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Pathogenesis and Immunity

Zoonotic Risk, Pathogenesis, and Transmission of Avian-Origin H3N2 Canine Influenza Virus

Hailiang Sun, Sherry Blackmon, Guohua Yang, Kaitlyn Waters, Tao Li, Ratanaporn Tangwangvivat, Yifei Xu, Daniel Shyu, Feng Wen, Jim Cooley, Lucy Senter, Xiaoxu Lin, Richard Jarman, Larry Hanson, Richard Webby, Xiu-Feng Wan
Jae U. Jung, Editor
Hailiang Sun
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Sherry Blackmon
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Guohua Yang
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Kaitlyn Waters
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Tao Li
bViral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
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Ratanaporn Tangwangvivat
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Yifei Xu
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Daniel Shyu
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Feng Wen
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Jim Cooley
cDepartment of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Lucy Senter
dDepartment of Clinical Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Xiaoxu Lin
bViral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
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Richard Jarman
bViral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland, USA
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Larry Hanson
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Richard Webby
eDepartment of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, USA
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Xiu-Feng Wan
aDepartment of Basic Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi, USA
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Jae U. Jung
University of Southern California
Roles: Editor
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DOI: 10.1128/JVI.00637-17
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  • FIG 1
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    FIG 1

    Ribonucleoprotein complex luciferase activity and reassortant virus frequency. The luciferase activities of all 16 RNP complexes between GD06 (shaded in brown) and CA09 (shaded in purple) were compared. The ratio of Renilla luciferase to firefly luciferase (Rluc/Fluc) is expressed as the mean + standard deviation from three independent experiments, and statistical analysis was performed using a one-way ANOVA with post hoc Tukey's multiple-comparison test. The reassortant virus RNP data were frequency counts from Tables 1 and 2.

  • FIG 2
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    FIG 2

    Viral lung titers of inoculated mice. Mice (n = 3) were intranasally inoculated with 50 μl of 106 TCID50/ml of virus per ml. At 4 dpi they were necropsied and lung tissues were collected for determination of virus titers. Titers are expressed as the mean ± standard deviation.

  • FIG 3
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    FIG 3

    Growth kinetics of viruses. The growth kinetics of each virus shown were characterized in MDCK cells (A) or A549 cells (B) at an MOI of 0.001. Virus titers are expressed as the mean ± standard deviation from three independent experiments. The limit of virus detection was 100.699 TCID50/ml. R109, reassortant 109.

  • FIG 4
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    FIG 4

    Viral titers in nasal wash fluids from ferrets. Ferrets were inoculated with 106 TCID50 of the GD06 virus (A, C) or the reassortant 109 virus (E, G). Naive ferrets were exposed either by direct contact with GD06-inoculated ferrets (B) or by aerosol contact with GD06-infected ferrets (D). (F, H) The same scheme described above was followed for reassortant 109, with naive ferrets being exposed by direct contact (F) or by aerosol exposure (H). At 3, 5, 7, and 10 dpi, nasal wash fluids were collected from ferrets and titrated in MDCK cells. The end titers are expressed as the number of log10 TCID50 per milliliter. The limit of virus detection was 100.699 TCID50/ml.

  • FIG 5
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    FIG 5

    Viral titers from ferret tissues. Ferrets were inoculated with 106 TCID50 of GD06, reassortant 109, or PBS as a control. At 5 dpi they were humanely euthanized and nasal turbinate, tracheal, and lung tissues were collected. The tissues were homogenized and then titrated in MDCK cells. The limit of virus detection was 100.699 TCID50/ml. No virus was detected in the lungs. Reassortant 109 replicated in nasal turbinate and tracheal tissues, whereas GD06 was detected only in nasal turbinate tissue.

  • FIG 6
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    FIG 6

    Histopathology of ferret nasal turbinate, tracheal, and lung tissues. Ferrets were inoculated with 106 TCID50 of GD06 virus, reassortant 109, or PBS as a control. At 5 dpi they were euthanized and nasal turbinate, tracheal, and lung tissues were collected. One GD06-infected ferret had moderate turbinate pathology (rhinitis with moderate lamina proprial lymphoplasmacellular infiltrates and a loss of cilia or replacement of the respiratory mucosal epithelium by stratified squamous epithelium), whereas the other had minimal pathology (minimal lamina proprial lymphoplasmacellular infiltrates). Both reassortant 109-infected ferrets had moderate to severe turbinate pathology, including lymphoplasmacellular rhinitis and a loss of cilia or replacement of the normal mucosal epithelium by stratified squamous epithelium. No significant lesions were seen in the trachea of any of the ferrets. There was mild lung pathology, including peribronchitis and peribronchiolitis, in one ferret infected with reassortant 109.

