Differential gene expression reveals host factors for viral shedding variation in mallards () infected with low-pathogenic avian influenza virus No Access

Abstract

Intraspecific variation in pathogen shedding impacts disease transmission dynamics; therefore, understanding the host factors associated with individual variation in pathogen shedding is key to controlling and preventing outbreaks. In this study, ileum and bursa of Fabricius tissues of wild-bred mallards () infected with low-pathogenic avian influenza (LPAIV) were evaluated at various post-infection time points to determine genetic host factors associated with intraspecific variation in viral shedding. By analysing transcriptome sequencing data (RNA-seq), we found that LPAIV-infected wild-bred mallards do not exhibit differential gene expression compared to uninfected birds, but that gene expression was associated with cloacal viral shedding quantity early in the infection. In both tissues, immune gene expression was higher in high/moderate shedding birds compared to low shedding birds, and significant positive relationships with viral shedding were observed. In the ileum, expression for host genes involved in viral cell entry was lower in low shedders compared to moderate shedders at 1 day post-infection (DPI), and expression for host genes promoting viral replication was higher in high shedders compared to low shedders at 2 DPI. Our findings indicate that viral shedding is a key factor for gene expression differences in LPAIV-infected wild-bred mallards, and the genes identified in this study could be important for understanding the molecular mechanisms driving intraspecific variation in pathogen shedding.

Keyword(s): influenza , shedding , transcriptomics and virus
Funding
This study was supported by the:
  • National Science Foundation (Award Career Grant 135077)
    • Principle Award Recipient: JenniferC. Owen
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/content/journal/jgv/10.1099/jgv.0.001724
2022-03-30
2024-03-29
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References

  1. Dolinski AC, Homola JJ, Jankowski MD, Robinson JD, Owen JC. Differential gene expression reveals host factors for viral shedding variation in mallards (anas platyrhynchos) infected with low-pathogenic avian influenza virus. Figshare 2022. DOI: 10.6084/m9.figshare.17035334
    [Google Scholar]
  2. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM. Superspreading and the effect of individual variation on disease emergence. Nature 2005; 438:355–359 [View Article] [PubMed]
    [Google Scholar]
  3. VanderWaal KL, Ezenwa VO, Hawley D. Heterogeneity in pathogen transmission: mechanisms and methodology. Funct Ecol 2016; 30:1606–1622 [View Article]
    [Google Scholar]
  4. Stein RA. Super-spreaders in infectious diseases. Int J Infect Dis 2011; 15:e510–3 [View Article] [PubMed]
    [Google Scholar]
  5. Paull SH, Song S, McClure KM, Sackett LC, Kilpatrick AM et al. From superspreaders to disease hotspots: linking transmission across hosts and space. Front Ecol Environ 2012; 10:75–82 [View Article] [PubMed]
    [Google Scholar]
  6. Galvani AP, May RM. Epidemiology: dimensions of superspreading. Nature 2005; 438:293–295
    [Google Scholar]
  7. Gupta S, Anderson RM, May RM. Networks of sexual contacts: implications for the pattern of spread of HIV. AIDS 1989; 3:807–817
    [Google Scholar]
  8. Hudson PJ, Perkins SE, Cattadori IM. The emergence of wildlife disease and the application of ecology. In Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems Princeton University Press; 2010 pp 347–367 [View Article]
    [Google Scholar]
  9. Al-Tawfiq JA, Rodriguez-Morales AJ. Super-spreading events and contribution to transmission of MERS, SARS, and SARS-CoV-2 (COVID-19. J Hosp Infect 2020; 105:111–112
    [Google Scholar]
  10. Mossong J, Hens N, Jit M, Beutels P, Auranen K et al. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med 2008; 5:0381–0391 [View Article]
    [Google Scholar]
  11. Godfrey SS. Networks and the ecology of parasite transmission: A framework for wildlife parasitology. Int J Parasitol Parasites Wildl 2013; 2:235–245 [View Article] [PubMed]
    [Google Scholar]
  12. Chase-Topping M, Gally D, Low C, Matthews L, Woolhouse M. Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat Rev Microbiol 2008; 6:904–912 [View Article] [PubMed]
    [Google Scholar]
  13. Matthews L, McKendrick IJ, Ternent H, Gunn GJ, Synge B et al. Super-shedding cattle and the transmission dynamics of Escherichia coli O157. Epidemiol Infect 2006; 134:131–142 [View Article] [PubMed]
    [Google Scholar]
  14. Capparelli R, Parlato M, Iannaccone M, Roperto S, Marabelli R et al. Heterogeneous shedding of Brucella abortus in milk and its effect on the control of animal brucellosis. J Appl Microbiol 2009; 106:2041–2047 [View Article] [PubMed]
    [Google Scholar]
  15. Tadiri CP, Dargent F, Scott ME. Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model. Parasitology 2013; 140:343–351 [View Article] [PubMed]
    [Google Scholar]
