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Helin, A. S., Wille, M., Atterby, C., Jarhult, J. D., Waldenström, J. & Chapman, J. R. (2018). A rapid and transient innate immune response to avian influenza infection in mallards. Molecular Immunology, 95, 64-72
Open this publication in new window or tab >>A rapid and transient innate immune response to avian influenza infection in mallards
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2018 (English)In: Molecular Immunology, ISSN 0161-5890, E-ISSN 1872-9142, Vol. 95, p. 64-72Article in journal (Refereed) Published
Abstract [en]

The vertebrate innate immune system provides hosts with a rapid, non-specific response to a wide range of invading pathogens. However, the speed and duration of innate responses will be influenced by the co-evolutionary dynamics of specific host-pathogen combinations. Here, we show that low pathogenic avian influenza virus (LPAI) subtype H1N1 elicits a strong but extremely transient innate immune response in its main wildlife reservoir, the mallard (Anas platyrhynchos). Using a series of experimental and methodological improvements over previous studies, we followed the expression of retinoic acid inducible gene 1 (RIG-I) and myxovirus resistance gene (Mx) in mallards semi-naturally infected with low pathogenic H1N1. One day post infection, both RIG-I and Mx were significantly upregulated in all investigated tissues. By two days post infection, the expression of both genes had generally returned to basal levels, and remained so for the remainder of the experiment. This is despite the fact that birds continued to actively shed viral particles throughout the study period. We additionally show that the spleen plays a particularly active role in the innate immune response to LPAI. Waterfowl and avian influenza viruses have a long co-evolutionary history, suggesting that the mallard innate immune response has evolved to provide a minimum effective response to LPAIs such that the viral infection is brought under control while minimising the damaging effects of a sustained immune response.

Place, publisher, year, edition, pages
Elsevier, 2018
Keywords
Anas platyrhynchos, Zoonotic disease, Avian disease, Gene expression, Retinoic acid inducible gene 1 RIG-I, Myxovirus resistance gene Mx, Influenza A virus, LPAI, HPAI, Ecoimmunology, Tolerance
National Category
Immunology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-72297 (URN)10.1016/j.molimm.2018.01.012 (DOI)000428096900008 ()29407578 (PubMedID)2-s2.0-85041644274 (Scopus ID)
Available from: 2018-04-06 Created: 2018-04-06 Last updated: 2019-08-29Bibliographically approved
Helin, A. S., Wille, M., Atterby, C., Jarhult, J., Waldenström, J. & Chapman, J. R. (2018). Expression of immune genes RIG-I and Mx in mallard ducks infected with low pathogenic avian influenza (LPAI): A dataset. Data in Brief, 18, 1562-1566
Open this publication in new window or tab >>Expression of immune genes RIG-I and Mx in mallard ducks infected with low pathogenic avian influenza (LPAI): A dataset
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2018 (English)In: Data in Brief, E-ISSN 2352-3409, Vol. 18, p. 1562-1566Article in journal (Refereed) Published
Abstract [en]

This article provides data on primer sequences used to amplify the innate immune genes RIG-I and Mx and a set of normalizing reference genes in mallards (Anal platyrhynchos), and shows which reference genes are stable, per tissue, for our experimental settings. Data on the expressional changes of these two genes over a time-course of infection with low pathogenic avian influenza virus (LPAI) are provided. Individual-level data are also presented, including LPAI infection load, and per tissue gene expression of RIG-I and Mx. Gene expression in two outlier individuals is explored in more depth. (C) 2018 The Authors. Published by Elsevier Inc.

Place, publisher, year, edition, pages
Elsevier, 2018
National Category
Immunology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-79497 (URN)10.1016/j.dib.2018.04.061 (DOI)000449815400215 ()29904657 (PubMedID)2-s2.0-85041687141 (Scopus ID)
Available from: 2019-01-15 Created: 2019-01-15 Last updated: 2019-08-29Bibliographically approved
van Dijk, J. G. B., Verhagen, J. H., Wille, M. & Waldenström, J. (2018). Host and virus ecology as determinants of influenza A virus transmission in wild birds. Current Opinion in Virology, 28, 26-36
Open this publication in new window or tab >>Host and virus ecology as determinants of influenza A virus transmission in wild birds
2018 (English)In: Current Opinion in Virology, ISSN 1879-6257, E-ISSN 1879-6265, Vol. 28, p. 26-36Article in journal (Refereed) Published
Abstract [en]

Low pathogenic influenza A virus (LPIAV) prevalence and subtype distribution differs between and across bird taxa. A crucial factor in the epidemiology of these viruses and virus subtypes is the ability to transmit between and within different host taxa and individuals. Successful viral transmission depends on availability of susceptible hosts and exposure of host to virus. Exposure to viruses and susceptibility to virus infection and/or disease are shaped by both host and virus traits. In this review we have identified key host and virus traits that can affect LPIAV transmission, both in terms of exposure and susceptibility. Furthermore we highlight current challenges in assessment of these traits and identify methodological considerations for future studies.

