The severe pathogenicity of alveolar macrophage-depleted ferrets infected with 2009 pandemic H1N1 influenza virus

Virology

Volumn 444, Issue 1-2, 2013, Pages 394-403

  Kim, Heui Man ^a   Kang, Young Myong ^a   Ku, Keun Bon ^a   Park, Eun Hye ^a   Yum, Jung ^a   Kim, Jeong Cheol ^a   Jin, Seo Yeon ^a   Lee, Joo Sub ^a   Kim, Hyun Soo ^a   Seo, Sang Heui ^a  

^a Chungnam National University   (South Korea)

Author keywords

Alveolar macrophages; Inflammatory responses; Influenza virus

Indexed keywords

CHEMOKINE; CXCL11 CHEMOKINE; CXCL19 CHEMOKINE; EOTAXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MONOCYTE CHEMOTACTIC PROTEIN 2; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG;

2009 H1N1 INFLUENZA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONTROLLED STUDY; DISEASE SEVERITY; FERRET; HISTOPATHOLOGY; INFECTION RISK; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE FUNCTION; MICROBIOLOGICAL PARAMETERS; NONHUMAN; PANDEMIC INFLUENZA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RISK REDUCTION; VIRUS TITER; VIRUS VIRULENCE; WEIGHT REDUCTION;

ALVEOLAR MACROPHAGES; INFLAMMATORY RESPONSES; INFLUENZA VIRUS;

ANIMALS; BODY TEMPERATURE; BODY WEIGHT; CYTOKINES; DISEASE MODELS, ANIMAL; FERRETS; INFLUENZA A VIRUS, H1N1 SUBTYPE; LEUKOCYTE REDUCTION PROCEDURES; LUNG; MACROPHAGES, ALVEOLAR; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS;

MUSTELA; ORTHOMYXOVIRIDAE;

EID: 84882928835     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.07.006     Document Type: Article

References (37)

