Skip to main content
Top
Published in: Medical Microbiology and Immunology 4/2007

01-12-2007 | Review

The threat of avian influenza a (H5N1): part II: Clues to pathogenicity and pathology

Authors: Jindrich Cinatl Jr, Martin Michaelis, Hans W. Doerr

Published in: Medical Microbiology and Immunology | Issue 4/2007

Login to get access

Abstract

Among emerging and re-emerging infectious diseases, influenza constitutes one of the major threats to mankind. In this review series epidemiologic, virologic and pathologic concerns raised by infections of humans with avian influenza virus A/H5N1 are discussed. The second part focuses on experimental and clinical results, which give insights in the pathogenic mechanisms of H5N1 infection in humans. H5N1 is poorly transmitted to humans. However, H5N1-induced disease is very severe. More information on the role entry barriers, H5N1 target cells and on H5N1-induced modulation of the host immune response is needed to learn more about the determinants of H5N1 pathogenicity.
Literature
1.
go back to reference Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, Shortridge KF, Cheung PT, To WK, Ho ET, Sung R, Cheng AF (1998) Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467–471PubMedCrossRef Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, Shortridge KF, Cheung PT, To WK, Ho ET, Sung R, Cheng AF (1998) Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467–471PubMedCrossRef
2.
go back to reference Chan PK (2002) Outbreak of avian influenza A (H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 34(Suppl 2):S58–S64PubMedCrossRef Chan PK (2002) Outbreak of avian influenza A (H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 34(Suppl 2):S58–S64PubMedCrossRef
3.
go back to reference Cinatl J Jr, Michaelis M, Doerr HW (2007) The threat of avian influenza A (H5N1) Part I: epidemiologic concerns and virulence determinants. Med Microbiol Immunol [Epub ahead of print] Cinatl J Jr, Michaelis M, Doerr HW (2007) The threat of avian influenza A (H5N1) Part I: epidemiologic concerns and virulence determinants. Med Microbiol Immunol [Epub ahead of print]
4.
go back to reference Webster RG, Govorkova EA (2006) H5N1 influenza- continuing evolurion and spread. N Engl J Med 335:2174–2177CrossRef Webster RG, Govorkova EA (2006) H5N1 influenza- continuing evolurion and spread. N Engl J Med 335:2174–2177CrossRef
5.
go back to reference de Jong MD, Bach VC, Phan TQ, Vo MH, Tran TT, Nguyen BH, Beld M, Le TP, Truong HK, Nguyen VV, Tran TH, Do QH, Farrar J (2005) Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N Engl J Med 352:686–691PubMedCrossRef de Jong MD, Bach VC, Phan TQ, Vo MH, Tran TT, Nguyen BH, Beld M, Le TP, Truong HK, Nguyen VV, Tran TH, Do QH, Farrar J (2005) Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N Engl J Med 352:686–691PubMedCrossRef
6.
go back to reference Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P (2005) Influenza A H5N1 replication sites in humans. Emerg Infect Dis 11:1036–1041PubMed Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P (2005) Influenza A H5N1 replication sites in humans. Emerg Infect Dis 11:1036–1041PubMed
7.
go back to reference Writing Committee of the World Health Organization (WHO) Consultation on Human Influenza A/H5 (2005) Avian influenza A (H5N1) infection in humans. N Engl J Med 353:1374–1385 Writing Committee of the World Health Organization (WHO) Consultation on Human Influenza A/H5 (2005) Avian influenza A (H5N1) infection in humans. N Engl J Med 353:1374–1385
8.
go back to reference To KF, Chan PK, Chan KF, Lee WK, Lam WY, Wong KF, Tang NL, Tsang DN, Sung RY, Buckley TA, Tam JS, Cheng AF (2001) Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 63:242–246PubMedCrossRef To KF, Chan PK, Chan KF, Lee WK, Lam WY, Wong KF, Tang NL, Tsang DN, Sung RY, Buckley TA, Tam JS, Cheng AF (2001) Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 63:242–246PubMedCrossRef
9.
go back to reference Peiris JS, Yu WC, Leung CW, Cheung CY, Ng WF, Nicholls JM, Ng TK, Chan KH, Lai ST, Lim WL, Yuen KY, Guan Y (2004) Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363:617–619PubMedCrossRef Peiris JS, Yu WC, Leung CW, Cheung CY, Ng WF, Nicholls JM, Ng TK, Chan KH, Lai ST, Lim WL, Yuen KY, Guan Y (2004) Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363:617–619PubMedCrossRef
10.
go back to reference de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203–1207PubMedCrossRef de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203–1207PubMedCrossRef
11.
go back to reference Lamblin G, Degroote S, Perini JM, Delmotte P, Scharfman A, Davril M, Lo-Guidice JM, Houdret N, Dumur V, Klein A, Rousse P (2001) Human airway mucin glycosylation: a combinatory of carbohydrate determinants which vary in cystic fibrosis. Glycoconj J 18:661–684PubMedCrossRef Lamblin G, Degroote S, Perini JM, Delmotte P, Scharfman A, Davril M, Lo-Guidice JM, Houdret N, Dumur V, Klein A, Rousse P (2001) Human airway mucin glycosylation: a combinatory of carbohydrate determinants which vary in cystic fibrosis. Glycoconj J 18:661–684PubMedCrossRef
12.