Place, publisher, year, edition, pages
Elsevier, 2018
National Category
Microbiology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-72299 (URN)10.1016/j.coviro.2017.10.006 (DOI)000427665300007 ()29121508 (PubMedID)2-s2.0-85032943205 (Scopus ID)
Available from: 2018-04-10 Created: 2018-04-10 Last updated: 2019-08-28Bibliographically approved
Wille, M., Latorre-Margalef, N., Tolf, C., Halpin, R., Wentworth, D., Fouchier, R. A. M., . . . Waldenström, J. (2018). Where do all the subtypes go?: Temporal dynamics of H8-H12 influenza A viruses in waterfowl. Virus Evolution, 4(2), Article ID vey025.
Open this publication in new window or tab >>Where do all the subtypes go?: Temporal dynamics of H8-H12 influenza A viruses in waterfowl
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2018 (English)In: Virus Evolution, E-ISSN 2057-1577, Vol. 4, no 2, article id vey025Article in journal (Refereed) Published
Abstract [en]

Influenza A virus (IAV) is ubiquitous in waterfowl. In the northern hemisphere IAV prevalence is highest during the autumn and coincides with a peak in viral subtype diversity. Although haemagglutinin subtypes H1-H12 are associated with waterfowl hosts, subtypes H8-H12 are detected very infrequently. To better understand the role of waterfowl in the maintenance of these rare subtypes, we sequenced H8-H12 viruses isolated from Mallards (Anas platyrhynchos) from 2002 to 2009. These rare viruses exhibited varying ecological and phylodynamic features. The Eurasian clades of H8 and H12 phylogenies were dominated by waterfowl sequences; mostly viruses sequenced in this study. H11, once believed to be a subtype that infected charadriiformes (shorebirds), exhibited patterns more typical of common virus subtypes. Finally, subtypes H9 and H10, which have maintained lineages in poultry, showed markedly different patterns: H10 was associated with all possible NA subtypes and this drove HA lineage diversity within years. Rare viruses belonging to subtypes H8-H12 were highly reassorted, indicating that these rare subtypes are part of the broader IAV pool. Our results suggest that waterfowl play a role in the maintenance of these rare subtypes, but we recommend additional sampling of non-traditional hosts to better understand the reservoirs of these rare viruses.

Place, publisher, year, edition, pages
Oxford University Press, 2018
Keywords
disease ecology, evolutionary genetics, influenza A, mallards, pathogen dynamics, subtype diversity
National Category
Microbiology
Research subject
Biomedical Sciences, Virology; Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-80290 (URN)10.1093/ve/vey025 (DOI)000456426800007 ()30151242 (PubMedID)
Available from: 2019-02-08 Created: 2019-02-08 Last updated: 2019-02-08Bibliographically approved
Wille, M., Latorre-Margalef, N., Tolf, C., Stallknecht, D. E. & Waldenström, J. (2017). No evidence for homosubtypic immunity of influenza H3 in Mallards following vaccination in a natural experimental system. Molecular Ecology, 26(5), 1420-1431
Open this publication in new window or tab >>No evidence for homosubtypic immunity of influenza H3 in Mallards following vaccination in a natural experimental system
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2017 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 26, no 5, p. 1420-1431Article in journal (Refereed) Published
Abstract [en]

