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VACCINE RESEARCH

DNA Vaccination Elicits Protective Immune Responses against Pandemic and Classic Swine Influenza Viruses in Pigs

J. Patrick Gorres, Kelly M. Lager, Wing-Pui Kong, Michael Royals, John-Paul Todd, Amy L. Vincent, Chih-Jen Wei, Crystal L. Loving, Eraldo L. Zanella, Bruce Janke, Marcus E. Kehrli Jr., Gary J. Nabel, Srinivas S. Rao
J. Patrick Gorres
1Laboratory Animal Medicine, Vaccine Research Center, National Institutes of Health, Bethesda, Maryland 20892
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Kelly M. Lager
2Virus and Prion Diseases Research Unit, National Animal Disease Center, U.S. Department of Agriculture Agricultural Research Service, Ames, Iowa 50010
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Wing-Pui Kong
3Vector Core, Vaccine Research Center, National Institutes of Health, Bethesda, Maryland 20892
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Michael Royals
4PharmaJet, Inc., Golden, Colorado 80401
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John-Paul Todd
1Laboratory Animal Medicine, Vaccine Research Center, National Institutes of Health, Bethesda, Maryland 20892
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Amy L. Vincent
2Virus and Prion Diseases Research Unit, National Animal Disease Center, U.S. Department of Agriculture Agricultural Research Service, Ames, Iowa 50010
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Chih-Jen Wei
3Vector Core, Vaccine Research Center, National Institutes of Health, Bethesda, Maryland 20892
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Crystal L. Loving
2Virus and Prion Diseases Research Unit, National Animal Disease Center, U.S. Department of Agriculture Agricultural Research Service, Ames, Iowa 50010
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Eraldo L. Zanella
5Universidade de Passo Fundo, Curso de Medicina Veterinária, Campus Universitário do Bairro São José, Caixa Postal 611, Passo Fundo RS 99001-970, Brazil
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Bruce Janke
6Iowa State University College of Veterinary Medicine, Vet Diagnostic and Production Animal Med, 1657 Vet Med, Ames, Iowa 50011
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Marcus E. Kehrli Jr.
2Virus and Prion Diseases Research Unit, National Animal Disease Center, U.S. Department of Agriculture Agricultural Research Service, Ames, Iowa 50010
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Gary J. Nabel
3Vector Core, Vaccine Research Center, National Institutes of Health, Bethesda, Maryland 20892
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Srinivas S. Rao
1Laboratory Animal Medicine, Vaccine Research Center, National Institutes of Health, Bethesda, Maryland 20892
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  • For correspondence: srao1@mail.nih.gov
DOI: 10.1128/CVI.05171-11
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  • Fig. 1.
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    Fig. 1.

    DNA vaccination elicits anti-H1N1 antibody responses detectable by an HI assay. Antibody titers against A/California/2009 and A/Ohio/2007 in vaccinated and control (sham DNA-vaccinated) pigs were determined by an HI assay, with 10 pigs/group. Log10 transformations of the data are plotted with error bars representing standard deviations (SD). For A/California/2009, data for five treatment groups are presented: animals receiving a monovalent NS vaccine, a monovalent NF vaccine, a trivalent NS vaccine, or a trivalent NF vaccine and controls. The same symbols are used for the HI tests against A/Ohio/2007, excluding the monovalent vaccine groups.

  • Fig. 2.
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    Fig. 2.

    A pseudotype lentiviral inhibition assay confirms anti-H1N1 neutralizing antibody responses in pooled sera. Neutralizing antibody responses against A/California/2009 and A/Ohio/2007 were confirmed by a pseudotype inhibition assay performed on pooled sera from each treatment group, with 10 pigs/group. Neutralizing antibody titers are presented as log10 transformations of half-maximal inhibitory concentrations (IC50). Data points are plotted for each treatment group with the same symbols used in Fig. 1.

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    Fig. 3.

    DNA vaccination elicits IFN-γ responses measured by an ELISpot assay with PBMCs collected 1 week prior to H1N1 challenge. An ELISpot assay was used to detect cells secreting IFN-γ against A/California/2009 and A/Ohio/2007 in vaccinated animals. Results are presented as single data points in a group, with lines indicating the mean and standard error of the mean (SEM) for each group. A Mann-Whitney t test was used for statistical analysis comparing values between immunized and nonimmunized control animals. P values of less than 0.05 are indicated: * represents a P value between 0.05 and 0.001, while ** indicates a P value of ≤0.001. θ indicates a value that is nonsignificant when Bonferroni's adjustment is applied.

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    Fig. 4.

