Evidence of expanded host range and mammalian-associated genetic changes in a duck H9N2 influenza virus following adaptation in quail and chickens.
H9N2 avian influenza viruses continue to circulate worldwide; in Asia, H9N2 viruses have caused disease outbreaks and established lineages in land-based poultry. Some H9N2 strains are considered potentially pandemic because they have infected humans causing mild respiratory disease. In addition, some of these H9N2 strains replicate efficiently in mice without prior adaptation suggesting that H9N2 strains are expanding their host range. In order to understand the molecular basis of the interspecies transmission of H9N2 viruses, we adapted in the laboratory a wildtype duck H9N2 virus, influenza A/duck/Hong Kong/702/79 (WT702) virus, in quail and chickens through serial lung passages. We carried out comparative analysis of the replication and transmission in quail and chickens of WT702 and the viruses obtained after 23 serial passages in quail (QA23) followed by 10 serial passages in chickens (QA23CkA10). Although the WT702 virus can replicate and transmit in quail, it replicates poorly and does not transmit in chickens. In contrast, the QA23CkA10 virus was very efficient at replicating and transmitting in quail and chickens. Nucleotide sequence analysis of the QA23 and QA23CkA10 viruses compared to the WT702 virus indicated several nucleotide substitutions resulting in amino acid changes within the surface and internal proteins. In addition, a 21-amino acid deletion was found in the stalk of the NA protein of the QA23 virus and was maintained without further modification in the QA23CkA10 adapted virus. More importantly, both the QA23 and the QA23CkA10 viruses, unlike the WT702 virus, were able to readily infect mice, produce a large-plaque phenotype, showed faster replication kinetics in tissue culture, and resulted in the quick selection of the K627 amino acid mammalian-associated signature in PB2. These results are in agreement with the notion that adaptation of H9 viruses to land-based birds can lead to strains with expanded host range.
Hossain
Md Jaber
MJ
Department of Veterinary Medicine, University of Maryland, College Park, Maryland, United States of America.
Hickman
Danielle
D
Perez
Daniel R
DR
D000818:Animals; D001483:Base Sequence; D018929:Cell Culture Techniques / Q000379:methods; D002645:Chickens; D017353:Gene Deletion; D016679:Genome, Viral; D053127:Influenza A Virus, H9N2 Subtype / Q000235:genetics*; D005585:Influenza in Birds / Q000235:genetics* / Q000821:virology*; D007422:Intestines / Q000821:virology; D008168:Lung / Q000378:metabolism / Q000821:virology; D051379:Mice; D008969:Molecular Sequence Data; D011784:Quail; D012689:Sequence Homology, Nucleic Acid; D013045:Species Specificity
J Virol. 2003 Mar;77(5):3148-56
12584339
Virology. 2005 Sep 15;340(1):70-83
16026813
Nature. 2004 Jul 8;430(6996):209-13
15241415
Virology. 2005 Aug 15;339(1):101-9
15964604
J Clin Microbiol. 2005 Nov;43(11):5760-7
16272514
Virology. 2003 May 25;310(1):8-15
12788625
Virology. 2000 Feb 15;267(2):279-88
10662623
Vaccine. 2007 Jul 26;25(30):5637-44
17126960
J Virol. 1999 Feb;73(2):1146-55
9882316
Microbes Infect. 2004 Aug;6(10):919-25
15310468
Lancet. 1999 Sep 11;354(9182):916-7
10489954
J Gen Virol. 2005 Feb;86(Pt 2):423-433
15659762
Arch Virol. 1991;119(1-2):37-42
1863223
Avian Dis. 2003;47(3 Suppl):828-31
14575072
J Virol. 2003 Mar;77(6):3816-23
12610156
J Gen Virol. 1994 Sep;75 ( Pt 9):2183-8
8077918
Proc Natl Acad Sci U S A. 2004 Feb 3;101(5):1356-61
14745020
J Virol. 2004 Aug;78(16):8609-14
15280470
Avian Dis. 2000 Jul-Sep;44(3):527-35
11006999
J Virol. 2007 Mar;81(6):2635-45
17192315
Virology. 2001 Mar 15;281(2):156-62
11277689
Vaccine. 2001 Oct 12;20(1-2):125-33
11567756
J Virol. 2005 Sep;79(18):12058-64
16140781
Vet Microbiol. 2006 Dec 20;118(3-4):169-76
16930870
J Virol. 2007 Jul;81(13):7011-21
17442719
Avian Dis. 2003;47(3 Suppl):1114-7
14575124
Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi. 1999 Jun 30;13(2):105-8
12569771
Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9654-8
10920197
Vaccine. 2002 Aug 19;20(25-26):3165-70
12163268
PLoS One. 2008 Aug 13;3(8):e2923
18698430
Vet Rec. 1999 Nov 6;145(19):560
10609578
Vet Microbiol. 2002 Aug 25;88(2):107-14
12135631
Infect Immun. 1982 Sep;37(3):1119-26
7129631
Semin Respir Infect. 1992 Mar;7(1):11-25
1609163
Avian Dis. 2007 Mar;51(1 Suppl):264-8
17494563
Infect Immun. 1981 Nov;34(2):354-61
7309229
Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9363-7
10430948
J Virol. 2007 Sep;81(17):9238-48
17596317
J Virol. 1993 Apr;67(4):1761-4
8445709
Virology. 2003 Jan 20;305(2):267-75
12573572
J Virol. 2000 Oct;74(20):9372-80
11000205
Avian Dis. 1970 Feb;14(1):66-74
4314007
J Virol. 2007 May;81(10):5181-91
17344280
J Clin Microbiol. 1999 Oct;37(10):3426-7
10488228
Avian Dis. 2003;47(3 Suppl):1079-82
14575115
Virology. 2000 Dec 5;278(1):36-41
11112478
Virology. 2007 Apr 25;361(1):45-55
17157891
Science. 2001 Sep 7;293(5536):1840-2
11546875
J Virol. 2001 Oct;75(20):9679-86
11559800
Virology. 2006 Mar 15;346(2):278-86
16325879
J Gen Virol. 2000 May;81(Pt 5):1283-91
10769071
J Virol. 2007 Jun;81(11):5995-6006
17376915