1887

Abstract

The pathogenesis of H9N2 subtype avian influenza virus (AIV) infection in hens is often related to oviduct tissue damage. Our previous study suggested that H9N2 AIV induces cellular apoptosis by activating reactive oxygen species (ROS) accumulation and mitochondria-mediated apoptotic signalling in chicken oviduct epithelial cells (COECs). Heme oxygenase-1 (HO-1) is an inducible enzyme that exerts protective effects against oxidative stress and activated HO-1 was recently shown to have antiviral activity. To study the potential involvement of HO-1 in H9N2 AIV proliferation, the role of its expression in H9N2-infected COECs was further investigated. Our results revealed that H9N2 AIV infection significantly up-regulated the expression of HO-1 and that HO-1 down-regulation by ZnPP, a classical inhibitor of HO-1, could inhibit H9N2 AIV replication in COECs. Similarly, the small interfering RNA (siRNA)-mediated knockdown of HO-1 also markedly decreased the virus production in H9N2-infected COECs. In contrast, adenoviral-mediated over-expression of HO-1 concomitantly promoted H9N2 AIV replication. Taken together, our study demonstrated the involvement of HO-1 in AIV H9N2 proliferation, and these findings suggested that HO-1 is a potential target for inhibition of AIV H9N2 replication.

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2018-01-01
2024-03-28
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References