  16. Arsnoe DM, Ip HS, Owen JC. Influence of body condition on influenza A virus infection in mallard ducks: experimental infection data. PLoS One 2011; 6:1–9 [View Article] [PubMed]
    [Google Scholar]
  17. Costa F, Wunder EA Jr, De Oliveira D, Bisht V, Rodrigues G et al. Patterns in Leptospira Shedding in Norway Rats (Rattus norvegicus) from Brazilian Slum Communities at High Risk of Disease Transmission. PLoS Negl Trop Dis 2015; 9:1–14 [View Article] [PubMed]
    [Google Scholar]
  18. Jolly PE, Inusah S, Lu B, Ellis WO, Nyarko A et al. Association between high aflatoxin B1 levels and high viral load in HIV-positive people. World Mycotoxin J 2013; 6:255–261 [View Article] [PubMed]
    [Google Scholar]
  19. Jankowski MD, Franson JC, Möstl E, Porter WP, Hofmeister EK. Testing independent and interactive effects of corticosterone and synergized resmethrin on the immune response to West Nile virus in chickens. Toxicology 2010; 269:81–88 [View Article] [PubMed]
    [Google Scholar]
  20. Costa TP, Brown JD, Howerth EW, Stallknecht DE. The effect of age on avian influenza viral shedding in mallards (Anas platyrhynchos). Avian Dis 2010; 54:581–585 [View Article] [PubMed]
    [Google Scholar]
  21. Zuk M, McKean KA. Sex differences in parasite infections: patterns and processes. Int J Parasitol 1996; 26:1009–1023 [View Article] [PubMed]
    [Google Scholar]
  22. Siva-Jothy JA, Vale PF. Dissecting genetic and sex-specific sources of host heterogeneity in pathogen shedding and spread. PLoS Pathog 2021; 17:1–22 [View Article] [PubMed]
    [Google Scholar]
  23. Dolinski AC, Jankowski MD, Fair JM, Owen JC. The association between SAα2,3Gal occurrence frequency and avian influenza viral load in mallards (Anas platyrhynchos) and blue-winged teals (Spatula discors). BMC Vet Res 2020; 16:1–17 [View Article] [PubMed]
    [Google Scholar]
  24. Cobbold RN, Hancock DD, Rice DH, Berg J, Stilborn R et al. Rectoanal junction colonization of feedlot cattle by Escherichia coli O157:H7 and its association with supershedders and excretion dynamics. Appl Environ Microbiol 2007; 73:1563–1568 [View Article] [PubMed]
    [Google Scholar]
  25. Wang O, McAllister TA, Plastow G, Stanford K, Selinger B et al. Host mechanisms involved in cattle Escherichia coli O157 shedding: a fundamental understanding for reducing foodborne pathogen in food animal production. Sci Rep 2017; 7:1–15 [View Article] [PubMed]
    [Google Scholar]
  26. Purcell MK, Lapatra SE, Woodson JC, Kurath G, Winton JR. Early viral replication and induced or constitutive immunity in rainbow trout families with differential resistance to Infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immunol 2010; 28:98–105 [View Article] [PubMed]
    [Google Scholar]
  27. Juliarena MA, Poli M, Sala L, Ceriani C, Gutierrez S et al. Association of BLV infection profiles with alleles of the BoLA-DRB3.2 gene. Anim Genet 2008; 39:432–438 [View Article] [PubMed]
    [Google Scholar]
  28. Deist MS, Gallardo RA, Bunn DA, Dekkers JCM, Zhou H et al. Resistant and susceptible chicken lines show distinctive responses to Newcastle disease virus infection in the lung transcriptome. BMC Genomics 2017; 18:1–15 [View Article] [PubMed]
    [Google Scholar]
  29. Cornelissen J, Post J, Peeters B, Vervelde L, Rebel JMJ. Differential innate responses of chickens and ducks to low-pathogenic avian influenza. Avian Pathol 2012; 41:519–529 [View Article] [PubMed]
    [Google Scholar]
  30. Hu W, Pasare C. Location, location, location: tissue-specific regulation of immune responses. J Leukoc Biol 2013; 94:409–421 [View Article] [PubMed]
    [Google Scholar]
  31. Koyama S, Ishii KJ, Coban C, Akira S. Innate immune response to viral infection. Cytokine 2008; 43:336–341 [View Article] [PubMed]
    [Google Scholar]
  32. Santhakumar D, Rubbenstroth D, Martinez-Sobrido L, Munir M. Avian interferons and their antiviral effectors. Front Immunol 2017; 8:1–19 [View Article] [PubMed]
    [Google Scholar]
  33. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011; 1:519–525 [View Article] [PubMed]
    [Google Scholar]
  34. Bonilla FA, Oettgen HC. Adaptive immunity. J Allergy Clin Immunol 2010; 125:S33–40 [View Article] [PubMed]
    [Google Scholar]
  35. Rong E, Wang X, Chen H, Yang C, Hu J et al. Molecular mechanisms for the adaptive switching between the OAS/RNase L and OASL/RIG-I pathways in birds and mammals. Front Immunol 2018; 9:1–14 [View Article] [PubMed]
    [Google Scholar]
  36. Suarez DL, Schultz-Cherry S. Immunology of avian influenza virus: a review. Dev Comp Immunol 2000; 24:269–283 [View Article] [PubMed]
    [Google Scholar]
  37. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56:152–179 [View Article] [PubMed]
    [Google Scholar]
  38. Roche B, Lebarbenchon C, Gauthier-Clerc M, Chang C-M, Thomas F et al. Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005-2006 epidemics in the Camargue area. Infect Genet Evol 2009; 9:800–805 [View Article] [PubMed]
    [Google Scholar]
  39. Jankowski MD, Williams CJ, Fair JM, Owen JC. Birds shed RNA-viruses according to the pareto principle. PLoS One 2013; 8:e72611 [View Article] [PubMed]
