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Erschienen in: Archives of Virology 6/2010

01.06.2010 | Original Article

Extrapulmonary tissue responses in cynomolgus macaques (Macaca fascicularis) infected with highly pathogenic avian influenza A (H5N1) virus

verfasst von: A.-E. Tolnay, C. R. Baskin, T. M. Tumpey, P. J. Sabourin, C. L. Sabourin, J. P. Long, J. A. Pyles, R. A. Albrecht, A. García-Sastre, M. G. Katze, H. Bielefeldt-Ohmann

Erschienen in: Archives of Virology | Ausgabe 6/2010

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Abstract

The mechanisms responsible for virulence of influenza viruses in humans remain poorly understood. A prevailing hypothesis is that the highly pathogenic virus isolates cause a severe cytokinemia precipitating acute respiratory distress syndrome and multiple organ dysfunction syndrome. Cynomolgus macaques (Macaca fascicularis) infected with a human highly pathogenic avian influenza (HPAI) H5N1 virus isolate (A/Vietnam/1203/2004) or reassortants of human influenza virus A/Texas/36/91 (H1N1) containing genes from the 1918 pandemic influenza A (H1N1) virus developed severe pneumonia within 24 h postinfection. However, virus spread beyond the lungs was only detected in the H5N1 group, and signs of extrapulmonary tissue reactions, including microglia activation and sustained up-regulation of inflammatory markers, most notably hypoxia inducible factor-1α (HIF-1α), were largely limited to this group. Extrapulmonary pathology may thus contribute to the morbidities induced by H5N1 viruses.
Literatur
1.
Zurück zum Zitat Korteweg C, Gu J (2008) Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am J Pathol 272:1155–1170CrossRef Korteweg C, Gu J (2008) Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am J Pathol 272:1155–1170CrossRef
2.
Zurück zum Zitat Taubenberger JK, Morens DM (2008) The pathology of influenza virus infections. Ann Rev Pathol Mech Dis 3:499–522CrossRef Taubenberger JK, Morens DM (2008) The pathology of influenza virus infections. Ann Rev Pathol Mech Dis 3:499–522CrossRef
3.
Zurück zum Zitat Lee N, Wong CK, Chan PK, Lun SW, Lui G, Wong B, Hui DS, Lam CW, Cockram CS, Choi KW, Yeung AC, Tang JW, Sung JJ (2007) Hypercytokinemia and hyperactivation of phospho-p38 mitogen-activated protein kinase in severe human influenza A virus infection. Clin Infect Dis 45:723–731CrossRefPubMed Lee N, Wong CK, Chan PK, Lun SW, Lui G, Wong B, Hui DS, Lam CW, Cockram CS, Choi KW, Yeung AC, Tang JW, Sung JJ (2007) Hypercytokinemia and hyperactivation of phospho-p38 mitogen-activated protein kinase in severe human influenza A virus infection. Clin Infect Dis 45:723–731CrossRefPubMed
4.
Zurück zum Zitat 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. New Engl J Med 352:686–691CrossRefPubMed 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. New Engl J Med 352:686–691CrossRefPubMed
5.
Zurück zum Zitat Gu J, Xie Z, Gao Z, Liu J, Korteweg C, Ye J, Lau LT, Lu J, Gao Z, Zhang B, McNutt MA, Lu M, Anderson VM, Gong E, Yu AC, Lipkin WI (2007) H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370:1137–1145CrossRefPubMed Gu J, Xie Z, Gao Z, Liu J, Korteweg C, Ye J, Lau LT, Lu J, Gao Z, Zhang B, McNutt MA, Lu M, Anderson VM, Gong E, Yu AC, Lipkin WI (2007) H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370:1137–1145CrossRefPubMed
6.
Zurück zum Zitat 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.
Zurück zum Zitat Nakai Y, Itoh M, Mizuguchi M, Ozawa H, Okazaki E, Kobayashi Y, Takahashi M, Ohtani K, Ogawa A, Narita M, Togashi T, Takashima S (2003) Apoptosis and microglial activation in influenza encephalopathy. Acta Neuropathol 105:233–239PubMed Nakai Y, Itoh M, Mizuguchi M, Ozawa H, Okazaki E, Kobayashi Y, Takahashi M, Ohtani K, Ogawa A, Narita M, Togashi T, Takashima S (2003) Apoptosis and microglial activation in influenza encephalopathy. Acta Neuropathol 105:233–239PubMed
8.
Zurück zum Zitat Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buanathai C, Lim W, Webster RG, Hoffman E (2005) Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191–2198CrossRefPubMed Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buanathai C, Lim W, Webster RG, Hoffman E (2005) Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191–2198CrossRefPubMed
