Skip to main content
Top
Published in: Virology Journal 1/2010

Open Access 01-12-2010 | Research

Full genome comparison and characterization of avian H10 viruses with different pathogenicity in Mink (Mustela vison) reveals genetic and functional differences in the non-structural gene

Authors: Siamak Zohari, Giorgi Metreveli, István Kiss, Sándor Belák, Mikael Berg

Published in: Virology Journal | Issue 1/2010

Login to get access

Abstract

Background

The unique property of some avian H10 viruses, particularly the ability to cause severe disease in mink without prior adaptation, enabled our study. Coupled with previous experimental data and genetic characterization here we tried to investigate the possible influence of different genes on the virulence of these H10 avian influenza viruses in mink.

Results

Phylogenetic analysis revealed a close relationship between the viruses studied. Our study also showed that there are no genetic differences in receptor specificity or the cleavability of the haemagglutinin proteins of these viruses regardless of whether they are of low or high pathogenicity in mink.
In poly I:C stimulated mink lung cells the NS1 protein of influenza A virus showing high pathogenicity in mink down regulated the type I interferon promoter activity to a greater extent than the NS1 protein of the virus showing low pathogenicity in mink.

Conclusions

Differences in pathogenicity and virulence in mink between these strains could be related to clear amino acid differences in the non structural 1 (NS1) protein. The NS gene of mink/84 appears to have contributed to the virulence of the virus in mink by helping the virus evade the innate immune responses.
Appendix
Available only for authorised users
Literature
1.
go back to reference Klingeborn B, Englund L, Rott R, Juntti N, Rockborn G: An avian influenza A virus killing a mammalian species-the mink. Arch Virol 1985, 86: 347-351. 10.1007/BF01309839PubMedCrossRef Klingeborn B, Englund L, Rott R, Juntti N, Rockborn G: An avian influenza A virus killing a mammalian species-the mink. Arch Virol 1985, 86: 347-351. 10.1007/BF01309839PubMedCrossRef
2.
go back to reference Englund L, Klingeborn B, Mejerland T: Avian influenza virus causing an outbreak of contageous interstitial pneumonia in mink. Acta vet scand 1986, 27: 497-504.PubMed Englund L, Klingeborn B, Mejerland T: Avian influenza virus causing an outbreak of contageous interstitial pneumonia in mink. Acta vet scand 1986, 27: 497-504.PubMed
3.
go back to reference Alexander DJ, Gough RE: Isolation of avian influenza virus from birds in Great Britain. Veterinary Record 1986, 118: 537-538. 10.1136/vr.118.19.537PubMedCrossRef Alexander DJ, Gough RE: Isolation of avian influenza virus from birds in Great Britain. Veterinary Record 1986, 118: 537-538. 10.1136/vr.118.19.537PubMedCrossRef
4.
go back to reference Berg M, Englund L, Abusugra IA, Klingeborn B, Linné T: Close relationship between mink influenza (H10N4) and concomitantly circulating avian influenza viruses. Arch Virol 1990, 113: 61-71. 10.1007/BF01318353PubMedCrossRef Berg M, Englund L, Abusugra IA, Klingeborn B, Linné T: Close relationship between mink influenza (H10N4) and concomitantly circulating avian influenza viruses. Arch Virol 1990, 113: 61-71. 10.1007/BF01318353PubMedCrossRef
5.
go back to reference Feldmann H, Kretzschmar E, Klingeborn B, Rott R, Klenk HD, Garten W: The structure of serotype H10 hemagglutinin of influenza A virus: comparison of an apathogenicavian and a mammalian strain pathogenic for mink. Virology 1988, 165: 428-437. 10.1016/0042-6822(88)90586-7PubMedCrossRef Feldmann H, Kretzschmar E, Klingeborn B, Rott R, Klenk HD, Garten W: The structure of serotype H10 hemagglutinin of influenza A virus: comparison of an apathogenicavian and a mammalian strain pathogenic for mink. Virology 1988, 165: 428-437. 10.1016/0042-6822(88)90586-7PubMedCrossRef
6.
go back to reference Reinhardt U, Scholtissek C: Comparison of the nucleoprotein genes of a chicken and a Mink influenza A H10 virus. Arch Virol 1988, 103: 139-145. 10.1007/BF01319816PubMedCrossRef Reinhardt U, Scholtissek C: Comparison of the nucleoprotein genes of a chicken and a Mink influenza A H10 virus. Arch Virol 1988, 103: 139-145. 10.1007/BF01319816PubMedCrossRef
7.
go back to reference Dinter Z: Eine variante des Virus der Geflügelpest in Bayern? Tierärztl Umschau 1949, 4: 185-186. Dinter Z: Eine variante des Virus der Geflügelpest in Bayern? Tierärztl Umschau 1949, 4: 185-186.
