Molecules and Cells

  • 제41권4호
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  • Pages.271-281
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  • 2018
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  • 1016-8478(pISSN)
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  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
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IFIT1 Expression Patterns Induced by H9N2 Virus and Inactivated Viral Particle in Human Umbilical Vein Endothelial Cells and Bronchus Epithelial Cells

  • Feng, Bo (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture) ;
  • Zhang, Qian (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture) ;
  • Wang, Jianfang (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture) ;
  • Dong, Hong (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture) ;
  • Mu, Xiang (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture) ;
  • Hu, Ge (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture) ;
  • Zhang, Tao (Beijing Key Laboratory of Traditional Chinese Veterinary Medicine, College of Animal Science and Technology, Beijing University of Agriculture)
  • 투고 : 2017.06.01
  • 심사 : 2018.01.07
  • 발행 : 2018.04.30
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초록

IFIT1 (also known as ISG56) is a member of the interferon-inducible protein with tetratricopeptide repeats (IFITs) family. IFITs are strongly induced by type I interferon (IFN), double-stranded RNA and virus infection. Here, we investigated IFIT1 expression in human umbilical vein endothelial cells (HUVECs) and in human bronchus epithelial cells (BEAS-2Bs) induced by the H9N2 virus and inactivated viral particle at different time points. We also investigated the effect of H9N2 virus and viral particle infection on $IFN-{\alpha}/{\beta}$ production, and assessed whether hemagglutinin or neuraminidase protein induced IFIT1 expression. Results showed that both H9N2 virus infection and viral particle inoculation induced the expression of IFIT1 at mRNA and protein levels in the two cell lines. Hemagglutinin or neuraminidase protein binding alone is not sufficient to induce IFIT1 expression. Surprisingly, the expression patterns of IFIT1 in response to H9N2 virus and viral particles in the two cell lines were opposite, and production kinetics of $IFN-{\alpha}/{\beta}$ also differed. An additional finding was that induction of IFIT1 in response to H9N2 virus infection or viral particle inoculation was more sensitive in HUVECs than in BEAS-2Bs. Our data offers new insight into the innate immune response of endothelial cells to H9N2 virus infection.

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참고문헌

  1. Barnes, B.J., Richards, J., Mancl, M., Hanash, S., Beretta, L., and Pitha, P.M. (2004). Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection. J. Biol. Chem. 279, 45194-45207. https://doi.org/10.1074/jbc.M400726200
  2. Bi, Y., Chen, Q., Wang, Q., Chen, J., Jin, T., Wong, G., Quan, C., Liu, J., Wu, J., and Yin, R., et al. (2016). Genesis, Evolution and Prevalence of H5N6 Avian Influenza Viruses in China. Cell Host Microbe. 20, 810-821. https://doi.org/10.1016/j.chom.2016.10.022
  3. Bluyssen, H.A., Vlietstra, R.J., Faber, P.W., Smit, E.M., Hagemeijer, A., and Trapman, J. (1994). Structure, chromosome localization, and regulation of expression of the interferon-regulated mouse Ifi54/Ifi56 gene family. Genomics 24, 137-148. https://doi.org/10.1006/geno.1994.1591