go back to reference Snyder MH, London WT, Tierney EL, Maassab HF, Murphy BR (1986) Restricted replication of a cold-adapted reassortant influenza A virus in the lower respiratory tract of chimpanzees. J Infect Dis 154:370–371PubMed Snyder MH, London WT, Tierney EL, Maassab HF, Murphy BR (1986) Restricted replication of a cold-adapted reassortant influenza A virus in the lower respiratory tract of chimpanzees. J Infect Dis 154:370–371PubMed
13.
go back to reference Subbarao K, Webster RG, Kawaoka Y, Murphy BR (1995) Are there alternative avian influenza viruses for generation of stable attenuated avian-human influenza A reassortant viruses? Virus Res 39:105–118PubMedCrossRef Subbarao K, Webster RG, Kawaoka Y, Murphy BR (1995) Are there alternative avian influenza viruses for generation of stable attenuated avian-human influenza A reassortant viruses? Virus Res 39:105–118PubMedCrossRef
14.
go back to reference Gagneux P, Cheriyan M, Hurtado-Ziola N, van der Linden EC, Anderson D, McClure H, Varki A, Varki NM (2003) Human-specific regulation of alpha 2-6-linked sialic acids. J Biol Chem 278:48245–48250PubMedCrossRef Gagneux P, Cheriyan M, Hurtado-Ziola N, van der Linden EC, Anderson D, McClure H, Varki A, Varki NM (2003) Human-specific regulation of alpha 2-6-linked sialic acids. J Biol Chem 278:48245–48250PubMedCrossRef
15.
go back to reference Olofsson S, Kumlin U, Dimock K, Arnberg N (2005) Avian influenza and sialic acid receptors: more than meets the eye? Lancet Infect Dis 5:184–188PubMed Olofsson S, Kumlin U, Dimock K, Arnberg N (2005) Avian influenza and sialic acid receptors: more than meets the eye? Lancet Infect Dis 5:184–188PubMed
16.
go back to reference Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD (2004) Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J Virol 78:12665–12667PubMedCrossRef Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD (2004) Neuraminidase is important for the initiation of influenza virus infection in human airway epithelium. J Virol 78:12665–12667PubMedCrossRef
18.
go back to reference Colman PM (1994) Influenza virus neuraminidase: structure, antibodies, and inhibitors. Protein Sci 3:1687–1696PubMedCrossRef Colman PM (1994) Influenza virus neuraminidase: structure, antibodies, and inhibitors. Protein Sci 3:1687–1696PubMedCrossRef
19.
go back to reference Bhatia A, Kast RE (2007) How influenza’s neuraminidase promotes virulence and creates localize lung mucosa immunodeficiency. Cell Mol Biol Lett 12:111–119PubMedCrossRef Bhatia A, Kast RE (2007) How influenza’s neuraminidase promotes virulence and creates localize lung mucosa immunodeficiency. Cell Mol Biol Lett 12:111–119PubMedCrossRef
20.
go back to reference Gong J, Xu W, Zhang J (2007) Structure and functions of influenza virus neuraminidase. Curr Med Chem 14:113–122PubMedCrossRef Gong J, Xu W, Zhang J (2007) Structure and functions of influenza virus neuraminidase. Curr Med Chem 14:113–122PubMedCrossRef
21.
go back to reference Kash JC, Basler CF, Garcia-Sastre A, Carter V, Billharz R, Swayne DE, Przygodzki RM, Taubenberger JK, Katze MG, Tumpey TM (2004) Global host immune response: pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J Virol 78:9499–9511PubMedCrossRef Kash JC, Basler CF, Garcia-Sastre A, Carter V, Billharz R, Swayne DE, Przygodzki RM, Taubenberger JK, Katze MG, Tumpey TM (2004) Global host immune response: pathogenesis and transcriptional profiling of type A influenza viruses expressing the hemagglutinin and neuraminidase genes from the 1918 pandemic virus. J Virol 78:9499–9511PubMedCrossRef
22.
go back to reference Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, Suzuki H, Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y (2004) Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703–707PubMedCrossRef Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, Suzuki H, Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y (2004) Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703–707PubMedCrossRef
23.
go back to reference Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solorzano A, Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P, Garcia-Sastre A (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77–80PubMedCrossRef Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solorzano A, Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P, Garcia-Sastre A (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77–80PubMedCrossRef
24.
go back to reference Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, Rakestraw KM, Webster RG, Hoffmann E, Krauss S, Zheng J, Zhang Z, Naeve CW (2006) Large-scale sequence analysis of avian influenza isolates. Science 311:1576–1580PubMedCrossRef Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, Rakestraw KM, Webster RG, Hoffmann E, Krauss S, Zheng J, Zhang Z, Naeve CW (2006) Large-scale sequence analysis of avian influenza isolates. Science 311:1576–1580PubMedCrossRef
25.
