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Viruses
Special Issues
Animal Models for Influenza Virus Research
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Animal Models for Influenza Virus Research

A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "Animal Viruses".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 21028

Special Issue Editors

Dr. Jessica A. Belser

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Guest Editor
Immunology and Pathogenesis Branch, Influenza Division, Centers for Disease Control and Prevention, Atlanta, GA 30333 USA
Interests: H7 subtype influenza viruses; ocular tropism; animal model development
Dr. Joanna A. Pulit-Penaloza

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Guest Editor
Immunology and Pathogenesis Branch, Influenza Division, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA
Interests: correlates of zoonotic virus transmission; aerobiology of influenza viruses; ferret model
Dr. Xiangjie Sun

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Guest Editor
Immunology and Pathogenesis Branch, Influenza Division, Centers for Disease Control and Prevention, Atlanta, GA 30333 USA
Interests: influenza virus pathogenesis, virus-host interactions, virus stability and airborne transmission

Special Issue Information

Dear Colleagues,

Responsible for annual epidemics and occasional pandemics in humans, influenza viruses represent a persistent threat to human health. The multifactorial nature of influenza virus–host interactions (including tropism, pathogenicity, transmissibility, and induction of innate and adaptive immune responses) necessitates in vivo study to fully elucidate its complex properties. As such, there is a need for well-characterized laboratory animal models to conduct research critical to human health protection and pandemic preparedness.

Reflecting the wide utility and applicability of animal models in the laboratory study of both human and zoonotic influenza viruses, this Special Issue will discuss a similarly diverse range of topics. These include the development and characterization of different model species, the refinement of established models to more closely recapitulate human infection and disease, and the assessment of wild-type and recombinant influenza viruses in these models. Studies employing animal models to evaluate the efficacy of vaccine and antiviral formulations and those investigating the role of host factors and molecular determinants of virulence and transmission in these models are similarly invited. We welcome all article types (including primary research articles and reviews) for publication consideration.

Dr. Jessica A. Belser
Dr. Joanna A. Pulit-Penaloza
Dr. Xiangjie Sun
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Viruses is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • influenza virus
  • animal models
  • virus–host interactions
  • pathogenesis
  • transmission
  • tropism
  • host response
  • vaccines
  • antivirals
  • virus diversity
  • mouse
  • ferret
  • Guinea pig

Published Papers (5 papers)

