期刊论文详细信息
BMC Genomics
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
David W. Burt2  Robert G. Webster1  Paul Digard2  J. Patrick Seiler1  Angela F. Danner1  Heather L. Forrest1  Maria Weronika Gutowska2  Ian R. Paton2  Le Yu2  Nikki Smith2  Jacqueline Smith2 
[1]St. Jude Children’s Research Hospital, Virology Division, Department of Infectious Diseases, 262 Danny Thomas Place, Memphis 38105, TN, USA
[2]The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK
关键词: Evolution and gene expression profiles;    Interferon-induced transmembrane proteins;    Pathogenicity;    Chicken;    Duck;    H5N2;    H5N1;    Avian influenza;   
Others  :  1222426
DOI  :  10.1186/s12864-015-1778-8
 received in 2014-08-26, accepted in 2015-07-14,  发布年份 2015
PDF
【 摘 要 】

Background

Chickens 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.

Results

Transcriptomic 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.

Conclusions

Taken 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.

【 授权许可】

   
2015 Smith et al.

【 预 览 】
附件列表
Files Size Format View
20150821021009802.pdf 2159KB PDF download
Fig. 7. 47KB Image download
Fig. 6. 96KB Image download
Fig. 5. 10KB Image download
Fig. 4. 50KB Image download
Fig. 3. 83KB Image download
Fig. 2. 84KB Image download
Fig. 1. 30KB Image download
【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

【 参考文献 】
  • [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, Webster RG, Magor KE. Avian influenza rapidly induces antiviral genes in duck lung and intestine. Mol Immunol. 2012; 51:316-324.
  • [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; 42:347-364.
  • [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; 78:4892-4901.
  • [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. BioMed Central Full Text
  • [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. BioMed Central Full Text
  • [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; 90:116-123.
  • [8]CNN article:. http://edition. cnn.com/2013/04/24/world/asia/china-birdflu/index.html webcite
  • [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):48245-48250.
  • [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; 101:4620-4624.
  • [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):143-151.
  • [13]Hughes AL, Friedman R. Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes. Mol Biol Evol. 2008; 25:2681-2688.
  • [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):776-783.
  • [15]Yilmaz A, Shen SX, Adelson DL, Xavier S, Zhu JJ. Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics. 2005; 56:743-753.
  • [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. BioMed Central Full Text
  • [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):377-388.
  • [18]Barber MR, Aldridge JR, Webster RG, Magor KE. Association of RIG-I with innate immunity of ducks to influenza. Proc Natl Acad Sci U S A. 2010; 107:5913-5918.
  • [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): Article ID 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):519-523.
  • [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: Article ID 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: Article ID 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):1243-1254.
  • [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):452-464.
  • [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):7837-7852.
  • [27]Pantin-Jackwood M, Swayne DE. Pathobiology of avian influenza virus infections in birds and mammals. In: In Avian Influenza . Swayne DE, editor. Blackwell Publishing, Iowa; 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; 87:12957-12966.
  • [29]Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001; 17(8):754-755.
  • [30]Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003; 19(12):1572-1574.
  • [31]Pond SL, Frost SD. Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005; 21:2531-2533.
  • [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: Article ID 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; 30:1196-1205.
  • [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 webcite
  • [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):1545-1559.
  • [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):14063-14068.
  • [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):11146-11158.
  • [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):11986-11992.
  • [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; 6:610-614.
  • [42]Yount JS, Karssemeijer RA, Hang HC. S-palmitoylation and ubiquination differentially regulate IFITM3-mediated resistance to influenza virus. J Biol Chem. 2012; 287:19631-19641.
  • [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; 15:280-290.
  • [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: Article ID e1003124
  • [45]BLAST. http://blast. ncbi.nlm.nih.gov/Blast.cgi/ webcite
  • [46]Genewise. http://www. ebi.ac.uk/Tools/psa/genewise/ webcite
  • [47]SMART. http://smart. embl-heidelberg.de/ webcite
  • [48]SOSUI. http://bp. nuap.nagoya-u.ac.jp/sosui/ webcite
  • [49]Expasy. http://www. expasy.org/ webcite
  • [50]T-coffee. http://www. tcoffee.org webcite
  • [51]Jalview. http://www. jalview.org webcite
  • [52]Weblogo. http://weblogo. threeplusone.com/ webcite
  • [53]GenBank. www. ncbi.nlm.nih.gov/ webcite
  • [54]Ensembl. www. ensembl.org/ webcite
  • [55]Avian Phylogenomic Project. http://phybirds. genomics.org.cn/ webcite
  • [56]MUSCLE. www. ebi.ac.uk webcite
  • [57]MrBayes. http://mrbayes. sourceforge.net/ webcite
  • [58]MEGA6. www. megasoftware.net/ webcite
  • [59]FigTree. www. molecularevolution.org webcite
  • [60]DATAMONKEY. www. datamonkey.org webcite
  • [61]Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24:1586-1591.
  • [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; 27:493-497.
  • [64]Livak KJ, Schmittgen TD. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 − ΔΔCT Method. Methods. 2001; 25:402-408.
  • [65]Pathway Express. http://vortex. cs.wayne.edu/ontoexpress/ webcite
  • [66]Ingenuity Pathway Analysis. http://www. ingenuity.com/ webcite
  • [67]Expander. http://acgt. cs.tau.ac.il/expander/ webcite
  • [68]MATLAB and Statistics Toolbox Release 2009, The MathWorks, Inc., Natick, Massachusetts, United States. www. mathworks.co.uk/products/matlab/ webcite
  • [69]DAVID. https://david. ncifcrf.gov/ webcite
  • [70]Dennis 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. BioMed Central Full Text
  文献评价指标  
  下载次数:91次 浏览次数:18次