Bacterial lipopolysaccharide inhibits influenza virus infection of human macrophages and the consequent induction of cd8+ t cell immunity

Journal of Innate Immunity

Volumn 6, Issue 2, 2014, Pages 129-139

  Short, Kirsty R ^a   Vissers, Marloes ^b   De Kleijn, Stan ^b   Zomer, Aldert L ^b   Kedzierska, Katherine ^a   Grant, Emma ^a   Reading, Patrick C ^a,c   Hermans, Peter W M ^b   Ferwerda, Gerben ^b   Diavatopoulos, Dimitri A ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

Author keywords

Antiviral response; Human macrophages; Influenza virus; Lipopolysaccharides

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; INTERFERON; BETA INTERFERON; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; ARTICLE; BASEMENT MEMBRANE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGRANULATION; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLUENZA A; LEUKOCYTE; LONGEVITY; MACROPHAGE; MONOCYTE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INHIBITION; VIRUS PARTICLE; VIRUS REPLICATION; ANIMAL; CELL CULTURE; COCULTURE; DNA MICROARRAY; DOG; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; HELA CELL LINE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLUENZA A VIRUS; MDCK CELL LINE; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; DOGS; FLOW CYTOMETRY; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; INTERFERON-BETA; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; MACROPHAGES; MADIN DARBY CANINE KIDNEY CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTOME; TUMOR NECROSIS FACTOR-ALPHA; VIRUS REPLICATION;

EID: 84896321073     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000353905     Document Type: Article

References (43)