    DNA vaccination reduces viral load and protects against H1N1 influenza virus challenge. Immunized and control animals were challenged with either H1N1 A/California/2009 or A/Ohio/2007. Postchallenge viral loads were assessed for up to 7 days using a plaque reduction assay. Viral titers are presented as the log of the TCID50 for each animal, with bars indicating means and error bars indicating SEMs. Differences between immunized animals and controls were analyzed for statistical significance using a Mann-Whitney t test. P values of less than 0.05 are indicated: * represents a P value between 0.05 and 0.001, while ** indicates a value of ≤0.001. θ indicates a value that is nonsignificant when Bonferroni's adjustment is applied.

  • Fig. 5.
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    Fig. 5.

    DNA vaccination elicits protection from lung disease induced by A/California/2009 challenge and prevents viral replication in the lung. Lungs were collected from 5 pigs per group at 5 dpc with A/California/2009. Hematoxylin and eosin staining was performed to assess histopathology, and immunohistochemistry analysis was performed to detect influenza virus antigens in the lung. Micrographs are representative for each treatment group (including monovalent NS and NF vaccine groups) at a magnification of ×20. See Results for lesion description. In panel A, the epithelium lining the bronchiole is irregular (arrow), and prominent peribronchiolar lymphocyte infiltration (*) is evident. In the control IHC photomicrograph in panel E, virus antigen in bronchiolar epithelial cells (arrow) appears as brown coloration of the nucleus and cytoplasm.

  • Fig. 6.
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    Fig. 6.

    DNA vaccination elicits protection from lung disease induced by A/Ohio/2007 challenge and prevents viral replication in the lung. Lungs were collected from 5 pigs per group at 5 dpc with A/Ohio/2007. Hematoxylin and eosin staining was performed to assess histopathology, and immunohistochemistry analysis was performed to detect influenza virus antigens in the lung. Micrographs are representative for each treatment group at a magnification of ×20, except for one animal immunized with a trivalent NF vaccine in which virus was detected. See Results for lesion description. In panel A, the epithelium lining the bronchiole is irregular (arrow), and prominent peribronchiolar lymphocyte infiltration (*) is evident. In the control IHC photomicrograph in panel D, virus antigen in bronchiolar epithelial cells (arrow) appears as brown coloration of the nucleus and cytoplasm.

Tables

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  • Table 1.

    Experimental schema evaluating immunogenicity, protection, and needle-free injectiona

    GroupDNA vaccine (delivery method)H1N1 challenge virus
    1Control (sham DNA) (NS injection)A/Ohio/2007
    2Control (sham DNA) (NS injection)A/California/2009
    3Trivalent (NS injection)A/Ohio/2007
    4Trivalent (NS injection)A/California/2009
    5Monovalent (NS injection)A/California/2009
    6Trivalent (NF delivery)A/Ohio/2007
    7Trivalent (NF delivery)A/California/2009
    8Monovalent (NF delivery)A/California/2009
    • ↵a The treatment group number, type of vaccine (and delivery method), and challenge virus are presented. The monovalent DNA vaccine encodes HA from H1N1 A/California/2009, while the trivalent DNA vaccine encodes HAs from H1N1 A/California/2009, H1N1 A/Ohio/2007, and H3N2 A/North Carolina/2008. The negative control group was inoculated with empty sham DNA. Each group contained 10 animals that received a 4-mg/ml dose of vaccine at weeks 0, 3, and 6. Animals were challenged with H1N1 virus at week 9.

Additional Files

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  • Supplemental Material

    Files in this Data Supplement:

    • Supplemental Figure 1 - Fig. S1. Trivalent DNA vaccination elicits humoral responses and protects against H3N2 challenge.
      TIF Image file, 1.1 MB.
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DNA Vaccination Elicits Protective Immune Responses against Pandemic and Classic Swine Influenza Viruses in Pigs
J. Patrick Gorres, Kelly M. Lager, Wing-Pui Kong, Michael Royals, John-Paul Todd, Amy L. Vincent, Chih-Jen Wei, Crystal L. Loving, Eraldo L. Zanella, Bruce Janke, Marcus E. Kehrli Jr., Gary J. Nabel, Srinivas S. Rao
Clinical and Vaccine Immunology Nov 2011, 18 (11) 1987-1995; DOI: 10.1128/CVI.05171-11

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DNA Vaccination Elicits Protective Immune Responses against Pandemic and Classic Swine Influenza Viruses in Pigs
J. Patrick Gorres, Kelly M. Lager, Wing-Pui Kong, Michael Royals, John-Paul Todd, Amy L. Vincent, Chih-Jen Wei, Crystal L. Loving, Eraldo L. Zanella, Bruce Janke, Marcus E. Kehrli Jr., Gary J. Nabel, Srinivas S. Rao
Clinical and Vaccine Immunology Nov 2011, 18 (11) 1987-1995; DOI: 10.1128/CVI.05171-11
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    • ABSTRACT
    • INTRODUCTION
    • MATERIALS AND METHODS
    • RESULTS
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    • ACKNOWLEDGMENTS
    • FOOTNOTES
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