1887

Abstract

The phosphatidylinositol-3-kinase (PI3K)/Akt/target of rapamycin (TOR) signalling pathway controls cell growth and survival, and is targeted by a number of viruses at different phases of their infection cycle to control translation. Whether and how insect viruses interact with this pathway remain poorly addressed. Here, we investigated the role of PI3K/Akt/TOR signalling during lethal infection of insect cells with an insect parvovirus. Using densovirus (JcDV; lepidopteran ambidensovirus 1) and susceptible insect cells as experimental models, we first described JcDV cytopathology, and showed that viral infection affects cell size, cell proliferation and survival. We deciphered the role of PI3K/Akt/TOR signalling in the course of infection and found that non-structural (NS) protein expression correlates with the inhibition of TOR and the shutdown of cellular synthesis, concomitant with the burst of viral protein expression. Together, these results suggest that NS proteins control the cellular translational machinery to favour the translation of viral mRNAs at the expense of cellular mRNAs. As a consequence of TOR inhibition, cell autophagy is activated. These results highlight new functions for NS proteins in the course of multiplication of an insect parvovirus.

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2016-01-01
2024-04-26
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References

  1. Abd-Alla A., Jousset F. X., Li Y., Fediere G., Cousserans F., Bergoin M. 2004; NS-3 protein of the Junonia coenia densovirus is essential for viral DNA replication in an Ld 652 cell line and Spodoptera littoralis larvae. J Virol 78:790–797 [CrossRef]
    [Google Scholar]
  2. Adeyemi R. O., Landry S., Davis M. E., Weitzman M. D., Pintel D. J. 2010; Parvovirus minute virus of mice induces a DNA damage response that facilitates viral replication. PLoS Pathog 6:e1001141 [View Article][PubMed]
    [Google Scholar]
  3. Aghdasi B., Ye K., Resnick A., Huang A., Ha H. C., Guo X., Dawson T. M., Dawson V. L., Snyder S. H. 2001; FKBP12, the 12-kDa FK506-binding protein, is a physiologic regulator of the cell cycle. Proc Natl Acad Sci U S A 98:2425–2430 [View Article][PubMed]
    [Google Scholar]
  4. Alessi D. R., Deak M., Casamayor A., Caudwell F. B., Morrice N., Norman D. G., Gaffney P., Reese C. B., MacDougall C. N., other authors. 1997; 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr Biol 7:776–789 [View Article][PubMed]
    [Google Scholar]
  5. Anjum R., Blenis J. 2008; The RSK family of kinases: emerging roles in cellular signalling. Nat Rev Mol Cell Biol 9:747–758 [View Article][PubMed]
    [Google Scholar]
  6. Arsic D., Guerin P. M. 2008; Nutrient content of diet affects the signaling activity of the insulin/target of rapamycin/p70 S6 kinase pathway in the African malaria mosquito Anopheles gambiae . J Insect Physiol 54:1226–1235 [View Article][PubMed]
    [Google Scholar]
  7. Bär S., Rommelaere J., Nüesch J. P. F. 2015; PKCη/Rdx-driven phosphorylation of PDK1: a novel mechanism promoting cancer cell survival and permissiveness for parvovirus-induced lysis. PLoS Pathog 11:e1004703[PubMed] [CrossRef]
    [Google Scholar]
  8. Bergoin M., Tijssen P. 2000; Molecular biology of Densovirinae. Contrib Microbiol 4:12–32 [View Article][PubMed]
    [Google Scholar]
  9. Bergoin M., Tijssen P. 2008; Parvoviruses of arthropods. In Encyclopedia of Virology vol 5 pp 76–85Edited by Mahy B. W. J., Van Regenmortel M. H. V. Oxford: Elsevier; [CrossRef]
    [Google Scholar]
  10. Buchkovich N. J., Yu Y., Zampieri C. A., Alwine J. C. 2008; The TORrid affairs of viruses: effects of mammalian DNA viruses on the PI3K–Akt–mTOR signalling pathway. Nat Rev Microbiol 6:266–275 [View Article][PubMed]
