Abstract
Newcastle disease virus (NDV) is an important pathogen hazardous to poultry industry, and the pathogenicity of NDV strains varies with different virulence. Peripheral blood serves as an important producer and carrier of viruses and cytokines in NDV infection. In order to explore the difference of cytokine expression in the peripheral blood between velogenic strain and lentogenic strain infection, NDV virulent strain F48E9 and vaccine strain Lasota were used to infect specific-pathogen-free (SPF) chickens separately, and peripheral blood was collected on 0, 3, 7, 10, 14, and 21 days post-infection (d.p.i.). Real-time PCR was then used to detect the expression of six kinds of immune-related cytokine genes. For the F48E9 group, a sharp increase of the expression of interferon-alpha (IFN-α), interferon-gamma (IFN-γ), interleukin-16 and IL-18 was observed on 3 d.p.i. before the NDV blood peak (7 d.p.i.), followed by a rapid decline to the level lower than that of control group, then the expression of IFN-α increased slowly and reached or exceeded the level of control group in the later phase of the infection, while the expression of IFN-γ, IL-16, and IL-18 fluctuated at the level of control group for the rest of study period. The increase of IL-2 expression was not obvious, and no increase of IL-15 expression was noted. For the Lasota (vaccine) group, the picture was quite different, a sharp increase of IFN-γ (but not IFN-α), IL-2 was observed on 7 d.p.i. before the NDV blood peak (10 d.p.i.). On the contrary, there was no dramatic increase of IL-16 and IL-18. Interestingly, in contrast to the F48E9 group, there was an increase of IL-15 on day 10 d.p.i., but it remained modest. There was also an increase of IFN-α on day 21 d.p.i. Our results revealed that infection with NDV strains of different virulence was associated with distinct cytokine expression patterns in peripheral blood, modulation of cytokine responses may play a key role in mediation of NDV pathogenesis.
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References
Alexander DJ, Senne DA (2008) Newcastle disease, other avian paramyxoviruses, and pneumovirus infections. In: Saif YM (ed) Diseases of swine, 12th edn. 2121 State Avenue, Ames, Wiley-Blackwell Publishing Professional, Iowa, pp 75–100
Jindal N, Chander Y, Chockalingam AK, de Abin M, Redig PT, Goyal SM (2009) Phylogenetic analysis of Newcastle disease viruses isolated from waterfowl in the upper midwest region of the United States. Virol J 6:191. doi:10.1186/1743-422X-6-191
Phillips RJ, Samson AC, Emmerson PT (1998) Nucleotide sequence of the 5′-terminus of Newcastle disease virus and assembly of the complete genomic sequence: agreement with the “rule of six”. Arch Virol 143:1993–2002
Miller PJ, Kim LM, Ip HS, Afonso CL (2009) Evolutionary dynamics of Newcastle disease virus. Virology 391:64–72. doi:10.1016/j.virol.2009.05.033
Huang Z, Panda A, Elankumaran S, Govindarajan D, Rockemann DD, Samal SK (2004) The hemagglutinin-neuraminidase protein of Newcastle disease virus determines tropism and virulence. J Virol 78:4176–4184
Mebatsion T, Verstegen S, De Vaan LT, Romer-Oberdorfer A, Schrier CC (2001) A recombinant Newcastle disease virus with low-level V protein expression is immunogenic and lacks pathogenicity for chicken embryos. J Virol 75:420–428. doi:10.1128/JVI.75.1.420-428.2001
Kaiser P, Underwood G, Davison F (2003) Differential cytokine responses following Marek’s disease virus infection of chickens differing in resistance to Marek’s disease. J Virol 77:762–768
Quere P, Rivas C, Ester K, Novak R, Ragland WL (2005) Abundance of IFN-alpha and IFN-gamma mRNA in blood of resistant and susceptible chickens infected with Marek’s disease virus (MDV) or vaccinated with turkey herpesvirus; and MDV inhibition of subsequent induction of IFN gene transcription. Arch Virol 150:507–519. doi:10.1007/s00705-004-0435-3
Jarosinski KW, Njaa BL, O’Connell PH, Schat KA (2005) Pro-inflammatory responses in chicken spleen and brain tissues after infection with very virulent plus Marek’s disease virus. Viral Immunol 18:148–161. doi:10.1089/vim.2005.18.148
Xing Z, Schat KA (2000) Expression of cytokine genes in Marek’s disease virus-infected chickens and chicken embryo fibroblast cultures. Immunology 100:70–76
Abdul-Careem MF, Hunter DB, Lambourne MD, Read LR, Parvizi P, Sharif S (2008) Expression of cytokine genes following pre- and post-hatch immunization of chickens with herpesvirus of turkeys. Vaccine 26:2369–2377. doi:10.1016/j.vaccine.2008.02.069
