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

Journal of Virology

Volumn 85, Issue 21, 2011, Pages 11146-11158

  Smith, Jacqueline ^a   Sadeyen, Jean Remy ^b   Paton, Ian R ^a   Hocking, Paul M ^a   Salmon, Nigel ^b   Fife, Mark ^b   Nair, Venugopal ^b   Burt, David W ^a   Kaiser, Pete ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING SITE; CHICKEN; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC VARIABILITY; HIC1 GENE; IMMUNE RESPONSE; IMMUNORESPONSIVE GENE 1; INFECTION RESISTANCE; INFECTION SENSITIVITY; MARDIVIRUS; MAREK DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE; ONCOGENE MEQ; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS GENE; VIRUS VIRULENCE;

ANIMALS; CHICKENS; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MARDIVIRUS; MAREK DISEASE; UNITED STATES;

ANIMALIA; GALLID HERPESVIRUS 2; GALLUS GALLUS;

EID: 80055122518     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05499-11     Document Type: Article

References (52)

1. Affymetrix. 2005. Guide to probe logarithmic intensity error (PLIER) estimation. Affymetrix I, Santa Clara, CA.
2. Asmundson, V. S., and J. Biely. 1932. Inheritance of resistance to fowl paralysis (neurolymphomatosis gallinarum). I. Differences in susceptibility. Can. J. Res. 6:171-176.
3. Baigent, S. J., and F. Davison. 2004. Marek's disease virus: biology and life cycle, p. 62-77. In F. Davison and V. Nair (ed.), Marek's disease: an evolving problem. Elsevier Academic Press, London, United Kingdom.
4. Brown, A. C., et al. 2006. Interaction of MEQ protein and C-terminalbinding protein is critical for induction of lymphomas by Marek's disease virus. Proc. Natl. Acad. Sci. U. S. A. 103:1687-1692.
5. Brownlie, R., et al. 2009. Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Mol. Immunol. 46:3163-3170.
6. Buza, J. J., and S. C. Burgess. 2007. Modeling the proteome of a Marek's disease transformed cell line: a natural animal model for CD30 overexpressing lymphomas. Proteomics 7:1316-1326.
7. Calnek, B. W. 1986. Marek's disease-a model for herpesvirus oncology. Crit. Rev. Microbiol. 12:293-320.
8. Calnek, B. W. 2001. Pathogenesis of Marek's disease virus infection. Curr. Top. Microbiol. Immunol. 255:25-55.
9. Chen, B., D. Zhang, and J. W. Pollard. 2003. Progesterone regulation of the mammalian ortholog of methylcitrate dehydratase (immune response gene 1) in the uterine epithelium during implantation through the protein kinase C pathway. Mol. Endocrinol. 17:2340-2354.
10. Cheng, H. H., Y. Zhang, and W. M. Muir. 2007. Evidence for widespread epistatic interactions influencing Marek's disease virus viremia levels in chicken. Cytogenet. Genome Res. 117:313-318.
11. Cheng, H. H., et al. 2008. Using integrative genomics to elucidate genetic resistance to Marek's disease in chickens. Dev. Biol. (Basel) 132:365-372.
12. Davison, F., and V. Nair. 2005. Use of Marek's disease vaccines: could they be driving the virus to increasing virulence? Expert Rev. Vaccines 4:77-88.
13. Degrandi, D., R. Hoffman, C. Beuter-Gunia, and K. Pfeffer. 2009. The proinflammatory cytokine-induced IRG1 protein associates with mitochondria. J. Interferon Cyt. Res. 29:55-68.
14. Derfuss, T., and E. Meinl. 2002. Herpesviral proteins regulating apoptosis. Curr. Top. Microbiol. Immunol. 269:257-272.
15. Draghici, S., et al. 2007. A systems biology approach for pathway level analysis. Genome Res. 17:1537-1545.
16. Gimeno, I. M. 2008. Marek's disease vaccines: a solution for today but a worry for tomorrow? Vaccine 26(Suppl. 3):C31-C41.
17. Guerardel, C., et al. 2001. Identification in the human candidate tumor suppressor gene HIC-1 of a new major alternative TATA-less promoter positively regulated by p53. J. Biol. Chem. 276:3078-3089.
18. Heidari, M., H. M. Zhang, and S. Sharif. 2008. Marek's disease virus induces Th-2 activity during cytolytic infection. Viral Immunol. 21:203-214.
19. Heifetz, E. M., et al. 2009. Mapping QTL affecting resistance to Marek's disease in an F6 advanced intercross population of commercial layer chickens. BMC Genomics 10:20.
20. Higgs, R., et al. 2006. Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74:1692-1698.
21. International Chicken Genome Sequencing Consortium. 2004. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695-716. (Erratum, 433:77, 2005.)
22. Kaiser, P., G. Underwood, and F. Davison. 2003. Differential cytokine responses following Marek's disease virus infection of chickens differing in resistance to Marek's disease. J. Virol. 77:762-768.
23. Kanehisa, M., and S. Goto. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28:27-30.
24. Kaufman, J. 2000. The simple chicken major histocompatibility complex: life and death in the face of pathogens and vaccines. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:1077-1084.
25. Keestra, A. M., M. R. de Zoete, L. I. Bouwman, and J. P. van Putten. 2010. Chicken TLR21 is an innate CpG DNA receptor distinct from mammalian TLR9. J. Immunol. 185:460-467.
