A., Cheng, G. & Deng, J. C. (2009). Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest 119, 1910-1920.
118. Shukla, S. D., Muller, H. K., Latham, R., Sohal, S. S. & Walters, E. H. (2016). Platelet-activating factor receptor (PAFr) is upregulated in small airways and alveoli of smokers and COPD patients. Respirology 21, 504-510.
119. Siegel, S. J., Roche, A. M. & Weiser, J. N. (2014). Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe 16, 55-67.
120. Small, C. L., Shaler, C. R., McCormick, S., Jeyanathan, M., Damjanovic, D., Brown, E. G., Arck, P., Jordana, M., Kaushic, C. & other authors (2010). Influenza infection leads to increased susceptibility to subsequent bacterial superinfection by impairing NK cell responses in the lung. J Immunol 184, 2048-2056.
121. Smith, C. M., Kulkarni, H., Radhakrishnan, P., Rutman, A., Bankart, M. J., Williams, G., Hirst, R. A., Easton, A. J., Andrew, P. W. & O’Callaghan, C. (2014a). Ciliary dyskinesia is an early feature of respiratory syncytial virus infection. Eur Respir J 43, 485-496.
122. Smith, C. M., Sandrini, S., Datta, S., Freestone, P., Shafeeq, S., Radhakrishnan, P., Williams, G., Glenn, S. M., Kuipers, O. P. & other authors (2014b). Respiratory syncytial virus increases the virulence of Streptococcus pneumoniae by binding to penicillin binding protein 1a. A new paradigm in respiratory infection. Am J Respir Crit Care Med 190, 196-207
123. Spelmink, L., Sender, V., Hentrich, K., Kuri, T., Plant, L. & Henriques-Normark, B. (2016). Toll-like receptor 3/TRIF-dependent IL-12p70 secretion mediated by Streptococcus pneumoniae RNA and its priming by influenza A virus coinfection in human dendritic cells. MBio 7, e00168-16.
124. Stark, J. M., Stark, M. A., Colasurdo, G. N. & LeVine, A. M. (2006). Decreased bacterial clearance from the lungs of mice following primary respiratory syncytial virus infection. J Med Virol 78, 829-838.
125. Stasakova, J., Ferko, B., Kittel, C., Sereinig, S., Romanova, J., Katinger, H. & Egorov, A. (2005). Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1beta and 18. J Gen Virol 86, 185-195.
126. Suarez-Arrabal, M. C., Mella, C., Lopez, S. M., Brown, N. V., Hall, M. W., Hammond, S., Shiels, W., Groner, J., Marcon, M. & other authors (2015). Nasopharyngeal bacterial burden and antibiotics: influence on inflammatory markers and disease severity in infants with respiratory syncytial virus bronchiolitis. J Infect 71, 458-469.
127. Sun, K. & Metzger, D. W. (2008). Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med 14, 558-564.
128. Suri, R., Mallia, P., Martin, J. E., Footitt, J., Zhu, J., Trujillo-Torralbo, M. B., Johnston, S. L. & Grigg, J. (2014). Bronchial plateletactivating factor receptor in chronic obstructive pulmonary disease. Respir Med 108, 898-904.
129. Tarabichi, Y., Li, K., Hu, S., Nguyen, C., Wang, X., Elashoff, D., Saira, K., Frank, B., Bihan, M. & other authors (2015). The administration of intranasal live attenuated influenza vaccine induces changes in the nasal microbiota and nasal epithelium gene expression profiles. Microbiome 3, 74.
130. Tristram, D. A., Hicks, W. Jr. & Hard, R. (1998). Respiratory syncytial virus and human bronchial epithelium. Arch Otolaryngol Head Neck Surg 124, 777-783.
131. Tuvim, M. J., Evans, S. E., Clement, C. G., Dickey, B. F. & Gilbert, B. E. (2009). Augmented lung inflammation protects against influenza A pneumonia. PLoS One 4, e4176.
132. Unger, B. L., Faris, A. N., Ganesan, S., Comstock, A. T., Hershenson, M. B. & Sajjan, U. S. (2012). Rhinovirus attenuates nontypeable Hemophilus influenzae-stimulated IL-8 responses via TLR2-dependent degradation of IRAK-1. PLoS Pathog 8, e1002969.
133. van der Sluijs, K. F., van Elden, L. J., Nijhuis, M., Schuurman, R., Pater, J. M., Florquin, S., Goldman, M., Jansen, H. M., Lutter, R. & van der Poll, T. (2004). IL-10 is an important mediator of the enhanced susceptibility to pneumococcal pneumonia after influenza infection. J Immunol 172, 7603-7609.
134. van der Sluijs, K. F., van Elden, L. J., Nijhuis, M., Schuurman, R., Florquin, S., Shimizu, T., Ishii, S., Jansen, H. M., Lutter, R. & van der Poll, T. (2006). Involvement of the platelet-activating factor receptor in host defense against Streptococcus pneumoniae during postinfluenza pneumonia. Am J Physiol Lung Cell Mol Physiol 290, L194-199.
