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Avian reovirus triggers autophagy in primary chicken fibroblast cells and Vero cells to promote virus production

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Abstract

Avian reovirus (ARV) is an important cause of disease in poultry. Although ARV is known to induce apoptosis in infected cells, the interaction between ARV and its target cells requires further elucidation. In this report, we show that the ARV isolate strain GX/2010/1 induces autophagy in both Vero and primary chicken embryonic fibroblast (CEF) cells based on the appearance of an increased number of double-membrane vesicles, the presence of GFP-microtubule-associated protein 1 light chain 3 (GFP-LC3) dot formation, and the elevated production of LC3II. We further demonstrate that the class I phosphoinositide 3-kinase (PI3K)/Akt/mTOR pathway contributes to autophagic induction by ARV infection. Moreover, treatment of ARV-infected cells with the autophagy inducer rapamycin increased viral yields, while inhibition of the autophagosomal pathway using chloroquine led to a decrease in virus production. Altogether, our studies strongly suggest that autophagy may play a critical role in determining viral yield during ARV infection.

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References

  1. Mertens PA (2004) The concept of dominance and the treatment of aggression in multidog homes: a comment on van Kerkhove’s commentary. J Appl Anim Welf Sci 7(4):287–291 (discussion 299–300)

    Google Scholar 

  2. Olland AM, Jane-Valbuena J, Schiff LA, Nibert ML, Harrison SC (2001) Structure of the reovirus outer capsid and dsRNA-binding protein sigma3 at 1.8 A resolution. EMBO J 20(5):979–989

    Article  PubMed  CAS  Google Scholar 

  3. Roessler DE, Rosenberger JK (1989) In vitro and in vivo characterization of avian reoviruses. III. Host factors affecting virulence and persistence. Avian Dis 33(3):555–565

    Article  PubMed  CAS  Google Scholar 

  4. Codogno P, Meijer AJ (2006) Atg5: more than an autophagy factor. Nat Cell Biol 8(10):1045–1047

    Article  PubMed  CAS  Google Scholar 

  5. Petiot A, Pattingre S, Arico S, Meley D, Codogno P (2002) Diversity of signaling controls of macroautophagy in mammalian cells. Cell Struct Funct 27(6):431–441

    Article  PubMed  Google Scholar 

  6. Dreux M, Gastaminza P, Wieland SF, Chisari FV (2009) The autophagy machinery is required to initiate hepatitis C virus replication. Proc Natl Acad Sci USA 106(33):14046–14051

    Article  PubMed  CAS  Google Scholar 

  7. O’Donnell V, Pacheco JM, LaRocco M, Burrage T, Jackson W, Rodriguez LL, Borca MV, Baxt B (2011) Foot-and-mouth disease virus utilizes an autophagic pathway during viral replication. Virology 410(1):142–150

    Article  PubMed  Google Scholar 

  8. Bian J, Wang K, Kong X, Liu H, Chen F, Hu M, Zhang X, Jiao X, Ge B, Wu Y, Meng S (2011) Caspase- and p38-MAPK-dependent induction of apoptosis in A549 lung cancer cells by Newcastle disease virus. Arch Virol 156(8):1335–1344

    Article  PubMed  CAS  Google Scholar 

  9. Pandha HS, Heinemann L, Simpson GR, Melcher A, Prestwich R, Errington F, Coffey M, Harrington KJ, Morgan R (2009) Synergistic effects of oncolytic reovirus and cisplatin chemotherapy in murine malignant melanoma. Clin Cancer Res 15(19):6158–6166

    Article  PubMed  CAS  Google Scholar 

  10. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25(3):1025–1040

    Article  PubMed  CAS  Google Scholar 

  11. Zaidi AU, McDonough JS, Klocke BJ, Latham CB, Korsmeyer SJ, Flavell RA, Schmidt RE, Roth KA (2001) Chloroquine-induced neuronal cell death is p53 and Bcl-2 family-dependent but caspase-independent. J Neuropathol Exp Neurol 60(10):937–945

    PubMed  CAS  Google Scholar 

  12. Geng Y, Kohli L, Klocke BJ, Roth KA (2010) Chloroquine-induced autophagic vacuole accumulation and cell death in glioma cells is p53 independent. Neuro Oncol 12(5):473–481

    PubMed  CAS  Google Scholar 

  13. Lin LT, Dawson PW, Richardson CD (2010) Viral interactions with macroautophagy: a double-edged sword. Virology 402(1):1–10

    Article  PubMed  CAS  Google Scholar 

  14. Dreux M, Chisari FV (2010) Viruses and the autophagy machinery. Cell Cycle 9(7):1295–1307

    Article  PubMed  CAS  Google Scholar 

  15. Berkova Z, Crawford SE, Trugnan G, Yoshimori T, Morris AP, Estes MK (2006) Rotavirus NSP4 induces a novel vesicular compartment regulated by calcium and associated with viroplasms. J Virol 80(12):6061–6071

    Article  PubMed  CAS  Google Scholar 

  16. Labrada L, Bodelon G, Vinuela J, Benavente J (2002) Avian reoviruses cause apoptosis in cultured cells: viral uncoating, but not viral gene expression, is required for apoptosis induction. J Virol 76(16):7932–7941

    Article  PubMed  CAS  Google Scholar 

  17. Shih WL, Hsu HW, Liao MH, Lee LH, Liu HJ (2004) Avian reovirus sigmaC protein induces apoptosis in cultured cells. Virology 321(1):65–74

    Article  PubMed  CAS  Google Scholar 

  18. Lin PY, Lee JW, Liao MH, Hsu HY, Chiu SJ, Liu HJ, Shih WL (2009) Modulation of p53 by mitogen-activated protein kinase pathways and protein kinase C delta during avian reovirus S1133-induced apoptosis. Virology 385(2):323–334

    Article  PubMed  CAS  Google Scholar 

  19. Kudchodkar SB, Levine B (2009) Viruses and autophagy. Rev Med Virol 19(6):359–378

    Article  PubMed  CAS  Google Scholar 

  20. Lin PY, Liu HJ, Liao MH, Chang CD, Chang CI, Cheng HL, Lee JW, Shih WL (2010) Activation of PI 3-kinase/Akt/NF-kappaB and Stat3 signaling by avian reovirus S1133 in the early stages of infection results in an inflammatory response and delayed apoptosis. Virology 400(1):104–114

    Article  PubMed  CAS  Google Scholar 

  21. Yeh CJ, Lin PY, Liao MH, Liu HJ, Lee JW, Chiu SJ, Hsu HY, Shih WL (2008) TNF-alpha mediates pseudorabies virus-induced apoptosis via the activation of p38 MAPK and JNK/SAPK signaling. Virology 381(1):55–66

    Article  PubMed  CAS  Google Scholar 

  22. Sir D, Ou JH (2010) Autophagy in viral replication and pathogenesis. Mol Cells 29(1):1–7

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the State Key Laboratory of Veterinary Biotechnology of China (SKLVBF201109), the China Agriculture Research System (CARS-41-K08), and the Program for Changjiang Scholars and Innovative Research Teams in University (IRT0978).

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None declared.

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Correspondence to Songshu Meng or Yantao Wu.

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S. Meng and K. Jiang contributed equally to this work.

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Meng, S., Jiang, K., Zhang, X. et al. Avian reovirus triggers autophagy in primary chicken fibroblast cells and Vero cells to promote virus production. Arch Virol 157, 661–668 (2012). https://doi.org/10.1007/s00705-012-1226-x

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  • DOI: https://doi.org/10.1007/s00705-012-1226-x

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