    [Google Scholar]
  11. Chen A. Y., Kleiboeker S., Qiu J. 2011; Productive parvovirus B19 infection of primary human erythroid progenitor cells at hypoxia is regulated by STAT5A and MEK signaling but not HIFα. PLoS Pathog 7:e1002088 [View Article][PubMed]
    [Google Scholar]
  12. Cooray S. 2004; The pivotal role of phosphatidylinositol 3-kinase–Akt signal transduction in virus survival. J Gen Virol 85:1065–1076 [View Article][PubMed]
    [Google Scholar]
  13. Cotmore S. F., Tattersall P. 2013; Parvovirus diversity and DNA damage responses. Cold Spring Harb Perspect Biol 5:a012989 [View Article][PubMed]
    [Google Scholar]
  14. Cotmore S. F., Agbandje-McKenna M., Chiorini J. A., Mukha D. V., Pintel D. J., Qiu J., Soderlund-Venermo M., Tattersall P., Tijssen P., other authors. 2014; The family Parvoviridae . Arch Virol 159:1239–1247 [View Article][PubMed]
    [Google Scholar]
  15. Dhar A. K., Robles-Sikisaka R., Saksmerprome V., Lakshman D. K. 2014; Biology, genome organization, and evolution of parvoviruses in marine shrimp. Adv Virus Res 89:85–139 [View Article][PubMed]
    [Google Scholar]
  16. Dibble C. C., Cantley L. C. 2015; Regulation of mTORC1 by PI3K signaling. Trends Cell Biol 25:545–555 [View Article][PubMed]
    [Google Scholar]
  17. Diehl N., Schaal H. 2013; Make yourself at home: viral hijacking of the PI3K/Akt signaling pathway. Viruses 5:3192–3212 [View Article][PubMed]
    [Google Scholar]
  18. Ding C., Urabe M., Bergoin M., Kotin R. M. 2002; Biochemical characterization of Junonia coenia densovirus nonstructural protein NS-1. J Virol 76:338–345 [View Article][PubMed]
    [Google Scholar]
  19. Dumas B., Jourdan M., Pascaud A. M., Bergoin M. 1992; Complete nucleotide sequence of the cloned infectious genome of Junonia coenia densovirus reveals an organization unique among parvoviruses. Virology 191:202–222 [View Article][PubMed]
    [Google Scholar]
  20. Gai Z., Zhang X., Islam M., Wang X., Li A., Yang Y., Li Y., Peng J., Hong H., Liu K. 2013; Characterization of Atg8 in lepidopteran insect cells. Arch Insect Biochem Physiol 84:57–77[PubMed]
    [Google Scholar]
  21. Garrey J. L., Lee Y.-Y., Au H. H. T., Bushell M., Jan E. 2010; Host and viral translational mechanisms during cricket paralysis virus infection. J Virol 84:1124–1138 [View Article][PubMed]
    [Google Scholar]
  22. Goodwin R. H., Tompkins G. J., McCawley P. 1978; Gypsy moth cell lines divergent in viral susceptibility. I. Culture and identification. In Vitro 14:485–494 [View Article][PubMed]
    [Google Scholar]
  23. Huang R., Xu Y., Wan W., Shou X., Qian J., You Z., Liu B., Chang C., Zhou T., other authors. 2015; Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell 57:456–466 [View Article][PubMed]
    [Google Scholar]
  24. Jan E. 2006; Divergent IRES elements in invertebrates. Virus Res 119:16–28 [View Article][PubMed]
    [Google Scholar]
  25. Katsuma S., Mita K., Shimada T. 2007; ERK- and JNK-dependent signaling pathways contribute to Bombyx mori nucleopolyhedrovirus infection. J Virol 81:13700–13709 [View Article][PubMed]
    [Google Scholar]
  26. Laplante M., Sabatini D. M. 2009; mTOR signaling at a glance. J Cell Sci 122:3589–3594 [View Article][PubMed]
    [Google Scholar]
  27. Li Y., Jousset F. X., Giraud C., Rolling F., Quiot J. M., Bergoin M. 1996; A titration procedure of the Junonia coenia densovirus and quantitation of transfection by its cloned genomic DNA in four lepidopteran cell lines. J Virol Methods 57:47–60 [View Article][PubMed]
    [Google Scholar]