9.
Zurück zum Zitat Gubareva LV, McCullers JA, Bethell RC, Webster RG (1998) Characterization of influenza A/Hong Kong/156/97 (H5N1) virus in a mouse model and protective effect of Zanamivir on H5N1 infection in mice. J Infect Dis 178:1592–1596CrossRefPubMed Gubareva LV, McCullers JA, Bethell RC, Webster RG (1998) Characterization of influenza A/Hong Kong/156/97 (H5N1) virus in a mouse model and protective effect of Zanamivir on H5N1 infection in mice. J Infect Dis 178:1592–1596CrossRefPubMed
10.
Zurück zum Zitat 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 79:11788–11800CrossRefPubMed 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 79:11788–11800CrossRefPubMed
11.
Zurück zum Zitat Kuiken T, Rimmelzwaan GF, Van Amerongen G, Osterhaus AD (2003) Pathology of human influenza A (H5N1) virus infection in cynomolgus macaques (Macaca fascicularis). Vet Pathol 40:304–310CrossRefPubMed Kuiken T, Rimmelzwaan GF, Van Amerongen G, Osterhaus AD (2003) Pathology of human influenza A (H5N1) virus infection in cynomolgus macaques (Macaca fascicularis). Vet Pathol 40:304–310CrossRefPubMed
12.
Zurück zum Zitat Rimmelzwaan GF, Kuiken T, van Amerongen G, Bestebroer TM, Fouchier RA, Osterhaus AD (2001) Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol 75:6687–6691CrossRefPubMed Rimmelzwaan GF, Kuiken T, van Amerongen G, Bestebroer TM, Fouchier RA, Osterhaus AD (2001) Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol 75:6687–6691CrossRefPubMed
13.
Zurück zum Zitat 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 168:176–183CrossRefPubMed 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 168:176–183CrossRefPubMed
14.
Zurück zum Zitat Zitzow LA, Rowe T, Morken T, Shieh WJ, Zaki S, Katz JM (2002) Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J Virol 76:4420–4429CrossRefPubMed Zitzow LA, Rowe T, Morken T, Shieh WJ, Zaki S, Katz JM (2002) Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J Virol 76:4420–4429CrossRefPubMed
15.
Zurück zum Zitat 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 312:399CrossRefPubMed 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 312:399CrossRefPubMed
16.
Zurück zum Zitat Chung E, Amrute SB, Abel K, Gupta G, Wang Y, Miller CJ, Fitzgerald-Bocarsly P (2005) Characterization of virus-responsive plasmacytoid dendritic cells in the rhesus macaque. Clin Diagn Lab Immunol 12:426–435PubMed Chung E, Amrute SB, Abel K, Gupta G, Wang Y, Miller CJ, Fitzgerald-Bocarsly P (2005) Characterization of virus-responsive plasmacytoid dendritic cells in the rhesus macaque. Clin Diagn Lab Immunol 12:426–435PubMed
17.
Zurück zum Zitat Kawada J, Kimura H, Kamachi Y, Nishikawa K, Taniguchi M, Nagaoka K, Kurahashi H, Kojima S, Morishima T (2006) Analysis of gene-expression profiles by oligonucleotide microarray in children with influenza. J Gen Virol 87:1677–1683CrossRefPubMed Kawada J, Kimura H, Kamachi Y, Nishikawa K, Taniguchi M, Nagaoka K, Kurahashi H, Kojima S, Morishima T (2006) Analysis of gene-expression profiles by oligonucleotide microarray in children with influenza. J Gen Virol 87:1677–1683CrossRefPubMed
18.
Zurück zum Zitat Kawada J, Kimura H, Ito Y, Hara S, Iriyama M, Yoshikawa T, Morishima T (2003) Systemic cytokine responses in patients with influenza-associated encephalopathy. J Infect Dis 188:690–698CrossRefPubMed Kawada J, Kimura H, Ito Y, Hara S, Iriyama M, Yoshikawa T, Morishima T (2003) Systemic cytokine responses in patients with influenza-associated encephalopathy. J Infect Dis 188:690–698CrossRefPubMed
19.
Zurück zum Zitat 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 194:61–70CrossRefPubMed 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 194:61–70CrossRefPubMed
20.
Zurück zum Zitat Hiromoto Y, Yamazaki Y, Fukushima T, Saito T, Lindstrom SE, Omoe K, Nerome R, Lim W, Sugita S, Nerome K (2000) Evolutionary characterization of the six internal genes of H5N1 human influenza A virus. J Gen Virol 81:1293–1303PubMed Hiromoto Y, Yamazaki Y, Fukushima T, Saito T, Lindstrom SE, Omoe K, Nerome R, Lim W, Sugita S, Nerome K (2000) Evolutionary characterization of the six internal genes of H5N1 human influenza A virus. J Gen Virol 81:1293–1303PubMed
21.