26. Koch, M., et al. 2007. Structures of an MHC class I molecule from B21 chickens illustrate promiscuous peptide binding. Immunity 27:885-899.
27. Kuhnlein, U., et al. 1997. DNA polymorphisms in the chicken growth hormone gene: response to selection for disease resistance and association with egg production. Anim. Genet. 28:116-123.
28. Lee, C. G., N. A. Jenkins, D. J. Gilbert, N. G. Copeland, and W. E. O'Brien. 1995. Cloning and analysis of gene regulation of a novel LPS-inducible cDNA. Immunogenetics 41:263-270.
29. Liu, H. C., H. H. Cheng, V. Tirunagaru, L. Sofer, and J. Burnside. 2001. A strategy to identify positional candidate genes conferring Marek's disease resistance by integrating DNA microarrays and genetic mapping. Anim. Genet. 32:351-359.
30. Liu, H. C., H. J. Kung, J. E. Fulton, R. W. Morgan, and H. H. Cheng. 2001. Growth hormone interacts with the Marek's disease virus SORF2 protein and is associated with disease resistance in chicken. Proc. Natl. Acad. Sci. U. S. A. 98:9203-9208.
31. Liu, H. C., M. Niikura, J. E. Fulton, and H. H. Cheng. 2003. Identification of chicken lymphocyte antigen 6 complex, locus E (LY6E, alias SCA2) as a putative Marek's disease resistance gene via a virus-host protein interaction screen. Cytogenet. Genome Res. 102:304-308.
32. Matys, V., et al. 2006. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 34:D108-D110.
33. McElroy, J. P., et al. 2005. Microsatellite markers associated with resistance to Marek's disease in commercial layer chickens. Poult. Sci. 84:1678-1688.
34. Morimura, T., et al. 1996. Apoptosis and CD8-down-regulation in the thymus of chickens infected with Marek's disease virus. Arch. Virol. 141:2243-2249.
35. Morimura, T., M. Hattori, K. Ohashi, C. Sugimoto, and M. Onuma. 1995. Immunomodulation of peripheral T cells in chickens infected with Marek's disease virus: involvement in immunosuppression. J. Gen. Virol. 76:2979-2985.
36. Morrow, C., and F. Fehler. 2004. Marek's disease: a worldwide problem, p. 49-61. In F. Davison and V. Nair (ed.), Marek's disease: an evolving problem. Elsevier Academic Press, London, United Kingdom.
37. Nerren, J. R., H. He, K. Genovese, and M. H. Kogut. 2010. Expression of the avian-specific toll-like receptor 15 in chicken heterophils is mediated by gram-negative and gram-positive bacteria, but not TLR agonists. Vet. Immunol. Immunopathol. 136:151-156.
38. Pazderka, F., B. M. Longenecker, G. R. J. Law, H. A. Stone, and R. F. Ruth. 1975. Histocompatability of chicken populations selected for resistance to Marek's disease. Immunogenetics 2:93-100.
39. Sallusto, F., et al. 1998. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28:2760-2769.
40. Sarson, A. J., M. F. Abdul-Careem, H. Zhou, and S. Sharif. 2006. Transcrip-tional analysis of host responses to Marek's disease viral infection. Viral Immunol. 19:747-758.
41. Sarson, A. J., P. Parvizi, D. Lepp, M. Quinton, and S. Sharif. 2008. Transcriptional analysis of host responses to Marek's disease virus infection in genetically resistant and susceptible chickens. Anim. Genet. 39:232-240.
42. Schat, K. A. 2004. Marek's disease immunosuppression, p. 142-155. In F. Davison and V. Nair (ed.), Marek's disease: an evolving problem. Elsevier Academic Press, London, United Kingdom.
43. Schat, K. A., and Z. Xing. 2000. Specific and nonspecific immune responses to Marek's disease virus. Dev. Comp. Immunol. 24:201-221.
44. Sharan, R., A. Maron-Katzm, and R. Shamir. 2003. CLICK and EXPANDER: a system for clustering and visualizing gene expression data. Bioinformatics 19:1787-1799.
45. Shek, W. R., B. W. Calnek, K. A. Schat, and C. H. Chen. 1983. Characterization of Marek's disease virus-infected lymphocytes: discrimination between cytolytically and latently infected cells. J. Natl. Cancer Inst. 70:485-491.
46. Talloen, W., et al. 2007. I/NI calls for the exclusion of non-informative genes: a highly effective filtering tool for microarray data. Bioinformatics 23:2897-2902.
47. Theocharidis, A., S. van Dongen, A. J. Enright, and T. C. Freeman. 2009. Network visualization and analysis of gene expression data using BioLayout Express (3D). Nat. Protoc. 4:1535-1550.
48. Vallejo, R. L., et al. 1998. Genetic mapping of quantitative trait loci affecting susceptibility to Marek's disease virus induced tumors in F2 intercross chickens. Genetics 148:349-360.
49. Wales, M. M., et al. 1995. p53 activates expression of HIC-1, a new candidate tumour suppressor gene on 17p13.3. Nat. Med. 1:570-577.
50. Witter, R. L. 1997. Increased virulence of Marek's disease virus field isolates. Avian Dis. 41:149-163.
51. Wu, Z., T. Hu, L. Rothwell, J. R. Young, and P. Kaiser. 2011. Chicken CCR6 and CCR7 are markers for immature and mature dendritic cells respectively. Dev. Comp. Immunol. 35:563-567.
52. Yonash, N., L. D. Bacon, R. L. Witter, and H. H. Cheng. 1999. High resolution mapping and identification of new quantitative trait loci (QTL) affecting susceptibility to Marek's disease. Anim. Genet. 30:126-135.