RNA sequencing-based analysis of the spleen transcriptome following infectious bronchitis virus infection of chickens selected for different mannose-binding lectin serum concentrations

详细信息    查看全文

• 作者：Edin Hamzić ; Rikke Brødsgaard Kjærup ; Núria Mach ; Guilietta Minozzi…
• 关键词：IBV ; Coronavirus ; Infectious bronchitis ; Chicken ; RNA sequencing ; Transcriptome ; Spleen ; Mannose ; binding lectin ; Immune response
• 刊名：BMC Genomics
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：17
• 期：1
• 全文大小：1,408 KB
• 参考文献：1.Jackwood MW, Hall D, Handel A. Molecular evolution and emergence of avian gammacoronaviruses. Infect Genet Evol. 2012;12:1305–11.CrossRef PubMed
  2.Jackwood MW, de Wit S. Infectious Bronchitis. In: Swayne DE, Glisson JR, McDougald LR, Nolan LK, Suarez DL, Nair VL, editors. Diseases of Poultry. 13th ed. Hoboken: Wiley-Blackwell; 2013. p. 139–59.
  3.Meeusen ENT, Walker J, Peters A, Pastoret P-P, Jungersen G. Current status of veterinary vaccines. Clin Microbiol Rev. 2007;20:489–510.PubMedCentral CrossRef PubMed
  4.Bande F, Arshad SS, Bejo MH, Moeini H, Omar AR. Progress and challenges toward the development of vaccines against avian infectious bronchitis. J Immunol Res. 2015;2015:424860.PubMedCentral CrossRef PubMed
  5.Abd El Rahman S, El-Kenawy AA, Neumann U, Herrler G, Winter C. Comparative analysis of the sialic acid binding activity and the tropism for the respiratory epithelium of four different strains of avian infectious bronchitis virus. Avian Pathol. 2009;38:41–5.CrossRef PubMed
  6.Guo X, Rosa AJM, Chen D-G, Wang X. Molecular mechanisms of primary and secondary mucosal immunity using avian infectious bronchitis virus as a model system. Vet Immunol Immunopathol. 2008;121:332–43.CrossRef PubMed
  7.Vervelde L, Rosa AJM, Oliverira HN, Rosa GJM, Guo X, Travnicek M, et al. Transcriptome of local innate and adaptive immunity during early phase of infectious bronchitis viral infection. Viral Immunol. 2006;19:768–74.CrossRef
  8.Vervelde L, Matthijs MGR, van Haarlem DA, de Wit JJ, Jansen CA. Rapid NK-cell activation in chicken after infection with infectious bronchitis virus M41. Vet Immunol Immunopathol. 2013;151:337–41.CrossRef PubMed
  9.Kameka AM, Haddadi S, Kim DS, Cork SC, Abdul-Careem MF. Induction of innate immune response following infectious bronchitis corona virus infection in the respiratory tract of chickens. Virology. 2014;450–451:114–21.CrossRef PubMed
  10.Collisson E. Cytotoxic T, lymphocytes are critical in the control of infectious bronchitis virus in poultry. Dev Comp Immunol. 2000;24:187–200.CrossRef PubMed
  11.Seo SH, Collisson EW. Specific cytotoxic T lymphocytes are involved in in vivo clearance of infectious bronchitis virus. J Virol. 1997;71:5173–7.PubMedCentral PubMed
  12.Martins NR, Mockett AP, Barrett AD, Cook JK. IgM responses in chicken serum to live and inactivated infectious bronchitis virus vaccines. Avian Dis. 1991;35:470–5.CrossRef PubMed
  13.Raj GD, Jones RC. Local antibody production in the oviduct and gut of hens infected with a variant strain of infectious bronchitis virus. Vet Immunol Immunopathol. 1996;53:147–61.CrossRef PubMed
  14.Cook KA, Otsuki K, Martins NR, Ellis MM, Huggins MB. The secretory antibody response of inbred lines of chicken to avian infectious bronchitis virus infection. Avian Pathol. 1992;21:681–92.CrossRef PubMed
  15.Gillette KG. Local antibody response in avian infectious bronchitis: virus-neutralizing antibody in tracheobronchial secretions. Avian Dis. 1981;25:431–43.CrossRef PubMed
  16.Juul-Madsen HR, Norup LR, Jørgensen PH, Handberg KJ, Wattrang E, Dalgaard TS. Crosstalk between innate and adaptive immune responses to infectious bronchitis virus after vaccination and challenge of chickens varying in serum mannose-binding lectin concentrations. Vaccine. 2011;29:9499–507.CrossRef PubMed
  17.Laursen SB, Hedemand JE, Nielsen OL, Thiel S, Koch C, Jensenius JC. Serum levels, ontogeny and heritability of chicken mannan-binding lectin (MBL). Immunology. 1998;94:587–93.PubMedCentral CrossRef PubMed