  4. Boehme, K.W., Singh, J., Perry, S.T., and Compton, T. (2004). Human cytomegalovirus elicits a coordinated cellular antiviral response via envelope glycoprotein B. J. Virol. 78, 1202-1211. https://doi.org/10.1128/JVI.78.3.1202-1211.2004
  5. Broz, P., and Monack, D.M. (2013). Newly described pattern recognition receptors team up against intracellular pathogens. Nat. Rev. Immunol. 13, 551-565. https://doi.org/10.1038/nri3479
  6. Chan, M.C., Chan, R.W., Yu, W.C., Ho, C.C., Chui, W.H., Lo, C.K., Yuen, K.M., Guan, Y.I., Nicholls, J.M., and Peiris, J.S. (2009). Influenza H5N1 virus infection of polarized human alveolar epithelial cells and lung microvascular endothelial cells. Respir. Res. 10, 102. https://doi.org/10.1186/1465-9921-10-102
  7. Chebath, J., Merlin, G., Metz, R., Benech, P., and Revel, M. (1983). Interferon-induced 56,000 Mr protein and its mRNA in human cells: molecular cloning and partial sequence of the cDNA. Nucleic Acids Res. 11, 1213-1226. https://doi.org/10.1093/nar/11.5.1213
  8. Chen, H., Yuan, H., Gao, R., Zhang, J., Wang, D., Xiong, Y., Fan, G., Yang, F., Li, X., and Zhou, J., et al. (2014). Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383, 714-721. https://doi.org/10.1016/S0140-6736(14)60111-2
  9. Cheng, V.C., Chan, J.F., Wen, X., Wu, W.L., Que, T.L., Chen, H., Chan, K.H., and Yuen, K.Y. (2011). Infection of immunocompromised patients by avian H9N2 influenza A virus. J. Infect. 62, 394-399. https://doi.org/10.1016/j.jinf.2011.02.007
  10. Daffis, S., Samuel, M.A., Keller, B.C., Gale, M.J., and Diamond, M.S. (2007). Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. Plos Pathog. 3, e106. https://doi.org/10.1371/journal.ppat.0030106
  11. Davidson, I., Shkoda, I., Golender, N., Perk, S., Lapin, K., Khinich, Y., and Panshin, A. (2013). Genetic characterization of HA gene of low pathogenic H9N2 influenza viruses isolated in Israel during 2006-2012 periods. Vir. Genes 46, 255-263. https://doi.org/10.1007/s11262-012-0852-4
  12. Diamond, M.S., and Farzan, M. (2013). The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 13, 46-57. https://doi.org/10.1038/nri3344
  13. Dirix, V., Verscheure, V., Vermeulen, F., De Schutter, I., Goetghebuer, T., Locht, C., and Mascart, F. (2012). Both CD4(+) and CD8(+) lymphocytes participate in the IFN-gamma response to filamentous hemagglutinin from Bordetella pertussis in infants, children, and adults. Clin. Dev. Immunol. 2012, 795958.
  14. Fensterl, V., and Sen, G.C. (2011). The ISG56/IFIT1 gene family. J. Interferon Cytokine Res. 31, 71-78. https://doi.org/10.1089/jir.2010.0101
  15. Fensterl, V., White, C.L., Yamashita, M., and Sen, G.C. (2008). Novel characteristics of the function and induction of murine p56 family proteins. J. Virol. 82, 11045-11053. https://doi.org/10.1128/JVI.01593-08
  16. Grandvaux, N., Servant, M.J., TenOever, B., Sen, G.C., Balachandran, S., Barber, G.N., Lin, R., and Hiscott, J. (2002). Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 76, 5532-5539. https://doi.org/10.1128/JVI.76.11.5532-5539.2002
  17. Herbert, C., Zeng, Q.X., Shanmugasundaram, R., Garthwaite, L., Oliver, B.G., and Kumar, R.K. (2014). Response of airway epithelial cells to double-stranded RNA in an allergic environment. Transl. Respir. Med. 2, 11. https://doi.org/10.1186/s40247-014-0011-6
  18. Ibricevic, A., Pekosz, A., Walter, M.J., Newby, C., Battaile, J.T., Brown, E.G., Holtzman, M.J., and Brody, S.L. (2006). Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J. Virol. 80, 7469-7480. https://doi.org/10.1128/JVI.02677-05