1. Fiers W, De Filette M, Birkett A, Neirynck S,Min Jou W: A 'universal' human influenza Avaccine. Virus Res 2004; 103: 173-176.
2. Short KR, Habets MN, Hermans PWM, Diavatopoulos DA: Interactions between Streptococcuspneumoniae and influenza virus: amutually beneficial relationship? Future Microbiol 2012; 7: 609-624.
3. Tashiro M, Ciborowski P, Klenk HD, PulvererG, Rott R: Role of Staphylococcus proteasein the development of influenza pneumonia.Nature 1987; 325: 536-537. (Pubitemid 17056736)
4. Tashiro M, Ciborowski P, Reinacher M, PulvererG, Klenk HD, Rott R: Synergistic role of staphylococcal proteases in the induction ofinfluenza virus pathogenicity. Virology 1987;157: 421-430. (Pubitemid 17047697)
5. Ayala VI, Teijaro JR, Farber DL, Dorsey SG, Carbonetti NH: Bordetella pertussis infectionexacerbates influenza virus infection throug hpertussis toxin-mediated suppression of in nateimmunity. PLoS One 2011; 6:e19016.
6. Ichinohe T, Pang IK, Kumamoto Y, PeaperDR, Ho JH, Murray TS, Iwasaki A: Microbiotaregulates immune defense against respiratorytract influenza A virus infection. ProcNatl Acad Sci USA 2011; 108: 5354-5359.
7. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF, Paley MA, Antenus M, Williams KL, Erikson J: Commensalbacteria calibrate the activationthreshold of innate antiviral immunity. Immunity2012; 37: 158-170.
8. Shinya K, Okamura T, Sueta S, Kasai N, Tanaka M, Ginting TE, Makino A, Eisfeld AJ,Kawaoka Y: Toll-like receptor pre-stimulationprotects mice against lethal infectionwith highly pathogenic influenza viruses. VirolJ 2011; 8: 97-102.
9. Zhao J, Wohlford-Lenane C, Fleming E, LaneTE, McCray PJ Jr, Perlman S: Intranasal treatmentwith poly(I:C) protects aged mice fromlethal respiratory viral infections. J Virol2012; 86: 11416-11424.
10. Winther B, Innes DJ Jr, Mills SE, Mygind N,Zito D, Hayden FG: Lymphocyte subsets innormal airway mucosa of the human nose.Arch Otolaryngol Head Neck Surg 1987; 113:59-62. (Pubitemid 18047521)
11. Murphy EA, Davis JM, McClellan JL, CarmichaelMD, Rooijen NV, Gangemi JD: Susceptibilityto infection and inflammatory responsefollowing influenza virus (H1N1, A/PR/8/34) challenge: role of macrophages. JInterferon Cytokine Res 2011; 31: 501-508.
12. Holt P: Down-regulation of immune responsesin the lower respiratory tract: the role ofalveolar macrophages. Clin Exp Immunol1986; 63: 261-270. (Pubitemid 16155797)
13. Manicassamy B, Manicassamy S, Belicha-VillanuevaA, Pisanelli G, Pulendran B, García-Sastre A: Analysis of in vivo dynamics of influenzavirus infection in mice using a GFPreporter virus. Proc Natl Acad Sci USA 2010;107: 11531-11536.
14. Diavatopoulos D, Short K, Price J, Wilksch J,Brown L, Briles D, Strugnell R, Wijburg O:Influenza A virus facilitates Streptococcuspneumoniae transmission and disease. FASEBJ 2010; 24: 1789-1798.
15. Anders EM, Hartley CA, Jackson DC: Bovineand mouse serum beta inhibitors of influenzaA viruses are mannose-binding lectins. ProcNatl Acad Sci USA 1990; 87: 4485-4489.
16. Hallak LK, Collins PL, Knudson W, PeeplesME: Iduronic acid-containing glycosaminoglycanson target cells are required for efficientrespiratory syncytial virus infection. Virology2000; 271: 264-275. (Pubitemid 30461305)
17. Vissers M, Remijn T, Oosting M, de Jong DJ,Diavatopoulos DA, Hermans PWM, Ferwerda G: Respiratory syncytial virus infectionaugments NOD2 signaling in an IFN-?-dependentmanner in human primary cells. EurJ Immunol 2012; 42: 2727-2735.
18. Hoffmann E, Stech J, Guan Y, Webster R, PerezD: Universal primer set for the full-lengthamplification of all influenza A viruses. ArchVirol 2001; 146: 2275-2289. (Pubitemid 34682391)
19. Short KR, Reading PC, Brown LE, Pedersen J,Gilbertson B, Job ER, Edenborough KM, HabetsMN, Zomer A, Hermans PW, DiavatopoulosDA, Wijburg OL: Influenza-inducedinflammation drives pneumococcal otitis media.Infect Immun 2013; 81: 645-652.
20. Storey JD, Tibshirani R: Statistical significancefor genomewide studies. Proc NatlAcad Sci USA 2003; 100: 9440.
21. Mostafavi S, Ray D, Warde-Farley D, GrouiosC, Morris Q: GeneMANIA: a real-time multipleassociation network integration algorithmfor predicting gene function. GenomeBiol 2008; 9(suppl 1):S4.
22. Micallef L, Rodgers PR: Application forDrawing 3 Set Area-Proportional Venn Diagrams.Canterbury, University of Kent, 2012.
23. Rodgers P, Flower J, Stapleton G, Howse J:Drawing Area-Proportional Venn-3 Diagramswith Convex Polygons; DiagrammaticRepresentation and Inference. Berlin, Springer,2010, pp 54-68.