go back to reference Matrosovich M, Zhou N, Kawaoka Y, Webster R (1999) The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 73:1146–1155PubMed Matrosovich M, Zhou N, Kawaoka Y, Webster R (1999) The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 73:1146–1155PubMed
26.
go back to reference Wang QZ, Long JX, Hu SL, Wu YT, Liu XF (2006) Biological significance of amino acids deletion in NA stalk of H5N1 avain influenza virus [Article in Chinese]. Wei Sheng Wu Xue Bao 46:542–546PubMed Wang QZ, Long JX, Hu SL, Wu YT, Liu XF (2006) Biological significance of amino acids deletion in NA stalk of H5N1 avain influenza virus [Article in Chinese]. Wei Sheng Wu Xue Bao 46:542–546PubMed
27.
go back to reference Hartshorn KL, White MR, Tecle T, Holmskov U, Crouch EC (2006) Innate defense against influenza A virus: activity of human neutrophil defensins and interactions of defensins with surfactant protein D. J Immunol 176:6962–6972PubMed Hartshorn KL, White MR, Tecle T, Holmskov U, Crouch EC (2006) Innate defense against influenza A virus: activity of human neutrophil defensins and interactions of defensins with surfactant protein D. J Immunol 176:6962–6972PubMed
28.
go back to reference Hartshorn KL, White MR, Tecle T, Tornoe I, Sorensen GL, Crouch EC, Holmskov U (2007) Reduced influenza viral neutralizing activity of natural human trimers of surfactant protein D. Respir Res 8:9PubMedCrossRef Hartshorn KL, White MR, Tecle T, Tornoe I, Sorensen GL, Crouch EC, Holmskov U (2007) Reduced influenza viral neutralizing activity of natural human trimers of surfactant protein D. Respir Res 8:9PubMedCrossRef
29.
go back to reference Wright PF, Webster RG (2001) Othomyxoviruses. In: Knipe DM, Howley PM (eds) Fields virology. Lippincott & Wilkins, Philadelphia, pp 1533–1579 Wright PF, Webster RG (2001) Othomyxoviruses. In: Knipe DM, Howley PM (eds) Fields virology. Lippincott & Wilkins, Philadelphia, pp 1533–1579
30.
go back to reference Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y (2006) Avian flu: influenza virus receptors in the human airway. Nature 440:435–436PubMedCrossRef Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y (2006) Avian flu: influenza virus receptors in the human airway. Nature 440:435–436PubMedCrossRef
31.
go back to reference van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T (2006) H5N1 virus attachment to lower respiratory tract. Science 312:399PubMedCrossRef van Riel D, Munster VJ, de Wit E, Rimmelzwaan GF, Fouchier RA, Osterhaus AD, Kuiken T (2006) H5N1 virus attachment to lower respiratory tract. Science 312:399PubMedCrossRef
32.
go back to reference Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RA, Osterhaus AD, Kuiken T (2006) Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol 168:176–183PubMedCrossRef Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RA, Osterhaus AD, Kuiken T (2006) Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol 168:176–183PubMedCrossRef
33.
go back to reference Songsermn T, Amonsin A, Jam-on R, Sae-Heng N, Meemak N, Pariyothorn N, Payungporn S, Theamboonlers A, Poovorawan Y (2006) Avian influenza H5N1 in naturally infected domestic cat. Emerg Infect Dis 12:681–683PubMed Songsermn T, Amonsin A, Jam-on R, Sae-Heng N, Meemak N, Pariyothorn N, Payungporn S, Theamboonlers A, Poovorawan Y (2006) Avian influenza H5N1 in naturally infected domestic cat. Emerg Infect Dis 12:681–683PubMed
34.
go back to reference Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG, Holtzman MJ, Brody SL (2006) Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol 80:7469–7480PubMedCrossRef Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG, Holtzman MJ, Brody SL (2006) Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol 80:7469–7480PubMedCrossRef
35.
go back to reference Maines TR, Lu XH, Erb SM, Edwards L, Guarner J, Greer PW, Nguyen DC, Szretter KJ, Chen LM, Thawatsupha P, Chittaganpitch M, Waicharoen S, Nguyen DT, Nguyen T, Nguyen HH, Kim JH, Hoang LT, Kang C, Phuong LS, Lim W, Zaki S, Donis RO, Cox NJ, Katz JM, Tumpey TM (2005) Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J Virol 79:11788–11800PubMedCrossRef Maines TR, Lu XH, Erb SM, Edwards L, Guarner J, Greer PW, Nguyen DC, Szretter KJ, Chen LM, Thawatsupha P, Chittaganpitch M, Waicharoen S, Nguyen DT, Nguyen T, Nguyen HH, Kim JH, Hoang LT, Kang C, Phuong LS, Lim W, Zaki S, Donis RO, Cox NJ, Katz JM, Tumpey TM (2005) Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J Virol 79:11788–11800PubMedCrossRef
36.
