A comparative analysis of host responses to avian influenza infection in ducks and chickens highlights a role for the interferon-induced transmembrane proteins in viral resistance

Abstract

BackgroundChickens are susceptible to infection with a limited number of Influenza A viruses and are a potential source of a human influenza pandemic. In particular, H5 and H7 haemagglutinin subtypes can evolve from low to highly pathogenic strains in gallinaceous poultry. Ducks on the other hand are a natural reservoir for these viruses and are able to withstand most avian influenza strains.ResultsTranscriptomic sequencing of lung and ileum tissue samples from birds infected with high (H5N1) and low (H5N2) pathogenic influenza viruses has allowed us to compare the early host response to these infections in both these species. Chickens (but not ducks) lack the intracellular receptor for viral ssRNA, RIG-I and the gene for an important RIG-I binding protein, RNF135. These differences in gene content partly explain the differences in host responses to low pathogenic and highly pathogenic avian influenza virus in chicken and ducks. We reveal very different patterns of expression of members of the interferon-induced transmembrane protein (IFITM) gene family in ducks and chickens. In ducks, IFITM1, 2 and 3 are strongly up regulated in response to highly pathogenic avian influenza, where little response is seen in chickens. Clustering of gene expression profiles suggests IFITM1 and 2 have an anti-viral response and IFITM3 may restrict avian influenza virus through cell membrane fusion. We also show, through molecular phylogenetic analyses, that avian IFITM1 and IFITM3 genes have been subject to both episodic and pervasive positive selection at specific codons. In particular, avian IFITM1 showed evidence of positive selection in the duck lineage at sites known to restrict influenza virus infection.ConclusionsTaken together these results support a model where the IFITM123 protein family and RIG-I all play a crucial role in the tolerance of ducks to highly pathogenic and low pathogenic strains of avian influenza viruses when compared to the chicken.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1778-8) contains supplementary material, which is available to authorized users.

Antiviral responses against chicken respiratory infections: Focus on avian influenza virus and infectious bronchitis virus

“…IFITM family is known to have a critical role in limiting AIV infection in chickens [114,115]. Clustering of gene expression profiles in chickens suggests that IFITM1 and 2 have an antiviral response and IFITM3 may act prior to viral membrane fusion and thus blocks viral entrance [114]. In physiological status, IFIRM5 is the main expressed IFITM in different embryonic and adult organs in chickens, except for the colon in which IFITM1 and 3 are the main expressed IFITMs.…”

“…IFITM3 is a viral restriction factor, which targets influenza A virus entry process in humans by blocking complete virus envelope fusion with cell endosome membranes [115,118]. It has been suggested that the chicken IFITM3 protein protect host cells from infection with AIV to a similar level as its human orthologue and in vitro experiments showed the anti-influenza activity of IFITM3 in chicken cells [114]. Barjesteh et al in vivo study demonstrated the up-regulation of IFITM5 in the chicken trachea cells following CpG ODN and Pam3CSK4 treatments [49].…”

Avian transcriptomics: opportunities and challenges

“…A particular interest in understanding what makes a species resistant or susceptible to a certain infectious disease has further led to a number of comparative immunological studies between different species of birds. Using transcriptomics, Smith et al (2015) found key differences in expression patterns of the interferon-induced transmembrane protein gene family in ducks and chickens, which the authors suggested might contribute to the large differences in susceptibility to AIV in these birds.…”

“…This has been of particular interest in avian species that are known carriers of zoonotic diseases, as this gives an insight into how birds deal with these infections. A number of studies have used transcriptomics to study the immune response to infectious diseases such as avian influenza virus (AIV) in non-model species of birds (Huang et al 2013;Smith et al 2015;Vijayakumar et al 2015). A particular interest in understanding what makes a species resistant or susceptible to a certain infectious disease has further led to a number of comparative immunological studies between different species of birds.…”

“…Chung et al 2015;Mueller et al 2015). Wright et al (2014) [3] {18, 22, 23}; Harrison et al (2015) [3] {18, 22, 23}; Li et al (2015) [2] {3, 22, 24}; Smith et al (2015) [2] {12, 16}; Wright et al (2015) [3] {18, 22, 23} Anser cygnoides Swan Goose a Harrison et al (2015) [3] {18, 22, 23}; Lu et al (2015) [1, 2] {15}; Tariq et al (2015) [2] {28}; Wright et al (2015) [3] {18, 22, 23}; Chen et al (2017b) [2] {28}; Cao et al (2017) Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2014) [3] {18, 22, 23}; Wright et al (2015) [3] {18, 22, 23} Numida meleagris Helmeted Guineafowl Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2015) [3] {18, 22, 23} Pavo cristatus Indian Peafowl Harrison et al (2015) [3] {18, 22, 23}; Wright et al (2015) [3] {18, 22, 23}…”