    [Google Scholar]
  40. Huang Y, Li Y, Burt DW, Chen H, Zhang Y et al. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet 2013; 45:776–783 [View Article] [PubMed]
    [Google Scholar]
  41. Ranaware PB, Mishra A, Vijayakumar P, Gandhale PN, Kumar H et al. Genome Wide Host Gene Expression Analysis in Chicken Lungs Infected with Avian Influenza Viruses. PLoS One 2016; 11:1–16 [View Article] [PubMed]
    [Google Scholar]
  42. Smith J, Smith N, Yu L, Paton IR, Gutowska MW et al. 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. BMC Genomics 2015; 16:1–19 [View Article] [PubMed]
    [Google Scholar]
  43. Vanderven HA, Petkau K, Ryan-Jean KEE, Aldridge JR Jr, Webster RG et al. Avian influenza rapidly induces antiviral genes in duck lung and intestine. Mol Immunol 2012; 51:316–324 [View Article] [PubMed]
    [Google Scholar]
  44. Fleming-Canepa X, Aldridge JR Jr, Canniff L, Kobewka M, Jax E et al. Duck innate immune responses to high and low pathogenicity H5 avian influenza viruses. Vet Microbiol 2019; 228:101–111 [View Article] [PubMed]
    [Google Scholar]
  45. Costa T, Chaves AJ, Valle R, Darji A, van Riel D et al. Distribution patterns of influenza virus receptors and viral attachment patterns in the respiratory and intestinal tracts of seven avian species. Vet Res 2012; 43:1–13 [View Article] [PubMed]
    [Google Scholar]
  46. Daoust P-Y, Kibenge FSB, Fouchier RAM, van de Bildt MWG, van Riel D et al. Replication of low pathogenic avian influenza virus in naturally infected Mallard ducks (Anas platyrhynchos) causes no morphologic lesions. J Wildl Dis 2011; 47:401–409 [View Article] [PubMed]
    [Google Scholar]
  47. Gambaryan A, Yamnikova S, Lvov D, Tuzikov A, Chinarev A et al. Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain. Virology 2005; 334:276–283 [View Article] [PubMed]
    [Google Scholar]
  48. Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG. Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 1978; 84:268–278 [View Article] [PubMed]
    [Google Scholar]
  49. Campbell LK, Magor KE. Pattern recognition receptor signaling and innate responses to influenza A viruses in the mallard duck, compared to humans and chickens. Front Cell Infect Microbiol 2020; 10:209 [View Article] [PubMed]
    [Google Scholar]
  50. Evseev D, Magor KE. Innate immune responses to avian influenza viruses in ducks and chickens. Vet Sci 2019; 6:E5 [View Article] [PubMed]
    [Google Scholar]
  51. Halvorson D, Karunakaran D, Senne D, Kelleher C, Bailey C et al. Epizootiology of avian influenza--simultaneous monitoring of sentinel ducks and turkeys in Minnesota. Avian Dis 1983; 27:77–85 [PubMed]
    [Google Scholar]
  52. Jimenez-Bluhm P, Di Pillo F, Bahl J, Osorio J, Schultz-Cherry S et al. Circulation of influenza in backyard productive systems in central Chile and evidence of spillover from wild birds. Prev Vet Med 2018; 153:1–6 [View Article]
    [Google Scholar]
  53. Li J, zu Dohna H, Anchell NL, Adams SC, Dao NT et al. Adaptation and transmission of a duck-origin avian influenza virus in poultry species. Virus Res 2010; 147:40–46 [View Article] [PubMed]
    [Google Scholar]
  54. Stallknecht DE, Brown JD. Ecology of avian influenza in wild birds. Avian Influenza 200843–58 [View Article]
    [Google Scholar]
  55. Fair JM, Paul E, Jones J. Guidelines to the use of wild birds in resUse of Wild Birds in Research. In Fair JM, Paul E, Jones J. eds The Ornithological Council Washington, DC: 2010
    [Google Scholar]
  56. Svobodová J, Pinkasová H, Hyršl P, Dvořáčková M, Zita L et al. Differences in the growth rate and immune strategies of farmed and wild mallard populations. PLoS One 2020; 15:1–19 [View Article] [PubMed]
    [Google Scholar]
  57. Woolcock PR. Avian influenza virus isolation and propagation in chicken eggs. Methods Mol Biol 2008; 436:35–46 [View Article] [PubMed]
    [Google Scholar]
  58. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints12. Am J Hyg 1938; 27:493–497 [View Article]
    [Google Scholar]
  59. Hénaux V, Samuel MD. Avian influenza shedding patterns in waterfowl: implications for surveillance, environmental transmission, and disease spread. J Wildl Dis 2011; 47:566–578 [View Article] [PubMed]
    [Google Scholar]
  60. Das A, Spackman E, Pantin-Jackwood MJ, Suarez DL. Removal of real-time reverse transcription polymerase chain reaction (RT-PCR) inhibitors associated with cloacal swab samples and tissues for improved diagnosis of Avian influenza virus by RT-PCR. J Vet Diagn Invest 2009; 21:771–778 [View Article] [PubMed]
    [Google Scholar]
  61. Spackman E, Suarez DL. Type a influenza virus detection and quantitation by real-time RT-PCR. Methods Mol Biol 2008; 436:19–26 [View Article]
    [Google Scholar]
  62. Jourdain E, Gunnarsson G, Wahlgren J, Latorre-Margalef N, Bröjer C et al. Influenza virus in a natural host, the mallard: experimental infection data. PLoS One 2010; 5:e8935 [View Article]
    [Google Scholar]
  63. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data Cambridge, UK: Babraham Institute; 2011
    [Google Scholar]