go back to reference Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ (2004) The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838–1842PubMedCrossRef Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ (2004) The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838–1842PubMedCrossRef
37.
go back to reference Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA (2004) Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866–1870PubMedCrossRef Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA (2004) Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866–1870PubMedCrossRef
38.
go back to reference Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y (2000) Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74:8502–8512PubMedCrossRef Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y (2000) Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74:8502–8512PubMedCrossRef
39.
go back to reference Gambaryan A, Tuzikov A, Pazynina G, Bovin N, Balish A, Klimov A (2006) Evolution of the receptor binding phenotype of influenza A (H5) viruses. Virology 344:432–438PubMedCrossRef Gambaryan A, Tuzikov A, Pazynina G, Bovin N, Balish A, Klimov A (2006) Evolution of the receptor binding phenotype of influenza A (H5) viruses. Virology 344:432–438PubMedCrossRef
40.
go back to reference Horimoto T, Kawaoka Y (2005) Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3:591–600PubMedCrossRef Horimoto T, Kawaoka Y (2005) Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3:591–600PubMedCrossRef
41.
go back to reference Maines TR, Chen LM, Matsuoka Y, Chen H, Rowe T, Ortin J, Falcon A, Nguyen TH, Mai le Q, Sedyaningsih ER, Harun S, Tumpey TM, Donis RO, Cox NJ, Subbarao K, Katz JM (2006) Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci USA 103:12121–12126PubMedCrossRef Maines TR, Chen LM, Matsuoka Y, Chen H, Rowe T, Ortin J, Falcon A, Nguyen TH, Mai le Q, Sedyaningsih ER, Harun S, Tumpey TM, Donis RO, Cox NJ, Subbarao K, Katz JM (2006) Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci USA 103:12121–12126PubMedCrossRef
42.
go back to reference Nicholls JM, Chan MC, Chan WY, Wong HK, Cheung CY, Kwong DL, Wong MP, Chui WH, Poon LL, Tsao SW, Guan Y, Peiris JS (2007) Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med 13:147–149PubMedCrossRef Nicholls JM, Chan MC, Chan WY, Wong HK, Cheung CY, Kwong DL, Wong MP, Chui WH, Poon LL, Tsao SW, Guan Y, Peiris JS (2007) Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med 13:147–149PubMedCrossRef
43.
go back to reference Flint SJ, Enquist LW, Racaniello VR, Skalka AM (2004) Principles of virology. Molecular biology, pathogenesis, and control animal viruses, 2nd edn. ASM Press, Washington, DC, USA Flint SJ, Enquist LW, Racaniello VR, Skalka AM (2004) Principles of virology. Molecular biology, pathogenesis, and control animal viruses, 2nd edn. ASM Press, Washington, DC, USA
44.
go back to reference Park CH, Ishinaka M, Takada A, Kida H, Kimura T, Ochiai K, Umemura T (2002) The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1) influenza virus into the central nervous system after respiratory infection in mice. Arch Virol 147:1425–1436PubMedCrossRef Park CH, Ishinaka M, Takada A, Kida H, Kimura T, Ochiai K, Umemura T (2002) The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1) influenza virus into the central nervous system after respiratory infection in mice. Arch Virol 147:1425–1436PubMedCrossRef
45.
go back to reference Ng WF, To KF, Lam WW, Ng TK, Lee KC (2006) The comparative pathology of severe acute respiratory syndrome and avian influenza A subtype H5N1—a review. Hum Pathol 37:381–390PubMedCrossRef Ng WF, To KF, Lam WW, Ng TK, Lee KC (2006) The comparative pathology of severe acute respiratory syndrome and avian influenza A subtype H5N1—a review. Hum Pathol 37:381–390PubMedCrossRef
46.
go back to reference Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E (2005) Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191–2198PubMedCrossRef Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E (2005) Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191–2198PubMedCrossRef
47.
go back to reference Yen HL, Monto AS, Webster RG, Govorkova EA (2005) Virulence may determine the necessary duration and dosage of oseltamivir treatment for highly pathogenic A/Vietnam/1203/04 influenza virus in mice. J Infect Dis 192:665–672PubMedCrossRef Yen HL, Monto AS, Webster RG, Govorkova EA (2005) Virulence may determine the necessary duration and dosage of oseltamivir treatment for highly pathogenic A/Vietnam/1203/04 influenza virus in mice. J Infect Dis 192:665–672PubMedCrossRef
48.
go back to reference de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J (2006)Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203–1207PubMedCrossRef de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J (2006)Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203–1207PubMedCrossRef
50.
go back to reference Hsieh SM, Chang SC (2006) Insufficient perforin expression in CD8+ T cells in response to hemagglutinin from avian influenza (H5N1) virus. J Immunol 176:4530–4533PubMed Hsieh SM, Chang SC (2006) Insufficient perforin expression in CD8+ T cells in response to hemagglutinin from avian influenza (H5N1) virus. J Immunol 176:4530–4533PubMed
51.
