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

Volumn 16, Issue 1, 2015, Pages

  Smith, Jacqueline ^a   Smith, Nikki ^a   Yu, Le ^a   Paton, Ian R ^a   Gutowska, Maria Weronika ^a   Forrest, Heather L ^b   Danner, Angela F ^b   Seiler, J Patrick ^b   Digard, Paul ^a   Webster, Robert G ^b   Burt, David W ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Avian influenza; Chicken; Duck; Evolution and gene expression profiles; H5N1; H5N2; Interferon induced transmembrane proteins; Pathogenicity

Indexed keywords

BINDING PROTEIN; IFITM123 PROTEIN; INTERFERON; INTERFERON INDUCED TRANSMEMBRANE PROTEIN; MEMBRANE PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; RIG I BINDING PROTEIN; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; VIRUS RECEPTOR; INTERFERON INDUCING AGENT;

ANIMAL TISSUE; ARTICLE; AVIAN INFLUENZA; CHICKEN; CODON; COMPARATIVE STUDY; CONTROLLED STUDY; DUCK; GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC SELECTION; IFITM GENE; IFITM1 GENE; IFITM2 GENE; IFITM3 GENE; ILEUM; IMMUNE RESPONSE; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS A H5N2; LUNG; MEMBRANE FUSION; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; RNF135 GENE; SPECIES DIFFERENCE; TRANSCRIPTOMICS; UPREGULATION; VIRUS RESISTANCE; ANIMAL; GENETICS; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS (H5N1); INFLUENZA A VIRUS (H5N2); METABOLISM; PANDEMIC; PATHOGENICITY; VIROLOGY;

ANAS; AVES; AVIAN INFLUENZA VIRUS; GALLUS GALLUS; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

ANIMALS; CHICKENS; DUCKS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA A VIRUS, H5N2 SUBTYPE; INFLUENZA IN BIRDS; INTERFERON INDUCERS; INTERFERONS; PANDEMICS; PHYLOGENY;

EID: 84938574550     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1778-8     Document Type: Article

References (70)