  64. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  65. Mallard assembly and gene annotation [Internet]; 2019 http://uswest.ensembl.org/Anas_platyrhynchos/Info/Annotation
  66. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013; 29:15–21 [View Article] [PubMed]
    [Google Scholar]
  67. Dobin A, Gingeras TR. Mapping RNA-seq Reads with STAR. Curr Protoc Bioinformatics 2015; 51:11 [View Article] [PubMed]
    [Google Scholar]
  68. Anders S, Pyl PT, Huber W. HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics 2015; 31:166–169 [View Article] [PubMed]
    [Google Scholar]
  69. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011; 12:323 [View Article] [PubMed]
    [Google Scholar]
  70. Cheviron ZA, Carling MD, Brumfield RT. Effects of postmortem interval and preservation method on RNA isolated from field-preserved avian tissues. The Condor 2011; 113:483–489 [View Article]
    [Google Scholar]
  71. Xiong B, Yang Y, Fineis FR, Wang JP. DegNorm: normalization of generalized transcript degradation improves accuracy in RNA-seq analysis. Genome Biol 2019; 20:1–18 [View Article] [PubMed]
    [Google Scholar]
  72. Copois V, Bibeau F, Bascoul-Mollevi C, Salvetat N, Chalbos P et al. Impact of RNA degradation on gene expression profiles: assessment of different methods to reliably determine RNA quality. J Biotechnol 2007; 127:549–559 [View Article] [PubMed]
    [Google Scholar]
  73. Gallego Romero I, Pai A, Tung J, Gilad Y. Impact of RNA degradation on measurements of gene expression. BMC Biol 2014; 12:1–13 [View Article]
    [Google Scholar]
  74. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [View Article] [PubMed]
    [Google Scholar]
  75. McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 2012; 40:4288–4297 [View Article] [PubMed]
    [Google Scholar]
  76. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 2015; 43:e47 [View Article] [PubMed]
    [Google Scholar]
  77. Law CW, Alhamdoosh M, Su S, Dong X, Tian L et al. RNA-seq analysis is easy as 1-2-3 with limma, Glimma and edgeR. F1000Res 2016; 5:1–29 [View Article] [PubMed]
    [Google Scholar]
  78. Frega M, Selten M, Mossink B, Keller JM, Linda K et al. Distinct pathogenic genes causing intellectual disability and autism exhibit a common neuronal network hyperactivity phenotype. Cell Rep 2020; 30:173–186 [View Article] [PubMed]
    [Google Scholar]
  79. Shi Z, Zhang Z, Schaffer L, Huang Z, Fu L et al. Dynamic transcriptome landscape in the song nucleus HVC between juvenile and adult zebra finches. Advanced Genetics 2021; 2:1–13 [View Article]
    [Google Scholar]
  80. Wubuli A, Gerlinger C, Reyer H, Oster M, Muráni E et al. Reduced phosphorus intake throughout gestation and lactation of sows is mitigated by transcriptional adaptations in kidney and intestine. BMC Genomics 2020; 21:1–11 [View Article] [PubMed]
    [Google Scholar]
  81. Branco AT, Brito RM, Lemos B. Sex-specific adaptation and genomic responses to Y chromosome presence in female reproductive and neural tissues. Proc R Soc B 2017; 284:20172062 [View Article]
    [Google Scholar]
  82. Shim JM, Kim J, Tenson T, Min JY, Kainov DE. Influenza virus infection, interferon response, viral counter-response, and apoptosis. Viruses 2017; 9:223 [View Article]
    [Google Scholar]
  83. Zhang X, Yang W, Wang X, Zhang X, Tian H et al. Identification of new type I interferon-stimulated genes and investigation of their involvement in IFN-β activation. Protein Cell 2018; 9:799–807 [View Article]
    [Google Scholar]
  84. Schoggins JW. Interferon-stimulated genes: what do they all do?. Annu Rev Virol 2019; 6:567–584 [View Article]
    [Google Scholar]
  85. Shaw ML, Stertz S. Role of host genes in influenza virus replication. In Roles of Host Gene and Non-Coding RNA Expression in Virus Infection Cham: Springer; 2017 pp 151–189 [View Article]
    [Google Scholar]
  86. Peacock TP, Sheppard CM, Staller E, Barclay WS. Host determinants of influenza RNA synthesis. Annu Rev Virol 2019; 6:215–233 [View Article] [PubMed]
    [Google Scholar]
  87. König R, Stertz S, Zhou Y, Inoue A, Hoffmann H-H et al. Human host factors required for influenza virus replication. Nature 2010; 463:813–817 [View Article] [PubMed]
    [Google Scholar]
  88. Dubois J, Terrier O, Rosa-Calatrava M. Influenza viruses and mRNA splicing: doing more with less. mBio 2014; 5:e00070–14 [View Article] [PubMed]
    [Google Scholar]
  89. Stambas J, Ye S, Izzard L, Dlugolenski DA, Tripp RA et al. ADAMTS5 and its substrate versican play a critical role in influenza virus immunity. J Immunol 2017; 198:121–123
    [Google Scholar]
  90. Cao Y, Huang Y, Xu K, Liu Y, Li X et al. Differential responses of innate immunity triggered by different subtypes of influenza a viruses in human and avian hosts. BMC Med Genomics 2017; 10:41–54 [View Article] [PubMed]
    [Google Scholar]
  91. Kuchipudi SV, Tellabati M, Sebastian S, Londt BZ, Jansen C et al. Highly pathogenic avian influenza virus infection in chickens but not ducks is associated with elevated host immune and pro-inflammatory responses. Vet Res 2014; 45:1–18 [View Article]