  19. Jakobsen, M.R., Bak, R.O., Andersen, A., Berg, R.K., Jensen, S.B., Tengchuan, J., Laustsen, A., Hansen, K., Ostergaard, L., and Fitzgerald, K.A., et al. (2013). IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc. Natl. Acad. Sci. USA 110, E4571-E4580. https://doi.org/10.1073/pnas.1311669110
  20. Jonges, M., Liu, W.M., van der Vries, E., Jacobi, R., Pronk, I., Boog, C., Koopmans, M., Meijer, A., and Soethout, E. (2010). Influenza virus inactivation for studies of antigenicity and phenotypic neuraminidase inhibitor resistance profiling. J. Clin. Microbiol. 48, 928-940. https://doi.org/10.1128/JCM.02045-09
  21. Kim, S., Kim, M.J., Park, D.Y., Chung, H.J., Kim, C.H., Yoon, J.H., and Kim, H.J. (2015). Mitochondrial reactive oxygen species modulate innate immune response to influenza A virus in human nasal epithelium. Antiviral Res. 119, 78-83. https://doi.org/10.1016/j.antiviral.2015.04.011
  22. Kohli, A., Zhang, X., Yang, J., Russell, R.S., Donnelly, R.P., Sheikh, F., Sherman, A., Young, H., Imamichi, T., and Lempicki, R.A., et al. (2012). Distinct and overlapping genomic profiles and antiviral effects of Interferon-lambda and -alpha on HCV-infected and noninfected hepatoma cells. J. Viral. Hepat. 19, 843-853. https://doi.org/10.1111/j.1365-2893.2012.01610.x
  23. Lam, E., Stein, S., and Falck-Pedersen, E. (2014). Adenovirus detection by the cGAS/STING/TBK1 DNA sensing cascade. J. Virol. 88, 974-981. https://doi.org/10.1128/JVI.02702-13
  24. Liu, D., Shi, W., Shi, Y., Wang, D., Xiao, H., Li, W., Bi, Y., Wu, Y., Li, X., and Yan, J., et al. (2013). Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses. Lancet 381, 1926-1932. https://doi.org/10.1016/S0140-6736(13)60938-1
  25. Lou, Y.J., Pan, X.R., Jia, P.M., Li, D., Xiao, S., Zhang, Z.L., Chen, S.J., Chen, Z., and Tong, J.H. (2009). IRF-9/STAT2 [corrected] functional interaction drives retinoic acid-induced gene G expression independently of STAT1. Cancer Res. 69, 3673-3680. https://doi.org/10.1158/0008-5472.CAN-08-4922
  26. Metz, P., Dazert, E., Ruggieri, A., Mazur, J., Kaderali, L., Kaul, A., Zeuge, U., Windisch, M.P., Trippler, M., and Lohmann, V., et al. (2012). Identification of type I and type II interferon-induced effectors controlling hepatitis C virus replication. Hepatology 56, 2082-2093. https://doi.org/10.1002/hep.25908
  27. Nicholls, J.M., Bourne, A.J., Chen, H., Guan, Y., and Peiris, J.S. (2007). Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir. Res. 8, 73. https://doi.org/10.1186/1465-9921-8-73
  28. Ogawa, S., Lozach, J., Benner, C., Pascual, G., Tangirala, R.K., Westin, S., Hoffmann, A., Subramaniam, S., David, M., and Rosenfeld, M.G., et al. (2005). Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell 122, 707-721. https://doi.org/10.1016/j.cell.2005.06.029
  29. Parker, C.D., Reid, S.M., Ball, A., Cox, W.J., Essen, S.C., Hanna, A., Mahmood, S., Slomka, M.J., Irvine, R.M., and Brown, I.H. (2012). First reported detection of a low pathogenicity avian influenza virus subtype H9 infection in domestic fowl in England. Vet. Rec. 171, 372. https://doi.org/10.1136/vr.100558
  30. Randall, R.E., and Goodbourn, S. (2008). Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen. Virol. 89, 1-47. https://doi.org/10.1099/vir.0.83391-0
  31. Raychoudhuri, A., Shrivastava, S., Steele, R., Kim, H., Ray, R., and Ray, R.B. (2011). ISG56 and IFITM1 proteins inhibit hepatitis C virus replication. J. Virol. 85, 12881-12889. https://doi.org/10.1128/JVI.05633-11
  32. Reynaud, J.M., Kim, D.Y., Atasheva, S., Rasalouskaya, A., White, J.P., Diamond, M.S., Weaver, S.C., Frolova, E.I., and Frolov, I. (2015). IFIT1 differentially interferes with translation and replication of alphavirus genomes and promotes induction of type I interferon. Plos Pathog. 11, e1004863. https://doi.org/10.1371/journal.ppat.1004863