8.
go back to reference Englund L, Hård af Segerstad C: Two avian H10 influenza A virus strains with different pathognicity for mink (Mustela vison). Arch Virol 1998, 143: 653-666. 10.1007/s007050050321PubMedCrossRef Englund L, Hård af Segerstad C: Two avian H10 influenza A virus strains with different pathognicity for mink (Mustela vison). Arch Virol 1998, 143: 653-666. 10.1007/s007050050321PubMedCrossRef
9.
go back to reference Englund L: Studies on influenza viruses H10N4 and H10N7 of avian origin in mink. Veterinary Microbiology 2000, 74: 101-107. 10.1016/S0378-1135(00)00170-XPubMedCrossRef Englund L: Studies on influenza viruses H10N4 and H10N7 of avian origin in mink. Veterinary Microbiology 2000, 74: 101-107. 10.1016/S0378-1135(00)00170-XPubMedCrossRef
10.
go back to reference Englund L: Influenza A virus, H10N4, Naturally Pathogenic for Mink ( Mustela vison ). Doctoral thesis, Swedish University of Agricultural sciences 1997. Veterinaria 25 Englund L: Influenza A virus, H10N4, Naturally Pathogenic for Mink ( Mustela vison ). Doctoral thesis, Swedish University of Agricultural sciences 1997. Veterinaria 25
11.
go back to reference Srivastava B, Błazejewska P, Heßmann M, Bruder D, Geffers R, Mauel S, Gruber AD, Schughart K: Host Genetic Background Strongly Influences the Response to Influenza A Virus Infections. PLoS ONE 2009, 4: e4857. doi:4810.1371/journal.pone.0004857. 10.1371/journal.pone.0004857PubMedPubMedCentralCrossRef Srivastava B, Błazejewska P, Heßmann M, Bruder D, Geffers R, Mauel S, Gruber AD, Schughart K: Host Genetic Background Strongly Influences the Response to Influenza A Virus Infections. PLoS ONE 2009, 4: e4857. doi:4810.1371/journal.pone.0004857. 10.1371/journal.pone.0004857PubMedPubMedCentralCrossRef
12.
go back to reference Taubenberger JK, Morens DM: The Pathology of Influenza Virus Infections. Annual Review of Pathology: Mechanisms of Disease 2008, 3: 499-522. 10.1146/annurev.pathmechdis.3.121806.154316CrossRef Taubenberger JK, Morens DM: The Pathology of Influenza Virus Infections. Annual Review of Pathology: Mechanisms of Disease 2008, 3: 499-522. 10.1146/annurev.pathmechdis.3.121806.154316CrossRef
14.
go back to reference Chen H, Bright RA, Subbarao K, Smith C, Cox NJ, Katz JM, Matsuoka Y: Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res 2007, 128: 159-163. 10.1016/j.virusres.2007.04.017PubMedCrossRef Chen H, Bright RA, Subbarao K, Smith C, Cox NJ, Katz JM, Matsuoka Y: Polygenic virulence factors involved in pathogenesis of 1997 Hong Kong H5N1 influenza viruses in mice. Virus Res 2007, 128: 159-163. 10.1016/j.virusres.2007.04.017PubMedCrossRef
15.
go back to reference Jackson D, Hossain MJ, Hickman D, Perez DR, Lamb RA: A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci USA 2008, 105: 4381-4386. 10.1073/pnas.0800482105PubMedPubMedCentralCrossRef Jackson D, Hossain MJ, Hickman D, Perez DR, Lamb RA: A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci USA 2008, 105: 4381-4386. 10.1073/pnas.0800482105PubMedPubMedCentralCrossRef
16.
go back to reference 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. 10.1128/JVI.01698-07PubMedPubMedCentralCrossRef 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. 10.1128/JVI.01698-07PubMedPubMedCentralCrossRef
17.
go back to reference Hatta M, Gao P, Halfmann P, Kawaoka Y: Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 2001, 293: 1840-1842. 10.1126/science.1062882PubMedCrossRef Hatta M, Gao P, Halfmann P, Kawaoka Y: Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 2001, 293: 1840-1842. 10.1126/science.1062882PubMedCrossRef
18.