Zurück zum Zitat Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, Zhou N, Klimov A, Cox N, Webster R, Lim W, Shortridge K, Subbarao K (2002) Molecular changes associated with the transmission of avian influenza H5N1 and H9N2 viruses to humans. J Med Virol 66:107–114CrossRefPubMed Shaw M, Cooper L, Xu X, Thompson W, Krauss S, Guan Y, Zhou N, Klimov A, Cox N, Webster R, Lim W, Shortridge K, Subbarao K (2002) Molecular changes associated with the transmission of avian influenza H5N1 and H9N2 viruses to humans. J Med Virol 66:107–114CrossRefPubMed
22.
Zurück zum Zitat Baskin CR, Garcia-Sastre A, Tumpey TM, Bielefeldt-Ohmann H, Carter VS, Katze MG (2004) Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J Virol 78:10420–10432CrossRefPubMed Baskin CR, Garcia-Sastre A, Tumpey TM, Bielefeldt-Ohmann H, Carter VS, Katze MG (2004) Integration of clinical data, pathology, and cDNA microarrays in influenza virus-infected pigtailed macaques (Macaca nemestrina). J Virol 78:10420–10432CrossRefPubMed
23.
Zurück zum Zitat Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, Garcia-Sastre A, Tolnay AE, Albrecht R, Pyles JA, Olson P, Aicher LD, Rosenzweig ER, Kaja MK, Clark EA, Kotur MS, Fornek JL, Proll S, Palermo RE, Sabourin CL, Katze MG (2009) Early and sustained inflammatory and innate host response defines pathology and death in high path influenza-infected non-human primates. Proc Nat Acad Sci USA 106:3455–3460CrossRefPubMed Baskin CR, Bielefeldt-Ohmann H, Tumpey TM, Sabourin PJ, Long JP, Garcia-Sastre A, Tolnay AE, Albrecht R, Pyles JA, Olson P, Aicher LD, Rosenzweig ER, Kaja MK, Clark EA, Kotur MS, Fornek JL, Proll S, Palermo RE, Sabourin CL, Katze MG (2009) Early and sustained inflammatory and innate host response defines pathology and death in high path influenza-infected non-human primates. Proc Nat Acad Sci USA 106:3455–3460CrossRefPubMed
24.
Zurück zum Zitat Cramer T, Yamanishi Y, Clausen BE, Förster I, Oawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber H-P, Ferrara N, Johnson RS (2003) HIF-1α is essential for myeloid cell-mediated inflammation. Cell 112:645–657CrossRefPubMed Cramer T, Yamanishi Y, Clausen BE, Förster I, Oawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber H-P, Ferrara N, Johnson RS (2003) HIF-1α is essential for myeloid cell-mediated inflammation. Cell 112:645–657CrossRefPubMed
25.
Zurück zum Zitat Hellwig-Burgel T, Stiehl DP, Wagner AE, Metzen E, Jelkmann W (2005) Review: hypoxia-inducible factor-1 (HIF-1): a novel transcription factor in immune reactions. J Interferon Cytokine Res 25:297–310CrossRefPubMed Hellwig-Burgel T, Stiehl DP, Wagner AE, Metzen E, Jelkmann W (2005) Review: hypoxia-inducible factor-1 (HIF-1): a novel transcription factor in immune reactions. J Interferon Cytokine Res 25:297–310CrossRefPubMed
26.
Zurück zum Zitat Köhl R, Zhou J, Brüne B (2006) Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1alpha stabilization. Free Rad Biol Med 40:1430–1442CrossRefPubMed Köhl R, Zhou J, Brüne B (2006) Reactive oxygen species attenuate nitric-oxide-mediated hypoxia-inducible factor-1alpha stabilization. Free Rad Biol Med 40:1430–1442CrossRefPubMed
27.
Zurück zum Zitat Semenza GL (2001) Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7:345–350CrossRefPubMed Semenza GL (2001) Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7:345–350CrossRefPubMed
28.
Zurück zum Zitat Zinkernagel AS, Johnson RS, Nizet V (2007) Hypoxia inducible factor (HIF) function in innate immunity and infection. J Mol Med 85:1339–1346CrossRefPubMed Zinkernagel AS, Johnson RS, Nizet V (2007) Hypoxia inducible factor (HIF) function in innate immunity and infection. J Mol Med 85:1339–1346CrossRefPubMed
29.
Zurück zum Zitat Baskin CR, Bielefeldt-Ohmann H, García-Sastre A, Tumpey TM, Van Hoeven N, Carter VS, Thomas MJ, Proll S, Solórzano A, Billharz R, Fornek JL, Thomas S, Chen CH, Clark EA, Kaja MK, Katze MG (2007) Functional genomic and serological analysis of the protective immune response resulting from vaccination of macaques with an NS1-truncated influenza virus. J Virol 81:11817–11827CrossRefPubMed Baskin CR, Bielefeldt-Ohmann H, García-Sastre A, Tumpey TM, Van Hoeven N, Carter VS, Thomas MJ, Proll S, Solórzano A, Billharz R, Fornek JL, Thomas S, Chen CH, Clark EA, Kaja MK, Katze MG (2007) Functional genomic and serological analysis of the protective immune response resulting from vaccination of macaques with an NS1-truncated influenza virus. J Virol 81:11817–11827CrossRefPubMed
