Home LiteratureArticle Details
PMID: 16971424 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The NS1 gene contributes to the virulence of H5N1 avian influenza viruses.

Journal of virology ·Vol. 80 ·No. 22 ·2006-11-00 ·Pages 11115-23

Li Z, Jiang Y, Jiao P, Wang A, Zhao F, Tian G, Wang X, Yu K, Bu Z, Chen H

Abstract

In the present study, we explored the genetic basis underlying the virulence and host range of two H5N1 influenza viruses in chickens. A/goose/Guangdong/1/96 (GS/GD/1/96) is a highly pathogenic virus for chickens, whereas A/goose/Guangdong/2/96 (GS/GD/2/96) is unable to replicate in chickens. These two H5N1 viruses differ in sequence by only five amino acids mapping to the PA, NP, M1, and NS1 genes. We used reverse genetics to create four single-gene recombinants that contained one of the sequence-differing genes from nonpathogenic GS/GD/2/96 and the remaining seven gene segments from highly pathogenic GS/GD/1/96. We determined that the NS1 gene of GS/GD/2/96 inhibited the replication of GS/GD/1/96 in chickens, while the substitution of the PA, NP, or M gene did not change the highly pathogenic properties of GS/GD/1/96. Conversely, of the recombinant viruses generated in the GS/GD/2/96 background, only the virus containing the NS1 gene of GS/GD/1/96 was able to replicate and cause disease and death in chickens. The single-amino-acid difference in the sequence of these two NS1 genes resides at position 149. We demonstrate that a recombinant virus expressing the GS/GD/1/96 NS1 protein with Ala149 is able to antagonize the induction of interferon protein levels in chicken embryo fibroblasts (CEFs), but a recombinant virus carrying a Val149 substitution is not capable of the same effect. These results indicate that the NS1 gene is critical for the pathogenicity of avian influenza virus in chickens and that the amino acid residue Ala149 correlates with the ability of these viruses to antagonize interferon induction in CEFs.

MeSH Terms
Amino Acid Substitution Animals Chick Embryo Chickens Disease Models, Animal Influenza A Virus, H5N1 Subtype/genetics,immunology,pathogenicity Influenza in Birds/virology Interferons/antagonists & inhibitors Mutation, Missense Nucleocapsid Proteins Nucleoproteins/genetics,physiology RNA-Binding Proteins/genetics,physiology RNA-Dependent RNA Polymerase/genetics,physiology Recombination, Genetic Viral Core Proteins/genetics,physiology Viral Matrix Proteins/genetics,physiology Viral Nonstructural Proteins/genetics,physiology Viral Proteins/genetics,physiology Virulence/genetics Virus Replication/genetics
Chemicals
INS1 protein, influenza virus M1 protein, Influenza A virus NP protein, Influenza A virus Nucleocapsid Proteins Nucleoproteins PA protein, influenza viruses RNA-Binding Proteins Viral Core Proteins Viral Matrix Proteins Viral Nonstructural Proteins Viral Proteins Interferons RNA-Dependent RNA Polymerase
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Li Zejun
Harbin Veterinary Research Institute, CAAS, 427 Maduan Street, Harbin 150001, People's Republic of China.
Jiang Yongping
Jiao Peirong
Wang Aiqin
Zhao Fengju
Tian Guobin
Wang Xijun
Yu Kangzhen
Bu Zhigao
Chen Hualan
References (32)
32 references, click to expand
  1. Influenza A and B viruses expressing altered NS1 proteins: A vaccine approach.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4309-14 PMID: 10725408
  2. Cellular antiviral responses against influenza A virus are countered at the posttranscriptional level by the viral NS1A protein via its binding to a cellular protein required for the 3' end processing of cellular pre-mRNAS.
    Virology. 2003 Mar 15;307(2):386-95 PMID: 12667806
  3. Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein.
    Virology. 2003 May 10;309(2):181-9 PMID: 12758165
  4. Newcastle disease virus V protein is a determinant of host range restriction.
    J Virol. 2003 Sep;77(17):9522-32 PMID: 12915566
  5. A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice.
    J Virol. 2003 Dec;77(24):13257-66 PMID: 14645582
  6. The evolution of H5N1 influenza viruses in ducks in southern China.
    Proc Natl Acad Sci U S A. 2004 Jul 13;101(28):10452-7 PMID: 15235128
  7. Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells.
    Proc Natl Acad Sci U S A. 1988 Jan;85(2):324-8 PMID: 2829180
  8. Naturally occurring NS gene variants in an avian influenza virus isolate.
    Virus Res. 1992 May;23(3):223-40 PMID: 1320795
  9. Recombinant vesicular stomatitis viruses from DNA.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4477-81 PMID: 7753828
  10. The influenza virus NS1 protein forms multimers in vitro and in vivo.
    Virology. 1995 Oct 1;212(2):422-8 PMID: 7571411
  11. 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 Apr-Jun;40(2):425-37 PMID: 8790895
  12. A system for functional analysis of Ebola virus glycoprotein.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14764-9 PMID: 9405687
  13. Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells.
    J Virol. 1998 Aug;72(8):6437-41 PMID: 9658085
  14. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems.
    Virology. 1998 Dec 20;252(2):324-30 PMID: 9878611
  15. 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 Feb;5(2):195-205 PMID: 10024172
  16. Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong.
    J Virol. 1999 Apr;73(4):3184-9 PMID: 10074171
  17. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans.
    J Virol. 1999 Jul;73(7):5903-11 PMID: 10364342
  18. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong.
    Virology. 1999 Aug 15;261(1):15-9 PMID: 10484749
  19. Rescue of influenza A virus from recombinant DNA.
    J Virol. 1999 Nov;73(11):9679-82 PMID: 10516084
  20. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls.
    J Virol. 2005 Mar;79(5):2814-22 PMID: 15709000
  21. Mutations in the NS1 protein of swine influenza virus impair anti-interferon activity and confer attenuation in pigs.
    J Virol. 2005 Jun;79(12):7535-43 PMID: 15919908
  22. Attenuation of equine influenza viruses through truncations of the NS1 protein.
    J Virol. 2005 Jul;79(13):8431-9 PMID: 15956587
  23. Avian flu: H5N1 virus outbreak in migratory waterfowl.
    Nature. 2005 Jul 14;436(7048):191-2 PMID: 16007072
  24. Highly pathogenic H5N1 influenza virus infection in migratory birds.
    Science. 2005 Aug 19;309(5738):1206 PMID: 16000410
  25. Evolution of H9N2 influenza viruses from domestic poultry in Mainland China.
    Virology. 2005 Sep 15;340(1):70-83 PMID: 16026813
  26. Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals.
    J Virol. 2005 Sep;79(18):11788-800 PMID: 16140756
  27. Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model.
    J Virol. 2005 Sep;79(18):12058-64 PMID: 16140781
  28. Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China.
    J Virol. 2006 Jun;80(12):5976-83 PMID: 16731936
  29. Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses.
    Science. 2001 Sep 7;293(5536):1840-2 PMID: 11546875
  30. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses.
    Nat Med. 2002 Sep;8(9):950-4 PMID: 12195436
  31. Functional replacement of the carboxy-terminal two-thirds of the influenza A virus NS1 protein with short heterologous dimerization domains.
    J Virol. 2002 Dec;76(24):12951-62 PMID: 12438621
  32. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein.
    J Virol. 2000 Sep;74(17):7989-96 PMID: 10933707
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2006-11-00
Epub
2006-00-13
Pages
11115-23
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1642184
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com