go back to reference Lee CW, Lee YJ, Senne DA, Suarez DL: Pathogenic potential of North American H7N2 avian influenza virus: a mutagenesis study using reverse genetics. Virology 2006, 353: 388-395. 10.1016/j.virol.2006.06.003PubMedCrossRef Lee CW, Lee YJ, Senne DA, Suarez DL: Pathogenic potential of North American H7N2 avian influenza virus: a mutagenesis study using reverse genetics. Virology 2006, 353: 388-395. 10.1016/j.virol.2006.06.003PubMedCrossRef
19.
go back to reference Skehel JJ, Wiley DC: RECEPTOR BINDING AND MEMBRANE FUSION IN VIRUS ENTRY: The Influenza Hemagglutinin. Annual Review of Biochemistry 2000, 69: 531-569. 10.1146/annurev.biochem.69.1.531PubMedCrossRef Skehel JJ, Wiley DC: RECEPTOR BINDING AND MEMBRANE FUSION IN VIRUS ENTRY: The Influenza Hemagglutinin. Annual Review of Biochemistry 2000, 69: 531-569. 10.1146/annurev.biochem.69.1.531PubMedCrossRef
20.
go back to reference Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K: Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 1991, 182: 475-485. 10.1016/0042-6822(91)90588-3PubMedCrossRef Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K: Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 1991, 182: 475-485. 10.1016/0042-6822(91)90588-3PubMedCrossRef
21.
go back to reference Wood GW, Banks J, Strong I, Parson G, Alexander DJ: An avian influenza virus of H10 subtype that is highly pathogenic for chickens, but lacks multiple basic amino acids at the haemagglutinin cleavage site. Avian Pathology 1996, 25: 799-806. 10.1080/03079459608419182PubMedCrossRef Wood GW, Banks J, Strong I, Parson G, Alexander DJ: An avian influenza virus of H10 subtype that is highly pathogenic for chickens, but lacks multiple basic amino acids at the haemagglutinin cleavage site. Avian Pathology 1996, 25: 799-806. 10.1080/03079459608419182PubMedCrossRef
22.
go back to reference Senne DA, Panigrahy B, Kawaoka Y, Pearson JE, Süss J, Lipkind M, Kida H, Webster RG: Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Dis 1996, 40: 425-437. 10.2307/1592241PubMedCrossRef Senne DA, Panigrahy B, Kawaoka Y, Pearson JE, Süss J, Lipkind M, Kida H, Webster RG: Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Dis 1996, 40: 425-437. 10.2307/1592241PubMedCrossRef
23.
go back to reference Vey M, Orlich M, Adler S, Klenk HD, Rott R, Garten W: Hemagglutinin activation of pathogenic avian influenza viruses of serotype H7 requires the protease recognition motif R-X-K/R-R. Virology 1992, 188: 408-413. 10.1016/0042-6822(92)90775-KPubMedCrossRef Vey M, Orlich M, Adler S, Klenk HD, Rott R, Garten W: Hemagglutinin activation of pathogenic avian influenza viruses of serotype H7 requires the protease recognition motif R-X-K/R-R. Virology 1992, 188: 408-413. 10.1016/0042-6822(92)90775-KPubMedCrossRef
24.
go back to reference Wood GW, McCauley JW, Bashiruddin JB, Alexander DJ: Deduced amino acid sequences at the haemagglutinin cleavage site of avian influenza A viruses of H5 and H7 subtype. Arch Virol 1993, 130: 209-217. 10.1007/BF01319010PubMedCrossRef Wood GW, McCauley JW, Bashiruddin JB, Alexander DJ: Deduced amino acid sequences at the haemagglutinin cleavage site of avian influenza A viruses of H5 and H7 subtype. Arch Virol 1993, 130: 209-217. 10.1007/BF01319010PubMedCrossRef
25.
go back to reference Air GM, Laver WG: The neuraminidase of influenza virus. Proteins 1989, 6: 341-356. 10.1002/prot.340060402PubMedCrossRef Air GM, Laver WG: The neuraminidase of influenza virus. Proteins 1989, 6: 341-356. 10.1002/prot.340060402PubMedCrossRef
26.
go back to reference Matrosovich M, Zhou N, Kawaoka Y, Webster RG: The Surface Glycoproteins of H5 Influenza Viruses Isolated from Humans, Chickens, and Wild Aquatic Birds Have Distinguishable Properties. Journal of Virology 1999, 73: 1146-1155.PubMedPubMedCentral Matrosovich M, Zhou N, Kawaoka Y, Webster RG: The Surface Glycoproteins of H5 Influenza Viruses Isolated from Humans, Chickens, and Wild Aquatic Birds Have Distinguishable Properties. Journal of Virology 1999, 73: 1146-1155.PubMedPubMedCentral
27.