24. Clute SC, Watkin LB, Cornberg M, NaumovYN, Sullivan JL, Luzuriaga K, Welsh RM, SelinLK: Cross-reactive influenza virus-specificCD8+ T cells contribute to lymphoproliferationin Epstein-Barr virus-associated infectiousmononucleosis. J Clin Invest 2005; 115:3602-3612. (Pubitemid 43121849)
25. Neveu B, Debeaupuis E, Echasserieau K, leMoullac-Vaidye B, Gassin M, Jegou L, DecalfJ, Albert M, Ferry N, Gournay J: Selection of high-avidity CD8 T cells correlates with controlof hepatitis C virus infection. Hepatology2008; 48: 713-722.
26. Betts MR, Brenchley JM, Price DA, De RosaSC, Douek DC, Roederer M, Koup RA: Sensitiveand viable identification of antigen-specificCD8+ T cells by a flow cytometric assayfor degranulation. J Immunol Methods 2003;281: 65-78. (Pubitemid 37324571)
27. Alexopoulou L, Holt AC, Medzhitov R, FlavellRA: Recognition of double-strandedRNA and activation of NF-kappaB by Tolllikereceptor 3. Nature 2001; 413: 732-738. (Pubitemid 33009951)
28. Thitithanyanont A, Engering A, EkchariyawatP, Wiboon-ut S, Limsalakpetch A,Yongvanitchit K, Kum-Arb U, KanchongkittiphonW, Utaisincharoen P, Sirisinha S: Highsusceptibility of human dendritic cells to avianinfluenza H5N1 virus infection and protectionby IFN-? and TLR ligands. J Immunol2007; 179: 5220-5227.
29. Cella M, Salio M, Sakakibara Y, Langen H,Julkunen I, Lanzavecchia A: Maturation, activation,and protection of dendritic cells inducedby double-stranded RNA. J Exp Med1999; 189: 821-829. (Pubitemid 29189687)
30. Short KR, Brooks AG, Reading PC, LondriganSL: The fate of influenza A virus after infectionof human macrophages and dendritic cells. JGen Virol 2012;93(Pt 11):2315-2325.
31. Hufford MM, Kim TS, Sun J, Braciale TJ: AntiviralCD8+ T cell effector activities in situare regulated by target cell type. J Exp Med2011; 208: 167-180.
32. Ingvarsson L, Lundgren K, Ursing J: The bacterialflora in the nasopharynx in healthy children.Acta Otolaryngol 1982; 93: 94-96.
33. Reimer T, Brcic M, Schweizer M, Jungi TW: Poly(I:C) and LPS induce distinct IRF3 and NF-kappa B signaling during type-I IFN and TNF responses in human macrophages. J Leukoc Biol 2008; 83: 1249-1257. (Pubitemid 351960357)
34. Honda K, Yanai H, Takaoka A, Taniguchi T:Regulation of the type I IFN induction: a currentview. Int Immunol 2005; 17: 1367-1378. (Pubitemid 41631313)
35. Zamanian-Daryoush M, Marques JT, GantierMP, Behlke MA, John M, Rayman P, Finke J,Williams BR: Determinants of cytokine inductionby small interfering RNA in humanperipheral blood mononuclear cells. J InterferonCytokine Res 2008; 28: 221-233. (Pubitemid 351591447)
36. Silverman RH: Viral encounters with 2 ?,5 ? -oligoadenylatesynthetase and RNase L duringthe interferon antiviral response. J Virol 2007;81: 12720-12729. (Pubitemid 350156909)
37. Simard S, Maurais É, Gilbert C, Tremblay MJ:LPS reduces HIV-1 replication in primary humanmacrophages partly through an endogenousproduction of type I interferons. ClinImmunol 2008; 127: 198-205.
38. Friesenhagen J, Boergeling Y, Hrincius E,Ludwig S, Roth J, Viemann D: Highly pathogenicavian influenza viruses inhibit effectiveimmune responses of human blood-derivedmacrophages. J Leukoc Biol 2012; 92: 11-20.
39. Didierlaurent A, Goulding J, Patel S, SnelgroveR, Low L, Bebien M, Lawrence T, van Rijt LS, Lambrecht BN, Sirard JC: Sustaineddesensitization to bacterial Toll-like receptorligands after resolution of respiratory influenzainfection. J Exp Med 2008; 205: 323-329. (Pubitemid 351281598)
40. Moltedo B, Li W, Yount JS, Moran TM:Unique type I interferon responses determinethe functional fate of migratory lung dendriticcells during influenza virus infection. PLoSPathog 2011; 7:e1002345.
41. Smed-Sörensen A, Chalouni C, Chatterjee B,Cohn L, Blattmann P, Nakamura N, DelamarreL, Mellman I: Influenza A virus infectionof human primary dendritic cells impairstheir ability to cross-present antigen to CD8T cells. PLoS Pathog 2012; 8:e1002572.
42. Faroudi M, Utzny C, Salio M, Cerundolo V,Guiraud M, Müller S, Valitutti S: Lytic versusstimulatory synapse in cytotoxic T lymphocyte/target cell interaction: manifestation of adual activation threshold. Proc Natl Acad Sci USA 2003; 100: 14145-14150. (Pubitemid 37499205)
43. Warshauer D, Goldstein E, Akers T, LippertW, Kim M: Effect of influenza viral infectionon the ingestion and killing of bacteria by alveolarmacrophages. Am Rev Respir Dis 1977;115: 269-277. (Pubitemid 8036164)