Infection of the Upper Respiratory Tract with Seasonal Influenza A(H3N2) Virus Induces Protective Immunity in Ferrets against Infection with A(H1N1)pdm09 Virus after Intranasal, but Not Intratracheal, Inoculation

Bodewes, Rogier; Kreijtz, Joost H. C. M.; Amerongen, Geert van; Hillaire, Marine L. B.; Trierum, Stella E. Vogelzang-van; Nieuwkoop, Nella J.; Run, Peter van; Kuiken, Thijs; Fouchier, Ron A. M.; Osterhaus, Albert D. M. E.; Rimmelzwaan, Guus F.

doi:10.1128/jvi.02536-12

Cited by 42 publications

(39 citation statements)

References 56 publications

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“…These antibodies would then also contribute to broad protection. Furthermore, conserved internal proteins like the nucleoprotein induce strong protective T-cell responses that contribute to protection as well (71)(72)(73)(74). We have conclusively shown that such a vaccination strategy based on the H1 HA stalk domain is able to broadly protect against group 1 HA-expressing viruses in mice but was unable to protect against an H3N2 challenge virus (21).…”

Section: Discussionmentioning

confidence: 99%

Assessment of Influenza Virus Hemagglutinin Stalk-Based Immunity in Ferrets

Krammer

Hai

Yondola

et al. 2014

J Virol

128

131

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Therapeutic monoclonal antibodies that target the conserved stalk domain of the influenza virus hemagglutinin and stalk-based universal influenza virus vaccine strategies are being developed as promising countermeasures for influenza virus infections. The pan-H1-reactive monoclonal antibody 6F12 has been extensively characterized and shows broad efficacy against divergent H1N1 strains in the mouse model. Here we demonstrate its efficacy against a pandemic H1N1 challenge virus in the ferret model of influenza disease. Furthermore, we recently developed a universal influenza virus vaccine strategy based on chimeric hemagglutinin constructs that focuses the immune response on the conserved stalk domain of the hemagglutinin. Here we set out to test this vaccination strategy in the ferret model. Both strategies, pretreatment of animals with a stalk-reactive monoclonal antibody and vaccination with chimeric hemagglutinin-based constructs, were able to significantly reduce viral titers in nasal turbinates, lungs, and olfactory bulbs. In addition, vaccinated animals also showed reduced nasal wash viral titers. In summary, both strategies showed efficacy in reducing viral loads after an influenza virus challenge in the ferret model. IMPORTANCEInfluenza virus hemagglutinin stalk-reactive antibodies tend to be less potent yet are more broadly reactive and can neutralize seasonal and pandemic influenza virus strains. The ferret model was used to assess the potential of hemagglutinin stalk-based immunity to provide protection against influenza virus infection. The novelty and significance of the findings described in this report support the development of vaccines stimulating stalk-specific antibody responses.

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Section: Discussionmentioning

confidence: 99%

Assessment of Influenza Virus Hemagglutinin Stalk-Based Immunity in Ferrets

Krammer

Hai

Yondola

et al. 2014

J Virol

128

131

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show abstract

“…T he route or site of inoculation has been shown to significantly influence disease outcome in numerous models of infection, including Leishmania (1-9), Toxoplasma (10), Plasmodium (11), Listeria (12)(13)(14), Borrelia (15), and influenza virus (16,17) infections. Vaccination by different routes has also been shown to influence the efficacy of vaccines against parasitic, bacterial, and viral infections, as well as cancer (3,(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28).…”