go back to reference Colman PM, Varghese JN, Laver WG: Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 1983, 303: 41-44. 10.1038/303041a0PubMedCrossRef Colman PM, Varghese JN, Laver WG: Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature 1983, 303: 41-44. 10.1038/303041a0PubMedCrossRef
28.
go back to reference Beare AS, Webster RG: Replication of avian influenza viruses in humans. Arch Virol 1991, 119: 37-42. 10.1007/BF01314321PubMedCrossRef Beare AS, Webster RG: Replication of avian influenza viruses in humans. Arch Virol 1991, 119: 37-42. 10.1007/BF01314321PubMedCrossRef
29.
go back to reference EID: Avian Influenza Virus A (H10N7) Circulating among Humans in Egypt. Emerging and Reemerging Infectious Diseases, Region of the Americas, EID-weekly uppdate 2004., 2: EID: Avian Influenza Virus A (H10N7) Circulating among Humans in Egypt. Emerging and Reemerging Infectious Diseases, Region of the Americas, EID-weekly uppdate 2004., 2:
30.
go back to reference Hurt AC, Ho HT, Barr I: Resistance to anti-influenza drugs: adamantanes and neuraminidase inhibitors. Expert Review of Anti-infective Therapy 2006, 4: 795-805. 10.1586/14787210.4.5.795PubMedCrossRef Hurt AC, Ho HT, Barr I: Resistance to anti-influenza drugs: adamantanes and neuraminidase inhibitors. Expert Review of Anti-infective Therapy 2006, 4: 795-805. 10.1586/14787210.4.5.795PubMedCrossRef
31.
go back to reference Baigent SJ, McCauley JW: Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture. Virus Res 2001, 79: 177-185. 10.1016/S0168-1702(01)00272-6PubMedCrossRef Baigent SJ, McCauley JW: Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture. Virus Res 2001, 79: 177-185. 10.1016/S0168-1702(01)00272-6PubMedCrossRef
32.
go back to reference Gabriel G, Dauber B, Wolv T, Planz O, Klenk HD, Stech J: The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 2005, 102: 18590-18595. 10.1073/pnas.0507415102PubMedPubMedCentralCrossRef Gabriel G, Dauber B, Wolv T, Planz O, Klenk HD, Stech J: The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 2005, 102: 18590-18595. 10.1073/pnas.0507415102PubMedPubMedCentralCrossRef
33.
go back to reference Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen HL, Hulse Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, et al.: The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 2006, 203: 689-697. 10.1084/jem.20051938PubMedPubMedCentralCrossRef Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen HL, Hulse Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, et al.: The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 2006, 203: 689-697. 10.1084/jem.20051938PubMedPubMedCentralCrossRef
34.
go back to reference Guang-Wu Chen, Shih-Cheng Chang, Chee-Keng Mok, Yu-Luan Lo, Yu-Nong Kung, Ji-Hung Huang, Yun-Han Shih, Ji-Yi Wang, Chiang Chiayn, Chi-Jene Chen, Shin-Ru S: Genomic signatures of human versus avian influenza A viruses. Emerg Infect Dis 2006, 12: 1353-1360.CrossRef Guang-Wu Chen, Shih-Cheng Chang, Chee-Keng Mok, Yu-Luan Lo, Yu-Nong Kung, Ji-Hung Huang, Yun-Han Shih, Ji-Yi Wang, Chiang Chiayn, Chi-Jene Chen, Shin-Ru S: Genomic signatures of human versus avian influenza A viruses. Emerg Infect Dis 2006, 12: 1353-1360.CrossRef
35.
go back to reference Finkelstein DB, Mukatira S, Mehta PK, Obenauer JC, Su X, Webster RG, Naeve CW: Persistent Host Markers in Pandemic and H5N1 Influenza Viruses. Journal of Virology 2007, 81: 10292-10299. 10.1128/JVI.00921-07PubMedPubMedCentralCrossRef Finkelstein DB, Mukatira S, Mehta PK, Obenauer JC, Su X, Webster RG, Naeve CW: Persistent Host Markers in Pandemic and H5N1 Influenza Viruses. Journal of Virology 2007, 81: 10292-10299. 10.1128/JVI.00921-07PubMedPubMedCentralCrossRef
36.