  18.Kjærup RM, Dalgaard TS, Norup LR, Hamzic E, Sørensen P, Juul-Madsen HR. Characterization of cellular and humoral immune responses after IBV infection in chicken lines differing in MBL serum concentration. Viral Immunol. 2014;27(10):529–42.PubMedCentral CrossRef PubMed
  19.Juul-Madsen HR, Norup LR, Handberg KJ, Jørgensen PH. Mannan-binding lectin (MBL) serum concentration in relation to propagation of infectious bronchitis virus (IBV) in chickens. Viral Immunol. 2007;20:562–70.CrossRef PubMed
  20.Norup LR, Dalgaard TS, Friggens NC, Sørensen P, Juul-Madsen HR. Influence of chicken serum mannose-binding lectin levels on the immune response towards Escherichia coli. Poult Sci. 2009;88:543–53.CrossRef PubMed
  21.Schou TW, Permin A, Christensen JP, Cu HP, Juul-Madsen HR. Mannan-binding lectin (MBL) in two chicken breeds and the correlation with experimental Pasteurella multocida infection. Comp Immunol Microbiol Infect Dis. 2010;33:183–95.CrossRef PubMed
  22.Kjærup RM, Dalgaard TS, Norup LR, Bergman I-M, Sørensen P, Juul-Madsen HR. Adjuvant effects of mannose-binding lectin ligands on the immune response to infectious bronchitis vaccine in chickens with high or low serum mannose-binding lectin concentrations. Immunobiology. 2014;219:263–74.CrossRef PubMed
  23.Downing I, Koch C, Kilpatrick DC. Immature dendritic cells possess a sugar-sensitive receptor for human mannan-binding lectin. Immunology. 2003;109:360–4.PubMedCentral CrossRef PubMed
  24.Anders S, McCarthy DJ, Chen Y, Okoniewski M, Smyth GK, Huber W, et al. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nat Protoc. 2013;8:1765–86.CrossRef PubMed
  25.Kjærup RM, Norup LR, Skjødt K, Dalgaard TS, Juul-Madsen HR. Chicken mannose-binding lectin (MBL) gene variants with influence on MBL serum concentrations. Immunogenetics. 2013;65:461–71.CrossRef PubMed
  26.Schat KA, Kaspers B, Kaiser P. Avian Immunology. 2nd ed. Cambridge: Academic; 2013.
  27.Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 2007;89:391–403.CrossRef PubMed
  28.Kean RP, Cahaner A, Freeman AE, Lamont SJ. Direct and correlated responses to multitrait, divergent selection for immunocompetence. Poult Sci. 1994;73:18–32.CrossRef PubMed
  29.Kimura M. Evolutionary rate at the molecular level. Nature. 1968;217:624–6.CrossRef PubMed
  30.Rauw W, Kanis E, Noordhuizen-Stassen E, Grommers F. Undesirable side effects of selection for high production efficiency in farm animals: a review. Livest Prod Sci. 1998;56:15–33.CrossRef
  31.Rothlin CV, Carrera-Silva EA, Bosurgi L, Ghosh S. TAM receptor signaling in immune homeostasis. Annu Rev Immunol. 2015;33:355–91.PubMedCentral CrossRef PubMed
  32.Paz S, Vilasco M, Werden SJ, Arguello M, Joseph-Pillai D, Zhao T, et al. A functional C-terminal TRAF3-binding site in MAVS participates in positive and negative regulation of the IFN antiviral response. Cell Res. 2011;21:895–910.PubMedCentral CrossRef PubMed
  33.Oganesyan G, Saha S-K, Guo B, He Q-J, Shahangian A, Zarnegar B. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature. 2006;439:208–11.CrossRef PubMed
  34.Shi C-S, Qi H-Y, Boularan C, Huang N-N, Abu-Asab M, Shelhamer JH, et al. SARS-coronavirus open reading frame-9b suppresses innate immunity by targeting mitochondria and the MAVS/TRAF3/TRAF6 signalosome. J Immunol. 2014;193:3080–9.PubMedCentral CrossRef PubMed
  35.Iqbal M, Philbin VJ, Smith AL. Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Vet Immunol Immunopathol. 2005;104:117–27.CrossRef PubMed
  36.Delisle J-S, Giroux M, Boucher G, Landry J-R, Hardy M-P, Lemieux S, et al. The TGF-β-Smad3 pathway inhibits CD28-dependent cell growth and proliferation of CD4 T cells. Genes Immun. 2013;14:115–26.CrossRef PubMed
  37.Schluns KS, Kieper WC, Jameson SC, Lefrançois L. Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo. Nat Immunol. 2000;1:426–32.CrossRef PubMed
  38.Seddon B, Tomlinson P, Zamoyska R. Interleukin 7 and T cell receptor signals regulate homeostasis of CD4 memory cells. Nat Immunol. 2003;4:680–6.CrossRef PubMed
