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Mitochondrion-mediated apoptosis induced by Rana grylio virus infection in fish cells

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Abstract

A fish cell line, fathead minnow (FHM) cell, was used to investigate the alteration of mitochondrial dynamics and the mechanism of apoptosis under Rana grylio virus (RGV) infection. Microscopy observations, flow-cytometry analysis and molecular marker detection revealed the apoptotic fate of the RGV-infected cells. Some typical apoptotic characteristics, such as chromatin condensation, DNA fragmentation and mitochondrial fragmentation, were observed, and significantly morphological changes of mitochondria, including size, shape, internal structure and distribution, were revealed. The mitochondria in RGV-infected cells were aggregated around the viromatrix, and the aggregation could be blocked by colchicine. Moreover, the Δψm collapse was induced, and caspase-9 and caspase-3 were activated in the RGV-infected cells. In addition, NF-κB activation and intracellular Ca2+ increase were also detected at different times after infection. The data revealed the detailed dynamics of mitochondrion-mediated apoptosis induced by an iridovirus, and provided the first report on mitochondrial fragmentation during virus-induced apoptosis in fish cells.

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References

  1. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776

    Article  PubMed  CAS  Google Scholar 

  2. Youle RJ, Karbowski M (2005) Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6:657–663

    Article  PubMed  CAS  Google Scholar 

  3. Perfettini JL, Roumier T, Kroemer G (2005) Mitochondrial fusion and fission in the control of apoptosis. Trends Cell Biol 15:179–183

    Article  PubMed  CAS  Google Scholar 

  4. Alirol E, Martinou JC (2006) Mitochondria and cancer: is there a morphological connection? Oncogene 25:4706–4716

    Article  PubMed  CAS  Google Scholar 

  5. Karbowski M, Youle RJ (2003) Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 10:870–880

    Article  PubMed  CAS  Google Scholar 

  6. Cereghetti GM, Scorrano L (2006) The many shapes of mitochondrial death. Oncogene 25:4717–4724

    Article  PubMed  CAS  Google Scholar 

  7. Delivani P, Adrain C, Taylor RC, Duriez PJ, Martin SJ (2006) Role for CED-9 and Egl-1 as regulators of mitochondrial fission and fusion dynamics. Mol Cell 21:761–773

    Article  PubMed  CAS  Google Scholar 

  8. Hay S, Kannourakis G (2002) A time to kill: viral manipulation of the cell death program. J Gen Virol 83:1547–1564

    PubMed  CAS  Google Scholar 

  9. O’Brien V (1998) Viruses and apoptosis. J Gen Virol 79:1833–1845

    PubMed  CAS  Google Scholar 

  10. Koyama AH, Fukumori T, Fujita M, Irie H, Adachi A (2000) Physiological significance of apoptosis in animal virus infection. Microbes Infect 2:1111–1117

    Article  PubMed  CAS  Google Scholar 

  11. Mi J, Li ZY, Ni S, Steinwaerder D, Lieber A (2001) Induced apoptosis supports spread of adenovirus vectors in tumors. Hum Gene Ther 12:1343–1352

    Article  PubMed  CAS  Google Scholar 

  12. Elankumaran S, Rockemann D, Samal SK (2006) Newcastle disease virus exerts oncolysis by both intrinsic and extrinsic caspase-dependent pathways of cell death. J Virol 80:7522–7534

    Article  PubMed  CAS  Google Scholar 

  13. Natoni A, Kass GEN, Carter MJ, Roberts LO (2006) The mitochondrial pathway of apoptosis is triggered during feline calicivirus infection. J Gen Virol 87:357–361

    Article  PubMed  CAS  Google Scholar 

  14. Chinchar VG, Bryan L, Wang J, Long S, Chinchar GD (2003) Induction of apoptosis in frog virus 3-infected cells. Virology 288:351–357

    Article  Google Scholar 

  15. Du C, Zhang Q, Li C, Miao D, Gui J (2004) Induction of apoptosis in a carp leucocyte cell line infected with turbot (Scophthalmus maximus L.) rhabdovirus. Virus Res 101:119–126

    Article  PubMed  CAS  Google Scholar 

  16. Santi N, Sandtro A, Sindre H et al (2005) Infectious pancreatic necrosis virus induces apoptosis in vitro and in vivo independent of VP5 expression. Virology 342:13–25

    Article  PubMed  CAS  Google Scholar 

  17. Zhang QY, Xiao F, Li ZQ, Gui JF, Mao J, Chinchar VG (2001) Characterization of an iridovirus from the cultured pig frog Rana grylio with lethal syndrome. Dis Aquat Organ 48:27–36

    CAS  Google Scholar 

  18. Huang XH, Huang YH, Zhang QY (2006) Electron microscopic examination of the viromatrix of Rana grylio virus in a fish cell line. J Virol Methods 133:117–123