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Research

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17 pages, 1640 KiB  
Article
N-Glycolylneuraminic Acid in Animal Models for Human Influenza A Virus
by Cindy M. Spruit, Nikoloz Nemanichvili, Masatoshi Okamatsu, Hiromu Takematsu, Geert-Jan Boons and Robert P. de Vries
Viruses 2021, 13(5), 815; https://doi.org/10.3390/v13050815 - 01 May 2021
Cited by 10 | Viewed by 3153
Abstract
The first step in influenza virus infection is the binding of hemagglutinin to sialic acid-containing glycans present on the cell surface. Over 50 different sialic acid modifications are known, of which N-acetylneuraminic acid (Neu5Ac) and N-glycolylneuraminic acid (Neu5Gc) are the two main species. [...] Read more.
The first step in influenza virus infection is the binding of hemagglutinin to sialic acid-containing glycans present on the cell surface. Over 50 different sialic acid modifications are known, of which N-acetylneuraminic acid (Neu5Ac) and N-glycolylneuraminic acid (Neu5Gc) are the two main species. Animal models with α2,6 linked Neu5Ac in the upper respiratory tract, similar to humans, are preferred to enable and mimic infection with unadapted human influenza A viruses. Animal models that are currently most often used to study human influenza are mice and ferrets. Additionally, guinea pigs, cotton rats, Syrian hamsters, tree shrews, domestic swine, and non-human primates (macaques and marmosets) are discussed. The presence of NeuGc and the distribution of sialic acid linkages in the most commonly used models is summarized and experimentally determined. We also evaluated the role of Neu5Gc in infection using Neu5Gc binding viruses and cytidine monophosphate-N-acetylneuraminic acid hydroxylase (CMAH)−/− knockout mice, which lack Neu5Gc and concluded that Neu5Gc is unlikely to be a decoy receptor. This article provides a base for choosing an appropriate animal model. Although mice are one of the most favored models, they are hardly naturally susceptible to infection with human influenza viruses, possibly because they express mainly α2,3 linked sialic acids with both Neu5Ac and Neu5Gc modifications. We suggest using ferrets, which resemble humans closely in the sialic acid content, both in the linkages and the lack of Neu5Gc, lung organization, susceptibility, and disease pathogenesis. Full article
(This article belongs to the Special Issue Animal Models for Influenza Virus Research)
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13 pages, 1967 KiB  
Article
Cell-Culture Adaptation of H3N2 Influenza Virus Impacts Acid Stability and Reduces Airborne Transmission in Ferret Model
by Valerie Le Sage, Karen A. Kormuth, Eric Nturibi, Juhye M. Lee, Sheila A. Frizzell, Michael M. Myerburg, Jesse D. Bloom and Seema S. Lakdawala
Viruses 2021, 13(5), 719; https://doi.org/10.3390/v13050719 - 21 Apr 2021
Cited by 8 | Viewed by 3090
Abstract
Airborne transmission of seasonal and pandemic influenza viruses is the reason for their epidemiological success and public health burden in humans. Efficient airborne transmission of the H1N1 influenza virus relies on the receptor specificity and pH of fusion of the surface glycoprotein hemagglutinin [...] Read more.
Airborne transmission of seasonal and pandemic influenza viruses is the reason for their epidemiological success and public health burden in humans. Efficient airborne transmission of the H1N1 influenza virus relies on the receptor specificity and pH of fusion of the surface glycoprotein hemagglutinin (HA). In this study, we examined the role of HA pH of fusion on transmissibility of a cell-culture-adapted H3N2 virus. Mutations in the HA head at positions 78 and 212 of A/Perth/16/2009 (H3N2), which were selected after cell culture adaptation, decreased the acid stability of the virus from pH 5.5 (WT) to pH 5.8 (mutant). In addition, the mutant H3N2 virus replicated to higher titers in cell culture but had reduced airborne transmission in the ferret model. These data demonstrate that, like H1N1 HA, the pH of fusion for H3N2 HA is a determinant of efficient airborne transmission. Surprisingly, noncoding regions of the NA segment can impact the pH of fusion of mutant viruses. Taken together, our data confirm that HA acid stability is an important characteristic of epidemiologically successful human influenza viruses and is influenced by HA/NA balance. Full article
(This article belongs to the Special Issue Animal Models for Influenza Virus Research)
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Review