  1. Abolnik C, Bisschop SP, Gerdes GH, Olivier AJ, Horner RF. Phylogenetic analysis of low-pathogenicity avian influenza H6N2 viruses from chicken outbreaks (2001–2005) suggest that they are reassortants of historic ostrich low-pathogenicity avian influenza H9N2 and H6N8 viruses. Avian Dis 2007; 51:279–284 [View Article][PubMed]
    [Google Scholar]
  2. Bi J, Deng G, Dong J, Kong F, Li X et al. Phylogenetic and molecular characterization of H9N2 influenza isolates from chickens in Northern China from 2007–2009. PLoS One 2010; 5:e13063 [View Article][PubMed]
    [Google Scholar]
  3. Kim JA, Cho SH, Kim HS, Seo SH. H9N2 influenza viruses isolated from poultry in Korean live bird markets continuously evolve and cause the severe clinical signs in layers. Vet Microbiol 2006; 118:169–176 [View Article][PubMed]
    [Google Scholar]
  4. Wang JY, Chen ZL, Li CS, Cao XL, Wang R et al. The distribution of sialic acid receptors of avian influenza virus in the reproductive tract of laying hens. Mol Cell Probes 2015; 29:129–134 [View Article][PubMed]
    [Google Scholar]
  5. Qi X, Tan D, Wu C, Tang C, Li T et al. Deterioration of eggshell quality in laying hens experimentally infected with H9N2 avian influenza virus. Vet Res 2016; 47:1–10 [View Article][PubMed]
    [Google Scholar]
  6. Wang J, Tang C, Wang Q, Li R, Chen Z et al. Apoptosis induction and release of inflammatory cytokines in the oviduct of egg-laying hens experimentally infected with H9N2 avian influenza virus. Vet Microbiol 2015; 177:302–314 [View Article][PubMed]
    [Google Scholar]
  7. Qi X, Zhang H, Wang Q, Wang J. The NS1 protein of avian influenza virus H9N2 induces oxidative-stress-mediated chicken oviduct epithelial cells apoptosis. J Gen Virol 2016; 97:3183–3192 [View Article][PubMed]
    [Google Scholar]
  8. Riquelme SA, Carreño LJ, Espinoza JA, Mackern-Oberti JP, Alvarez-Lobos MM et al. Modulation of antigen processing by haem-oxygenase 1. Implications on inflammation and tolerance. Immunology 2016; 149:1–12 [View Article][PubMed]
    [Google Scholar]
  9. Ozen M, Zhao H, Lewis DB, Wong RJ, Stevenson DK. Heme oxygenase and the immune system in normal and pathological pregnancies. Front Pharmacol 2015; 6:84 [View Article][PubMed]
    [Google Scholar]
  10. Maines MD. The heme oxygenase system: update 2005. Antioxid Redox Signal 2005; 7:1761–1766 [View Article][PubMed]
    [Google Scholar]
  11. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 2010; 80:1895–1903 [View Article][PubMed]
    [Google Scholar]
  12. Chung SW, Hall SR, Perrella MA. Role of haem oxygenase-1 in microbial host defence. Cell Microbiol 2009; 11:199–207 [View Article][PubMed]
    [Google Scholar]
  13. Hill-Batorski L, Halfmann P, Neumann G, Kawaoka Y. The cytoprotective enzyme heme oxygenase-1 suppresses Ebola virus replication. J Virol 2013; 87:13795–13802 [View Article][PubMed]
    [Google Scholar]
  14. Xiao S, Zhang A, Zhang C, Ni H, Gao J et al. Heme oxygenase-1 acts as an antiviral factor for porcine reproductive and respiratory syndrome virus infection and over-expression inhibits virus replication in vitro. Antiviral Res 2014; 110:60–69 [View Article][PubMed]
    [Google Scholar]
  15. Choi AM, Knobil K, Otterbein SL, Eastman DA, Jacoby DB. Oxidant stress responses in influenza virus pneumonia: gene expression and transcription factor activation. Am J Physiol 1996; 271:L383–L391[PubMed]
    [Google Scholar]
  16. La P, Fernando AP, Wang Z, Salahudeen A, Yang G et al. Zinc protoporphyrin regulates cyclin D1 expression independent of heme oxygenase inhibition. J Biol Chem 2009; 284:36302–36311 [View Article][PubMed]
    [Google Scholar]
  17. Bauer M, Huse K, Settmacher U, Claus RA. The heme oxygenase-carbon monoxide system: regulation and role in stress response and organ failure. Intensive Care Med 2008; 34:640–648 [View Article][PubMed]
    [Google Scholar]
  18. Cummins NW, Weaver EA, May SM, Croatt AJ, Foreman O et al. Heme oxygenase-1 regulates the immune response to influenza virus infection and vaccination in aged mice. Faseb J 2012; 26:2911–2918 [View Article][PubMed]
    [Google Scholar]
  19. Ma LL, Wang HQ, Wu P, Hu J, Yin JQ et al. Rupestonic acid derivative YZH-106 suppresses influenza virus replication by activation of heme oxygenase-1-mediated interferon response. Free Radic Biol Med 2016; 96:347–361 [View Article][PubMed]
    [Google Scholar]
  20. Gou H, Zhao M, Xu H, Yuan J, He W et al. CSFV induced mitochondrial fission and mitophagy to inhibit apoptosis. Oncotarget 2017; 8:39382–39400 [View Article][PubMed]
    [Google Scholar]
  21. Pyo CW, Shin N, Jung KI, Choi JH, Choi SY. Alteration of copper-zinc superoxide dismutase 1 expression by influenza A virus is correlated with virus replication. Biochem Biophys Res Commun 2014; 450:711–716 [View Article][PubMed]
    [Google Scholar]
  22. Seronello S, Ito C, Wakita T, Choi J. Ethanol enhances hepatitis C virus replication through lipid metabolism and elevated NADH/NAD+. J Biol Chem 2010; 285:845–854 [View Article][PubMed]
    [Google Scholar]
  23. Qi X, Liu C, Li R, Zhang H, Xu X et al. Modulation of the innate immune-related genes expression in H9N2 avian influenza virus-infected chicken macrophage-like cells (HD11) in response to Escherichia coli LPS stimulation. Res Vet Sci 2017; 111:36–42 [View Article][PubMed]
    [Google Scholar]
  24. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg 1938; 27:493–497
    [Google Scholar]
  25. Lei M, Qin L, Wang A, Jin Y, Zhao X et al. Fn14 receptor appears as a modulator of ovarian steroid-related regulation of goat endometrial epithelial cell IL-18 expression. Am J Reprod Immunol 2015; 73:428–436 [View Article][PubMed]
    [Google Scholar]
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