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confidence: 99%

Site-Dependent Recruitment of Inflammatory Cells Determines the Effective Dose of Leishmania major

et al. 2014

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“…A non‐exhaustive list of strategies to induce heterosubtypic immunity against influenza evaluated in ferrets include: HA stem vaccination; prime‐boost with chimeric HA‐based vaccines; use of conserved influenza proteins such as nucleoprotein (NP), matrix‐1 (M1), matrix‐2 (M2) and RNA polymerase subunit B1 (PB1); replication‐deficient viruses; live attenuated formulations; the use of potent adjuvants such as Protollin, glucopyranosyl lipid adjuvant—aqueous formulation (GLA‐AF), CoVaccine HT, cationic adjuvant formulation and poly‐g‐glutamic/chitosan nanogel; Escherichia coli ‐derived vaccines; DNA, mRNA and viral vector vaccines; and the use of virus‐like particles (VLP) . Additional examples of important ferret studies include (but are not limited to) evaluating the influence of changing the route of influenza inoculation on subsequent immunity and the use of neuraminidase (NA) inhibitors as prophylaxis …”

Section: Ferrets For Influenza Surveillance and Vaccine Developmentmentioning

confidence: 99%

Improving immunological insights into the ferret model of human viral infectious disease

Wong

Layton

Wheatley

et al. 2019

Influenza Resp Viruses

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Influenza Other Respi Viruses. 2019;13:535-546. | 535 wileyonlinelibrary.com/journal/irv 1 | INTRODUC TI ON Animal models have proved critical in developing concepts of immunity to infection. Non-human primates (NHP) are a highly humanrelevant disease model for infectious agents due to high genetic conservation between humans and NHP. 1-3 However, significant cost and ethical issues often necessitate the use of smaller animal models for both basic and translational research. Mice (Mus musculus) are a favoured small animal model due to widespread availability, incisive transgenic models, comprehensive genomic information 4 and readily available reagents. However, for many viruses, alternative animal models better recapitulate human physiology and disease. Ferrets (Mustela putorius furo) have been employed to study the pathogenesis of a variety of human pathogens, including human and avian influenzas, coronaviruses including severe acute respiratory syndrome (SARS-CoV), 5-14 human respiratory syncytial virus (HRSV), 15-20 human metapneumovirus (HMPV), 21 Ebola virus 22-28 and henipavirus (Nipah virus and Hendra virus). 29-34 While ferretscan be productively infected with many of these viruses, a lack of some tools to interrogate ferret immunological responses to infection limits insights that might impact the development of vaccines and/or therapeutics. Here, we review recent insights gained from ferret models of human respiratory diseases, with a major focus on influenza, and highlight several knowledge gaps whose closure will greatly enhance the informational gain from ferret models to advance development of human vaccines and therapeutics. AbstractFerrets are a well-established model for studying both the pathogenesis and transmission of human respiratory viruses and evaluation of antiviral vaccines. Advanced immunological studies would add substantial value to the ferret models of disease but are hindered by the low number of ferret-reactive reagents available for flow cytometry and immunohistochemistry. Nevertheless, progress has been made to understand immune responses in the ferret model with a limited set of ferret-specific reagents and assays. This review examines current immunological insights gained from the ferret model across relevant human respiratory diseases, with a focus on influenza viruses. We highlight key knowledge gaps that need to be bridged to advance the utility of ferrets for immunological studies. K E Y W O R D S ferret, immunology, influenza How to cite this article: Wong J, Layton D, Wheatley AK, Kent SJ. Improving immunological insights into the ferret model of human viral infectious disease. Influenza Other Respi Viruses. 2019;13:535-546. https ://doi.

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Infection of the Upper Respiratory Tract with Seasonal Influenza A(H3N2) Virus Induces Protective Immunity in Ferrets against Infection with A(H1N1)pdm09 Virus after Intranasal, but Not Intratracheal, Inoculation

Cited by 42 publications

References 56 publications

Assessment of Influenza Virus Hemagglutinin Stalk-Based Immunity in Ferrets

Assessment of Influenza Virus Hemagglutinin Stalk-Based Immunity in Ferrets

Site-Dependent Recruitment of Inflammatory Cells Determines the Effective Dose of Leishmania major

Improving immunological insights into the ferret model of human viral infectious disease

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