go back to reference Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, et al.: Lethality to Ferrets of H5N1 Influenza Viruses Isolated from Humans and Poultry in 2004. Journal of Virology 2005, 79: 2191-2198. 10.1128/JVI.79.4.2191-2198.2005PubMedPubMedCentralCrossRef Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, et al.: Lethality to Ferrets of H5N1 Influenza Viruses Isolated from Humans and Poultry in 2004. Journal of Virology 2005, 79: 2191-2198. 10.1128/JVI.79.4.2191-2198.2005PubMedPubMedCentralCrossRef
37.
go back to reference Li Z, Jiang Y, Jiao P, Wang A, Zhao F, Tian G, Wang X, Yu K, Bu Z, Chen H: The NS1 Gene Contributes to the Virulence of H5N1 Avian Influenza Viruse. J Virol 2006, 80: 11115-11123. 10.1128/JVI.00993-06PubMedPubMedCentralCrossRef Li Z, Jiang Y, Jiao P, Wang A, Zhao F, Tian G, Wang X, Yu K, Bu Z, Chen H: The NS1 Gene Contributes to the Virulence of H5N1 Avian Influenza Viruse. J Virol 2006, 80: 11115-11123. 10.1128/JVI.00993-06PubMedPubMedCentralCrossRef
38.
go back to reference Maines TR, Lu XH, Erb SM, Edwards L, Guarner J, Greer PW, Nguyen DC, Szretter KJ, Chen LM, Thawatsupha P, et al.: Avian Influenza (H5N1) Viruses Isolated from Humans in Asia in 2004 Exhibit Increased Virulence in Mammals. Journal of Virology 2005, 79: 11788-11800. 10.1128/JVI.79.18.11788-11800.2005PubMedPubMedCentralCrossRef Maines TR, Lu XH, Erb SM, Edwards L, Guarner J, Greer PW, Nguyen DC, Szretter KJ, Chen LM, Thawatsupha P, et al.: Avian Influenza (H5N1) Viruses Isolated from Humans in Asia in 2004 Exhibit Increased Virulence in Mammals. Journal of Virology 2005, 79: 11788-11800. 10.1128/JVI.79.18.11788-11800.2005PubMedPubMedCentralCrossRef
39.
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, et al.: A novel influenza A virus mitochondrial protein that induces cell death. Nature Medicine 2001, 7: 1306-1312. 10.1038/nm1201-1306PubMedCrossRef Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O'Neill R, Schickli J, Palese P, et al.: A novel influenza A virus mitochondrial protein that induces cell death. Nature Medicine 2001, 7: 1306-1312. 10.1038/nm1201-1306PubMedCrossRef
40.
go back to reference Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P: A Single Mutation in the PB1-F2 of H5N1 (HK/97) and 1918 Influenza A Viruses Contributes to Increased Virulence. PLoS Pathog 2007, 3: e141. 10.1371/journal.ppat.0030141PubMedCentralCrossRef Conenello GM, Zamarin D, Perrone LA, Tumpey T, Palese P: A Single Mutation in the PB1-F2 of H5N1 (HK/97) and 1918 Influenza A Viruses Contributes to Increased Virulence. PLoS Pathog 2007, 3: e141. 10.1371/journal.ppat.0030141PubMedCentralCrossRef
41.
go back to reference Suzuki H, Saito R, Masuda H, Oshitani H, Sato M, Sato I: Emergence of amantadine-resistance influenza A viruses: epidemiological study. J Infect Chemother 2003, 9: 195-200. 10.1007/s10156-003-0262-6PubMedCrossRef Suzuki H, Saito R, Masuda H, Oshitani H, Sato M, Sato I: Emergence of amantadine-resistance influenza A viruses: epidemiological study. J Infect Chemother 2003, 9: 195-200. 10.1007/s10156-003-0262-6PubMedCrossRef
42.
go back to reference Ludwig S, Schultz U, Mandler J, Fitch WM, Scholtissek C: Phylogenetic relationship of the nonstructural (NS) genes of influenza A viruses. Virology 1991, 183: 566-577. 10.1016/0042-6822(91)90985-KPubMedCrossRef Ludwig S, Schultz U, Mandler J, Fitch WM, Scholtissek C: Phylogenetic relationship of the nonstructural (NS) genes of influenza A viruses. Virology 1991, 183: 566-577. 10.1016/0042-6822(91)90985-KPubMedCrossRef
43.