    [Google Scholar]
  92. Barber MRW, Aldridge JR, Fleming-Canepa X, Wang Y-D, Webster RG et al. Identification of avian RIG-I responsive genes during influenza infection. Mol Immunol 2013; 54:89–97 [View Article]
    [Google Scholar]
  93. Anne Harduin-Lepers. Comprehensive Analysis of Sialyltransferases in Vertebrate Genomes. Glycobiol Insights 2010; 2:29–61 [View Article]
    [Google Scholar]
  94. Pinheiro J, Bates D, DebRoy S, Sarkar D. Linear and nonlinear mixed effects models. R Packag version 3 20071–97
    [Google Scholar]
  95. Costa TP, Brown JD, Howerth EW, Stallknecht DE. Variation in viral shedding patterns between different wild bird species infected experimentally with low-pathogenicity avian influenza viruses that originated from wild birds. Avian Pathol 2011; 40:119–124 [View Article] [PubMed]
    [Google Scholar]
  96. Franca M, Stallknecht DE, Poulson R, Brown J, Howerth EW. The pathogenesis of low pathogenic avian influenza in mallards research note — the pathogenesis of low pathogenic avian influ enza in mallards. Avian Dis 2012; 56:976–980 [View Article]
    [Google Scholar]
  97. Maughan MN, Dougherty LS, Preskenis LA, Ladman BS, Gelb J Jr et al. Transcriptional analysis of the innate immune response of ducks to different species-of-origin low pathogenic H7 avian influenza viruses. Virol J 2013; 10:1–11 [View Article] [PubMed]
    [Google Scholar]
  98. Söderquist P, Elmberg J, Gunnarsson G, Thulin C-G, Champagnon J et al. Admixture between released and wild game birds: a changing genetic landscape in European mallards (Anas platyrhynchos). Eur J Wildl Res 2017; 63: [View Article]
    [Google Scholar]
  99. Champagnon J, Guillemain M, Elmberg J, Massez G, Cavallo F et al. Low survival after release into the wild: assessing “the burden of captivity” on Mallard physiology and behaviour. Eur J Wildl Res 2011; 58:255–267 [View Article]
    [Google Scholar]
  100. Moore SJ, Battley PF. Differences in the digestive organ morphology of captive and wild Brown Teal Anas chlorotis and implications for releases. Bird Conservation International 2006; 16:253–264 [View Article]
    [Google Scholar]
  101. Foletta VC, Segal DH, Cohen DR. Transcriptional regulation in the immune system: all roads lead to AP-1. J Leukoc Biol 1998; 63:139–152 [View Article] [PubMed]
    [Google Scholar]
  102. Stricher F, Macri C, Ruff M, Muller S. HSPA8/HSC70 chaperone protein: structure, function, and chemical targeting. Autophagy 2013; 9:1937–1954 [View Article] [PubMed]
    [Google Scholar]
  103. Watanabe K, Fuse T, Asano I, Tsukahara F, Maru Y et al. Identification of Hsc70 as an influenza virus matrix protein (M1) binding factor involved in the virus life cycle. FEBS Lett 2006; 580:5785–5790 [View Article] [PubMed]
    [Google Scholar]
  104. Sanchez EL, Lagunoff M. Viral activation of cellular metabolism. Virology 2015; 479–480:609–618 [View Article] [PubMed]
    [Google Scholar]
  105. Zhou Y, Pu J, Wu Y. The Role of Lipid Metabolism in Influenza A Virus Infection. Pathogens 2021; 10:1–11 [View Article] [PubMed]
    [Google Scholar]
  106. Meineke R, Rimmelzwaan GF, Elbahesh H. Influenza Virus Infections and Cellular Kinases. Viruses 2019; 11:E171 [View Article] [PubMed]
    [Google Scholar]
  107. Watanabe T, Watanabe S, Kawaoka Y. Cellular networks involved in the influenza virus life cycle. Cell Host Microbe 2010; 7:427–439 [View Article] [PubMed]
    [Google Scholar]
  108. Rohaim MA, Santhakumar D, Naggar RFE, Iqbal M, Hussein HA et al. Chickens Expressing IFIT5 Ameliorate Clinical Outcome and Pathology of Highly Pathogenic Avian Influenza and Velogenic Newcastle Disease Viruses. Front Immunol 2018; 9:1–17 [View Article] [PubMed]
    [Google Scholar]
  109. Helin AS, Wille M, Atterby C, Järhult JD, Waldenström J et al. A rapid and transient innate immune response to avian influenza infection in mallards. Mol Immunol 2018; 95:64–72 [View Article] [PubMed]
    [Google Scholar]
  110. Sreekantapuram S, Lehnert T, Prauße MTE, Berndt A, Berens C et al. Dynamic Interplay of Host and Pathogens in an Avian Whole-Blood Model. Front Immunol 2020; 11:1–20 [View Article] [PubMed]
    [Google Scholar]
  111. Zeng M, Chen S, Wang M, Jia R, Zhu D et al. Molecular identification and comparative transcriptional analysis of myxovirus resistance GTPase (Mx) gene in goose (Anser cygnoide) after H9N2 AIV infection. Comp Immunol Microbiol Infect Dis 2016; 47:32–40 [View Article] [PubMed]
    [Google Scholar]
  112. van der Goot JA, de Jong MCM, Koch G, Van Boven M. Comparison of the transmission characteristics of low and high pathogenicity avian influenza A virus (H5N2). Epidemiol Infect 2003; 131:1003–1013 [View Article] [PubMed]
    [Google Scholar]
  113. Zhang J, Huang Y, Li L, Dong J, Liao M et al. Transcriptome analysis reveals the neuro-immune interactions in duck Tembusu virus-infected brain. Int J Mol Sci 2020; 21:E2402 [View Article]
    [Google Scholar]
  114. Zhao Y, Wang K, Wang WL, Yin TT, Dong WQ et al. A high-throughput SNP discovery strategy for RNA-seq data. BMC Genomics 2019; 20:1–10 [View Article]