go back to reference Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O (2001) Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 31:2680–2689PubMedCrossRef Arnon TI, Lev M, Katz G, Chernobrov Y, Porgador A, Mandelboim O (2001) Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur J Immunol 31:2680–2689PubMedCrossRef
52.
go back to reference Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A (2001) Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409:1055–1060PubMedCrossRef Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, Davis DM, Strominger JL, Yewdell JW, Porgador A (2001) Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409:1055–1060PubMedCrossRef
53.
go back to reference Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E, Zakay-Rones Z, Porgador A, Mandelboim O (2006) Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol 7:517–523PubMedCrossRef Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E, Zakay-Rones Z, Porgador A, Mandelboim O (2006) Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol 7:517–523PubMedCrossRef
54.
go back to reference Siren J, Sareneva T, Pirhonen J, Strengell M, Veckman V, Julkunen I, Matikainen S (2004) Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J Gen Virol 85:2357–2364PubMedCrossRef Siren J, Sareneva T, Pirhonen J, Strengell M, Veckman V, Julkunen I, Matikainen S (2004) Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J Gen Virol 85:2357–2364PubMedCrossRef
55.
go back to reference Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, Cosman D, Moretta A, Valiante NM, Parham P (2007) NKp46 and NKG2D recognition of infected iendritic cells is necessary for NK cell activation in the human response to influenza infection. J Immunol 178:2688–2698PubMed Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, Cosman D, Moretta A, Valiante NM, Parham P (2007) NKp46 and NKG2D recognition of infected iendritic cells is necessary for NK cell activation in the human response to influenza infection. J Immunol 178:2688–2698PubMed
56.
go back to reference Piqueras B, Connolly J, Freitas H, Palucka AK, Banchereau J (2006) Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107:2613–2618PubMedCrossRef Piqueras B, Connolly J, Freitas H, Palucka AK, Banchereau J (2006) Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107:2613–2618PubMedCrossRef
57.
go back to reference Ennis FA, Meager A, Beare AS, Qi YH, Riley D, Schwarz G, Schild GC, Rook AH (1981) Interferon induction and increased natural killer-cell activity in influenza infections in man. Lancet 24:891–893CrossRef Ennis FA, Meager A, Beare AS, Qi YH, Riley D, Schwarz G, Schild GC, Rook AH (1981) Interferon induction and increased natural killer-cell activity in influenza infections in man. Lancet 24:891–893CrossRef
58.
go back to reference Lewis DE, Gilbert BE, Knight V (1986) Influenza virus infection induces functional alterations in peripheral blood lymphocytes. J Immunol 137:3777–3781PubMed Lewis DE, Gilbert BE, Knight V (1986) Influenza virus infection induces functional alterations in peripheral blood lymphocytes. J Immunol 137:3777–3781PubMed
59.
go back to reference Fernandez-Sesma A, Marukian S, Ebersole BJ, Kaminski D, Park MS, Yuen T, Sealfon SC, Garcia-Sastre A, Moran TM (2006) Influenza virus evades innate and adaptive immunity via the NS1 protein. J Virol 80:6295–6304PubMedCrossRef Fernandez-Sesma A, Marukian S, Ebersole BJ, Kaminski D, Park MS, Yuen T, Sealfon SC, Garcia-Sastre A, Moran TM (2006) Influenza virus evades innate and adaptive immunity via the NS1 protein. J Virol 80:6295–6304PubMedCrossRef
60.
go back to reference Seo SH, Hoffmann E, Webster RG (2002) Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8:950–954PubMedCrossRef Seo SH, Hoffmann E, Webster RG (2002) Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8:950–954PubMedCrossRef
61.
go back to reference Seo SH, Hoffmann E, Webster RG (2004) The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine sponses. Virus Res 103:107–113PubMedCrossRef Seo SH, Hoffmann E, Webster RG (2004) The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine sponses. Virus Res 103:107–113PubMedCrossRef
62.
go back to reference García-Sastre A (2006) Antiviral response in pandemic influenza viruses. Emerg Infect Dis 12:44–49PubMed García-Sastre A (2006) Antiviral response in pandemic influenza viruses. Emerg Infect Dis 12:44–49PubMed
63.
go back to reference Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF, Gordon S, Guan Y, Peiris JS (2002) Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360:1831–1837PubMedCrossRef Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF, Gordon S, Guan Y, Peiris JS (2002) Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360:1831–1837PubMedCrossRef
64.
go back to reference Zhou J, Law HK, Cheung CY, Ng IH, Peiris JS, Lau YL (2006) Differential expression of chemokines and their receptors in adult and neonatal macrophages infected with human or avian influenza viruses. J Infect Dis 194:61–70PubMedCrossRef Zhou J, Law HK, Cheung CY, Ng IH, Peiris JS, Lau YL (2006) Differential expression of chemokines and their receptors in adult and neonatal macrophages infected with human or avian influenza viruses. J Infect Dis 194:61–70PubMedCrossRef
65.
