Differential host gene responses in mice infected with two highly pathogenic avian influenza viruses of subtype H5N1 isolated from wild birds in Thailand

Virology

Volumn 412, Issue 1, 2011, Pages 9-18

  Hayashi, Tsuyoshi ^a,b   Chaichoune, Kridsada ^c   Patchimasiri, Tuangthong ^d   Hiromoto, Yasuaki ^a,b   Kawasaki, Yuri ^a,b   Wiriyarat, Witthawat ^c   Chakritbudsabong, Warunya ^c   Prayoonwong, Natanan ^c   Chaisilp, Natnapat ^c   Parchariyanon, Sujira ^d   Ratanakorn, Parntep ^c   Uchida, Yuko ^a,b   Tsuda, Tomoyuki ^b   Saito, Takehiko ^a,b  

^a Thailand Japan Zoonotic Diseases Collaboration Center   (Thailand)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^c MAHIDOL UNIVERSITY   (Thailand)

^d NATIONAL INSTITUTE OF ANIMAL HEALTH   (Thailand)

Author keywords

Cytokine; Highly pathogenic avian influenza virus; Inflammation; Mice; Neutrophil; Wild bird

Indexed keywords

CYTOKINE; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA VIRUS; BIRD; CONTROLLED STUDY; EMBRYO; ENCEPHALITIS; FEMALE; HOST; INFLUENZA A (H5N1); INFLUENZA VIRUS A H5N1; INTERSTITIAL PNEUMONIA; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PIGEON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPARROW; THAILAND; VIRUS GENE; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS VIRULENCE; WILD ANIMAL;

ANIMALS; BIRDS; BRAIN; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; LUNG; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE INFECTIONS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SURVIVAL ANALYSIS; THAILAND;

AVES; AVIAN INFLUENZA VIRUS; MUS;

EID: 79952532729     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.12.040     Document Type: Article

References (44)