Tables

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  • TABLE 1

    Reassortant viruses expressing a high-growth phenotypea

    TABLE 1
    • ↵a A high-growth phenotype was growth of ≥106 TCID50/ml. Data are for 19 reassortants. Reassortant viruses were generated from in vitro transfection of cocultured MDCK and 293T cells with plasmids from CA04 viruses (shaded in brown) and GD06 viruses (shaded in purple), and virus titers were obtained after a single propagation in MDCK cells.

  • TABLE 2

    Reassortant viruses expressing a moderate-growth phenotypea

    TABLE 2
    • ↵a A moderate-growth phenotype was growth of <106 TCID50/ml. Data are for 32 reassortants. Reassortant viruses were generated from in vitro transfection of cocultured MDCK and 293T cells with plasmids from CA04 viruses (shaded in brown) and GD06 viruses (shaded in purple), and virus titers were obtained after a single propagation in MDCK cells.

  • TABLE 3

    HI titers for serum samples from ferrets inoculated with IAV and from PBS-inoculated control ferrets in aerosol and direct-contact exposure experiments

    Virus, experimental groupaHI titerb
    Ferret 1Ferret 2Ferret 3
    GD06
        Aerosol
            Inoculated ferret3201,2801,280
            Exposed ferret<10<10—c
        Direct contact
            Inoculated ferret——640
            Exposed ferret<106401,280
    Reassortant 109
        Aerosol
            Inoculated ferret6401,2801,280
            Exposed ferret<10<10—
        Direct contact
            Inoculated ferret——2,560
            Exposed ferret2,5606401,280
    PBS control——<10
    • ↵a IAV-inoculated ferrets were intranasally inoculated with 106 TCID50 of virus; control ferrets were inoculated with 1 ml of PBS.

    • ↵b Serum samples were collected at 21 days postinoculation, and HI titers were determined using 0.5% turkey erythrocytes.

    • ↵c The hemagglutination inhibition titer was not available because the ferret was euthanized.

Additional Files

  • Figures
  • Tables
  • Supplemental material

    • Supplemental file 1 -

      Fig. S1 (Body weight variations in infected mice.)

      Table S1 (Genomic constellation of reassortant viruses that could not be generated.)

      Table S2 (HI titer of serum collected from mice at 14 days postinfection.)

      PDF, 556K

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Zoonotic Risk, Pathogenesis, and Transmission of Avian-Origin H3N2 Canine Influenza Virus
Hailiang Sun, Sherry Blackmon, Guohua Yang, Kaitlyn Waters, Tao Li, Ratanaporn Tangwangvivat, Yifei Xu, Daniel Shyu, Feng Wen, Jim Cooley, Lucy Senter, Xiaoxu Lin, Richard Jarman, Larry Hanson, Richard Webby, Xiu-Feng Wan
Journal of Virology Oct 2017, 91 (21) e00637-17; DOI: 10.1128/JVI.00637-17

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Zoonotic Risk, Pathogenesis, and Transmission of Avian-Origin H3N2 Canine Influenza Virus
Hailiang Sun, Sherry Blackmon, Guohua Yang, Kaitlyn Waters, Tao Li, Ratanaporn Tangwangvivat, Yifei Xu, Daniel Shyu, Feng Wen, Jim Cooley, Lucy Senter, Xiaoxu Lin, Richard Jarman, Larry Hanson, Richard Webby, Xiu-Feng Wan
Journal of Virology Oct 2017, 91 (21) e00637-17; DOI: 10.1128/JVI.00637-17
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    • ABSTRACT
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KEYWORDS

Dog Diseases
Influenza A Virus, H1N1 Subtype
Influenza A Virus, H3N2 Subtype
lung
Orthomyxoviridae Infections
zoonoses
influenza A virus
canine influenza virus
H3N2
A(H1N1)pdm09
2009 H1N1 influenza A virus
risk assessment
zoonosis
reassortment
aerosol transmission
viral pathogenesis

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