    [Google Scholar]
  115. Juliarena MA, Barrios CN, Ceriani MC, Esteban EN. Hot topic: Bovine leukemia virus (BLV)-infected cows with low proviral load are not a source of infection for BLV-free cattle. J Dairy Sci 2016; 99:4586–4589 [View Article] [PubMed]
    [Google Scholar]
  116. Matthews L, Low JC, Gally DL, Pearce MC, Mellor DJ et al. Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proc Natl Acad Sci U S A 2006; 103:547–552 [View Article] [PubMed]
    [Google Scholar]
  117. Shin A, Toy T, Rothenfusser S, Robson N, Vorac J et al. P2Y receptor signaling regulates phenotype and IFN-alpha secretion of human plasmacytoid dendritic cells. Blood 2008; 111:3062–3069 [View Article] [PubMed]
    [Google Scholar]
  118. Tripathi S, Pohl MO, Zhou Y, Rodriguez-Frandsen A, Wang G et al. Meta- and Orthogonal Integration of Influenza “OMICs” Data Defines a Role for UBR4 in Virus Budding. Cell Host Microbe 2015; 18:723–735 [View Article] [PubMed]
    [Google Scholar]
  119. Song G, Liu B, Li Z, Wu H, Wang P et al. E3 ubiquitin ligase RNF128 promotes innate antiviral immunity through K63-linked ubiquitination of TBK1. Nat Immunol 2016; 17:1342–1351 [View Article] [PubMed]
    [Google Scholar]
  120. Hirota K, Matsui M, Iwata S, Nishiyama A, Mori K et al. AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. Proc Natl Acad Sci U S A 1997; 94:3633–3638 [View Article] [PubMed]
    [Google Scholar]
  121. Zhao Q, Hu Z-. Y, Zhang J-. P, Jiang J-. D, Ma Y-. Y et al. Dual Roles of Two Isoforms of Autophagy-related Gene ATG10 in HCV-Subgenomic replicon Mediated Autophagy Flux and Innate Immunity. Sci Rep 2017; 7:1–15 [View Article]
    [Google Scholar]
  122. Angelov D, Molla A, Perche P-Y, Hans F, Côté J et al. The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol Cell 2003; 11:1033–1041 [View Article] [PubMed]
    [Google Scholar]
  123. Gewurz BE, Towfic F, Mar JC, Shinners NP, Takasaki K et al. Genome-wide siRNA screen for mediators of NF-κB activation. Proc Natl Acad Sci U S A 2012; 109:2467–2472 [View Article] [PubMed]
    [Google Scholar]
  124. Lin L, Pan S, Zhao J, Liu C, Wang P et al. HSPD1 Interacts with IRF3 to Facilitate Interferon-Beta Induction. PLoS ONE 2014; 9:e114874 [View Article]
    [Google Scholar]
  125. Jørgensen SE, Al-Mousawi A, Assing K, Hartling U, Grosen D et al. STK4 Deficiency Impairs Innate Immunity and Interferon Production Through Negative Regulation of TBK1-IRF3 Signaling. J Clin Immunol 2021; 41:109–124 [View Article] [PubMed]
    [Google Scholar]
  126. Meng F, Zhou R, Wu S, Zhang Q, Jin Q et al. Mst1 shuts off cytosolic antiviral defense through IRF3 phosphorylation. Genes Dev 2016; 30:1086–1100 [View Article] [PubMed]
    [Google Scholar]
  127. Bagashev A, Fitzgerald MC, LaRosa DF, Rose PP, Cherry S et al. Leucine-Rich Repeat (in Flightless I) Interacting Protein-1 Regulates a Rapid Type I Interferon Response. Journal of Interferon & Cytokine Research 2010; 30:843–852 [View Article]
    [Google Scholar]
  128. Dai P, Jeong SY, Yu Y, Leng T, Wu W et al. Modulation of TLR signaling by multiple MyD88-interacting partners including leucine-rich repeat Fli-I-interacting proteins. J Immunol 2009; 182:3450–3460 [View Article] [PubMed]
    [Google Scholar]
  129. Bonvin M, Achermann F, Greeve I, Stroka D, Keogh A et al. Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 2006; 43:1364–1374 [View Article] [PubMed]
    [Google Scholar]
  130. Wang FX, Huang J, Zhang H, Ma X, Zhang H. APOBEC3G upregulation by alpha interferon restricts human immunodeficiency virus type 1 infection in human peripheral plasmacytoid dendritic cells. J Gen Virol 2008; 89:722–730 [View Article] [PubMed]
    [Google Scholar]
  131. Chen Y-W, Guo T, Shen L, Wong K-Y, Tao Q et al. Receptor-type tyrosine-protein phosphatase κ directly targets STAT3 activation for tumor suppression in nasal NK/T-cell lymphoma. Blood 2015; 125:1589–1600 [View Article] [PubMed]
    [Google Scholar]
  132. Lin R-. J, Chang B-. L, Yu H-. P, Liao C-. L, Lin Y-L. Blocking of interferon-induced Jak-Stat signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J Virol 2006; 80:5908–5918 [View Article] [PubMed]
    [Google Scholar]
  133. Kim Y-H, Lee J-R, Hahn M-J. Regulation of inflammatory gene expression in macrophages by epithelial-stromal interaction 1 (Epsti1). Biochem Biophys Res Commun 2018; 496:778–783 [View Article] [PubMed]
    [Google Scholar]
  134. Rong E, Hu J, Yang C, Chen H, Wang Z et al. Broad-spectrum antiviral functions of duck interferon-induced protein with tetratricopeptide repeats (AvIFIT). Dev Comp Immunol 2018; 84:71–81 [View Article]
    [Google Scholar]
  135. Alonso MA, Weissman SM. cDNA cloning and sequence of MAL, a hydrophobic protein associated with human T-cell differentiation. Proc Natl Acad Sci U S A 1987; 84:1997–2001 [View Article] [PubMed]
    [Google Scholar]
  136. Gatto M, Iaccarino L, Ghirardello A, Bassi N, Pontisso P et al. Serpins, immunity and autoimmunity: old molecules, new functions. Clin Rev Allergy Immunol 2013; 45:267–280 [View Article] [PubMed]
    [Google Scholar]