  39.Goldrath AW, Sivakumar PV, Glaccum M, Kennedy MK, Bevan MJ, Benoist C, et al. Cytokine requirements for acute and Basal homeostatic proliferation of naive and memory CD8+ T cells. J Exp Med. 2002;195:1515–22.PubMedCentral CrossRef PubMed
  40.Pfefferle S, Schöpf J, Kögl M, Friedel CC, Müller MA, Carbajo-Lozoya J, et al. The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog. 2011;7, e1002331.PubMedCentral CrossRef PubMed
  41.Van Oers K, Buchanan KL, Thomas TE, Drent PJ. Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality. Anim Behav. 2011;81:1055–61.CrossRef
  42.Dommett RM, Klein N, Turner MW. Mannose-binding lectin in innate immunity: past, present and future. Tissue Antigens. 2006;68:193–209.CrossRef PubMed
  43.Liu G, Wang Q, Liu N, Xiao Y, Tong T, Liu S, et al. Infectious bronchitis virus nucleoprotein specific CTL response is generated prior to serum IgG. Vet Immunol Immunopathol. 2012;148:353–8.CrossRef PubMed
  44.Chaix J, Nish SA, Lin W-HW, Rothman NJ, Ding L, Wherry EJ, et al. Cutting edge: CXCR4 is critical for CD8+ memory T cell homeostatic self-renewal but not rechallenge self-renewal. J Immunol. 2014;193:1013–6.PubMedCentral CrossRef PubMed
  45.Cong F, Liu X, Han Z, Shao Y, Kong X, Liu S. Transcriptome analysis of chicken kidney tissues following coronavirus avian infectious bronchitis virus infection. BMC Genomics. 2013;14:743.PubMedCentral CrossRef PubMed
  46.Waring P, Müllbacher A. Cell death induced by the Fas/Fas ligand pathway and its role in pathology. Immunol Cell Biol. 1999;77:312–7.CrossRef PubMed
  47.Nie Q, Sandford EE, Zhang X, Nolan LK, Lamont SJ. Deep sequencing-based transcriptome analysis of chicken spleen in response to avian pathogenic Escherichia coli (APEC) infection. PLoS One. 2012;7, e41645.PubMedCentral CrossRef PubMed
  48.Damle NK, Aruffo A. Vascular cell adhesion molecule 1 induces T-cell antigen receptor-dependent activation of CD4 + T lymphocytes. Proc Natl Acad Sci U S A. 1991;88:6403–7.PubMedCentral CrossRef PubMed
  49.Chen C-F, Feng X, Liao H-Y, Jin W-J, Zhang J, Wang Y, et al. Regulation of T cell proliferation by JMJD6 and PDGF-BB during chronic hepatitis B infection. Sci Rep. 2014;4:6359.PubMedCentral CrossRef PubMed
  50.Wang M, Zhang Y, Chen Y, Zhang L, Lu X, Chen Z. Mannan-binding lectin regulates dendritic cell maturation and cytokine production induced by lipopolysaccharide. BMC Immunol. 2011;12:1.PubMedCentral CrossRef PubMed
  51.Ulrich-Lynge SL, Dalgaard TS, Norup LR, Kjærup RM, Olsen JE, Sørensen P, et al. The consequence of low mannose-binding lectin plasma concentration in relation to susceptibility to Salmonella Infantis in chickens. Vet Immunol Immunopathol. 2015;163:23–32.CrossRef PubMed
  52.Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2010. http://​www.​bioinformatics.​babraham.​ac.​uk/​projects/​fastqc/​ .
  53.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20.PubMedCentral CrossRef PubMed
  54.Hillier LW, Miller W, Birney E, Warren W, Hardison RC, Ponting CP, et al. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432:695–716.CrossRef
  55.Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36.PubMedCentral CrossRef PubMed
  56.Wang L, Wang S, Li W. RSeQC: quality control of RNA-seq experiments. Bioinformatics. 2012;28:2184–5.CrossRef PubMed
  57.Anders S, Pyl PT, Huber W. HTSeq - A Python framework to work with high-throughput sequencing data. Bioinformatics. 2014;31(2):166–9.PubMedCentral CrossRef PubMed
  58.Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–40.PubMedCentral CrossRef PubMed
  59.Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47.PubMedCentral CrossRef PubMed
  60.McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40:4288–97.PubMedCentral CrossRef PubMed
  61.Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289–300.
  62.Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc. 2007;2:2366–82.PubMedCentral CrossRef PubMed
  63.Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics. 2011;27:431–2.PubMedCentral CrossRef PubMed
  64.Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091–3.PubMedCentral CrossRef PubMed
  
