1887

Abstract

Macrophages are essential for protection against influenza A virus infection, but are also implicated in the morbidity and mortality associated with severe influenza disease, particularly during infection with highly pathogenic avian influenza (HPAI) H5N1 virus. While influenza virus infection of macrophages was once thought to be abortive, it is now clear that certain virus strains can replicate productively in macrophages. This may have important consequences for the antiviral functions of macrophages, the course of disease and the outcome of infection for the host. In this article, we review findings related to influenza virus replication in macrophages and the impact of productive replication on macrophage antiviral functions. A clear understanding of the interactions between influenza viruses and macrophages may lead to new antiviral therapies to relieve the burden of severe disease associated with influenza viruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000922
2017-10-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/10/2401.html?itemId=/content/journal/jgv/10.1099/jgv.0.000922&mimeType=html&fmt=ahah

References

  1. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J et al. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 2008; 4:e1000076 [View Article][PubMed]
    [Google Scholar]
  2. Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen Hadisoedarsuno W et al. Three Indonesian clusters of H5N1 virus infection in 2005. N Engl J Med 2006; 355:2186–2194 [View Article][PubMed]
    [Google Scholar]
  3. Peiris JS, de Jong MD, Guan Y. Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 2007; 20:243–267 [View Article][PubMed]
    [Google Scholar]
  4. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B et al. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc Natl Acad Sci USA 2010; 107:11531–11536 [View Article][PubMed]
    [Google Scholar]
  5. Ogiwara H, Yasui F, Munekata K, Takagi-Kamiya A, Munakata T et al. Histopathological evaluation of the diversity of cells susceptible to H5N1 virulent avian influenza virus. Am J Pathol 2014; 184:171–183 [View Article][PubMed]
    [Google Scholar]
  6. Wonderlich ER, Swan ZD, Bissel SJ, Hartman AL, Carney JP et al. Widespread virus replication in alveoli drives acute respiratory distress syndrome in aerosolized H5N1 influenza infection of macaques. J Immunol 2017; 198:1616–1626 [View Article][PubMed]
    [Google Scholar]
  7. Lietzén N, Ohman T, Rintahaka J, Julkunen I, Aittokallio T et al. Quantitative subcellular proteome and secretome profiling of influenza A virus-infected human primary macrophages. PLoS Pathog 2011; 7:e1001340 [View Article][PubMed]
    [Google Scholar]
  8. Kim HM, Lee YW, Lee KJ, Kim HS, Cho SW et al. Alveolar macrophages are indispensable for controlling influenza viruses in lungs of pigs. J Virol 2008; 82:4265–4274 [View Article][PubMed]
    [Google Scholar]
  9. Purnama C, Ng SL, Tetlak P, Setiagani YA, Kandasamy M et al. Transient ablation of alveolar macrophages leads to massive pathology of influenza infection without affecting cellular adaptive immunity. Eur J Immunol 2014; 44:2003–2012 [View Article][PubMed]
    [Google Scholar]
  10. Schneider C, Nobs SP, Heer AK, Kurrer M, Klinke G et al. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog 2014; 10:e1004053 [View Article][PubMed]
    [Google Scholar]
  11. Tate MD, Pickett DL, van Rooijen N, Brooks AG, Reading PC. Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 2010; 84:7569–7580 [View Article][PubMed]
    [Google Scholar]
  12. Tumpey TM, García-Sastre A, Taubenberger JK, Palese P, Swayne DE et al. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 2005; 79:14933–14944 [View Article][PubMed]