The Mallard (Anas platyrhynchos) is an important reservoir species for influenza A viruses (IAV), and in this host, prevalence and virus diversity are high. Studies have demonstrated the presence of homosubtypic immunity, where individuals are unlikely to be reinfected with the same subtype within an autumn season. Further, evidence for heterosubtypic immunity exists, whereby immune responses specific for one subtype offer partial or complete protection against related HA subtypes. We utilized a natural experimental system to determine whether homo- or heterospecific immunity could be induced following experimental vaccination. Thirty Mallards were vaccinated with an inactivated H3, H6 or a sham vaccine and after seroconversion were exposed to naturally infected wild conspecifics. All ducks were infected within 2days and had both primary and secondary infections. Overall, there was no observable difference between groups; all individuals were infected with H3 and H10 IAV. At the cessation of the experiment, most individuals had anti-NP antibodies and neutralizing antibodies against H10. Not all individuals had H3 neutralizing antibodies. The isolated H3 IAVs revealed genetic dissimilarity to the H3 vaccine strain, specifically substitutions in the vicinity of the receptor-binding site. There was no evidence of vaccine-induced homosubtypic immunity to H3, a likely result of both a poor H3 immune response in the ducks and H3 immune escape. Likewise, there was no observed heterosubtypic protection related to H6 vaccination. This study highlights the need for experimental approaches to assess how exposure to pathogens and resulting immune processes translates to individual and population disease dynamics.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2017
Keywords
Anas platyrhynchos, H3, homosubtypic immunity, humoral immunity, immunity, influenza A virus, Mallard
National Category
Ecology Microbiology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-64211 (URN)10.1111/mec.13967 (DOI)000395700600015 ()27997047 (PubMedID)2-s2.0-85013040569 (Scopus ID)
Available from: 2017-05-23 Created: 2017-05-23 Last updated: 2019-08-29Bibliographically approved
Chapman, J. R., Helin, A. S., Wille, M., Atterby, C., Jarhult, J. D., Fridlund, J. & Waldenström, J. (2016). A Panel of Stably Expressed Reference Genes for Real-Time qPCR Gene Expression Studies of Mallards (Anas platyrhynchos). PLoS ONE, 11(2), Article ID e0149454.
Open this publication in new window or tab >>A Panel of Stably Expressed Reference Genes for Real-Time qPCR Gene Expression Studies of Mallards (Anas platyrhynchos)
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2016 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 2, article id e0149454Article in journal (Refereed) Published
Abstract [en]

Determining which reference genes have the highest stability, and are therefore appropriate for normalising data, is a crucial step in the design of real-time quantitative PCR (qPCR) gene expression studies. This is particularly warranted in non-model and ecologically important species for which appropriate reference genes are lacking, such as the mallard-a key reservoir of many diseases with relevance for human and livestock health. Previous studies assessing gene expression changes as a consequence of infection in mallards have nearly universally used beta-actin and/or GAPDH as reference genes without confirming their suitability as normalisers. The use of reference genes at random, without regard for stability of expression across treatment groups, can result in erroneous interpretation of data. Here, eleven putative reference genes for use in gene expression studies of the mallard were evaluated, across six different tissues, using a low pathogenic avian influenza A virus infection model. Tissue type influenced the selection of reference genes, whereby different genes were stable in blood, spleen, lung, gastrointestinal tract and colon. beta-actin and GAPDH generally displayed low stability and are therefore inappropriate reference genes in many cases. The use of different algorithms (GeNorm and NormFinder) affected stability rankings, but for both algorithms it was possible to find a combination of two stable reference genes with which to normalise qPCR data in mallards. These results highlight the importance of validating the choice of normalising reference genes before conducting gene expression studies in ducks. The fact that nearly all previous studies of the influence of pathogen infection on mallard gene expression have used a single, non-validated reference gene is problematic. The toolkit of putative reference genes provided here offers a solid foundation for future studies of gene expression in mallards and other waterfowl.

National Category
Ecology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-51591 (URN)10.1371/journal.pone.0149454 (DOI)000371218400085 ()26886224 (PubMedID)2-s2.0-84960902443 (Scopus ID)
Available from: 2016-03-30 Created: 2016-03-30 Last updated: 2018-11-15Bibliographically approved
Lang, A. S., Lebarbenchon, C., Ramey, A. M., Robertson, G. J., Waldenström, J. & Wille, M. (2016). Assessing the Role of Seabirds in the Ecology of Influenza A Viruses. Paper presented at 9th International Symposium on Avian Influenza, APR 12-15, 2015, Univ Georgia, Ctr Continuing Educ, Athens, GA. Avian diseases, 60(1), 378-386
Open this publication in new window or tab >>Assessing the Role of Seabirds in the Ecology of Influenza A Viruses
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2016 (English)In: Avian diseases, ISSN 0005-2086, E-ISSN 1938-4351, Vol. 60, no 1, p. 378-386Article in journal (Refereed) Published
Abstract [en]