    Article  PubMed  CAS  Google Scholar 

  19. Zhang QY, Li ZQ, Jiang YL, Liang SC, Gui JF (1996) Preliminary studies on virus isolation and cell infection from disease frogs Rana grylio. Acta Hydrobiol Sin 20:390–392 (in Chinese with English abstract)

    Google Scholar 

  20. Du C, Zhang Q, Li C, Miao D, Gui J (2004) Induction of apoptosis in a carp leucocyte cell line infected with turbot (Scophthalmus maximus L.) rhabdovirus. Virus Res 101:119–126

    Article  PubMed  CAS  Google Scholar 

  21. Johnson LV, Wslsh ML, Bockus BJ, Chen LB (1981) Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J Cell Biol 88:526–535

    Article  PubMed  CAS  Google Scholar 

  22. Essbauer S, Ahne W (2002) The epizootic haematopoietic necrosis virus (Iridoviridae) induces apoptosis in vitro. J Vet Med B Infect Dis Vet Public Health 49:25–30

    PubMed  CAS  Google Scholar 

  23. Hu GB, Cong RS, Fan TJ, Mei XG (2004) Induction of apoptosis in a flounder gill cell line by lymphocystis disease virus infection. J Fish Dis 27:657–662

    Article  PubMed  Google Scholar 

  24. Imajoh M, Sugiura H, Oshima S (2004) Morphological changes contribute to apoptotic cell death and are affected by caspase-3 and caspase-6 inhibitors during red sea bream iridovirus permissive replication. Virology 322:220–230

    Article  PubMed  CAS  Google Scholar 

  25. Martinou JC, Youle RJ (2006) Which came first, the cytochrome c release or the mitochondrial fission? Cell Death Differ 13:1291–1295

    Article  PubMed  CAS  Google Scholar 

  26. Murata T, Goshima F, Daikoku T, Inagaki-Ohara K, Takakuwa H, Nishiyamak Y (2000) Mitochondrial distribution and function in herpes simplex virus-infected cells. J Gen Virol 81:401–406

    PubMed  CAS  Google Scholar 

  27. Haga N, Fujita N, Tsuruo T (2003) Mitochondrial aggregation precedes cytochrome c release from mitochondria during apoptosis. Oncogene 22:5579–5585

    Article  PubMed  CAS  Google Scholar 

  28. Rojo G, Chamorro M, Salas ML, Vinuela E, Cuezva JM, Salas J (1998) Migration of mitochondria to viral assembly sites in African swine fever virus-infected cells. J Virol 72:7583–7588

    PubMed  CAS  Google Scholar 

  29. McCormick AL, Smith VL, Chow D, Mocarski ES (2003) Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J Virol 77:631–641

    Article  PubMed  CAS  Google Scholar 

  30. Desagher S, Martinou JC (2000) Mitochondrial as the central control point of apoptosis. Trends Cell Biol 10:369–377

    Article  PubMed  CAS  Google Scholar 

  31. Marchetti P, Hirsch T, Zamzami N et al (1996) Mitochondrial permeability transition triggers lymphocyte apoptosis. J Immunol 157:4830–4836

    PubMed  CAS  Google Scholar 

  32. Skulachev VP (2006) Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11:473–485

    Article  PubMed  CAS  Google Scholar 

  33. Ishihara N, Jofuku A, Eura Y, Mihara K (2003) Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells. Biochem Biophys Res Commun 301:891–898

    Article  PubMed  CAS  Google Scholar 

  34. Dutta J, Fan Y, Gupta N, Fan G, Gelinas C (2006) Current insights into the regulation of programmed cell death by NF-kappaB. Oncogene 25:6800–6816

    Article  PubMed  CAS  Google Scholar 

  35. Karin M, Lin A (2002) NF-κB at the crossroads of life and death. Nat Immunol 3:221–227

    Article  PubMed  CAS  Google Scholar 

  36. Clarke P, Debiasi RL, Meintzer SM, Robinson BA, Tyler KL (2005) Inhibition of NF-kappa B activity and cFLIP expression contribute to viral-induced apoptosis. Apoptosis 10:513–524

    Article  PubMed  CAS  Google Scholar 

  37. Hail N Jr, Konopleva M, Sporn M, Lotan R, Andreeff M (2004) Evidence supporting a role for calcium in apoptosis induction by the synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid (CDDO). J Biol Chem 279:11179–11187

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Grateful thanks for Ms. Zheng-Qiu Li and Xiu-Ping Yuan who provide great help. This study was supported by grants from the National Major Basic Research Program (2004CB117403), the National 863 High Technology Research Foundation of China (2006AA09Z445 and 2006AA100309), the National Natural Science Foundation of China (30671616 and U0631008) and the Project of Chinese Academy of Sciences (KSCX2-YW-N-021).

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Correspondence to Qi-Ya Zhang.

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Huang, YH., Huang, XH., Gui, JF. et al. Mitochondrion-mediated apoptosis induced by Rana grylio virus infection in fish cells. Apoptosis 12, 1569–1577 (2007). https://doi.org/10.1007/s10495-007-0089-1

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