    [Google Scholar]
  13. Ghoneim HE, Thomas PG, Mccullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 2013; 191:1250–1259 [View Article][PubMed]
    [Google Scholar]
  14. Högner K, Wolff T, Pleschka S, Plog S, Gruber AD et al. Macrophage-expressed IFN-β contributes to apoptotic alveolar epithelial cell injury in severe influenza virus pneumonia. PLoS Pathog 2013; 9:e1003188 [View Article][PubMed]
    [Google Scholar]
  15. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007; 445:319–323 [View Article][PubMed]
    [Google Scholar]
  16. Lee SM, Gardy JL, Cheung CY, Cheung TK, Hui KP et al. Systems-level comparison of host-responses elicited by avian H5N1 and seasonal H1N1 influenza viruses in primary human macrophages. PLoS One 2009; 4:e8072 [View Article][PubMed]
    [Google Scholar]
  17. Perrone LA, Plowden JK, García-Sastre A, Katz JM, Tumpey TM. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 2008; 4:e1000115 [View Article][PubMed]
    [Google Scholar]
  18. de Jong MD, Bach VC, Phan TQ, Vo MH, Tran TT et al. Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N Engl J Med 2005; 352:686–691 [View Article][PubMed]
    [Google Scholar]
  19. Zhou JJ, Fang DY, Fu J, Tian J, Zhou JM et al. Infection and replication of avian influenza H5N1 virus in an infected human. Virus Genes 2009; 39:76–80 [View Article][PubMed]
    [Google Scholar]
  20. Klepper A, Branch AD. Macrophages and the viral dissemination super highway. EC Microbiol 2015; 2:328–336[PubMed]
    [Google Scholar]
  21. Brana C, Biggs TE, Barton CH, Sundstrom LE, Mann DA. A soluble factor produced by macrophages mediates the neurotoxic effects of HIV-1 Tat in vitro . AIDS 1999; 13:1443–1452 [View Article][PubMed]
    [Google Scholar]
  22. Steurbaut S, Merckx E, Rombaut B, Vrijsen R. Modulation of viral replication in macrophages persistently infected with the DA strain of Theiler's murine encephalomyelitis virus. Virol J 2008; 5:89 [View Article][PubMed]
    [Google Scholar]
  23. Zhang R, Bloch N, Nguyen LA, Kim B, Landau NR. SAMHD1 restricts HIV-1 replication and regulates interferon production in mouse myeloid cells. PLoS One 2014; 9:e89558 [View Article][PubMed]
    [Google Scholar]
  24. Rodgers B, Mims CA. Interaction of influenza virus with mouse macrophages. Infect Immun 1981; 31:751–757[PubMed]
    [Google Scholar]
  25. Wells MA, Albrecht P, Daniel S, Ennis FA. Host defense mechanisms against influenza virus: interaction of influenza virus with murine macrophages in vitro . Infect Immun 1978; 22:758–762[PubMed]
    [Google Scholar]
  26. Rodgers BC, Mims CA. Influenza virus replication in human alveolar macrophages. J Med Virol 1982; 9:177–184 [View Article][PubMed]
    [Google Scholar]
  27. Londrigan SL, Short KR, Ma J, Gillespie L, Rockman SP et al. Infection of mouse macrophages by seasonal influenza viruses can be restricted at the level of virus entry and at a late stage in the virus life cycle. J Virol 2015; 89:12319–12329 [View Article][PubMed]
    [Google Scholar]
  28. Tate MD, Schilter HC, Brooks AG, Reading PC. Responses of mouse airway epithelial cells and alveolar macrophages to virulent and avirulent strains of influenza A virus. Viral Immunol 2011; 24:77–88 [View Article][PubMed]
    [Google Scholar]
  29. Wang J, Nikrad MP, Travanty EA, Zhou B, Phang T et al. Innate immune response of human alveolar macrophages during influenza A infection. PLoS One 2012; 7:e29879 [View Article][PubMed]
    [Google Scholar]