30.
Zurück zum Zitat Miura TA, Travanty EA, Oko L, Bielefeldt-Ohmann H, Weiss SR, Beauchemin N, Holmes KV (2008) The spike glycoprotein of murine coronavirus MHV-JHM mediates receptor-independent infection in the central nervous system of Ceacam1a−/− mice. J Virol 82:755–763CrossRefPubMed Miura TA, Travanty EA, Oko L, Bielefeldt-Ohmann H, Weiss SR, Beauchemin N, Holmes KV (2008) The spike glycoprotein of murine coronavirus MHV-JHM mediates receptor-independent infection in the central nervous system of Ceacam1a−/− mice. J Virol 82:755–763CrossRefPubMed
31.
Zurück zum Zitat Bielefeldt-Ohmann H, Tolnay AE, Reisenhauer CE, Hansen TR, Smirnova N, Van Campen H (2008) Transplacental infection with non-cytopathic bovine viral diarrhoea virus types1b and 2: viral spread and molecular neuropathology. J Comp Pathol 138:72–85PubMed Bielefeldt-Ohmann H, Tolnay AE, Reisenhauer CE, Hansen TR, Smirnova N, Van Campen H (2008) Transplacental infection with non-cytopathic bovine viral diarrhoea virus types1b and 2: viral spread and molecular neuropathology. J Comp Pathol 138:72–85PubMed
32.
Zurück zum Zitat Bielefeldt-Ohmann H, Ballanca RU, Crockett CM, Curnow E, Eiffert K, Gillen M, Glanister D, Hayes E, Kelley S, Minoshima S, Vogel K (2004) Subacute necrotizing encephalopathy in a pig-tailed macaque (Macaca nemestrina) resembling mitochondrial encephalopathy in humans. Comp Med 54:422–433PubMed Bielefeldt-Ohmann H, Ballanca RU, Crockett CM, Curnow E, Eiffert K, Gillen M, Glanister D, Hayes E, Kelley S, Minoshima S, Vogel K (2004) Subacute necrotizing encephalopathy in a pig-tailed macaque (Macaca nemestrina) resembling mitochondrial encephalopathy in humans. Comp Med 54:422–433PubMed
33.
Zurück zum Zitat Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonto 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 445:319–323CrossRefPubMed Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonto 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 445:319–323CrossRefPubMed
34.
Zurück zum Zitat Pappas C, Aquilar PV, Basler CF, Solόrzano A, Zeng H, Perrone LA, Palese P, Garcia-Sastre A, Katz JM, Tumpey TM (2008) Single gene reassortants identify a critical role for PB1, HA, and NA in the high virulence of the 1918 pandemic influenza virus. Proc Nat Acad Sci USA 105:3064–3069CrossRefPubMed Pappas C, Aquilar PV, Basler CF, Solόrzano A, Zeng H, Perrone LA, Palese P, Garcia-Sastre A, Katz JM, Tumpey TM (2008) Single gene reassortants identify a critical role for PB1, HA, and NA in the high virulence of the 1918 pandemic influenza virus. Proc Nat Acad Sci USA 105:3064–3069CrossRefPubMed
35.
Zurück zum Zitat Keawcharoen J, Oraveerakul K, Kuiken T, Fouchier RA, Amonsin A, Payungpom S, Noppompanth S, Wattanodom S, Theambooniers A, Tantilertcharoen R, Pattanarangsan R, Arya N, Ratanakom P, Osterhaus ADM, Poovorawan Y (2004) Avian influenza H5N1 in tigers and leopards. Emerg Infect Dis 10:2189–2191PubMed Keawcharoen J, Oraveerakul K, Kuiken T, Fouchier RA, Amonsin A, Payungpom S, Noppompanth S, Wattanodom S, Theambooniers A, Tantilertcharoen R, Pattanarangsan R, Arya N, Ratanakom P, Osterhaus ADM, Poovorawan Y (2004) Avian influenza H5N1 in tigers and leopards. Emerg Infect Dis 10:2189–2191PubMed
36.
Zurück zum Zitat Fredenburgh LE, Perrella MA, Mitsialis SA (2007) Heme oxygenase-1: a multifaceted triple-threat molecule; the role of heme oxygenase-1 in pulmonary disease. Am J Resp Cell Mol Biol 36:158–165CrossRef Fredenburgh LE, Perrella MA, Mitsialis SA (2007) Heme oxygenase-1: a multifaceted triple-threat molecule; the role of heme oxygenase-1 in pulmonary disease. Am J Resp Cell Mol Biol 36:158–165CrossRef
37.
Zurück zum Zitat Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449–455CrossRefPubMed Otterbein LE, Soares MP, Yamashita K, Bach FH (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol 24:449–455CrossRefPubMed
38.
Zurück zum Zitat Haddad JJ, Harb HL (2005) Cytokines and the regulation of hypoxia-inducible factor (HIF)-1α. Intern Immunopharm 5:461–483CrossRef Haddad JJ, Harb HL (2005) Cytokines and the regulation of hypoxia-inducible factor (HIF)-1α. Intern Immunopharm 5:461–483CrossRef