1. Alexander DJ. A review of avian influenza in different bird species. Vet Microbiol. 2000;74:3-13.
2. Vanderven HA, Petkau K, Ryan-Jean KE, Aldridge Jr JR, Webster RG, Magor KE. Avian influenza rapidly induces antiviral genes in duck lung and intestine. Mol Immunol. 2012;51:316-24.
3. Cornelissen JB, Vervelde L, Post J, Rebel JM. Differences in highly pathogenic avian influenza viral pathogenesis and associated early inflammatory response in chickens and ducks. Avian Pathol. 2013;42:347-64.
4. Sturm-Ramirez KM, Ellis T, Bousfield B, Bissett L, Dyrting K, Rehg JE, et al. Reemerging H5N1 influenza viruses in Hong Kong in 2002 are highly pathogenic to ducks. J Virol. 2004;78:4892-901.
5. Kajihara M, Sakoda Y, Soda K, Minari K, Okamatsu M, Takada A, et al. The PB2, PA, HA, NP, and NS genes of a highly pathogenic avian influenza virus A/whooper swan/Mongolia/3/2005 (H5N1) are responsible for pathogenicity in ducks. Virol J. 2013;10:45.
6. Pantin-Jackwood M, Swayne DE, Smith D, Shepherd E. Effect of species, breed and route of virus inoculation on the pathogenicity of H5N1 highly pathogenic influenza (HPAI) viruses in domestic ducks. Vet Res. 2013;44:62.
7. Kuchipudi SV, Dunham SP, Nelli R, White GA, Coward VJ, Slomka MJ, et al. Rapid death of duck cells infected with influenza: a potential mechanism for host resistance to H5N1. Immunol Cell Biol. 2012;90:116-23.
8. CNN article: [ http://edition.cnn.com/2013/04/24/world/asia/china-birdflu/index.html ]
9. Nunes-Alves C. Viral pathogenesis: The pandemic potential of H10N8. Nat Rev Microbiol. 2014;12(7):461.
10. Gagneux P, Cheriyan M, Hurtado-Ziola N, van der Linden EC, Anderson D, McClure H, et al. Human-specific regulation of alpha 2-6-linked sialic acids. J Biol Chem. 2003;278(48):48245-50.
11. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004;101:4620-4.
12. Kuchipudi SV, Nelli R, White GA, Bain M, Chang KC, Dunham S. Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. J Mol Genet Med. 2009;3(1):143-51.
13. Hughes AL, Friedman R. Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes. Mol Biol Evol. 2008;25:2681-8.
14. Huang Y, Li Y, Burt DW, Chen H, Zhang Y, Qian W, et al. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet. 2013;45(7):776-83.
15. Yilmaz A, Shen SX, Adelson DL, Xavier S, Zhu JJ. Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics. 2005;56:743-53.
16. Temperley ND, Berlin S, Paton IR, Griffin DK. Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics. 2008;9:62.
17. Magor KE, Miranzo Navarro D, Barber MR, Petkau K, Fleming-Canepa X, Blyth GA, et al. Defense genes missing from the flight division. Dev Comp Immunol. 2013;41(3):377-88.
18. Barber MR, Aldridge Jr JR, Webster RG, Magor KE. Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci U S A. 2010;107:5913-8.
19. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM, Chiang JJ, et al. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 2011;7(1), e1001258.
20. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, et al. Gordon SB; GenISIS Investigators; MOSAIC Investigators, Smyth RL, Openshaw PJ, Dougan G, Brass AL, Kellam P: IFITM3 restricts the morbidity and mortality associated with influenza. Nature. 2012;484(7395):519-23.
21. Sällman Almén M, Bringeland N, Fredriksson R, Schiöth HB. The dispanins: a novel gene family of ancient origin that contains 14 human members. PLoS One. 2012;7, e31961.
22. Zhang Z, Liu J, Li M, Yang H, Zhang C. Evolutionary dynamics of the interferon-induced transmembrane gene family in vertebrates. PLoS One. 2012;7, e49265.
23. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell. 2009;139(7):1243-54.
24. Diamond MS, Farzan M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol. 2013;13:46-57.
25. Amini-Bavil-Olyaee S, Choi YJ, Lee JH, Shi M, Huang IC, Farzan M, et al. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe. 2013;13(4):452-64.
26. John SP, Chin CR, Perreira JM, Feeley EM, Aker AM, Savidis G, et al. The CD225 domain of IFITM3 is required for both IFITM protein association and inhibition of influenza A virus and dengue virus replication. J Virol. 2013;87(14):7837-52.
27. Pantin-Jackwood M, Swayne DE. Pathobiology of avian influenza virus infections in birds and mammals. In: Swayne DE, editor. In Avian Influenza. Iowa: Blackwell Publishing; 2008. p. 87-122.
