Activation of the intrinsic mitochondrial apoptotic pathway in swine influenza virus-mediated cell death

Choe, Yong-Gi;Kim, Tae-Gyeong;Kim, Cheol-Jung;Lee, Jung-Seop;O, Se-Yeong;Ju, Han-Su;Hong, Gi-Chang;Yu, Seung-Gwon;Kim, Hyeong-Gi
최용기;김태경;김철중;이중섭;오세영;주한수;홍기창;유승권;김형기

  • Published : 20060000

Abstract

The mitochondrial pathway of swine influenza virus (SIV)-induced apoptosis was investigated using porcine kidney (PK-15) cells, swine testicle (ST) cells, and HeLa cervical carcinoma cells which are known not to support viral replication. As judged by cell tation, PK-15 and ST cells infected with three different subtypes of SIV (H1N1, H3N2, and H1N2) were obviously killed by apoptosis, not necrosis. SIV infection in PK-15 and HeLa cells was shown to decrease the cellular levels of Bcl-2 protein com-pared to that of mock-infected control cells at 24 h post-infection, whereas expression levels of Bax protein increased in the PK-15 cells, but did not increase in HeLa cells by SIV infection. Cytochrome c upregulation was also observed in cytosolic frac-tions of the PK-15 and HeLa cells infected with SIV. Apoptosome (a multi-protein complex consisting of cytochrome c, Apaf-1, caspase-9, and ATP) forma-tion was confirmed by immunoprecipitation using cytochrome c antibody. Furthermore, SIV infection increased the cellular levels of TAJ, an activator of the JNK- stressing pathway, and the c-Jun protein in the PK-15 and HeLa cells. Taken together, these results suggest that the mitochondrial pathway should be implicated in the apoptosis of PK-15 cells induced by SIV infection.