39.
Zurück zum Zitat de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BRG (2001) Functional classification of interferon-stimulated genes identified using microarrays. J Leuk Biol 69:912–920 de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, Silverman RH, Williams BRG (2001) Functional classification of interferon-stimulated genes identified using microarrays. J Leuk Biol 69:912–920
40.
Zurück zum Zitat Hwang IIL, Watson IR, Der SD, Ohh M (2006) Loss of VHL confers hypoxia-inducible factor (HIF)-dependent resistance to vesicular stomatitis virus: role of HIF in antiviral response. J Virol 80:10712–10723CrossRefPubMed Hwang IIL, Watson IR, Der SD, Ohh M (2006) Loss of VHL confers hypoxia-inducible factor (HIF)-dependent resistance to vesicular stomatitis virus: role of HIF in antiviral response. J Virol 80:10712–10723CrossRefPubMed
41.
Zurück zum Zitat Lee DCW, Cheung CY, Law AHY, Mok CKP, Peiris M, Lau ASY (2005) p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol 79:10147–10154CrossRefPubMed Lee DCW, Cheung CY, Law AHY, Mok CKP, Peiris M, Lau ASY (2005) p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol 79:10147–10154CrossRefPubMed
42.
Zurück zum Zitat Semmler A, Okulla T, Sastre M, Dumitrescu-Ozimek L, Heneka MT (2005) Systemic inflammation induces apoptosis with variable vulnerability of different brain regions. J Chem Neuroanat 30:144–157CrossRefPubMed Semmler A, Okulla T, Sastre M, Dumitrescu-Ozimek L, Heneka MT (2005) Systemic inflammation induces apoptosis with variable vulnerability of different brain regions. J Chem Neuroanat 30:144–157CrossRefPubMed
43.
Zurück zum Zitat Ichiyama T, Endo S, Kaneko M, Isumi H, Matsubara T, Furukawa S (2003) Serum cytokine concentrations of influenza-associated acute necrotizing encephalopathy. Pediat Intern 45:734–736CrossRef Ichiyama T, Endo S, Kaneko M, Isumi H, Matsubara T, Furukawa S (2003) Serum cytokine concentrations of influenza-associated acute necrotizing encephalopathy. Pediat Intern 45:734–736CrossRef
44.
Zurück zum Zitat Ichiyama T, Nishikawa M, Yoshitomi T, Hayashi T, Furukawa S (1998) Tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-6 in cerebrospinal fluid from children with prolonged febrile seizures: comparison with acute encephalitis/encephalopathy. Neurology 50:407–411PubMed Ichiyama T, Nishikawa M, Yoshitomi T, Hayashi T, Furukawa S (1998) Tumor necrosis factor-alpha, interleukin-1 beta, and interleukin-6 in cerebrospinal fluid from children with prolonged febrile seizures: comparison with acute encephalitis/encephalopathy. Neurology 50:407–411PubMed
45.
Zurück zum Zitat Ito Y, Ichiyama T, Kimura H, Shibata M, Ishiwada N, Kuroki H, Furukawa S, Morishima T (1999) Detection of influenza virus RNA by reverse transcription-PCR and proinflammatory cytokines in influenza-virus-associated encephalopathy. J Med Virol 58:420–425CrossRefPubMed Ito Y, Ichiyama T, Kimura H, Shibata M, Ishiwada N, Kuroki H, Furukawa S, Morishima T (1999) Detection of influenza virus RNA by reverse transcription-PCR and proinflammatory cytokines in influenza-virus-associated encephalopathy. J Med Virol 58:420–425CrossRefPubMed
46.
Zurück zum Zitat The Australia and New Zealand Extracorporal Membrane Organization (ANZ ECMO) Influenza Investigators (2009) Extracorporeal membrane oxygenation for 2009 influenza a(H1N1) acute respiratory distress syndrome. JAMA 309. doi:10.1001/jama.2009.1535 The Australia and New Zealand Extracorporal Membrane Organization (ANZ ECMO) Influenza Investigators (2009) Extracorporeal membrane oxygenation for 2009 influenza a(H1N1) acute respiratory distress syndrome. JAMA 309. doi:10.​1001/​jama.​2009.​1535
Metadaten
Titel
Extrapulmonary tissue responses in cynomolgus macaques (Macaca fascicularis) infected with highly pathogenic avian influenza A (H5N1) virus
verfasst von
A.-E. Tolnay
C. R. Baskin
T. M. Tumpey
P. J. Sabourin
C. L. Sabourin
J. P. Long
J. A. Pyles
R. A. Albrecht
A. García-Sastre
M. G. Katze
H. Bielefeldt-Ohmann
Publikationsdatum
01.06.2010
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 6/2010
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-010-0662-8