28. Smith SE, Gibson MS, Wash RS, Ferrara F, Wright E, Temperton N, et al. Chicken interferon-inducible transmembrane protein 3 restricts influenza viruses and lyssaviruses in vitro. J Virol. 2013;87:12957-66.
29. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8):754-5.
30. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572-4.
31. Pond SL, Frost SD. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005;21:2531-3.
32. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Pond SLK. Detecting individual; sites subject to episodic diversifying selection. PLoS Genet. 2012;8, e1002764.
33. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Pond SLK, et al. FUBAR: a fast, unconstrained bayesian approximation for Inferring Selection. Mol Biol Evol. 2013;30:1196-205.
34. Upla P, Hyypiä T, Marjomäk V. Role of lipid rafts in virus infection. Future Virol. 2009;4:487-500.
35. Tanner LB: Lipidomics of influenza virus: implications of host cell choline and sphingolipid metabolism. PhD Thesis. National University of Singapore & University of Basel; 2012. http://www.scholarbank.nus.edu.sg/handle/10635/36115 .
36. Jang H, Boltz D, McClaren J, Pani AK, Smeyne M, Korff A, et al. Inflammatory effects of highly pathogenic H5N1 influenza virus infection in the CNS of mice. J Neurosci. 2012;32(5):1545-59.
37. Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, et al. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A. 2009;106(33):14063-8.
38. Wiwanitkit S, Wiwanitkit V. Brain involvement in H7N9 bird flu: a topic for consideration. Arq Neuropsiquiatr. 2013;71:825.
39. Smith J, Sadeyen JR, Paton IR, Hocking PM, Salmon N, Fife M, et al. Systems analysis of immune responses in Marek's disease virus-infected chickens identifies a gene involved in susceptibility and highlights a possible novel pathogenicity mechanism. J Virol. 2011;85(21):11146-58.
40. Chesarino NM, McMichael TM, Hach JC, Yount JS. Phosphorylation of the antiviral protein interferon-inducible transmembrane protein 3 (IFITM3) dually regulates its endocytosis and ubiquitination. J Biol Chem. 2014;289(17):11986-92.
41. Yount JS, Moltedo B, Yang Y-Y, Charron G, Moran TM, Lopez CB, et al. Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3. Nat Chem Biol. 2010;6:610-4.
42. Yount JS, Karssemeijer RA, Hang HC. S-palmitoylation and ubiquination differentially regulate IFITM3-mediated resistance to influenza virus. J Biol Chem. 2012;287:19631-41.
43. Chutiwitoonchai N, Hiyoshi M, Hiyoshi-Yoshidomi Y, Hashimoto M, Tokunaga K, Suzu S. Characteristics of IFITM, the newly identified IFN-inducible anti-HIV-1 family proteins. Microbes Infect. 2013;15:280-90.
44. Li K, Markosyan RM, Zheng Y-M, Golfetto O, Bungart B, Li M, et al. IFITM proteins restrict viral membrane hemifusion. PLoS Pathog. 2013;9, e1003124.
45. BLAST. [ http://blast.ncbi.nlm.nih.gov/Blast.cgi/ ]
46. Genewise. [ http://www.ebi.ac.uk/Tools/psa/genewise/ ]
47. SMART. [ http://smart.embl-heidelberg.de/ ]
48. SOSUI. [ http://bp.nuap.nagoya-u.ac.jp/sosui/ ]
49. Expasy. [ http://www.expasy.org/ ]
50. T-coffee. [ http://www.tcoffee.org ]
51. Jalview. [ http://www.jalview.org ]
52. Weblogo. [ http://weblogo.threeplusone.com/ ]
53. GenBank. [ www.ncbi.nlm.nih.gov/ ]
54. Ensembl. [ www.ensembl.org/ ]
55. Avian Phylogenomic Project. [ http://phybirds.genomics.org.cn/ ]
56. MUSCLE. [ www.ebi.ac.uk ]
57. MrBayes. [ http://mrbayes.sourceforge.net/ ]
58. MEGA6. [ www.megasoftware.net/ ]
59. FigTree. [ www.molecularevolution.org ]
60. DATAMONKEY. [ www.datamonkey.org ]
61. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24:1586-91.
62. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346(6215):1320-31. doi:10.1126/science.1253451 . PubMed PMID: 25504713; PubMed Central PMCID: PMC4405904.
63. Reed LJ, Muench H. A simple method for estimating fifty percent endpoints. Am J Hyg. 1938;27:493-7.
64. Livak KJ, Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-ΔCT Method. Methods. 2001;25:402-8.
65. Pathway Express [ http://vortex.cs.wayne.edu/ontoexpress/ ]
66. Ingenuity Pathway Analysis. [ http://www.ingenuity.com/ ]
67. Expander. [ http://acgt.cs.tau.ac.il/expander/ ]
68. MATLAB and Statistics Toolbox Release 2009, The MathWorks, Inc., Natick, Massachusetts, United States [ www.mathworks.co.uk/products/matlab/ ].
69. DAVID. [ https://david.ncifcrf.gov/ ]
70. Dennis Jr G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, et al. DAVID. Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003;4(5):3.