1. Bancroft J.D., Stevens A. Theory and Practice of Histological Techniques 1996, Chrchill Livingstone, New York. 4th ed.
2. Baskin C.R., Bielefeldt-Ohmann H., Tumpey T.M., Sabourin P.J., Long J.P., García-Sastre A., Tolnay A.E., Albrecht R., Pyles J.A., Olson P.H., Aicher L.D., Rosenzweig E.R., Murali-Krishna K., Clark E.A., Kotur M.S., Fornek J.L., Proll S., Palermo R.E., Sabourin C.L., Katze M.G. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. USA 2009, 106(9):3455-3460.
3. Belser J.A., Jayaraman A., Raman R., Pappas C., Zeng H., Cox N.J., Katz J.M., Sasisekharan R., Tumpey T.M. Effect of D222G mutation in the hemagglutinin protein on receptor binding, pathogenesis and transmissibility of the 2009 pandemic H1N1 influenza virus. PLoS One 2011, 6(9):e25091.
4. Belser J.A., Gustin K.M., Maines T.R., Blau D.M., Zaki S.R., Katz J.M., Tumpey T.M. Pathogenesis and transmission of triple-reassortant swine H1N1 influenza viruses isolated before the 2009 H1N1 pandemic. J. Virol. 2011, 85(4):1563-1572.
5. Bosio C.M., Dow S.W. Francisella tularensis induces aberrant activation of pulmonary dendritic cells. J. Immunol. 2005, 175(10):6792-6801.
6. Bouvier N.M, Palese P. The biology of influenza viruses. Vaccine 2008, 26(4):D49-D53.
7. CDC Swine influenza A (H1N1) infection in two children-Southern California, March-April. MMWR Morb. Mortal Wkly. Rep. 2009, 58(15):400. (Centers for Disease Control and Prevention).
8. Cameron C.M., Cameron M.J., Bermejo-Martin J.F., Ran L., Xu L., Turner P.V., Ran R., Danesh A., Fang Y., Chan P.K., Mytle N., Sullivan T.J., Collins T.L., Johnson M.G., Medina J.C., Rowe T., Kelvin D.J. Gene expression analysis of host innate immune responses during Lethal H5N1 infection in ferrets. J. Virol. 2008, 82(22):11308-11317.
9. Duan M., Li W.C., Vlahos R., Maxwell M.J., Anderson G.P., Hibbs M.L. Distinct macrophage subpopulations characterize acute infection and chronic inflammatory lung disease. J. Immunol. 2012, 189(2):946-955.
10. Fouchier R.A., Munster V., Wallensten A., Bestebroer T.M., Herfst S., Smith D., Rimmelzwaan G.F., Olsen B., Osterhaus A.D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005, 79:2814-2822.
11. Gao W., Sun W., Qu B., Cardona C.J., Powell K., Wegner M., Shi Y., Xing Z. Distinct regulation of host responses by ERK and JNK MAP kinases in swine macrophages infected with pandemic (H1N1) 2009 influenza virus. PLoS One 2012, 7(1):e30328.
12. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., Sessions W.M., Xu X., Skepner E., Deyde V., Okomo-Adhiambo M., Gubareva L., Barnes J., Smith C.B., Emery S.L., Hillman M.J., Rivailler P., Smagala J., de Graaf M., Burke D.F., Fouchier R.A., Pappas C., Alpuche-Aranda C.M., López-Gatell H., Olivera H., López I., Myers C.A., Faix D., Blair P.J., Yu C., Keene K.M., Dotson P.D., Boxrud D., Sambol A.R., Abid S.H., St George K., Bannerman T., Moore A.L., Stringer D.J., Blevins P., Demmler-Harrison G.J., Ginsberg M., Kriner P., Waterman S., Smole S., Guevara H.F., Belongia E.A., Clark P.A., Beatrice S.T., Donis R., Katz J., Finelli L., Bridges C.B., Shaw M., Jernigan D.B., Uyeki T.M., Smith D.J., Klimov A.I., Cox N.J. Ntigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325(5937):197-201.
13. Gordon S, Martinez F.O. Alternative activation of macrophages: mechanism and functions. Immunity 2010, 32(5):593-604.
14. Itoh Y., Shinya K., Kiso M., Watanabe T., Sakoda Y., Hatta M., Muramoto Y., Tamura D., Sakai-Tagawa Y., Noda T., Sakabe S., Imai M., Hatta Y., Watanabe S., Li C., Yamada S., Fujii K., Murakami S., Imai H., Kakugawa S., Ito M., Takano R., Iwatsuki-Horimoto K., Shimojima M., Horimoto T., Goto H., Takahashi K., Makino A., Ishigaki H., Nakayama M., Okamatsu M., Takahashi K., Warshauer D., Shult P.A., Saito R., Suzuki H., Furuta Y., Yamashita M., Mitamura K., Nakano K., Nakamura M., Brockman-Schneider R., Mitamura H., Yamazaki M., Sugaya N., Suresh M., Ozawa M., Neumann G., Gern J., Kida H., Ogasawara K., Kawaoka Y. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 2009, 460(7258):1021-1025.