  33. Sarkar, S.N., and Sen, G.C. (2004). Novel functions of proteins encoded by viral stress-inducible genes. Pharmacol. Ther. 103, 245-259. https://doi.org/10.1016/j.pharmthera.2004.07.007
  34. Schmolke, M., Viemann, D., Roth, J., and Ludwig, S. (2009). Essential impact of NF-kappaB signaling on the H5N1 influenza A virusinduced transcriptome. J. Immunol. 183, 5180-5189. https://doi.org/10.4049/jimmunol.0804198
  35. Shi, S.H., Yang, W.T., Yang, G.L., Cong, Y.L., Huang, H.B., Wang, Q., Cai, R.P., Ye, L.P., Hu, J.T., and Zhou, J.Y., et al. (2014). Immunoprotection against influenza virus H9N2 by the oral administration of recombinant Lactobacillus plantarumNC8 expressing hemagglutinin in BALB/c mice. Virology 464-465, 166-176. https://doi.org/10.1016/j.virol.2014.07.011
  36. Siednienko, J., Maratha, A., Yang, S., Mitkiewicz, M., Miggin, S.M., and Moynagh, P.N. (2011). Nuclear factor kappaB subunits RelB and cRel negatively regulate Toll-like receptor 3-mediated beta-interferon production via induction of transcriptional repressor protein YY1. J. Biol. Chem. 286, 44750-44763. https://doi.org/10.1074/jbc.M111.250894
  37. Teijaro, J.R., Walsh, K.B., Cahalan, S., Fremgen, D.M., Roberts, E., Scott, F., Martinborough, E., Peach, R., Oldstone, M.B., and Rosen, H. (2011). Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 146, 980-991. https://doi.org/10.1016/j.cell.2011.08.015
  38. Terenzi, F., Hui, D.J., Merrick, W.C., and Sen, G.C. (2006). Distinct induction patterns and functions of two closely related interferon-inducible human genes, ISG54 and ISG56. J. Biol. Chem. 281, 34064-34071. https://doi.org/10.1074/jbc.M605771200
  39. Terenzi, F., White, C., Pal, S., Williams, B.R., and Sen, G.C. (2007). Tissue-specific and inducer-specific differential induction of ISG56 and ISG54 in mice. J. Virol. 81, 8656-8665. https://doi.org/10.1128/JVI.00322-07
  40. Tobita, K., Sugiura, A., Enomote, C., and Furuyama, M. (1975). Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med. Microbiol. Immunol. 162, 9-14. https://doi.org/10.1007/BF02123572
  41. Tombari, W., Paul, M., Bettaieb, J., Larbi, I., Nsiri, J., Elbehi, I., Gribaa, L., and Ghram, A. (2013). Risk factors and characteristics of low pathogenic avian influenza virus isolated from commercial poultry in Tunisia. Plos One 8, e53524. https://doi.org/10.1371/journal.pone.0053524
  42. van Riel, D., Munster, V.J., de Wit, E., Rimmelzwaan, G.F., Fouchier, R.A., Osterhaus, A.D., and Kuiken, T. (2006). H5N1 virus attachment to lower respiratory tract. Science 312, 399. https://doi.org/10.1126/science.1125548
  43. van Riel, D., Munster, V.J., de Wit, E., Rimmelzwaan, G.F., Fouchier, R.A., Osterhaus, A.D., and Kuiken, T. (2007). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am. J. Pathol. 171, 1215-1223. https://doi.org/10.2353/ajpath.2007.070248
  44. van Riel, D., den Bakker, M.A., Leijten, L.M., Chutinimitkul, S., Munster, V.J., de Wit, E., Rimmelzwaan, G.F., Fouchier, R.A., Osterhaus, A.D., and Kuiken, T. (2010). Seasonal and pandemic human influenza viruses attach better to human upper respiratory tract epithelium than avian influenza viruses. Am. J. Pathol. 176, 1614-1618. https://doi.org/10.2353/ajpath.2010.090949
  45. Viemann, D., Schmolke, M., Lueken, A., Boergeling, Y., Friesenhagen, J., Wittkowski, H., Ludwig, S., and Roth, J. (2011). H5N1 virus activates signaling pathways in human endothelial cells resulting in a specific imbalanced inflammatory response. J. Immunol. 186, 164-173. https://doi.org/10.4049/jimmunol.0904170