1. Amonsin A., Payungporn S., Theamboonlers A., Thanawongnuwech R., Suradhat S., Pariyothorn N., Tantilertcharoen R., Damrongwantanapokin S., Buranathai C., Chaisingh A., Songserm T., Poovorawan Y. Genetic characterization of H5N1 influenza A viruses isolated from zoo tigers in Thailand. Virology 2006, 344:480-491.
2. Cheeran M.C.J., Hu S., Palmquist J.M., Bakken T., Gekker G., Lokensgard J.R. Dysregulated interferon-gamma responses during lethal cytomegalovirus brain infection of IL-10-deficient mice. Virus Res. 2007, 130:96.
3. Chen H., Li Y., Li Z., Shi J., Shinya K., Deng G., Qi Q., Tian G., Fan S., Zhao H., Sun Y., Kawaoka Y. Properties and Dissemination of H5N1 Viruses Isolated during an Influenza Outbreak in Migratory Waterfowl in Western China. J. Virol. 2006, 80:5976-5983.
4. Chen H., Smith G.J.D., Zhang S.Y., Qin K., Wang J., Li K.S., Webster R.G., Peiris J.S.M., Guan Y. Avian flu H5N1 virus outbreak in migratory waterfowl. Nature 2005, 436:191.
5. Chotpitayasunondh T., Ungchusak K., Hanshaoworakul W., Chunsuthiwat S., Sawanpanyalert P., Kijphati R., Lochindarat S., Srisan P., Suwan P., Osotthanakorn Y., Anantasetagoon T., Kanjanawasri S., Tanupattarachai S., Weerakul J., Chaiwirattana R., Maneerattanaporn M., Poolsavathitikool R., Chokephaibulkit K., Apisarnthanarak A., Dowell S. Human disease from influenza A (H5N1), Thailand, 2004. Emerg. Infect. Dis. 2005, 11:201-209.
6. de Jong M.D., Simmons C.P., Thanh T.T., Hien V.M., Smith G.J.D., Chau T.N.B., Hoang D.M., Van Vinh Chau N., Khanh T.H., Dong V.C., Qui P.T., Van Cam B., Ha D.Q., Guan Y., Peiris J.S.M., Chinh N.T., Hien T.T., Farrar J. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 2006, 12:1203-1207.
7. Fornek J.L., Gillim-Ross L., Santos C., Carter V., Ward J.M., Cheng L.I., Proll S., Katze M.G., Subbarao K. A single-amino-acid substitution in a polymerase protein of an H5N1 influenza virus is associated with systemic infection and impaired T-cell activation in mice. J. Virol. 2009, 83:11102-11115.
8. Ghoshal K., Majumder S., Zhu Q., Hunzeker J., Datta J., Shah M., Sheridan J.F., Jacob S.T. Influenza virus infection induces metallothionein gene expression in the mouse liver and lung by overlapping but distinct molecular mechanisms. Mol. Cell. Biol. 2001, 21:8301-8317.
9. Gilsdorf A., Boxall N., Gasimov V., Agayev I., Mammadzade F., Ursu P., Gasimov E., Brown C., Mardel S., Jankovic D., Pimentel G., Ayoub I., Elassal E., Salvi C., Legros D., Silva C.P.D., Hay A., Andraghetti R., Rodier G., Ganter B. Two clusters of human infection with influenza A/H5N1 virus in the Republic of Azerbaijan, February-March 2006. Euro Surveill. 2006, 11:122-126.
10. Guilligay D., Tarendeau F., Resa-Infante P., Coloma R., Crepin T., Sehr P., Lewis J., Ruigrok R.W.H., Ortin J., Hart D.J., Cusack S. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat. Struct. Mol. Biol. 2008, 15:500-506.
11. Guo L., Hu-Li J., Paul W.E. Probabilistic regulation in TH2 cells accounts for monoallelic expression of IL-4 and IL-13. Immunity 2005, 23:89-99.
12. Inoue K., Shiota S., Yamada K., Gotoh K., Suganuma M., Fujioka T., Ahmed K., Iha H., Nishizono A. Evaluation of a new tumor necrosis factor-alpha-inducing membrane protein of Helicobacter pylori as a prophylactic vaccine antigen. Helicobacter 2009, 14:135-143.
13. Jiankuo M., Xingbing W., Baojun H., Xiongwin W., Zhuoya L., Ping X., Yong X., Anting L., Chunsong H., Feili G., Jinquan T. Peptide nucleic acid antisense prolongs skin allograft survival by means of blockade of CXCR3 expression directing T cells into graft. J. Immunol. 2003, 170:1556-1565.
14. Jiao P., Tian G., Li Y., Deng G., Jiang Y., Liu C., Liu W., Bu Z., Kawaoka Y., Chen H. A Single-Amino-Acid Substitution in the NS1 Protein Changes the Pathogenicity of H5N1 Avian Influenza Viruses in Mice. J. Virol. 2008, 82:1146-1154.
15. Ka-Fai T., Paul K.S.C., Kui-Fat C., Wai-Ki L., Woon-Yee L., Kit-Fai W., Nelson L.S.T., Dominic N.C.T., Rita Y.T.S., Thomas A.B., John S.T., Augustine F.C. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J. Med. Virol. 2001, 63:242-246.
16. Keawcharoen J., Oraveerakul K., Kuiken T., Fouchier R.A.M., Amonsin A., Payungporn S., Noppornpanth S., Wattanodorn S., Theamboonlers A., Tantilertcharoen R., Pattanarangsan R., Arya N., Ratanakorn P., Osterhaus A.D.M.E., Poovorawan Y. Avian influenza H5N1 in tigers and leopards. Emerg. Infect. Dis. 2004, 10:2189-2191.
17. Korteweg C., Gu J. Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 2008, 172:1155-1170.
18. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008, 9:299-306.
19. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔCT method. Methods 2001, 25:402.
20. Monrad S., Killen P., Anderson M., Bradke A., Kaplan M. The role of aldosterone blockade in murine lupus nephritis. Arthritis Res. Ther. 2008, 10:R5.
21. Monteerarat Y., Sakabe S., Ngamurulert S., Srichatraphimuk S., Jiamtom W., Chaichuen K., Thitithanyanont A., Permpikul P., Songserm T., Puthavathana P., Nidom C., Mai L., Iwatsuki-Horimoto K., Kawaoka Y., Auewarakul P. Induction of TNF-alpha in human macrophages by avian and human influenza viruses. Arch. Virol. 2010, 155:1273-1279.