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13 pages, 2424 KiB  
Review
In Vivo Models to Study the Pathogenesis of Extra-Respiratory Complications of Influenza A Virus Infection
by Edwin Veldhuis Kroeze, Lisa Bauer, Valentina Caliendo and Debby van Riel
Viruses 2021, 13(5), 848; https://doi.org/10.3390/v13050848 - 06 May 2021
Cited by 7 | Viewed by 2546
Abstract
Animal models are an inimitable method to study the systemic pathogenesis of virus-induced disease. Extra-respiratory complications of influenza A virus infections are not extensively studied even though they are often associated with severe disease and mortality. Here we review and recommend mammalian animal [...] Read more.
Animal models are an inimitable method to study the systemic pathogenesis of virus-induced disease. Extra-respiratory complications of influenza A virus infections are not extensively studied even though they are often associated with severe disease and mortality. Here we review and recommend mammalian animal models that can be used to study extra-respiratory complications of the central nervous system and cardiovascular system as well as involvement of the eye, placenta, fetus, lacteal gland, liver, pancreas, intestinal tract, and lymphoid tissues during influenza A virus infections. Full article
(This article belongs to the Special Issue Animal Models for Influenza Virus Research)
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32 pages, 1628 KiB  
Review
Hemagglutinin Stability and Its Impact on Influenza A Virus Infectivity, Pathogenicity, and Transmissibility in Avians, Mice, Swine, Seals, Ferrets, and Humans
by Charles J. Russell
Viruses 2021, 13(5), 746; https://doi.org/10.3390/v13050746 - 24 Apr 2021
Cited by 35 | Viewed by 8190
Abstract
Genetically diverse influenza A viruses (IAVs) circulate in wild aquatic birds. From this reservoir, IAVs sporadically cause outbreaks, epidemics, and pandemics in wild and domestic avians, wild land and sea mammals, horses, canines, felines, swine, humans, and other species. One molecular trait shown [...] Read more.
Genetically diverse influenza A viruses (IAVs) circulate in wild aquatic birds. From this reservoir, IAVs sporadically cause outbreaks, epidemics, and pandemics in wild and domestic avians, wild land and sea mammals, horses, canines, felines, swine, humans, and other species. One molecular trait shown to modulate IAV host range is the stability of the hemagglutinin (HA) surface glycoprotein. The HA protein is the major antigen and during virus entry, this trimeric envelope glycoprotein binds sialic acid-containing receptors before being triggered by endosomal low pH to undergo irreversible structural changes that cause membrane fusion. The HA proteins from different IAV isolates can vary in the pH at which HA protein structural changes are triggered, the protein causes membrane fusion, or outside the cell the virion becomes inactivated. HA activation pH values generally range from pH 4.8 to 6.2. Human-adapted HA proteins tend to have relatively stable HA proteins activated at pH 5.5 or below. Here, studies are reviewed that report HA stability values and investigate the biological impact of variations in HA stability on replication, pathogenicity, and transmissibility in experimental animal models. Overall, a stabilized HA protein appears to be necessary for human pandemic potential and should be considered when assessing human pandemic risk. Full article
(This article belongs to the Special Issue Animal Models for Influenza Virus Research)
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24 pages, 959 KiB  
Review
The Intersection of Age and Influenza Severity: Utility of Ferrets for Dissecting the Age-Dependent Immune Responses and Relevance to Age-Specific Vaccine Development
by Melissa Rioux, Magen E. Francis, Cynthia L. Swan, Anni Ge, Andrea Kroeker and Alyson A. Kelvin
Viruses 2021, 13(4), 678; https://doi.org/10.3390/v13040678 - 15 Apr 2021
Cited by 7 | Viewed by 3110
Abstract
Many factors impact the host response to influenza virus infection and vaccination. Ferrets have been an indispensable reagent for influenza virus research for almost one hundred years. One of the most significant and well-known factors affecting human disease after infection is host age. [...] Read more.
Many factors impact the host response to influenza virus infection and vaccination. Ferrets have been an indispensable reagent for influenza virus research for almost one hundred years. One of the most significant and well-known factors affecting human disease after infection is host age. Another significant factor is the virus, as strain-specific disease severity is well known. Studying age-related impacts on viral infection and vaccination outcomes requires an animal model that reflects both the physiological and immunological changes that occur with human aging, and sensitivity to differentially virulent influenza viruses. The ferret is uniquely susceptible to a plethora of influenza viruses impacting humans and has proven extremely useful in studying the clinical and immunological pictures of influenza virus infection. Moreover, ferrets developmentally have several of the age-related physiological changes that occur in humans throughout infancy, adulthood, old age, and pregnancy. In this review, we discuss ferret susceptibility to influenza viruses, summarize previous influenza studies using ferrets as models of age, and finally, highlight the application of ferret age models in the pursuit of prophylactic and therapeutic agents to address age-related influenza disease severity. Full article
(This article belongs to the Special Issue Animal Models for Influenza Virus Research)
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