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Erhebliches Risiko für Kehlkopfkrebs bei mäßiger Dysplasie

29.05.2024 Larynxkarzinom Nachrichten

Fast ein Viertel der Personen mit mäßig dysplastischen Stimmlippenläsionen entwickelt einen Kehlkopftumor. Solche Personen benötigen daher eine besonders enge ärztliche Überwachung.

Nach Herzinfarkt mit Typ-1-Diabetes schlechtere Karten als mit Typ 2?

29.05.2024 Herzinfarkt Nachrichten

Bei Menschen mit Typ-2-Diabetes sind die Chancen, einen Myokardinfarkt zu überleben, in den letzten 15 Jahren deutlich gestiegen – nicht jedoch bei Betroffenen mit Typ 1.

15% bedauern gewählte Blasenkrebs-Therapie

29.05.2024 Urothelkarzinom Nachrichten

Ob Patienten und Patientinnen mit neu diagnostiziertem Blasenkrebs ein Jahr später Bedauern über die Therapieentscheidung empfinden, wird einer Studie aus England zufolge von der Radikalität und dem Erfolg des Eingriffs beeinflusst.

Costims – das nächste heiße Ding in der Krebstherapie?

28.05.2024 Onkologische Immuntherapie Nachrichten

„Kalte“ Tumoren werden heiß – CD28-kostimulatorische Antikörper sollen dies ermöglichen. Am besten könnten diese in Kombination mit BiTEs und Checkpointhemmern wirken. Erste klinische Studien laufen bereits.

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