• 作者单位：Edin Hamzić (1) (2) (3)
  Rikke Brødsgaard Kjærup (4)
  Núria Mach (2)
  Guilietta Minozzi (5) (6)
  Francesco Strozzi (5)
  Valentina Gualdi (5)
  John L. Williams (5) (7)
  Jun Chen (8)
  Eva Wattrang (9)
  Bart Buitenhuis (3)
  Helle Risdahl Juul-Madsen (4)
  Tina Sørensen Dalgaard (4)
  
  1. UMR1313 Animal Genetics and Integrative Biology Unit, AgroParisTech, Université Paris-Saclay, 16 rue Claude Bernard, 75005, Paris, France
  2. UMR1313 Animal Genetics and Integrative Biology Unit, INRA, Université Paris-Saclay, Domaine de Vilvert, 78350, Jouy-en-Josas, France
  3. Department of Molecular Biology and Genetics, Center for Quantitative Genetics and Genomics, Aarhus University, Blichers Allé 20, P.O. Box 50, 8830, Tjele, Denmark
  4. Department of Animal Science, Aarhus University, Blichers Allé 20, P.O. Box 50, 8830, Tjele, Denmark
  5. Parco Tecnologico Padano, Via Einstein, 26900, Lodi, Italy
  6. University of Milan, DIVET, Via Celoria 10, 20133, Milan, Italy
  7. School of Animal and Veterinary Sciences, University of Adelaide, SA, 5371, Roseworthy, Australia
  8. Cobb-Vantress Inc, US-412 Road, Siloam Springs, AR, 72761, USA
  9. National Veterinary Institute, Ulls väg 2B, 751 89, Uppsala, Sweden
  
• 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
• 出版者：BioMed Central
• ISSN：1471-2164

文摘

Background Avian infectious bronchitis is a highly contagious disease of the upper-respiratory tract caused by infectious bronchitis virus (IBV). Understanding the molecular mechanisms involved in the interaction between innate and adaptive immune responses to IBV infection is a crucial element for further improvements in strategies to control IB. To this end, two chicken lines, selected for high (L10H line) and low (L10L line) serum concentration of mannose-binding lectin (MBL) were studied. In total, 32 birds from each line were used. Sixteen birds from each line were infected with IBV and sixteen were left uninfected. Eight uninfected and infected birds from each line were euthanized at 1 and 3 weeks post infection. RNA sequencing was performed on spleen samples from all 64 birds and differential gene expression analysis was performed for four comparisons: L10L line versus L10H line for uninfected birds at weeks 1 and 3, respectively, and in the same way for infected birds. Functional analysis was performed using Gene Ontology (GO) Immune System Process terms specific for Gallus gallus.