go back to reference Szretter KJ, Gangappa S, Lu X, Smith C, Shieh WJ, Zaki SR, Sambhara S, Tumpey TM, Katz JM (2007) Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J Virol 81:2736–2744PubMedCrossRef Szretter KJ, Gangappa S, Lu X, Smith C, Shieh WJ, Zaki SR, Sambhara S, Tumpey TM, Katz JM (2007) Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J Virol 81:2736–2744PubMedCrossRef
66.
go back to reference Lee DC, Cheung CY, Law AH, Mok CK, Peiris M, Lau AS (2005) p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol 79:10147–10154PubMedCrossRef Lee DC, Cheung CY, Law AH, Mok CK, Peiris M, Lau AS (2005) p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol 79:10147–10154PubMedCrossRef
67.
go back to reference Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, Lipatov AS, Chan KH, Sturm-Ramirez KM, Cheung CL, Leung YH, Yuen KY, Webster RG, Peiris JS (2004) H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci USA 101:8156–8161PubMedCrossRef Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, Lipatov AS, Chan KH, Sturm-Ramirez KM, Cheung CL, Leung YH, Yuen KY, Webster RG, Peiris JS (2004) H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci USA 101:8156–8161PubMedCrossRef
68.
go back to reference Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, Chan YO, Chan RW, Long HT, Poon LL, Guan Y, Peiris JS (2005) Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir Res 6:135PubMedCrossRef Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, Chan YO, Chan RW, Long HT, Poon LL, Guan Y, Peiris JS (2005) Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir Res 6:135PubMedCrossRef
69.
go back to reference Zhou J, Law HK, Cheung CY, Ng IH, Peiris JS, Lau YL (2006) Functional tumor necrosis factor-related apoptosis-inducing ligand production by avian influenza virus-infected macrophages. J Infect Dis 193:945–953PubMedCrossRef Zhou J, Law HK, Cheung CY, Ng IH, Peiris JS, Lau YL (2006) Functional tumor necrosis factor-related apoptosis-inducing ligand production by avian influenza virus-infected macrophages. J Infect Dis 193:945–953PubMedCrossRef
70.
71.
go back to reference Henter JI, Chow CB, Leung CW, Lau YL (2006) Cytotoxic therapy for severe avian influenza A (H5N1) infection. Lancet 367:870–873PubMedCrossRef Henter JI, Chow CB, Leung CW, Lau YL (2006) Cytotoxic therapy for severe avian influenza A (H5N1) infection. Lancet 367:870–873PubMedCrossRef
72.
go back to reference Chokephaibulkit K, Uiprasertkul M, Puthavathana P, Chearskul P, Auewarakul P, Dowell SF, Vanprapar N (2005) A child with avian influenza A (H5N1) infection. Pediatr Infect Dis J 24:162–166PubMedCrossRef Chokephaibulkit K, Uiprasertkul M, Puthavathana P, Chearskul P, Auewarakul P, Dowell SF, Vanprapar N (2005) A child with avian influenza A (H5N1) infection. Pediatr Infect Dis J 24:162–166PubMedCrossRef
73.
go back to reference Verbsky JW, Grossman WJ (2006) Hemophagocytic lymphohistiocytosis: diagnosis, pathophysiology, treatment, and future perspectives. Ann Med 38:20–31PubMedCrossRef Verbsky JW, Grossman WJ (2006) Hemophagocytic lymphohistiocytosis: diagnosis, pathophysiology, treatment, and future perspectives. Ann Med 38:20–31PubMedCrossRef
74.
go back to reference Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, Nguyen VC, Pham TS, Vo CD, Le TQ, Ngo TT, Dao BK, Le PP, Nguyen TT, Hoang TL, Cao VT, Le TG, Nguyen DT, Le HN, Nguyen KT, Le HS, Le VT, Christiane D, Tran TT, Menno de J, Schultsz C, Cheng P, Lim W, Horby P, Farrar J; World Health Organization International Avian Influenza Investigative Team (2004) Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 350:1179–1188 Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, Nguyen VC, Pham TS, Vo CD, Le TQ, Ngo TT, Dao BK, Le PP, Nguyen TT, Hoang TL, Cao VT, Le TG, Nguyen DT, Le HN, Nguyen KT, Le HS, Le VT, Christiane D, Tran TT, Menno de J, Schultsz C, Cheng P, Lim W, Horby P, Farrar J; World Health Organization International Avian Influenza Investigative Team (2004) Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 350:1179–1188
75.
go back to reference 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 SF (2005) Human disease from influenza A (H5N1), Thailand, 2004. Emerg Infect Dis 11:201–209PubMed 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 SF (2005) Human disease from influenza A (H5N1), Thailand, 2004. Emerg Infect Dis 11:201–209PubMed
76.