go back to reference Suarez DL, Perdue ML: Multiple alignment comparison of the non-structural genes of influenza A viruses. Virus Res 1998, 54: 59-69. 10.1016/S0168-1702(98)00011-2PubMedCrossRef Suarez DL, Perdue ML: Multiple alignment comparison of the non-structural genes of influenza A viruses. Virus Res 1998, 54: 59-69. 10.1016/S0168-1702(98)00011-2PubMedCrossRef
44.
go back to reference Seo SH, Hoffmann E, Webster RG: The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine responses. Virus Res 2004, 103: 107-113. 10.1016/j.virusres.2004.02.022PubMedCrossRef Seo SH, Hoffmann E, Webster RG: The NS1 gene of H5N1 influenza viruses circumvents the host anti-viral cytokine responses. Virus Res 2004, 103: 107-113. 10.1016/j.virusres.2004.02.022PubMedCrossRef
45.
go back to reference Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, et al.: Large-Scale Sequence Analysis of Avian Influenza Isolates. Science 2006, 311: 1576-1580. 10.1126/science.1121586PubMedCrossRef Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, et al.: Large-Scale Sequence Analysis of Avian Influenza Isolates. Science 2006, 311: 1576-1580. 10.1126/science.1121586PubMedCrossRef
46.
go back to reference Lamb RA, Krug RM: Orthomyxoviridae: the viruses and their replication. In FieldsVirology Edited by: Knipe DN, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE. 2001, 1487-1531. Lamb RA, Krug RM: Orthomyxoviridae: the viruses and their replication. In FieldsVirology Edited by: Knipe DN, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE. 2001, 1487-1531.
47.
go back to reference Krug RM, Yuan W, Noah DL, Latham AG: Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 2003, 309: 181-189. 10.1016/S0042-6822(03)00119-3PubMedCrossRef Krug RM, Yuan W, Noah DL, Latham AG: Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 2003, 309: 181-189. 10.1016/S0042-6822(03)00119-3PubMedCrossRef
48.
go back to reference Hale BG, Randall RE, Ortin J, Jackson D: The multifunctional NS1 protein of influenza A viruses. J Gen Virol 2008, 89: 2359-2376. 10.1099/vir.0.2008/004606-0PubMedCrossRef Hale BG, Randall RE, Ortin J, Jackson D: The multifunctional NS1 protein of influenza A viruses. J Gen Virol 2008, 89: 2359-2376. 10.1099/vir.0.2008/004606-0PubMedCrossRef
49.
go back to reference Durbin JE, Hackenmiller R, Simon MC, Levy DE: Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996, 84: 443-450. 10.1016/S0092-8674(00)81289-1PubMedCrossRef Durbin JE, Hackenmiller R, Simon MC, Levy DE: Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996, 84: 443-450. 10.1016/S0092-8674(00)81289-1PubMedCrossRef
50.
go back to reference Garcia-Sastre A: Inhibition of Interferon-Mediated Antiviral Responses by Influenza A Viruses and Other Negative-Strand RNA Viruses. Virology 2001, 279: 375-384. 10.1006/viro.2000.0756PubMedCrossRef Garcia-Sastre A: Inhibition of Interferon-Mediated Antiviral Responses by Influenza A Viruses and Other Negative-Strand RNA Viruses. Virology 2001, 279: 375-384. 10.1006/viro.2000.0756PubMedCrossRef
51.
go back to reference Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T: Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 1998, 252: 324-330. 10.1006/viro.1998.9508PubMedCrossRef Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T: Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 1998, 252: 324-330. 10.1006/viro.1998.9508PubMedCrossRef
52.
go back to reference Meraz MA, White JM, Sheehan KC, Bach EA, Rodig SJ, Dighe AS, Kaplan DH, Riley JK, Greenlund AC, Campbell D, et al.: Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 1996, 84: 431-442. 10.1016/S0092-8674(00)81288-XPubMedCrossRef Meraz MA, White JM, Sheehan KC, Bach EA, Rodig SJ, Dighe AS, Kaplan DH, Riley JK, Greenlund AC, Campbell D, et al.: Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 1996, 84: 431-442. 10.1016/S0092-8674(00)81288-XPubMedCrossRef
53.
go back to reference Lu Y, Wambach M, Katze MG, Krug RM: Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 1995, 214: 222-228. 10.1006/viro.1995.9937PubMedCrossRef Lu Y, Wambach M, Katze MG, Krug RM: Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 1995, 214: 222-228. 10.1006/viro.1995.9937PubMedCrossRef
54.