  30. Chan RW, Leung CY, Nicholls JM, Peiris JS, Chan MC. Proinflammatory cytokine response and viral replication in mouse bone marrow derived macrophages infected with influenza H1N1 and H5N1 viruses. PLoS One 2012; 7:e51057 [View Article][PubMed]
    [Google Scholar]
  31. Hoeve MA, Nash AA, Jackson D, Randall RE, Dransfield I. Influenza virus A infection of human monocyte and macrophage subpopulations reveals increased susceptibility associated with cell differentiation. PLoS One 2012; 7:e29443 [View Article][PubMed]
    [Google Scholar]
  32. Marvin SA, Russier M, Huerta CT, Russell CJ, Schultz-Cherry S. Influenza virus overcomes cellular blocks to productively replicate, impacting macrophage function. J Virol 2017; 91:e01417-16 [View Article][PubMed]
    [Google Scholar]
  33. Yu WC, Chan RW, Wang J, Travanty EA, Nicholls JM et al. Viral replication and innate host responses in primary human alveolar epithelial cells and alveolar macrophages infected with influenza H5N1 and H1N1 viruses. J Virol 2011; 85:6844–6855 [View Article][PubMed]
    [Google Scholar]
  34. Short KR, Brooks AG, Reading PC, Londrigan SL. The fate of influenza A virus after infection of human macrophages and dendritic cells. J Gen Virol 2012; 93:2315–2325 [View Article][PubMed]
    [Google Scholar]
  35. Mok CK, Lee DC, Cheung CY, Peiris M, Lau AS. Differential onset of apoptosis in influenza A virus H5N1- and H1N1-infected human blood macrophages. J Gen Virol 2007; 88:1275–1280 [View Article][PubMed]
    [Google Scholar]
  36. Sakabe S, Iwatsuki-Horimoto K, Takano R, Nidom CA, Le M et al. Cytokine production by primary human macrophages infected with highly pathogenic H5N1 or pandemic H1N1 2009 influenza viruses. J Gen Virol 2011; 92:1428–1434 [View Article][PubMed]
    [Google Scholar]
  37. van Riel D, Leijten LM, van der Eerden M, Hoogsteden HC, Boven LA et al. Highly pathogenic avian influenza virus H5N1 infects alveolar macrophages without virus production or excessive TNF-alpha induction. PLoS Pathog 2011; 7:e1002099 [View Article][PubMed]
    [Google Scholar]
  38. Friesenhagen J, Boergeling Y, Hrincius E, Ludwig S, Roth J et al. Highly pathogenic avian influenza viruses inhibit effective immune responses of human blood-derived macrophages. J Leukoc Biol 2012; 92:11–20 [View Article][PubMed]
    [Google Scholar]
  39. Cline TD, Karlsson EA, Seufzer BJ, Schultz-Cherry S. The hemagglutinin protein of highly pathogenic H5N1 influenza viruses overcomes an early block in the replication cycle to promote productive replication in macrophages. J Virol 2013; 87:1411–1419 [View Article][PubMed]
    [Google Scholar]
  40. Takahata M, Iwasaki N, Nakagawa H, Abe Y, Watanabe T et al. Sialylation of cell surface glycoconjugates is essential for osteoclastogenesis. Bone 2007; 41:77–86 [View Article][PubMed]
    [Google Scholar]
  41. Ng WC, Liong S, Tate MD, Irimura T, Denda-Nagai K et al. The macrophage galactose-type lectin can function as an attachment and entry receptor for influenza virus. J Virol 2014; 88:1659–1672 [View Article][PubMed]
    [Google Scholar]
  42. Meng B, Marriott AC, Dimmock NJ. The receptor preference of influenza viruses. Influenza Other Respir Viruses 2010; 4:147–153 [View Article][PubMed]
    [Google Scholar]
  43. Chang WC, White MR, Moyo P, McClear S, Thiel S et al. Lack of the pattern recognition molecule mannose-binding lectin increases susceptibility to influenza A virus infection. BMC Immunol 2010; 11:64 [View Article][PubMed]
    [Google Scholar]
  44. Nelson B, Zhou X, White M, Hartshorn K, Takahashi K et al. Recombinant human mannose-binding lectin dampens human alveolar macrophage inflammatory responses to influenza A virus in vitro . J Leukoc Biol 2014; 95:715–722 [View Article][PubMed]
    [Google Scholar]
