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PLoS pathogens2021; 17(12); e1010174; doi: 10.1371/journal.ppat.1010174

Long-term adaptation following influenza A virus host shifts results in increased within-host viral fitness due to higher replication rates, broader dissemination within the respiratory epithelium and reduced tissue damage.

Abstract: The mechanisms and consequences of genome evolution on viral fitness following host shifts are poorly understood. In addition, viral fitness -the ability of an organism to reproduce and survive- is multifactorial and thus difficult to quantify. Influenza A viruses (IAVs) circulate broadly among wild birds and have jumped into and become endemic in multiple mammalian hosts, including humans, pigs, dogs, seals, and horses. H3N8 equine influenza virus (EIV) is an endemic virus of horses that originated in birds and has been circulating uninterruptedly in equine populations since the early 1960s. Here, we used EIV to quantify changes in infection phenotype associated to viral fitness due to genome-wide changes acquired during long-term adaptation. We performed experimental infections of two mammalian cell lines and equine tracheal explants using the earliest H3N8 EIV isolated (A/equine/Uruguay/63 [EIV/63]), and A/equine/Ohio/2003 (EIV/2003), a monophyletic descendant of EIV/63 isolated 40 years after the emergence of H3N8 EIV. We show that EIV/2003 exhibits increased resistance to interferon, enhanced viral replication, and a more efficient cell-to-cell spread in cells and tissues. Transcriptomics analyses revealed virus-specific responses to each virus, mainly affecting host immunity and inflammation. Image analyses of infected equine respiratory explants showed that despite replicating at higher levels and spreading over larger areas of the respiratory epithelium, EIV/2003 induced milder lesions compared to EIV/63, suggesting that adaptation led to reduced tissue pathogenicity. Our results reveal previously unknown links between virus genotype and the host response to infection, providing new insights on the relationship between virus evolution and fitness.
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Publication Date: 2021-12-17 PubMed ID: 34919598PubMed Central: PMC8735595DOI: 10.1371/journal.ppat.1010174Google Scholar: Lookup
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  • Journal Article
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  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research examines how long-term adaptation of the influenza A viruses (IAVs) following a host shift (from birds to horses in this case) leads to changes in the virus’s ability to replicate, spread within the host, and cause tissue damage, all aspects related to viral fitness. The study used H3N8 equine influenza virus (EIV) as a model to study these phenomena, comparing an early isolated variant of the virus and a later isolated variant to measure changes in the virus’s behavior.

Methodology

  • The researchers performed experimental infections on two different mammalian cell lines and on equine tracheal explants. This was done using two variants of the H3N8 EIV, one isolated in 1963 (referred as EIV/63) and another from 2003 (EIV/2003), which is a direct descendant of the 1963 variant.
  • The two virus variants were then compared to understand the changes in viral behavior over the 40-year period.

Key Findings

  • The results revealed that the EIV/2003 variant had developed increased resistance to interferon, a kind of protein that hosts produce to defend against viral infections. This means that the virus has adapted to better survive and propagate within the host’s body.
  • The later variant (EIV/2003) was found to have improved in its replication rate and its ability to spread from cell to cell, suggesting that long-term adaptation has led to enhanced viral fitness.
  • Despite having higher replication rates and broader dissemination, EIV/2003 caused milder lesions on the equine respiratory explants than its predecessor EIV/63, indicating that the virus has adapted to cause less tissue damage, possibly to sustain longer infections.

Significance of the Research

  • The observations provide valuable insights into the mechanisms of viral fitness and how adaptations over time following a host shift can shape the infection phenotype of a virus.
  • This unique link between the virus’s genotype and host’s response has implications for understanding and predicting the evolution of viruses and their potential impacts on new hosts.
  • Findings from this research could be crucial for predicting and managing future influenza epidemics or pandemics that arise due to a host shift.

Cite This Article

APA
Amat JAR, Patton V, Chauché C, Goldfarb D, Crispell J, Gu Q, Coburn AM, Gonzalez G, Mair D, Tong L, Martinez-Sobrido L, Marshall JF, Marchesi F, Murcia PR. (2021). Long-term adaptation following influenza A virus host shifts results in increased within-host viral fitness due to higher replication rates, broader dissemination within the respiratory epithelium and reduced tissue damage. PLoS Pathog, 17(12), e1010174. https://doi.org/10.1371/journal.ppat.1010174

Publication

PLoS pathogens
ISSN: 1553-7374
NlmUniqueID: 101238921
Country: United States
Language: English
Volume: 17
Issue: 12
Pages: e1010174

Researcher Affiliations

Amat, Julien A R
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
  • School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Patton, Veronica
  • School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Chauché, Caroline
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
  • Centre for Inflammation Research, University of Edinburgh, The Queen's Medical Research Institute, Edinburgh, Scotland, United Kingdom.
Goldfarb, Daniel
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Crispell, Joanna
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Gu, Quan
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Coburn, Alice M
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Gonzalez, Gaelle
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
  • Ecole Nationale Vétérinaire d'Alfort, Université Paris-Est, Maisons-Alfort, France.
Mair, Daniel
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Tong, Lily
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Martinez-Sobrido, Luis
  • Texas Biomedical Research Institute, San Antonio, Texas, United States of America.
Marshall, John F
  • School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Marchesi, Francesco
  • School of Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.
Murcia, Pablo R
  • MRC-University of Glasgow Centre for Virus Research, Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland, United Kingdom.

MeSH Terms

  • Adaptation, Physiological / physiology
  • Animals
  • Genetic Fitness / physiology
  • Horses
  • Host-Pathogen Interactions / physiology
  • Influenza A Virus, H3N8 Subtype / pathogenicity
  • Influenza A Virus, H3N8 Subtype / physiology
  • Orthomyxoviridae Infections / virology

Grant Funding

  • BB/V002821/1 / Biotechnology and Biological Sciences Research Council
  • MC_UU_12014/12 / Medical Research Council
  • BB/V004697/1 / Biotechnology and Biological Sciences Research Council
  • MC_UU_12014/9 / Medical Research Council
  • R01 AI145332 / NIAID NIH HHS

Conflict of Interest Statement

The authors have declared that no competing interests exist.

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