15. Jain S., Kamimoto L., Bramley A.M., Schmitz A.M., Benoit S.R., Louie J., Sugerman D.E., Druckenmiller J.K., Ritger K.A., Chugh R., Jasuja S., Deutscher M., Chen S., Walker J.D., Duchin J.S., Lett S., Soliva S., Wells E.V., Swerdlow D., Uyeki T.M., Fiore A.E., Olsen S.J., Fry A.M., Bridges C.B., Finelli L. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N. Engl. J. Med. 2009, 361(20):1935-1944. Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team 2009.
16. Johnson N.P., Mueller J. Updating the accounts: global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull. Hist. Med. 2002, 76(1):105-115.
17. Kang Y.M., Song B.M., Lee J.S., Kim H.S., Seo S.H. Pandemic H1N1 influenza virus causes a stronger inflammatory response than seasonal H1N1 influenza virus in ferrets. Arch. Virol. 2011, 156(5):759-767.
18. Kawaoka Y., Krauss S., Webster R.G. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J. Virol. 1989, 63(11):4603-4608.
19. Kelvin A.A., Banner D., Danesh A., Seneviratne C., Ochi A. Ferret TNF-α and IFN-γ immunoassays. Trends Immunolabelled Related Tech. 2012, 133-160.
20. Kim H.M., Lee Y.W., Lee K.J., Kim H.S., Cho S.W., van Rooijen N., Guan Y., Seo S.H. Alveolar macrophages are indispensable for controlling influenza viruses in lungs of pigs. J. Virol. 2008, 82(9):4265-4274.
21. Kim H.M., Kang Y.M., Song B.M., Kim H.S., Seo S.H. The 2009 pandemic H1N1 influenza virus is more pathogenic in pregnant mice than seasonal H1N1. Influenza Virus Viral Immunol. 2012, 25(5):402-410.
22. Kim Y.H., Kim H.S., Cho S.H., Seo S.H. Influenza B virus causes milder pathogenesis and weaker inflammatory responses in ferrets than influenza A virus. Viral Immunol. 2009, 22(6):423-430.
23. McGill J., Van Rooijen N., Legge K.L. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J. Exp. Med. 2008, 205(7):1635-1646.
24. Munster V.J., de Wit E., van den Brand J.M., Herfst S., Schrauwen E.J., Bestebroer T.M., van de Vijver D., Boucher C.A., Koopmans M., Rimmelzwaan G.F., Kuiken T., Osterhaus A.D., Fouchier R.A. Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 2009, 325(5939):481-483.
25. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11(11):723-737.
26. Osterlund P., Pirhonen J., Ikonen N., Rönkkö E., Strengell M., Mäkelä S.M., Broman M., Hamming O.J., Hartmann R., Ziegler T., Julkunen I. Pandemic H1N1 2009 influenza A virus induces weak cytokine responses in human macrophages and dendritic cells and is highly sensitive to the antiviral actions of interferons. J. Virol. 2010, 84(3):1414-1422.
27. Reed L.E., Muench H. A simple method for estimating fifty percent endpoints. Am. J. Hyg. 1938, 27:493-497.
28. Roberts K.L., Shelton H., Stilwell P., Barclay W.S. Transmission of a 2009 H1N1 pandemic influenza virus occurs before fever is detected, in the Ferret model. PLoS One 2012, 7(8):e43303.
29. Scholtissek C., Rohde W., Von Hoyningen V., Rott R. On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 1978, 87(1):13-20.
30. Seibert C.W., Kaminski M., Philipp J., Rubbenstroth D., Albrecht R.A., Schwalm F., Stertz S., Medina R.A., Kochs G., García-Sastre A., Staeheli P., Palese P. Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J. Virol. 2010, 84(21):11219-11226.
31. Sun X., Sui H., Fisher J.T., Yan Z., Liu X., Cho H.J., Joo N.S., Zhang Y., Zhou W., Yi Y., Kinyon J.M., Lei-Butters D.C., Griffin M.A., Naumann P., Luo M., Ascher J., Wang K., Frana T., Wine J.J., Meyerholz D.K., Engelhardt J.F. Disease phenotype of a ferret CFTR-knockout model of cystic fibrosis. J. Clin. Invest. 2010, 120(9):3149-3160.
32. Tate M.D., Pickett D.L., van Rooijen N., Brooks A.G., Reading P.C. Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J. Virol. 2010, 84(15):7569-7580.
33. Taubenberger J.K., Reid A.H., Krafft A.E., Bijwaard K.E., Fanning T.G. Initial genetic characterization of the 1918 "Spanish" influenza virus. Science 1997, 275(5307):1793-1796.
34. Taubenberger J.K., Reid A.H., Lourens R.M., Wang R., Jin G., Fanning T.G. Characterization of the 1918 influenza virus polymerase genes. Nature 2005, 437(7060):889-893.
35. Tumpey T.M., García-Sastre A., Taubenberger J.K., Palese P., Swayne D.E., Pantin-Jackwood M.J., Schultz-Cherry S., Solórzano A., Van Rooijen N., Katz J.M., Basler C.F. 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(23):14933-14944.
36. Van Rooijen N. The liposome-mediated macrophage 'suicide' technique. J. Immunol. Methods 1989, 124(1):1-6.
37. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56(1):152-179.