Wild waterbirds, specifically waterfowl, gulls, and shorebirds, are recognized as the primordial reservoir of influenza A viruses (IAVs). However, the role of seabirds, an abundant, diverse, and globally distributed group of birds, in the perpetuation and transmission of IAVs is less clear. Here we summarize published and publicly available data for influenza viruses in seabirds, which for the purposes of this study are defined as birds that exhibit a largely or exclusively pelagic lifestyle and exclude waterfowl, gulls, and shorebirds, and we review this collective dataset to assess the role of seabirds in the influenza A ecology. Since 1961, more than 40,000 samples have been collected worldwide from the seabirds considered here and screened, using a variety of techniques, for evidence of active or past IAV infection. From these data, the overall prevalence of active infection has been estimated to be very low; however, serological data provide evidence that some seabird species are more frequently exposed to IAVs. Sequence data for viruses from seabirds are limited, except for murres (common murre, Uria aalge, and thick-billed murre, Uria lomvia; family Alcidae) for which there are full or partial genome sequences available for more than 80 viruses. Characterization of these viruses suggests that murres are infected with Group 1 hemagglutinin subtype viruses more frequently as compared to Group 2 and also indicates that these northern, circumpolar birds are frequently infected by intercontinental reassortant viruses. Greater temporal and spatial sampling and characterization of additional viruses are required to better understand the role of seabirds in global IAV dynamics.

Keywords
murre, tern, penguin, shearwater, marine, virus ecology, influenza
National Category
Biological Sciences
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-54686 (URN)000378085900040 ()27309082 (PubMedID)2-s2.0-84987719424 (Scopus ID)
Conference
9th International Symposium on Avian Influenza, APR 12-15, 2015, Univ Georgia, Ctr Continuing Educ, Athens, GA
Available from: 2016-07-22 Created: 2016-07-21 Last updated: 2019-08-09Bibliographically approved
Wille, M., Muradrasoli, S., Nilsson, A. & Jarhult, J. D. (2016). High Prevalence and Putative Lineage Maintenance of Avian Coronaviruses in Scandinavian Waterfowl. PLoS ONE, 11(3), Article ID e0150198.
Open this publication in new window or tab >>High Prevalence and Putative Lineage Maintenance of Avian Coronaviruses in Scandinavian Waterfowl
2016 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 11, no 3, article id e0150198Article in journal (Refereed) Published
Abstract [en]

Coronaviruses (CoVs) are found in a wide variety of wild and domestic animals, and constitute a risk for zoonotic and emerging infectious disease. In poultry, the genetic diversity, evolution, distribution and taxonomy of some coronaviruses have been well described, but little is known about the features of CoVs in wild birds. In this study we screened 764 samples from 22 avian species of the orders Anseriformes and Charadriiformes in Sweden collected in 2006/2007 for CoV, with an overall CoV prevalence of 18.7%, which is higher than many other wild bird surveys. The highest prevalence was found in the diving duck-smainly Greater Scaup (Aythya marila; 51.5%)-and the dabbling duck Mallard (Anas platyrhynchos; 19.2%). Sequences from two of the Greater Scaup CoV fell into an infrequently detected lineage, shared only with a Tufted Duck (Aythya fuligula) CoV. Coronavirus sequences from Mallards in this study were highly similar to CoV sequences from the sample species and location in 2011, suggesting long-term maintenance in this population. A single Black-headed Gull represented the only positive sample from the order Charadriiformes. Globally, Anas species represent the largest fraction of avian CoV sequences, and there seems to be no host species, geographical or temporal structure. To better understand the eitiology, epidemiology and ecology of these viruses more systematic surveillance of wild birds and subsequent sequencing of detected CoV is imperative.

National Category
Microbiology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-51854 (URN)10.1371/journal.pone.0150198 (DOI)000371735200062 ()26938459 (PubMedID)2-s2.0-84961792789 (Scopus ID)
Available from: 2016-04-01 Created: 2016-04-01 Last updated: 2018-11-15Bibliographically approved
Isaksson, J., Christerson, L., Blomqvist, M., Wille, M., Alladio, L. A., Sachse, K., . . . Herrmann, B. (2015). Chlamydiaceae-like bacterium, but no Chlamydia psittaci, in sea birds from Antarctica. Polar Biology, 38(11), 1931-1936
Open this publication in new window or tab >>Chlamydiaceae-like bacterium, but no Chlamydia psittaci, in sea birds from Antarctica
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2015 (English)In: Polar Biology, ISSN 0722-4060, E-ISSN 1432-2056, Vol. 38, no 11, p. 1931-1936Article in journal (Refereed) Published
Abstract [en]