  28. Liu C., Yamamoto K., Cheng T. C., Kadono-Okuda K., Narukawa J., Liu S. P., Han Y., Futahashi R., Kidokoro K., other authors. 2010; Repression of tyrosine hydroxylase is responsible for the sex-linked chocolate mutation of the silkworm, Bombyx mori . Proc Natl Acad Sci U S A 107:12980–12985 [View Article][PubMed]
    [Google Scholar]
  29. Nagata S., Hakuno F., Takahashi S., Nagasawa H. 2008; Identification of Bombyx mori Akt and its phosphorylation by bombyxin stimulation. Comp Biochem Physiol B Biochem Mol Biol 151:355–360 [View Article][PubMed]
    [Google Scholar]
  30. Nakashima N., Uchiumi T. 2009; Functional analysis of structural motifs in dicistroviruses. Virus Res 139:137–147 [View Article][PubMed]
    [Google Scholar]
  31. Reggiori F., Monastyrska I., Verheije M. H., Calì T., Ulasli M., Bianchi S., Bernasconi R., de Haan C. A. M., Molinari M. 2010; Coronaviruses hijack the LC3-I-positive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 7:500–508 [View Article][PubMed]
    [Google Scholar]
  32. Riolobos L., Valle N., Hernando E., Maroto B., Kann M., Almendral J. M. 2010; Viral oncolysis that targets Raf-1 signaling control of nuclear transport. J Virol 84:2090–2099 [View Article][PubMed]
    [Google Scholar]
  33. Robinson S. M., Tsueng G., Sin J., Mangale V., Rahawi S., McIntyre L. L., Williams W., Kha N., Cruz C., other authors. 2014; Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLoS Pathog 10:e1004045 [View Article][PubMed]
    [Google Scholar]
  34. Rolling F. 1992 Vecteurs dérivés du densovirus de Junonia coenia (JcDNV) exprimant sous forme épisomale ou intégrée des gènes étrangers dans des cellules d'insectes episomal or integrated vectors derived from the Junonia coenia densovirus (JcDNV) expressing foreign genes in insect cells PhD thesis, University of Aix-Marseille II, Marseille, France.
    [Google Scholar]
  35. Ryabov E. V., Keane G., Naish N., Evered C., Winstanley D. 2009; Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea . Proc Natl Acad Sci U S A 106:8465–8470 [View Article][PubMed]
    [Google Scholar]
  36. Schneider R. J., Mohr I. 2003; Translation initiation and viral tricks. Trends Biochem Sci 28:130–136 [View Article][PubMed]
    [Google Scholar]
  37. Vendeville A., Ravallec M., Jousset F. X., Devise M., Mutuel D., López-Ferber M., Fournier P., Dupressoir T., Ogliastro M. 2009; Densovirus infectious pathway requires clathrin-mediated endocytosis followed by trafficking to the nucleus. J Virol 83:4678–4689 [View Article][PubMed]
    [Google Scholar]
  38. Wang Y., Abd-Alla A. M., Bossin H., Li Y., Bergoin M. 2013a; Analysis of the transcription strategy of the Junonia coenia densovirus (JcDNV) genome. Virus Res 174:101–107 [View Article][PubMed]
    [Google Scholar]
  39. Wang Y., Gosselin Grenet A. S., Castelli I., Cermenati G., Ravallec M., Fiandra L., Debaisieux S., Multeau C., Lautredou N., other authors. 2013b; Densovirus crosses the insect midgut by transcytosis and disturbs the epithelial barrier function. J Virol 87:12380–12391 [View Article][PubMed]
    [Google Scholar]
  40. Xiao W., Yang Y., Weng Q., Lin T., Yuan M., Yang K., Pang Y. 2009; The role of the PI3K–Akt signal transduction pathway in Autographa californica multiple nucleopolyhedrovirus infection of Spodoptera frugiperda cells. Virology 391:83–89 [View Article][PubMed]
    [Google Scholar]
  41. Xu P., Liu Y., Graham R. I., Wilson K., Wu K. 2014; Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide. PLoS Pathog 10:e1004490 [View Article][PubMed]
    [Google Scholar]
  42. Zhang X., Hu Z. Y., Li W. F., Li Q. R., Deng X. J., Yang W. Y., Cao Y., Zhou C. Z. 2009; Systematic cloning and analysis of autophagy-related genes from the silkworm Bombyx mori . BMC Mol Biol 10:50 [View Article][PubMed]
    [Google Scholar]
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