Abdul-Careem MF, Hunter DB, Thanthrige-Don N, Haghighi HR, Lambourne MD, Sharif S (2008) Cellular and cytokine responses associated with dinitrofluorobenzene-induced contact hypersensitivity in the chicken. Vet Immunol Immunopathol 122:275–284. doi:10.1016/j.vetimm.2008.01.029
Abdul-Careem MF, Read LR, Parvizi P, Thanthrige-Don N, Sharif S (2009) Marek’s disease virus-induced expression of cytokine genes in feathers of genetically defined chickens. Dev Comp Immunol 33:618–623. doi:0.1016/j.dci.2008.11.003
Djeraba A, Musset E, Bernardet N, Le Vern Y, Quere P (2002) Similar pattern of iNOS expression, NO production and cytokine response in genetic and vaccination-acquired resistance to Marek’s disease. Vet Immunol Immunopathol 85:63–75
Carvajal BG, Methner U, Pieper J, Berndt A (2008) Effects of Salmonella enterica serovar enteritidis on cellular recruitment and cytokine gene expression in caecum of vaccinated chickens. Vaccine 26:5423–5433. doi:S0165242701004123
Swaggerty CL, He H, Genovese KJ, Kaiser P, Pevzner IY, Kogut MH (2006) The feathering gene is linked to degranulation and oxidative burst not cytokine/chemokine mRNA expression levels or Salmonella enteritidis organ invasion in broilers. Avian Pathol 35:465–470. doi:10.1080/03079450601028829
Hong YH, Lillehoj HS, Lee SH, Dalloul RA, Lillehoj EP (2006) Analysis of chicken cytokine and chemokine gene expression following Eimeria acervulina and Eimeria tenella infections. Vet Immunol Immunopathol 114:209–223. doi:10.1016/j.vetimm.2006.07.007
Degen WG, Daal N, Rothwell L, Kaiser P, Schijns VE (2005) Th1/Th2 polarization by viral and helminth infection in birds. Vet Microbiol 105:163–167. doi:10.1016/j.vetmic.2004.12.001
Martinez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre JC (2006) Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 80:9192–9199. doi:10.1128/JVI.00555-06
Wang D, Li X, Xu L, Hu Y, Zhang B, Liu J (2006) Immunologic synergism with IL-2 and effects of cCHMIs on mRNA expression of IL-2 and IFN-gamma in chicken peripheral T lymphocyte. Vaccine 24:7109–7114. doi:10.1128/JVI.00555-06
Lowenthal JW, Digby MR, York JJ (1995) Production of interferon-gamma by chicken T cells. J Interferon Cytokine Res 15:933–938
Digby MR, Lowenthal JW (1995) Cloning and expression of the chicken interferon-gamma gene. J Interferon Cytokine Res 15:939–945
Rothwell L, Young JR, Zoorob R, Whittaker CA, Hesketh P, Archer A, Smith AL, Kaiser P (2004) Cloning and characterization of chicken IL-10 and its role in the immune response to Eimeria maxima. J Immunol 173:2675–2682
Hilton LS, Bean AG, Kimpton WG, Lowenthal JW (2002) Interleukin-2 directly induces activation and proliferation of chicken T cells in vivo. J Interferon Cytokine Res 22:755–763. doi:10.1089/107999002320271341
Schauenstein K, Kromer G, Fassler R, Wick G (1987) Implications of IL-2 in normal and disturbed immune functions in the chicken. Prog Clin Biol Res 233:69–77
Sundick RS, Gill-Dixon C (1997) A cloned chicken lymphokine homologous to both mammalian IL-2 and IL-15. J Immunol 159:720–725
Lillehoj HS, Min W, Choi KD, Babu US, Burnside J, Miyamoto T, Rosenthal BM, Lillehoj EP (2001) Molecular, cellular, and functional characterization of chicken cytokines homologous to mammalian IL-15 and IL-2. Vet Immunol Immunopathol 82:229–244
Gobel TW, Schneider K, Schaerer B, Mejri I, Puehler F, Weigend S, Staeheli P, Kaspers B (2003) IL-18 stimulates the proliferation and IFN-gamma release of CD4+ T cells in the chicken: conservation of a Th1-like system in a nonmammalian species. J Immunol 171:1809–1815
Kogut MH, Rothwell L, Kaiser P (2003) Priming by recombinant chicken interleukin-2 induces selective expression of IL-8 and IL-18 mRNA in chicken heterophils during receptor-mediated phagocytosis of opsonized and nonopsonized Salmonella enterica serovar enteritidis. Mol Immunol 40:603–610
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The study was financially supported by Sichuan Youth Science and Technology Foundation (Grant number: 2007Q14-034) and China Postdoctoral Science Foundation (Grant number: 2005037805) and a postdoctoral fund from Sichuan Agricultural University, as well as Program for Changjiang Scholars and Innovative Research Team in University “PCSIRT” (Grant No: IRTO848).
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Liu, WQ., Tian, MX., Wang, YP. et al. The different expression of immune-related cytokine genes in response to velogenic and lentogenic Newcastle disease viruses infection in chicken peripheral blood. Mol Biol Rep 39, 3611–3618 (2012). https://doi.org/10.1007/s11033-011-1135-1
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DOI: https://doi.org/10.1007/s11033-011-1135-1