Within the growing order of Chlamydiales, there are a number of pathogens. One is Chlamydia psittaci, a zoonotic pathogen, with birds as natural hosts that may be transmitted to humans and cause severe respiratory disease, psittacosis. The prevalence of this pathogen in Antarctic birds is almost unknown as well as the ramifications of its potential spread in na < ve bird populations. To investigate the prevalence of chlamydia organisms, cloacal and fecal samples were collected from 264 penguins and 263 seabirds on the Antarctic Peninsula and in Southern Chile. No C. psittaci could be detected by 23S rRNA real-time PCR. However, DNA sequencing of the 16S rRNA 298-bp signature sequence revealed a Chlamydiaceae-like bacterium previously found in seabirds from the subarctic zone, demonstrating that this not yet fully characterized bacterium is widespread. In conclusion, the prevalence of C. psittaci among wild birds on the Antarctic Peninsula seems to be low, but other types of chlamydial organisms are common. Further studies are required to taxonomically define and finally understand the role of these non-classified Chlamydiae.

Keywords
Chlamydia psittaci, Chlamydiaceae, Pygoscelis antarcticus, Spheniscus magellanicus, Stercorarius antarcticus, Antarctic
National Category
Microbiology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-47686 (URN)10.1007/s00300-015-1748-2 (DOI)000364023800012 ()2-s2.0-84945486322 (Scopus ID)
Available from: 2015-12-01 Created: 2015-12-01 Last updated: 2018-11-15Bibliographically approved
Gillman, A., Nykvist, M., Muradrasoli, S., Söderström, H., Wille, M., Daggfeldt, A., . . . Jarhult, J. D. (2015). Influenza A(H7N9) Virus Acquires Resistance-Related Neuraminidase I222T Substitution When Infected Mallards Are Exposed to Low Levels of Oseltamivir in Water. Antimicrobial Agents and Chemotherapy, 59(9), 5196-5202
Open this publication in new window or tab >>Influenza A(H7N9) Virus Acquires Resistance-Related Neuraminidase I222T Substitution When Infected Mallards Are Exposed to Low Levels of Oseltamivir in Water
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2015 (English)In: Antimicrobial Agents and Chemotherapy, ISSN 0066-4804, E-ISSN 1098-6596, Vol. 59, no 9, p. 5196-5202Article in journal (Refereed) Published
Abstract [en]

Influenza A virus (IAV) has its natural reservoir in wild waterfowl, and new human IAVs often contain gene segments originating from avian IAVs. Treatment options for severe human influenza are principally restricted to neuraminidase inhibitors (NAIs), among which oseltamivir is stockpiled in preparedness for influenza pandemics. There is evolutionary pressure in the environment for resistance development to oseltamivir in avian IAVs, as the active metabolite oseltamivir carboxylate (OC) passes largely undegraded through sewage treatment to river water where waterfowl reside. In an in vivo mallard (Anas platyrhynchos) model, we tested if low-pathogenic avian influenza A(H7N9) virus might become resistant if the host was exposed to low levels of OC. Ducks were experimentally infected, and OC was added to their water, after which infection and transmission were maintained by successive introductions of uninfected birds. Daily fecal samples were tested for IAV excretion, genotype, and phenotype. Following mallard exposure to 2.5 mu g/liter OC, the resistance-related neuraminidase (NA) I222T substitution, was detected within 2 days during the first passage and was found in all viruses sequenced from subsequently introduced ducks. The substitution generated 8-fold and 2.4-fold increases in the 50% inhibitory concentration (IC50) for OC (P < 0.001) and zanamivir (P = 0.016), respectively. We conclude that OC exposure of IAV hosts, in the same concentration magnitude as found in the environment, may result in amino acid substitutions, leading to changed antiviral sensitivity in an IAV subtype that can be highly pathogenic to humans. Prudent use of oseltamivir and resistance surveillance of IAVs in wild birds are warranted.

National Category
Microbiology
Research subject
Ecology, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-47716 (URN)10.1128/AAC.00886-15 (DOI)000364343900014 ()26077257 (PubMedID)2-s2.0-84940936073 (Scopus ID)
Available from: 2015-12-04 Created: 2015-12-04 Last updated: 2019-01-23Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-5629-0196

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