135. Van Ewijk, B. E., Wolfs, T. F., Aerts, P. C., Van Kessel, K. P., Fleer, A., Kimpen, J. L. & Van der Ent, C. K. (2007). RSV mediates Pseudomonas aeruginosa binding to cystic fibrosis and normal epithelial cells. Pediatr Res 61, 398-403.
136. Vareille, M., Kieninger, E., Edwards, M. R. & Regamey, N. (2011). The airway epithelium: soldier in the fight against respiratory viruses. Clin Microbiol Rev 24, 210-229.
137. Verkaik, N. J., Nguyen, D. T., de Vogel, C. P., Moll, H. A., Verbrugh, H. A., Jaddoe, V. W., Hofman, A., van Wamel, W. J., van den Hoogen, B. G. & other authors (2011). Streptococcus pneumoniae exposure is associated with human metapneumovirus seroconversion and increased susceptibility to in vitro HMPV infection. Clin Microbiol Infect 17, 1840-1844.
138. Wang, J., Li, F., Sun, R., Gao, X., Wei, H., Li, L. J. & Tian, Z. (2013). Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat Commun 4, 2106.
139. Wang, J., Nikrad, M. P., Travanty, E. A., Zhou, B., Phang, T., Gao, B., Alford, T., Ito, Y., Nahreini, P. & other authors (2012). Innate immune response of human alveolar macrophages during influenza A infection. PLoS One 7, e29879.
140. Wang, J. H., Kwon, H. J. & Jang, Y. J. (2009). Rhinovirus enhances various bacterial adhesions to nasal epithelial cells simultaneously. Laryngoscope 119, 1406-1411.
141. Warshauer, D., Goldstein, E., Akers, T., Lippert, W. & Kim, M. (1977). Effect of influenza viral infection on the ingestion and killing of bacteria by alveolar macrophages. Am Rev Respir Dis 115, 269-277.
142. Welsh, R. M., Che, J. W., Brehm, M. A. & Selin, L. K. (2010). Heterologous immunity between viruses. Immunol Rev 235, 244-266.
143. Werner, J. L. & Steele, C. (2014). Innate receptors and cellular defense against pulmonary infections. J Immunol 193, 3842-3850.
144. Wilkinson, T. M., Hurst, J. R., Perera, W. R., Wilks, M., Donaldson, G. C. & Wedzicha, J. A. (2006). Effect of interactions between lower airway bacterial and rhinoviral infection in exacerbations of COPD. Chest 129, 317-324.
145. Williams, A. E., Edwards, L., Humphreys, I. R., Snelgrove, R., Rae, A., Rappuoli, R. & Hussell, T. (2004). Innate imprinting by the modified heat-labile toxin of Escherichia coli (LTK63) provides generic protection against lung infectious disease. J Immunol 173, 7435-7443.
146. Wolf, A. I., Strauman, M. C., Mozdzanowska, K., Whittle, J. R., Williams, K. L., Sharpe, A. H., Weiser, J. N., Caton, A. J., Hensley, S. E. & Erikson, J. (2014). Coinfection with Streptococcus pneumoniae modulates the B cell response to influenza virus. J Virol 88, 11995-12005.
147. Wu, Y., Tu, W., Lam, K. T., Chow, K. H., Ho, P. L., Guan, Y., Peiris, J. S. & Lau, Y. L. (2015). Lethal coinfection of influenza virus and Streptococcus pneumoniae lowers antibody response to influenza virus in lung and reduces numbers of germinal center B cells, T follicular helper cells, and plasma cells in mediastinal lymph node. J Virol 89, 2013-2023.
148. Yokota, S., Okabayashi, T., Yoto, Y., Hori, T., Tsutsumi, H. & Fujii, N. (2010). Fosfomycin suppresses RS-virus-induced Streptococcus pneumoniae and Haemophilus influenzae adhesion to respiratory epithelial cells via the platelet-activating factor receptor. FEMS Microbiol Lett 310, 84-90.
149. Zalacain, R., Sobradillo, V., Amilibia, J., Barrón, J., Achótegui, V., Pijoan, J. I. & Llorente, J. L. (1999). Predisposing factors to bacterial colonization in chronic obstructive pulmonary disease. Eur Respir J 13, 343-348.
150. Zeng, H., Goldsmith, C. S., Maines, T. R., Belser, J. A., Gustin, K. M., Pekosz, A., Zaki, S. R., Katz, J. M. & Tumpey, T. M. (2013). Tropism and infectivity of influenza virus, including highly pathogenic avian H5N1 virus, in ferret tracheal differentiated primary epithelial cell cultures. J Virol 87, 2597-2607.
151. Zheng, J., Yang, P., Tang, Y., Pan, Z. & Zhao, D. (2015). Respiratory syncytial virus nonstructural proteins upregulate SOCS1 and SOCS3 in the different manner from endogenous IFN signaling. J Immunol Res 2015, 738547.
152. Zhu, L., Lee, B., Zhao, F., Zhou, X., Chin, V., Ling, S. C. & Chen, Y. (2014). Modulation of airway epithelial antiviral immunity by fungal exposure. Am J Respir Cell Mol Biol 50, 1136-1143.