go back to reference Hatada E, Saito S, Fukuda R: Mutant influenza viruses with a defective NS1 protein cannot block the activation of PKR in infected cells. J Virol 1999, 73: 2425-2433.PubMedPubMedCentral Hatada E, Saito S, Fukuda R: Mutant influenza viruses with a defective NS1 protein cannot block the activation of PKR in infected cells. J Virol 1999, 73: 2425-2433.PubMedPubMedCentral
55.
go back to reference Bergmann M, Garcia-Sastre A, Carnero E, Pehamberger H, Wolff K, Palese P, Muster T: Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. Journal Of Virology 2000, 74: 6203-6206. 10.1128/JVI.74.13.6203-6206.2000PubMedPubMedCentralCrossRef Bergmann M, Garcia-Sastre A, Carnero E, Pehamberger H, Wolff K, Palese P, Muster T: Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. Journal Of Virology 2000, 74: 6203-6206. 10.1128/JVI.74.13.6203-6206.2000PubMedPubMedCentralCrossRef
56.
go back to reference Wang X, Li M, Zheng H, Muster T, Palese P, Beg AA, Garcia-Sastre A: Influenza A virus NS1 protein prevents activation of NF-kappaβ and induction of alpha/beta interferon. Journal Of Virology 2000, 74: 11566-11573. 10.1128/JVI.74.24.11566-11573.2000PubMedPubMedCentralCrossRef Wang X, Li M, Zheng H, Muster T, Palese P, Beg AA, Garcia-Sastre A: Influenza A virus NS1 protein prevents activation of NF-kappaβ and induction of alpha/beta interferon. Journal Of Virology 2000, 74: 11566-11573. 10.1128/JVI.74.24.11566-11573.2000PubMedPubMedCentralCrossRef
57.
go back to reference Talon J, Horvath CM, Polley R, Basler CF, Muster T, Palese P, Garcia-Sastre A: Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. Journal Of Virology 2000, 74: 7989-7996. 10.1128/JVI.74.17.7989-7996.2000PubMedPubMedCentralCrossRef Talon J, Horvath CM, Polley R, Basler CF, Muster T, Palese P, Garcia-Sastre A: Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. Journal Of Virology 2000, 74: 7989-7996. 10.1128/JVI.74.17.7989-7996.2000PubMedPubMedCentralCrossRef
58.
go back to reference Min JY, Krug RM: The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 2'-5' oligo (A) synthetase/RNase L pathway. Proceedings of the National Academy of Sciences 2006, 103: 7100-7105. 10.1073/pnas.0602184103CrossRef Min JY, Krug RM: The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 2'-5' oligo (A) synthetase/RNase L pathway. Proceedings of the National Academy of Sciences 2006, 103: 7100-7105. 10.1073/pnas.0602184103CrossRef
59.
go back to reference Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M Jr, Garcia-Sastre A: Inhibition of Retinoic Acid-Inducible Gene I-Mediated Induction of Beta Interferon by the NS1 Protein of Influenza A Virus. J Virol 2007, 81: 514-524. 10.1128/JVI.01265-06PubMedPubMedCentralCrossRef Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M Jr, Garcia-Sastre A: Inhibition of Retinoic Acid-Inducible Gene I-Mediated Induction of Beta Interferon by the NS1 Protein of Influenza A Virus. J Virol 2007, 81: 514-524. 10.1128/JVI.01265-06PubMedPubMedCentralCrossRef
60.
go back to reference Opitz B, Rejaibi A, Dauber B, Eckhard J, Vinzing M, Schmeck B, Hippenstiel S, Suttorp N, Wolff T: IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell Microbiol 2007, 9: 930-938. 10.1111/j.1462-5822.2006.00841.xPubMedCrossRef Opitz B, Rejaibi A, Dauber B, Eckhard J, Vinzing M, Schmeck B, Hippenstiel S, Suttorp N, Wolff T: IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell Microbiol 2007, 9: 930-938. 10.1111/j.1462-5822.2006.00841.xPubMedCrossRef
61.
go back to reference Biron CA: Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr Opin Microbiol 1999, 2: 374-381. 10.1016/S1369-5274(99)80066-6PubMedCrossRef Biron CA: Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr Opin Microbiol 1999, 2: 374-381. 10.1016/S1369-5274(99)80066-6PubMedCrossRef
62.
go back to reference Grandvaux N, tenOever BR, Servant MJ, Hiscott J: The interferon antiviral response: from viral invasion to evasion. Curr Opin Infect Dis 2002, 15: 259-267.PubMedCrossRef Grandvaux N, tenOever BR, Servant MJ, Hiscott J: The interferon antiviral response: from viral invasion to evasion. Curr Opin Infect Dis 2002, 15: 259-267.PubMedCrossRef
63.