  137. Bao J, Pan G, Poncz M, Wei J, Ran M et al. Serpin functions in host-pathogen interactions. PeerJ 2018; 6:1–16 [View Article] [PubMed]
    [Google Scholar]
  138. Hong YH, Lillehoj HS, Lee SH, Park DW, Lillehoj EP. Molecular cloning and characterization of chicken lipopolysaccharide-induced TNF-alpha factor (LITAF). Dev Comp Immunol 2006; 30:919–929 [View Article] [PubMed]
    [Google Scholar]
  139. Kaiser P, Staheli P. Avian cytokines and chemokines. Avian Immunology 2013189–204
    [Google Scholar]
  140. Perusina Lanfranca M, Lin Y, Fang J, Zou W, Frankel T. Biological and pathological activities of interleukin-22. J Mol Med 2016; 94:523–534 [View Article]
    [Google Scholar]
  141. Zhu L, Ly H, Liang Y. PLC-γ1 signaling plays a subtype-specific role in postbinding cell entry of influenza A virus. J Virol 2014; 88:417–424 [View Article] [PubMed]
    [Google Scholar]
  142. Kudo K, Uchida T, Sawada M, Nakamura Y, Yoneda A et al. Phospholipase C δ1 in macrophages negatively regulates TLR4-induced proinflammatory cytokine production and Fcγ receptor-mediated phagocytosis. Adv Biol Regul 2016; 61:68–79 [View Article] [PubMed]
    [Google Scholar]
  143. McGinn OJ, English WR, Roberts S, Ager A, Newham P et al. Modulation of integrin α4β1 by ADAM28 promotes lymphocyte adhesion and transendothelial migration. Cell Biol Int 2011; 35:1043–1053 [View Article] [PubMed]
    [Google Scholar]
  144. Koretzky GA, Picus J, Schultz T, Weiss A. Tyrosine phosphatase CD45 is required for T-cell antigen receptor and CD2-mediated activation of a protein tyrosine kinase and interleukin 2 production. Proc Natl Acad Sci U S A 1991; 88:2037–2041 [View Article] [PubMed]
    [Google Scholar]
  145. Hercus TR, Thomas D, Guthridge MA, Ekert PG, King-Scott J et al. The granulocyte-macrophage colony-stimulating factor receptor: linking its structure to cell signaling and its role in disease. Blood 2009; 114:1289–1298 [View Article] [PubMed]
    [Google Scholar]
  146. Lei Y, Takahama Y. XCL1 and XCR1 in the immune system. Microbes and Infection 2012; 14:262–267 [View Article] [PubMed]
    [Google Scholar]
  147. Hansell C, Zhu XW, Brooks H, Sheppard M, Withanage S et al. Unique Features and Distribution of the Chicken CD83 + Cell. J Immunol 2007; 179:5117–5125 [View Article] [PubMed]
    [Google Scholar]
  148. Kuwano Y, Prazma CM, Yazawa N, Watanabe R, Ishiura N et al. CD83 influences cell-surface MHC class II expression on B cells and other antigen-presenting cells. Int Immunol 2007; 19:977–992 [View Article]
    [Google Scholar]
  149. Huang Y-W, Yan M, Collins RF, DiCiccio JE, Grinstein S et al. Mammalian Septins Are Required for Phagosome Formation. MBoC 2008; 19:1717–1726 [View Article] [PubMed]
    [Google Scholar]
  150. Attardi LD, Reczek EE, Cosmas C, Demicco EG, McCurrach ME et al. PERP, an apoptosis-associated target of p53, is a novel member of the PMP-22/gas3 family. Genes Dev 2000; 14:704–718 [View Article] [PubMed]
    [Google Scholar]
  151. Zheng M, Karki R, Vogel P, Kanneganti TD. Caspase-6 Is a Key Regulator of Innate Immunity, Inflammasome Activation, and Host Defense. Cell 2020; 181:674–687 [View Article] [PubMed]
    [Google Scholar]
  152. Chen S, Evans HG, Evans DR. FAM129B/MINERVA, a novel adherens junction-associated protein, suppresses apoptosis in HeLa cells. J Biol Chem 2011; 286:10201–10209 [View Article] [PubMed]
    [Google Scholar]
  153. Rishi AK, Zhang L, Boyanapalli M, Wali A, Mohammad RM et al. Identification and characterization of a cell cycle and apoptosis regulatory protein-1 as a novel mediator of apoptosis signaling by retinoid CD437. J Biol Chem 2003; 278:33422–33435 [View Article] [PubMed]
    [Google Scholar]
  154. Brass AL, Huang I-C, Benita Y, John SP, Krishnan MN et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009; 139:1243–1254 [View Article] [PubMed]
    [Google Scholar]
  155. Basters A, Knobeloch KP, Fritz G. USP18 - a multifunctional component in the interferon response. Biosci Rep 2018; 38:1–9 [View Article] [PubMed]
    [Google Scholar]
  156. Das A, Dinh PX, Panda D, Pattnaik AK. Interferon-inducible protein IFI35 negatively regulates RIG-I antiviral signaling and supports vesicular stomatitis virus replication. J Virol 2014; 88:3103–3113 [View Article] [PubMed]
    [Google Scholar]
  157. Hayashi H, Kubo Y, Izumida M, Takahashi E, Kido H et al. Enterokinase Enhances Influenza A Virus Infection by Activating Trypsinogen in Human Cell Lines. Front Cell Infect Microbiol 2018; 8:1–14 [View Article] [PubMed]
    [Google Scholar]
  158. Florin L, Lang T. Tetraspanin Assemblies in Virus Infection. Front Immunol 2018; 9:1–9 [View Article] [PubMed]
    [Google Scholar]
  159. Ampomah PB, Kong WT, Zharkova O, Chua SCJH, Perumal Samy R et al. Annexins in influenza virus replication and pathogenesis. Front Pharmacol 2018; 9:1–9 [View Article]
    [Google Scholar]
  160. LeBouder F, Morello E, Rimmelzwaan GF, Bosse F, Péchoux C et al. Annexin II incorporated into influenza virus particles supports virus replication by converting plasminogen into plasmin. J Virol 2008; 82:6820–6828 [View Article]