go back to reference Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen DPH, Hadisoedarsuno W, Purba W, Santoso H, Septiawati C, Tresnaningsih E, Heriyanto B, Yuwono D, Harun S, Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen, Hadisoedarsuno W, Purba W, Santoso H, Septiawati C, Tresnaningsih E, Heriyanto B, Yuwono D, Harun S, Soeroso S, Giriputra S, Blair PJ, Jeremijenko A, Kosasih H, Putnam SD, Samaan G, Silitonga M, Chan KH, Poon LL, Lim W, Klimov A, Lindstrom S, Guan Y, Donis R, Katz J, Cox N, Peiris M, Uyeki TM (2006) Three Indonesian clusters of H5N1 virus infection in 2005. N Engl J Med 355:2186–2194PubMedCrossRef Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen DPH, Hadisoedarsuno W, Purba W, Santoso H, Septiawati C, Tresnaningsih E, Heriyanto B, Yuwono D, Harun S, Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen, Hadisoedarsuno W, Purba W, Santoso H, Septiawati C, Tresnaningsih E, Heriyanto B, Yuwono D, Harun S, Soeroso S, Giriputra S, Blair PJ, Jeremijenko A, Kosasih H, Putnam SD, Samaan G, Silitonga M, Chan KH, Poon LL, Lim W, Klimov A, Lindstrom S, Guan Y, Donis R, Katz J, Cox N, Peiris M, Uyeki TM (2006) Three Indonesian clusters of H5N1 virus infection in 2005. N Engl J Med 355:2186–2194PubMedCrossRef
77.
go back to reference Oner AF, Bay A, Arslan S, Akdeniz H, Sahin HA, Cesur Y, Epcacan S, Yilmaz N, Deger I, Kizilyildiz B, Karsen H, Ceyhan M (2006) Avian influenza A (H5N1) infection in eastern Turkey in 2006. N Engl J Med 355:2179–2185PubMedCrossRef Oner AF, Bay A, Arslan S, Akdeniz H, Sahin HA, Cesur Y, Epcacan S, Yilmaz N, Deger I, Kizilyildiz B, Karsen H, Ceyhan M (2006) Avian influenza A (H5N1) infection in eastern Turkey in 2006. N Engl J Med 355:2179–2185PubMedCrossRef
78.
go back to reference Nebeshima S, Murata M, Kikuchi K, Ikematsu H, Kashiwagi S, Hayashi J (2002) A reduction in the number of peripheral CD28+CD8+ T cells in the acute pahse of influenza. Clin Exp Immunol 128:339–346CrossRef Nebeshima S, Murata M, Kikuchi K, Ikematsu H, Kashiwagi S, Hayashi J (2002) A reduction in the number of peripheral CD28+CD8+ T cells in the acute pahse of influenza. Clin Exp Immunol 128:339–346CrossRef
79.
go back to reference Ludwig S, Pleschka S, Planz O, Wolff T (2006) Ringing the alarm bells: signalling and apoptosis in influenza virus infected cells. Cell Microbiol 8:375–386PubMedCrossRef Ludwig S, Pleschka S, Planz O, Wolff T (2006) Ringing the alarm bells: signalling and apoptosis in influenza virus infected cells. Cell Microbiol 8:375–386PubMedCrossRef
80.
go back to reference Wurzer WJ, Ehrhardt C, Pleschka S, Berberich-Siebelt F, Wolff T, Walczak H, Planz O, Ludwig S (2004) NF-kappaB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J Biol Chem 279:30931–30937PubMedCrossRef Wurzer WJ, Ehrhardt C, Pleschka S, Berberich-Siebelt F, Wolff T, Walczak H, Planz O, Ludwig S (2004) NF-kappaB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J Biol Chem 279:30931–30937PubMedCrossRef
81.
go back to reference Tyner JW, Uchida O, Kajiwara N, Kim EY, Patel AC, O’Sullivan MP, Walter MJ, Schwendener RA, Cook DN, Danoff TM, Holtzman MJ (2005) CCL5-CCR5 interaction provides antiapoptotic signals for macrophage survival during viral infection. Nat Med 11:1180–1187PubMedCrossRef Tyner JW, Uchida O, Kajiwara N, Kim EY, Patel AC, O’Sullivan MP, Walter MJ, Schwendener RA, Cook DN, Danoff TM, Holtzman MJ (2005) CCL5-CCR5 interaction provides antiapoptotic signals for macrophage survival during viral infection. Nat Med 11:1180–1187PubMedCrossRef
82.
go back to reference Brydon EW, Smith H, Sweet C (2003) Influenza A virus-induced apoptosis in bronchiolar epithelial (NCI-H292) cells limits pro-inflammatory cytokine release. J Gen Virol 84:2389–2400PubMedCrossRef Brydon EW, Smith H, Sweet C (2003) Influenza A virus-induced apoptosis in bronchiolar epithelial (NCI-H292) cells limits pro-inflammatory cytokine release. J Gen Virol 84:2389–2400PubMedCrossRef
83.
go back to reference Schultz-Cherry S, Dybdahl-Sissoko N, Neumann G, Kawaoka Y, Hinshaw VS (2001) Influenza virus ns1 protein induces apoptosis in cultured cells. J Virol 75:7875–7881PubMedCrossRef Schultz-Cherry S, Dybdahl-Sissoko N, Neumann G, Kawaoka Y, Hinshaw VS (2001) Influenza virus ns1 protein induces apoptosis in cultured cells. J Virol 75:7875–7881PubMedCrossRef
84.