  45. Reading PC, Miller JL, Anders EM. Involvement of the mannose receptor in infection of macrophages by influenza virus. J Virol 2000; 74:5190–5197 [View Article][PubMed]
    [Google Scholar]
  46. Job ER, Deng YM, Barfod KK, Tate MD, Caldwell N et al. Addition of glycosylation to influenza A virus hemagglutinin modulates antibody-mediated recognition of H1N1 2009 pandemic viruses. J Immunol 2013; 190:2169–2177 [View Article][PubMed]
    [Google Scholar]
  47. Sun S, Wang Q, Zhao F, Chen W, Li Z. Glycosylation site alteration in the evolution of influenza A (H1N1) viruses. PLoS One 2011; 6:e22844 [View Article][PubMed]
    [Google Scholar]
  48. Reed ML, Bridges OA, Seiler P, Kim JK, Yen HL et al. The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus pathogenicity and transmissibility in ducks. J Virol 2010; 84:1527–1535 [View Article][PubMed]
    [Google Scholar]
  49. Scholtissek C. Stability of infectious influenza A viruses at low pH and at elevated temperature. Vaccine 1985; 3:215–218 [View Article][PubMed]
    [Google Scholar]
  50. Zaraket H, Bridges OA, Russell CJ. The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus replication and pathogenesis in mice. J Virol 2013; 87:4826–4834 [View Article][PubMed]
    [Google Scholar]
  51. Cline TD, Karlsson EA, Freiden P, Seufzer BJ, Rehg JE et al. Increased pathogenicity of a reassortant 2009 pandemic H1N1 influenza virus containing an H5N1 hemagglutinin. J Virol 2011; 85:12262–12270 [View Article][PubMed]
    [Google Scholar]
  52. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL et al. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease?. Lancet 2002; 360:1831–1837 [View Article][PubMed]
    [Google Scholar]
  53. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 2006; 12:1203–1207 [View Article][PubMed]
    [Google Scholar]
  54. Maines TR, Szretter KJ, Perrone L, Belser JA, Bright RA et al. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol Rev 2008; 225:68–84 [View Article][PubMed]
    [Google Scholar]
  55. Hui KP, Lee SM, Cheung CY, Ng IH, Poon LL et al. Induction of proinflammatory cytokines in primary human macrophages by influenza A virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol 2009; 182:1088–1098 [View Article][PubMed]
    [Google Scholar]
  56. Choi YK, Nguyen TD, Ozaki H, Webby RJ, Puthavathana P et al. Studies of H5N1 influenza virus infection of pigs by using viruses isolated in Vietnam and Thailand in 2004. J Virol 2005; 79:10821–10825 [View Article][PubMed]
    [Google Scholar]
  57. Lipatov AS, Kwon YK, Sarmento LV, Lager KM, Spackman E et al. Domestic pigs have low susceptibility to H5N1 highly pathogenic avian influenza viruses. PLoS Pathog 2008; 4:e1000102 [View Article][PubMed]
    [Google Scholar]
  58. Nelli RK, Dunham SP, Kuchipudi SV, White GA, Baquero-Perez B et al. Mammalian innate resistance to highly pathogenic avian influenza H5N1 virus infection is mediated through reduced proinflammation and infectious virus release. J Virol 2012; 86:9201–9210 [View Article][PubMed]
    [Google Scholar]
  59. Geiler J, Michaelis M, Sithisarn P, Cinatl J. Comparison of pro-inflammatory cytokine expression and cellular signal transduction in human macrophages infected with different influenza A viruses. Med Microbiol Immunol 2011; 200:53–60 [View Article][PubMed]
    [Google Scholar]
  60. Monteerarat Y, Sakabe S, Ngamurulert S, Srichatraphimuk S, Jiamtom W et al. Induction of TNF-alpha in human macrophages by avian and human influenza viruses. Arch Virol 2010; 155:1273–1279 [View Article][PubMed]
    [Google Scholar]