    [Google Scholar]
  161. Larson GP, Tran V, S, Caì Y, Higgins CA et al. EPS8 Facilitates Uncoating of Influenza A Virus. Cell Rep 2019; 29:2175–2183 [View Article]
    [Google Scholar]
  162. Puertollano R, Martín-Belmonte F, Millán J, de Marco MC, Albar JP et al. The mal proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J Cell Biol 1999; 145:141–151 [View Article]
    [Google Scholar]
  163. Wang H, Jiang C. Influenza A virus H5N1 entry into host cells is through clathrin-dependent endocytosis. Sci China C Life Sci 2009; 52:464–469 [View Article]
    [Google Scholar]
  164. Guinea R, Carrasco L. Requirement for vacuolar proton-ATPase activity during entry of influenza virus into cells. J Virol 1995; 69:2306–2312 [View Article] [PubMed]
    [Google Scholar]
  165. Qiu XB, Shao YM, Miao S, Wang L. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci 2006; 63:2560–2570 [View Article] [PubMed]
    [Google Scholar]
  166. Shi Z, Zhang J, Zheng S. What we know about ST13, a co-factor of heat shock protein, or a tumor suppressor?. J Zhejiang Univ Sci B 2007; 8:170–176 [View Article] [PubMed]
    [Google Scholar]
  167. Klempner SJ, Ou S-H. ROS1 (ROS proto-oncogene 1, receptor tyrosine kinase). Atlas Genet Cytogenet Oncol Haematol 2017; 19:337–339 [View Article]
    [Google Scholar]
  168. Kumar N, Liang Y, Parslow TG, Liang Y. Receptor tyrosine kinase inhibitors block multiple steps of influenza a virus replication. J Virol 2011; 85:2818–2827 [View Article] [PubMed]
    [Google Scholar]
  169. Mi SF, Li Y, Yan JH, Gao GF. Na(+)/K (+)-ATPase β1 subunit interacts with M2 proteins of influenza A and B viruses and affects the virus replication. Sci China Life Sci 2010; 53:1098–1105 [View Article] [PubMed]
    [Google Scholar]
  170. Edinger TO, Pohl MO, Yángüez E, Stertz S, Palese P. Cathepsin W Is Required for Escape of Influenza A Virus from Late Endosomes. mBio 2015; 6:1–12 [View Article]
    [Google Scholar]
  171. Coleman MD, Ha SD, Haeryfar M, Dominic Barr S, Ouk Kim S. Cathepsin B Plays a Key Role in Optimal Production of the Influenza A- Virus. J Virol Antivir Res 2018; 07:1–16 [View Article]
    [Google Scholar]
  172. Heaton NS, Moshkina N, Fenouil R, Gardner TJ, Aguirre S et al. Targeting Viral Proteostasis Limits Influenza Virus, HIV, and Dengue Virus Infection. Immunity 2016; 44:46–58 [View Article] [PubMed]
    [Google Scholar]
  173. Zhang J, Li G, Ye X. Cyclin T1/CDK9 interacts with influenza A virus polymerase and facilitates its association with cellular RNA polymerase II. J Virol 2010; 84:12619–12627 [View Article] [PubMed]
    [Google Scholar]
  174. Su W-. C, Hsu S-. F, Lee Y-. Y, Jeng K-. S, Lai MMC. A Nucleolar Protein, Ribosomal RNA Processing 1 Homolog B (RRP1B), Enhances the Recruitment of Cellular mRNA in Influenza Virus Transcription. J Virol 2015; 89:11245–11255 [View Article] [PubMed]
    [Google Scholar]
  175. Minakuchi M, Sugiyama K, Kato Y, Naito T, Okuwaki M et al. Pre-mRNA Processing Factor Prp18 Is a Stimulatory Factor of Influenza Virus RNA Synthesis and Possesses Nucleoprotein Chaperone Activity. J Virol 2017; 91:1–11 [View Article]
    [Google Scholar]
  176. Bayoumi M, Rohaim MA, Munir M. Structural and Virus Regulatory Insights Into Avian N6-Methyladenosine (m6A) Machinery. Front Cell Dev Biol 2020; 8:1–14 [View Article]
    [Google Scholar]
  177. Cao M, Wei C, Zhao L, Wang J, Jia Q et al. DnaJA1/Hsp40 is co-opted by influenza A virus to enhance its viral RNA polymerase activity. J Virol 2014; 88:14078–14089 [View Article] [PubMed]
    [Google Scholar]
  178. Naito T, Momose F, Kawaguchi A, Nagata K. Involvement of Hsp90 in assembly and nuclear import of influenza virus RNA polymerase subunits. J Virol 2007; 81:1339–1349 [View Article] [PubMed]
    [Google Scholar]
  179. Predicala R, Zhou Y. The role of Ran-binding protein 3 during influenza A virus replication. J Gen Virol 2013; 94:977–984 [View Article] [PubMed]
    [Google Scholar]
  180. Bruce EA, Digard P, Stuart AD. The Rab11 pathway is required for influenza A virus budding and filament formation. J Virol 2010; 84:5848–5859 [View Article] [PubMed]
    [Google Scholar]
  181. Amorim MJ, Bruce EA, Read EKC, Foeglein A, Mahen R et al. A Rab11- and microtubule-dependent mechanism for cytoplasmic transport of influenza A virus viral RNA. J Virol 2011; 85:4143–4156 [View Article] [PubMed]
    [Google Scholar]
  182. Singh I, Doms RW, Wagner KR, Helenius A. Intracellular transport of soluble and membrane-bound glycoproteins: folding, assembly and secretion of anchor-free influenza hemagglutinin. EMBO J 1990; 9:631–639 [PubMed]
    [Google Scholar]
  183. Hogue BG, Nayak DP. Synthesis and processing of the influenza virus neuraminidase, a type II transmembrane glycoprotein. Virology 1992; 188:510–517 [View Article] [PubMed]
    [Google Scholar]
  184. Tokhtaeva E, Capri J, Marcus EA, Whitelegge JP, Khuzakhmetova V et al. Septin dynamics are essential for exocytosis. J Biol Chem 2015; 290:5280–5297 [View Article] [PubMed]
    [Google Scholar]
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