go back to reference Zhirnov OP, Konakova TE, Wolff T, Klenk HD (2002) NS1 protein of influenza A virus down-regulates apoptosis. J Virol 76:1617–1625PubMedCrossRef Zhirnov OP, Konakova TE, Wolff T, Klenk HD (2002) NS1 protein of influenza A virus down-regulates apoptosis. J Virol 76:1617–1625PubMedCrossRef
85.
go back to reference Zhirnov OP, Ksenofontov AL, Kuzmina SG, Klenk HD (2002) Interaction of influenza A virus M1 matrix protein with caspases. Biochemistry (Mosc) 67:534–539CrossRef Zhirnov OP, Ksenofontov AL, Kuzmina SG, Klenk HD (2002) Interaction of influenza A virus M1 matrix protein with caspases. Biochemistry (Mosc) 67:534–539CrossRef
86.
go back to reference Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O’Neill R, Schickli J, Palese P, Henklein P, Bennink JR, Yewdell JW (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312PubMedCrossRef Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O’Neill R, Schickli J, Palese P, Henklein P, Bennink JR, Yewdell JW (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312PubMedCrossRef
87.
go back to reference Zamarin D, Ortigoza MB, Palese P (2006) Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 80:7976–7983PubMedCrossRef Zamarin D, Ortigoza MB, Palese P (2006) Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 80:7976–7983PubMedCrossRef
88.
go back to reference Smith GJ, Naipospos TS, Nguyen TD, de Jong MD, Vijaykrishna D, Usman TB, Hassan SS, Nguyen TV, Dao TV, Bui NA, Leung YH, Cheung CL, Rayner JM, Zhang JX, Zhang LJ, Poon LL, Li KS, Nguyen VC, Hien TT, Farrar J, Webster RG, Chen H, Peiris JS, Guan Y (2006) Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350:258–268PubMedCrossRef Smith GJ, Naipospos TS, Nguyen TD, de Jong MD, Vijaykrishna D, Usman TB, Hassan SS, Nguyen TV, Dao TV, Bui NA, Leung YH, Cheung CL, Rayner JM, Zhang JX, Zhang LJ, Poon LL, Li KS, Nguyen VC, Hien TT, Farrar J, Webster RG, Chen H, Peiris JS, Guan Y (2006) Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350:258–268PubMedCrossRef
89.
go back to reference Zamarin D, Garcia-Sastre A, Xiao X, Wang R, Palese P (2005) Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 1:e4PubMedCrossRef Zamarin D, Garcia-Sastre A, Xiao X, Wang R, Palese P (2005) Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 1:e4PubMedCrossRef
90.
go back to reference Coleman JR (2007) The PB1-F2 protein of Influenza A virus: increasing pathogenicity by disrupting alveolar macrophages. Virol J 4:9PubMedCrossRef Coleman JR (2007) The PB1-F2 protein of Influenza A virus: increasing pathogenicity by disrupting alveolar macrophages. Virol J 4:9PubMedCrossRef
91.
go back to reference Schultz-Cherry S, Hinshaw VS (1996) Influenza virus neuraminidase activates latent transforming growth factor beta. J Virol 70:8624–8629PubMed Schultz-Cherry S, Hinshaw VS (1996) Influenza virus neuraminidase activates latent transforming growth factor beta. J Virol 70:8624–8629PubMed
92.
go back to reference Oxford JS (2000) Influenza A pandemics of the 20th century with special reference to 1918: virology, pathology and epidemiology. Rev Med Virol 10:119–133PubMedCrossRef Oxford JS (2000) Influenza A pandemics of the 20th century with special reference to 1918: virology, pathology and epidemiology. Rev Med Virol 10:119–133PubMedCrossRef
93.
go back to reference Kash JC, Tumpey TM, Proll SC, Carter V, Perwitasari O, Thomas MJ, Basler CF, Palese P, Taubenberger JK, Garcia-Sastre A, Swayne DE, Katze MG (2006) Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443:578–581PubMed Kash JC, Tumpey TM, Proll SC, Carter V, Perwitasari O, Thomas MJ, Basler CF, Palese P, Taubenberger JK, Garcia-Sastre A, Swayne DE, Katze MG (2006) Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443:578–581PubMed
94.
go back to reference Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonti JB, Fernando L, Li Y, Katze MG, Feldmann H, Kawaoka Y (2007) Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319–323PubMedCrossRef Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonti JB, Fernando L, Li Y, Katze MG, Feldmann H, Kawaoka Y (2007) Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319–323PubMedCrossRef
Metadata
Title
The threat of avian influenza a (H5N1): part II: Clues to pathogenicity and pathology
Authors
Jindrich Cinatl Jr
Martin Michaelis
Hans W. Doerr
Publication date
01-12-2007
Publisher
Springer-Verlag
Published in
Medical Microbiology and Immunology / Issue 4/2007
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-007-0045-2

Other articles of this Issue 4/2007

Medical Microbiology and Immunology 4/2007 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.