  61. Jonges M, Liu WM, van der Vries E, Jacobi R, Pronk I et al. Influenza virus inactivation for studies of antigenicity and phenotypic neuraminidase inhibitor resistance profiling. J Clin Microbiol 2010; 48:928–940 [View Article][PubMed]
    [Google Scholar]
  62. Fujimoto I, Pan J, Takizawa T, Nakanishi Y. Virus clearance through apoptosis-dependent phagocytosis of influenza A virus-infected cells by macrophages. J Virol 2000; 74:3399–3403 [View Article][PubMed]
    [Google Scholar]
  63. Hashimoto Y, Moki T, Takizawa T, Shiratsuchi A, Nakanishi Y. Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice. J Immunol 2007; 178:2448–2457 [View Article][PubMed]
    [Google Scholar]
  64. Watanabe Y, Hashimoto Y, Shiratsuchi A, Takizawa T, Nakanishi Y. Augmentation of fatality of influenza in mice by inhibition of phagocytosis. Biochem Biophys Res Commun 2005; 337:881–886 [View Article][PubMed]
    [Google Scholar]
  65. Park SY, Jung MY, Kim HJ, Lee SJ, Kim SY et al. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ 2008; 15:192–201 [View Article][PubMed]
    [Google Scholar]
  66. Park SY, Jung MY, Lee SJ, Kang KB, Gratchev A et al. Stabilin-1 mediates phosphatidylserine-dependent clearance of cell corpses in alternatively activated macrophages. J Cell Sci 2009; 122:3365–3373 [View Article][PubMed]
    [Google Scholar]
  67. Kobayashi N, Karisola P, Peña-Cruz V, Dorfman DM, Jinushi M et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 2007; 27:927–940 [View Article][PubMed]
    [Google Scholar]
  68. Leverrier Y, Okkenhaug K, Sawyer C, Bilancio A, Vanhaesebroeck B et al. Class I phosphoinositide 3-kinase p110β is required for apoptotic cell and Fcgamma receptor-mediated phagocytosis by macrophages. J Biol Chem 2003; 278:38437–38442 [View Article][PubMed]
    [Google Scholar]
  69. Wang P, He Y, Li D, Han R, Liu G et al. Class I PI3K inhibitor ZSTK474 mediates a shift in microglial/macrophage phenotype and inhibits inflammatory response in mice with cerebral ischemia/reperfusion injury. J Neuroinflammation 2016; 13:192 [View Article][PubMed]
    [Google Scholar]
  70. Li W, Wang G, Zhang H, Shen Y, Dai J et al. Inability of NS1 protein from an H5N1 influenza virus to activate PI3K/Akt signaling pathway correlates to the enhanced virus replication upon PI3K inhibition. Vet Res 2012; 43:36 [View Article][PubMed]
    [Google Scholar]
  71. Zhao X, Dai J, Xiao X, Wu L, Zeng J et al. PI3K/Akt signaling pathway modulates influenza virus induced mouse alveolar macrophage polarization to M1/M2b. PLoS One 2014; 9:e104506 [View Article][PubMed]
    [Google Scholar]
  72. Smith AM, McCullers JA. Secondary bacterial infections in influenza virus infection pathogenesis. Curr Top Microbiol Immunol 2014; 385:327–356 [View Article][PubMed]
    [Google Scholar]
  73. Jakab GJ. Immune impairment of alveolar macrophage phagocytosis during influenza virus pneumonia. Am Rev Respir Dis 1982; 126:778–782 [View Article][PubMed]
    [Google Scholar]
  74. Arredouani MS, Yang Z, Imrich A, Ning Y, Qin G et al. The macrophage scavenger receptor SR-AI/II and lung defense against pneumococci and particles. Am J Respir Cell Mol Biol 2006; 35:474–478 [View Article][PubMed]
    [Google Scholar]
  75. Thomas CA, Li Y, Kodama T, Suzuki H, Silverstein SC et al. Protection from lethal gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J Exp Med 2000; 191:147–156 [View Article][PubMed]
    [Google Scholar]
  76. Gordon S. Alternative activation of macrophages. Nat Rev Immunol 2003; 3:23–35 [View Article][PubMed]
    [Google Scholar]
  77. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010; 32:593–604 [View Article][PubMed]
    [Google Scholar]