  46. von Recum-Knepper, J., Sadewasser, A., Weinheimer, V.K., and Wolff, T. (2015). Fluorescence-activated cell sorting-based analysis reveals an asymmetric induction of interferon-stimulated genes in response to seasonal influenza A virus. J. Virol. 89, 6982-6993. https://doi.org/10.1128/JVI.00857-15
  47. Wacher, C., Muller, M., Hofer, M.J., Getts, D.R., Zabaras, R., Ousman, S.S., Terenzi, F., Sen, G.C., King, N.J., and Campbell, I.L. (2007). Coordinated regulation and widespread cellular expression of interferon-stimulated genes (ISG) ISG-49, ISG-54, and ISG-56 in the central nervous system after infection with distinct viruses. J. Virol. 81, 860-871. https://doi.org/10.1128/JVI.01167-06
  48. Wang, W., Mu, X., Zhao, L., Wang, J., Chu, Y., Feng, X., Feng, B., Wang, X., Zhang, J., and Qiao, J. (2015). Transcriptional response of human umbilical vein endothelial cell to H9N2 influenza virus infection. Virology 482, 117-127. https://doi.org/10.1016/j.virol.2015.03.037
  49. Weibel, E.R., and Knight, B.W. (1964). A morphometric study on the thickness of the pulmonary air-blood barrier. J. Cell Biol. 21, 367-396. https://doi.org/10.1083/jcb.21.3.367
  50. Xing, Z., Harper, R., Anunciacion, J., Yang, Z., Gao, W., Qu, B., Guan, Y., and Cardona, C.J. (2011). Host immune and apoptotic responses to avian influenza virus H9N2 in human tracheobronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 44, 24-33. https://doi.org/10.1165/rcmb.2009-0120OC
  51. Yao, L., Korteweg, C., Hsueh, W., and Gu, J. (2008). Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB J. 22, 733-740. https://doi.org/10.1096/fj.06-7880com
  52. Yu, H., Zhou, Y.J., Li, G.X., Ma, J.H., Yan, L.P., Wang, B., Yang, F.R., Huang, M., and Tong, G.Z. (2011). Genetic diversity of H9N2 influenza viruses from pigs in China: a potential threat to human health? Vet. Microbiol. 149, 254-261. https://doi.org/10.1016/j.vetmic.2010.11.008
  53. Zeng, H., Pappas, C., Belser, J.A., Houser, K.V., Zhong, W., Wadford, D.A., Stevens, T., Balczon, R., Katz, J.M., and Tumpey, T.M. (2012). Human pulmonary microvascular endothelial cells support productive replication of highly pathogenic avian influenza viruses: possible involvement in the pathogenesis of human H5N1 virus infection. J. Virol. 86, 667-678. https://doi.org/10.1128/JVI.06348-11
  54. Zeng, H., Belser, J.A., Goldsmith, C.S., Gustin, K.M., Veguilla, V., Katz, J.M., and Tumpey, T.M. (2015). A(H7N9) virus results in early induction of proinflammatory cytokine responses in both human lung epithelial and endothelial cells and shows increased human adaptation compared with avian H5N1 virus. J. Virol. 89, 4655-4667. https://doi.org/10.1128/JVI.03095-14
  55. Zhang, K., Xu, W., Zhang, Z., Wang, T., Sang, X., Cheng, K., Yu, Z., Zheng, X., Wang, H., and Zhao, Y., et al. (2013). Experimental infection of non-human primates with avian influenza virus (H9N2). Arch. Virol. 158, 2127-2134. https://doi.org/10.1007/s00705-013-1721-8
  56. Zhang, K., Zhang, Z., Yu, Z., Li, L., Cheng, K., Wang, T., Huang, G., Yang, S., Zhao, Y., and Feng, N., et al. (2013). Domestic cats and dogs are susceptible to H9N2 avian influenza virus. Virus Res. 175, 52-57. https://doi.org/10.1016/j.virusres.2013.04.004
  57. Zhou, Q., and Amar, S. (2007). Identification of signaling pathways in macrophage exposed to Porphyromonas gingivalis or to its purified cell wall components. J. Immunol. 179, 7777-7790. https://doi.org/10.4049/jimmunol.179.11.7777

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