go back to reference Theofilopoulos AN, Baccala R, Beutler B, Kono DH: Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 2005, 23: 307-336. 10.1146/annurev.immunol.23.021704.115843PubMedCrossRef Theofilopoulos AN, Baccala R, Beutler B, Kono DH: Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 2005, 23: 307-336. 10.1146/annurev.immunol.23.021704.115843PubMedCrossRef
64.
go back to reference Li S, Min JY, Krug RM, Sen GC: Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 2006, 349: 13-21. 10.1016/j.virol.2006.01.005PubMedCrossRef Li S, Min JY, Krug RM, Sen GC: Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 2006, 349: 13-21. 10.1016/j.virol.2006.01.005PubMedCrossRef
65.
go back to reference Wang W, Riedel K, Lynch P, Chien CY, Montelione GT, Krug RM: RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. RNA 1999, 5: 195-205. 10.1017/S1355838299981621PubMedPubMedCentralCrossRef Wang W, Riedel K, Lynch P, Chien CY, Montelione GT, Krug RM: RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. RNA 1999, 5: 195-205. 10.1017/S1355838299981621PubMedPubMedCentralCrossRef
66.
go back to reference Nemeroff ME, Barabino SML, Li Y, Keller W, Krug RM: Influenza Virus NS1 Protein Interacts with the Cellular 30 kDa Subunit of CPSF and Inhibits 3' End Formation of Cellular Pre-mRNAs. Molecular Cell 1998, 1: 991-1000. 10.1016/S1097-2765(00)80099-4PubMedCrossRef Nemeroff ME, Barabino SML, Li Y, Keller W, Krug RM: Influenza Virus NS1 Protein Interacts with the Cellular 30 kDa Subunit of CPSF and Inhibits 3' End Formation of Cellular Pre-mRNAs. Molecular Cell 1998, 1: 991-1000. 10.1016/S1097-2765(00)80099-4PubMedCrossRef
67.
go back to reference Chen Z, Li Y, Krug R: Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3'-end processing machinery. EMBO J 1999, 18: 2273-2283. 10.1093/emboj/18.8.2273PubMedPubMedCentralCrossRef Chen Z, Li Y, Krug R: Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3'-end processing machinery. EMBO J 1999, 18: 2273-2283. 10.1093/emboj/18.8.2273PubMedPubMedCentralCrossRef
68.
go back to reference Li Y, Chen ZY, Wang W, Baker CC, Krug RM: The 3'-end-processing factor CPSF is required for the splicing of single-intron pre-mRNAs in vivo. RNA 2001, 7: 920-931. 10.1017/S1355838201010226PubMedPubMedCentralCrossRef Li Y, Chen ZY, Wang W, Baker CC, Krug RM: The 3'-end-processing factor CPSF is required for the splicing of single-intron pre-mRNAs in vivo. RNA 2001, 7: 920-931. 10.1017/S1355838201010226PubMedPubMedCentralCrossRef
69.
go back to reference Kochs G, Garcia-Sastre A, Martinez-Sobrido L: Multiple Anti-Interferon Actions of the Influenza A Virus NS1 Protein. J Virol 2007, 81: 7011-7021. 10.1128/JVI.02581-06PubMedPubMedCentralCrossRef Kochs G, Garcia-Sastre A, Martinez-Sobrido L: Multiple Anti-Interferon Actions of the Influenza A Virus NS1 Protein. J Virol 2007, 81: 7011-7021. 10.1128/JVI.02581-06PubMedPubMedCentralCrossRef
70.
go back to reference Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysisprogram for Windows 95/98/NT. Nucleic Acids Symposium Series 1999, 41: 95-98. Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysisprogram for Windows 95/98/NT. Nucleic Acids Symposium Series 1999, 41: 95-98.
71.
go back to reference Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22: 4673-4680. 10.1093/nar/22.22.4673PubMedPubMedCentralCrossRef Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22: 4673-4680. 10.1093/nar/22.22.4673PubMedPubMedCentralCrossRef
72.
go back to reference Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007. 10.1093/molbev/msm09. Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007. 10.1093/molbev/msm09.
Metadata
Title
Full genome comparison and characterization of avian H10 viruses with different pathogenicity in Mink (Mustela vison) reveals genetic and functional differences in the non-structural gene
Authors
Siamak Zohari
Giorgi Metreveli
István Kiss
Sándor Belák
Mikael Berg
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2010
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-7-145

Other articles of this Issue 1/2010

Virology Journal 1/2010 Go to the issue