  78. Jablonski KA, Amici SA, Webb LM, Ruiz-Rosado JD, Popovich PG et al. Novel markers to delineate murine M1 and M2 macrophages. PLoS One 2015; 10:e0145342 [View Article][PubMed]
    [Google Scholar]
  79. Sang Y, Miller LC, Blecha F. Macrophage polarization in virus-host interactions. J Clin Cell Immunol 2015; 6: [View Article][PubMed]
    [Google Scholar]
  80. Edin S, Wikberg ML, Dahlin AM, Rutegård J, Öberg Å et al. The distribution of macrophages with a M1 or M2 phenotype in relation to prognosis and the molecular characteristics of colorectal cancer. PLoS One 2012; 7:e47045 [View Article][PubMed]
    [Google Scholar]
  81. Isabelle Dutry JL, Li PH, Bruzzone R, Malik Peiris JS, Jamue M. The effects of macrophage polarity on influenza virus replication and innate immune responses. J Clin Cell Immunol 2015; 6:297
    [Google Scholar]
  82. Rőszer T. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediators Inflamm 2015; 2015:816460 [View Article][PubMed]
    [Google Scholar]
  83. Campbell GM, Nicol MQ, Dransfield I, Shaw DJ, Nash AA et al. Susceptibility of bone marrow-derived macrophages to influenza virus infection is dependent on macrophage phenotype. J Gen Virol 2015; 96:2951–2960 [View Article][PubMed]
    [Google Scholar]
  84. Arriola CS, Nelson DI, Deliberto TJ, Blanton L, Kniss K et al. Infection risk for persons exposed to highly pathogenic avian influenza A H5 virus-infected birds, United States, December 2014-March 2015. Emerg Infect Dis 2015; 21:2135–2140 [View Article][PubMed]
    [Google Scholar]
  85. Briand FX, Schmitz A, Ogor K, Le Prioux A, Guillou-Cloarec C et al. Emerging highly pathogenic H5 avian influenza viruses in France during winter 2015/16: phylogenetic analyses and markers for zoonotic potential. Euro Surveill 2017; 22:pii: 30473 [View Article][PubMed]
    [Google Scholar]
  86. Lee DH, Bahl J, Torchetti MK, Killian ML, Ip HS et al. Highly pathogenic avian influenza viruses and generation of novel reassortants, United States, 2014–2015. Emerg Infect Dis 2016; 22:1283–1285 [View Article][PubMed]
    [Google Scholar]
  87. Global Consortium for H5N8 and Related Influenza Viruses Role for migratory wild birds in the global spread of avian influenza H5N8. Science 2016; 354:213–217 [View Article][PubMed]
    [Google Scholar]
  88. Fukuyama S, Katsura H, Zhao D, Ozawa M, Ando T et al. Multi-spectral fluorescent reporter influenza viruses (Color-flu) as powerful tools for in vivo studies. Nat Commun 2015; 6:6600 [View Article][PubMed]
    [Google Scholar]
  89. Lakdawala SS, Shih AR, Jayaraman A, Lamirande EW, Moore I et al. Receptor specificity does not affect replication or virulence of the 2009 pandemic H1N1 influenza virus in mice and ferrets. Virology 2013; 446:349–356 [View Article][PubMed]
    [Google Scholar]
  90. Lyon JA, Hinshaw VS. Replication of influenza A viruses in an avian macrophage cell line. J Gen Virol 1991; 72:2011–2013 [View Article][PubMed]
    [Google Scholar]
  91. Kasloff SB, Weingartl HM. Swine alveolar macrophage cell model allows optimal replication of influenza A viruses regardless of their origin. Virology 2016; 490:91–98 [View Article][PubMed]
    [Google Scholar]
  92. Powe JR, Castleman WL. Canine influenza virus replicates in alveolar macrophages and induces TNF-α. Vet Pathol 2009; 46:1187–1196 [View Article][PubMed]
    [Google Scholar]
  93. van Campen H, Easterday BC, Hinshaw VS. Virulent avian influenza A viruses: their effect on avian lymphocytes and macrophages in vivo and in vitro . J Gen Virol 1989; 70:2887–2895 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000922
Loading
/content/journal/jgv/10.1099/jgv.0.000922
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error