Keywords

References

  1. Choi YK, Goyal SM, Joo HS. Prevalence of swine influenza virus subtypes on swine farms in the United States. Arch Virol 2002;147:1209-20 https://doi.org/10.1007/s00705-002-0788-4
  2. Conti L, Rainaldi G, Matarrese P, Varano B, Rivabene R, Columba S, Sato A, Belardelli F, Malorni W, Gessani S. The HIV-1 vpr protein acts as a negative regulator of apoptosis in a human lymphoblastoid T cell line: possible implications for the pathogenesis of AIDS. J Exp Med 1998;187:403-13 https://doi.org/10.1084/jem.187.3.403
  3. Duncan R, Muller J, Lee N, Esmaili A, Nakhasi HL. Rubella virus-induced apoptosis varies among cell lines and is modulated by Bcl-XL and caspase inhibitors. Virology 1999;255:117-28 https://doi.org/10.1006/viro.1998.9562
  4. Eby MT, Jasmin A, Kumar A, Sharma K, Chaudhary PM. TAJ, a novel member of the tumor necrosis factor receptor family, activates the c-Jun N-terminal kinase pathway and mediates caspase-independent cell death. J Biol Chem 2000;275:15336-42 https://doi.org/10.1074/jbc.275.20.15336
  5. Fujimoto I, Takizawa T, Ohba Y, Nakanishi Y. Co-expression of Fas and Fas-ligand on the surface of influenza virus-infected cells. Cell Death Differ 1998;5:426-31 https://doi.org/10.1038/sj.cdd.4400362
  6. Gong X, Wang M, Wu Z, Tashiro S, Onodera S, Ikejima T. Pseudolaric acid B induces apoptosis via activation of c-Jun N-terminal kinase and caspase-3 in HeLa cells. Exp Mol Med 2004;36:551-6 https://doi.org/10.1038/emm.2004.70
  7. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407:770-6 https://doi.org/10.1038/35037710
  8. Hinshaw VS, Olsen CW, Dybdahl-Sissoko N, Evans D. Apoptosis: a mechanism of cell killing by influenza A and B viruses. J Virol 1994;68:3667-73
  9. Hong JR, Wu JL. Induction of apoptotic death in cells via Bad gene expression by infectious pancreatic necrosis virus infection. Cell Death Differ 2002;9:113-24 https://doi.org/10.1038/sj.cdd.4400933
  10. Jacobson MD, Weil M, Raff MC. Programmed cell death in animal development. Cell 1997;88:347-54 https://doi.org/10.1016/S0092-8674(00)81873-5
  11. Kim YS, Jhon DY, Lee KY. Involvement of ROS and JNK1 in selenite-induced apoptosis in Chang liver cells. Exp Mol Med 2004;36:157-64 https://doi.org/10.1038/emm.2004.22
  12. Kumar S. Mechanisms mediating caspase activation in cell death. Cell Death Differ 1999;6:1060-6 https://doi.org/10.1038/sj.cdd.4400600
  13. Lewis J, Oyler GA, Ueno K, Fannjiang YR, Chau BN, Vornov J, Korsmeyer SJ, Zou S, Hardwick JM. Inhibition of virus-induced neuronal apoptosis by Bax. Nat Med 1999;5:832-5 https://doi.org/10.1038/10556
  14. Lin C, Zimmer SG, Lu Z, Holland RE Jr, Dong Q, Chambers TM. The involvement of a stress-activated pathway in equine influenza virus-mediated apoptosis. Virology 2001;287:202-13 https://doi.org/10.1006/viro.2001.1010
  15. Ludwig S, Pleschka S, Wolff T. A fatal relationship--influenza virus interactions with the host cell. Viral Immunol 1999;12: 175-96 https://doi.org/10.1089/vim.1999.12.175
  16. Majno G, Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995;146:3-15
  17. Mastrangelo AJ, Hardwick JM, Bex F, Betenbaugh MJ. Part I. Bcl-2 and Bcl-x (L) limit apoptosis upon infection with alphavirus vectors. Biotechnol Bioeng 2000;67:544-54 https://doi.org/10.1002/(SICI)1097-0290(20000305)67:5<544::AID-BIT5>3.0.CO;2-#
  18. Meguro H, Bryant JD, Torrence AE, Wright PF. Canine kidney cell line for isolation of respiratory viruses. J Clin Microbiol 1979;9:175-9
  19. Mori I, Komatsu T, Takeuchi K, Nakakuki K, Sudo M, Kimura Y. In vivo induction of apoptosis by influenza virus. J Gen Virol 1995;76:2869-73 https://doi.org/10.1099/0022-1317-76-11-2869
  20. Morris SJ, Price GE, Barnett JM, Hiscox SA, Smith H, Sweet C. Role of neuraminidase in influenza virus-induced apoptosis. J Gen Virol 1999;80:137-46 https://doi.org/10.1099/0022-1317-80-1-137
  21. Olsen CW, Kehren JC, Dybdahl-Sissoko NR, Hinshaw VS. bcl-2 alters influenza virus yield, spread, and hemagglutinin glycosylation. J Virol 1996;70:663-6
  22. Rich T, Allen RL, Wyllie AH. Defying death after DNA damage. Nature 2000;407:777-83 https://doi.org/10.1038/35037717
  23. Roulston A, Marcellus RC, Branton PE. Viruses and apoptosis. Annu Rev Microbiol 1999;53:577-628 https://doi.org/10.1146/annurev.micro.53.1.577
  24. Sawai H, Okazaki T, Yamamoto H, Okano H, Takeda Y, Tashima M, Sawada H, Okuma M, Ishikura H, Umehara H, Domae N. Requirement of AP-1 for ceramide-induced apoptosis in human leukemia HL-60 cells. J Biol Chem 1995;270:27326-31 https://doi.org/10.1074/jbc.270.45.27326
  25. Schultz-Cherry S, Dybdahl-Sissoko N, Neumann G, Kawaoka Y, Hinshaw VS. Influenza virus ns1 protein induces apoptosis in cultured cells. J Virol 2001;75:7875-81 https://doi.org/10.1128/JVI.75.17.7875-7881.2001
  26. Takizawa T, Fukuda R, Miyawaki T, Ohashi K, Nakanishi Y. Activation of the apoptotic Fas antigen-encoding gene upon influenza virus infection involving spontaneously produced beta-interferon. Virology 1995;209:288-96 https://doi.org/10.1006/viro.1995.1260
  27. Takizawa T, Tatematsu C, Ohashi K, Nakanishi Y. Recruitment of apoptotic cysteine proteases (caspases) in influenza virus- induced cell death. Microbiol Immunol 1999;43:245-52 https://doi.org/10.1111/j.1348-0421.1999.tb02400.x
  28. Teodoro JG, Branton PE. Regulation of apoptosis by viral gene products. J Virol 1997;71:1739-46
  29. Wada N, Matsumura M, Ohba Y, Kobayashi N, Takizawa T, Nakanishi Y. Transcription stimulation of the Fas-encoding gene by nuclear factor for interleukin-6 expression upon influenza virus infection. J Biol Chem 1995;270:18007-12 https://doi.org/10.1074/jbc.270.30.18007
  30. Young LS, Dawson CW, Eliopoulos AG. Viruses and apoptosis. Br Med Bull 1997;53:509-21 https://doi.org/10.1093/oxfordjournals.bmb.a011627
  31. Zheng TS, Schlosser SF, Dao T, Hingorani R, Crispe IN, Boyer JL, Flavell RA. Caspase-3 controls both cytoplasmic and nuclear events associated with Fas-mediated apoptosis in vivo. Proc Natl Acad Sci USA 1998;95:13618-23 https://doi.org/10.1073/pnas.95.23.13618