22. Ng A.K.-L., Zhang H., Tan K., Li Z., Liu J.-H., Chan P.K.-S., Li S.-M., Chan W.-Y., Au S.W.-N., Joachimiak A., Walz T., Wang J.-H., Shaw P.-C. Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J. 2008, 22:3638-3647.
23. Peiris J., Yu W., Leung C., Cheung C., Ng W., Nicholls J., Ng T., Chan K., Lai S., Lim W., Yuen K., Guan Y. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 2004, 21:617-619.
24. Perrone L.A., Plowden J.K., García-Sastre A., Katz J.M., Tumpey T.M. 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.
25. Reed L., Muench H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 1938, 27:493-497.
26. Salomon R., Hoffmann E., Webster R.G. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc. Natl Acad. Sci. USA 2007, 104:12479-12481.
27. Satoh J. Interferon -beta therapy in multiple sclerosis. Nippon Rinsho 2006, 64:1297-1309.
28. Shapiro A.M., Jack C.S., Lapierre Y., Arbour N., Bar-Or A., Antel J.P. Potential for interferon beta-induced serum antibodies in multiple sclerosis to inhibit endogenous interferon-regulated chemokine/cytokine responses within the central nervous system. Arch. Neurol. 2006, 63:1296-1299.
29. Siengsanan J., Chaichoune K., Phonaknguen R., Sariya L., Prompiram P., Kocharin W., Tangsudjai S., Suwanpukdee S., Wiriyarat W., Pattanarangsan R., Robertson I., Blacksell S.D., Ratanakorn P. Comparison of outbreaks of H5N1 highly pathogenic avian influenza in wild birds and poultry in Thailand. J. Wildl. Dis. 2009, 45:740-747.
30. Smits S.L., de Lang A., van den Brand J.M.A., Leijten L.M., van Ijcken W.F., Eijkemans M.J.C., van Amerongen G., Kuiken T., Andeweg A.C., Osterhaus A.D.M.E., Haagmans B.L. Exacerbated innate host response to SARS-CoV in aged non-human primates. PLoS Pathog. 2010, 6:e1000756.
31. Songserm T., Amonsin A., Jam-on R., Sae-Heng N., Meemak N., Pariyothorn N., Payungporn S., Theamboonlers A., Poovorawan Y. Avian influenza H5N1 in naturally infected domestic cat. Emerg. Infect. Dis. 2006, 12:681-683.
32. Songserm T., Amonsin A., Jam-on R., Sae-Heng N., Pariyothorn N., Payungporn S., Theamboonlers A., Chutinimitkul S., Thanawongnuwech R., Poovorawan Y. Fatal avian influenza A H5N1 in a dog. Emerg. Infect. Dis. 2006, 12:1744-1747.
33. Tarendeau F., Crepin T., Guilligay D., Ruigrok R.W.H., Cusack S., Hart D.J. Host determinant residue lysine 627 lies on the surface of a discrete, folded domain of influenza virus polymerase PB2 subunit. PLoS Pathog. 2008, 4:e1000136.
34. Terrazzino S., Bauleo A., Baldan A., Leon A. Peripheral LPS administrations up-regulate Fas and FasL on brain microglial cells: a brain protective or pathogenic event?. J. Neuroimmunol. 2002, 124:45-53.
35. The Writing Committee of the World Health Organization Consultation on Human Influenza Avian Influenza A (H5N1) Infection in Humans. N. Engl. J. Med. 2005, 353:1374-1385.
36. Tiensin T., Chaitaweesub P., Songserm T., Chaisingh A., Hoonsuwan W., Buranathai C., Parakamawongsa T., Premashthira S., Amonsin A., Gilbert M., Nielen M., Stegeman A. Highly pathogenic avian influenza H5N1, Thailand, 2004. Emerg. Infect. Dis. 2005, 11:1664-1672.
37. Tumpey T.M., Lu X., Morken T., Zaki S.R., Katz J.M. Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (H5N1) virus isolated from humans. J. Virol. 2000, 74:6105-6116.
38. Uchida Y., Chaichoune K., Wiriyarat W., Watanabe C., Hayashi T., Patchimasiri T., Nuansrichay B., Parchariyanon S., Okamatsu M., Tsukamoto K., Takemae N., Ratanakorn P., Yamaguchi S., Saito T. Molecular epidemiological analysis of highly pathogenic avian influenza H5N1 subtype isolated from poultry and wild bird in Thailand. Virus Res. 2008, 138:70-80.
39. Uiprasertkul M., Kitphati R., Puthavathana P., Kriwong R., Kongchanagul A., Ungchusak K., Angkasekwinai S., Chokephaibulkit K., Srisook K., Vanprapar N., Auewarakul P. Apoptosis and pathogenesis of avian influenza A (H5N1) virus in humans. Emerg. Infect. Dis. 2007, 13:708-712.
40. Wang G., Zhang J., Li W., Xin G., Su Y., Gao Y., Zhang H., Lin G., Jiao X., Li K. Apoptosis and proinflammatory cytokine responses of primary mouse microglia and astrocytes induced by human H1N1 and avian H5N1 influenza viruses. Cell. Mol. Immunol. 2008, 5:113.
41. Xu T., Qiao J., Zhao L., Wang G., He G., Li K., Tian Y., Gao M., Wang J., Wang H., Dong C. Acute respiratory distress syndrome induced by avian influenza A (H5N1) virus in mice. Am. J. Respir. Crit. Care Med. 2006, 174:1011-1017.
42. Zaheer A., Sahu S.K., Wu Y., Zaheer A., Haas J., Lee K., Yang B. Diminished cytokine and chemokine expression in the central nervous system of GMF-deficient mice with experimental autoimmune encephalomyelitis. Brain Res. 2007, 1144:239-247.
43. Zhang J., Li Y., Zheng X., Gao Q., Liu Z., Qu R., Borneman J., Elias S.B., Chopp M. Bone marrow stromal cells protect oligodendrocytes from oxygen-glucose deprivation injury. J. Neurosci. Res. 2008, 86:1501-1510.
44. Zhou J.-Y., Shen H.-G., Chen H.-X., Tong G.-Z., Liao M., Yang H.-C., Liu J.-X. Characterization of a highly pathogenic H5N1 influenza virus derived from bar-headed geese in China. J. Gen. Virol. 2006, 87:1823-1833.