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Enterovirus 71 transmission by exosomes establishes a productive infection in human neuroblastoma cells

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Abstract

Exosomes are small secreted cellular vesicles for intercellular communications which contain proteins, mRNAs, and microRNAs (miRNAs). Recent studies have shown that exosomes play an important role in the transmission of infectious agents including hepatitis C virus, human immunodeficiency virus, and so on. However, the role of exosomes in the transfer of enterovirus 71 (EV71) between host cells remains unknown. In this study, we show that the exosomes derived from EV71-infected rhabdomyosarcoma cells contain EV71 RNA and capsid protein VP1, determined by quantitative reverse transcription-PCR (QRT-PCR) and Western blot analysis. The shedding of exosomes containing virus can establish a productive infection in human neuroblastoma cell line (SK-N-SH). A comparative analysis of neutralization by EV71-specific immunoglobulins showed different levels of neutralization of exosomes-mediated infection compared with free virus. In conclusion, exosomes from EV71-infected cells may play an important role in virus dissemination and are partially resisted to antibody neutralization. Our results suggest that there is an exosomal route of EV71 transmission infection.

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References

  1. C. Thery, L. Zitvogel, S. Amigorena, Nat. Rev. Immunol. 2, 569–579 (2002)

    CAS  PubMed  Google Scholar 

  2. J.S. Schorey, S. Bhatnagar, Traffic 9, 871–881 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. B.T. Pan, K. Teng, C. Wu, M. Adam, R.M. Johnstone, J. Cell Biol. 101, 942–948 (1985)

    Article  CAS  PubMed  Google Scholar 

  4. R.L. Williams, S. Urbe, Nat. Rev. Mol. Cell Biol. 8, 355–368 (2007)

    Article  CAS  PubMed  Google Scholar 

  5. R.J. Simpson, S.S. Jensen, J.W.E. Lim, J.W. Lim, Proteomics 8, 4083–4099 (2008)

    Article  CAS  PubMed  Google Scholar 

  6. S.E.L. Andaloussi, I. Mager, X.O. Breakefield, M.J. Wood, Nat. Rev. Drug. Discov. 12, 347–357 (2013)

    Article  Google Scholar 

  7. M. Simons, G. Raposo, Curr. Opin. Cell Biol. 21, 575–581 (2009)

    Article  CAS  PubMed  Google Scholar 

  8. S. Mathivanan, C.J. Fahner, G.E. Reid, R.J. Simpson, Nucleic Acids Res. 40, D1241–1244 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. R. Sullivan, F. Saez, J. Girouard, G. Frenette, Blood Cells Mol. Dis. 35, 1–10 (2005)

    Article  CAS  PubMed  Google Scholar 

  10. B. Fevrier, D. Vilette, F. Archer, D. Loew, W. Faigle, M. Vidal, H. Laude, G. Raposo, Proc. Natl. Acad. Sci. USA 29, 9683–9688 (2004)

    Article  Google Scholar 

  11. R. Valenti, V. Huber, P. Filipazzi, L. Pilla, G. Sovena, A. Villa, A. Corbelli, S. Fais, G. Parmiani, L. Rivoltini, Cancer Res. 66, 9290–9298 (2006)

    Article  CAS  PubMed  Google Scholar 

  12. J.E. Park, H.S. Tan, A. Datta, R.C. Lai, H. Zhang, W. Meng, S.K. Lim, S.K. Sze, Mol. Cell. Proteomics 9, 1085–1099 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. A. Janowska-Wieczorek, M. Wysoczynski, J. Kijowski, L. Marquez-Curtis, B. Machalinski, J. Ratajczak, M.Z. Ratajczak, Int. J. Cancer 113, 752–760 (2005)

    Article  CAS  PubMed  Google Scholar 

  14. G. Camussi, M.C. Deregibus, S. Bruno, V. Cantaluppi, L. Biancone, Kidney Int. 78, 838–848 (2010)

    Article  CAS  PubMed  Google Scholar 

  15. M.A. Antonyak, B. Li, L.K. Boroughs, J.L. Johnson, J.E. Druso, K.L. Bryant, D.A. Holowka, R.A. Cerione, Proc. Natl. Acad. Sci. U.S.A. 108, 4852–4857 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. L.J. Costa, N. Chen, A. Lopes, R.S. Aguiar, A. Tanuri, A. Plemenitas, B.M. Peterlin, Retrovirology 3, 33 (2006)

    Article  PubMed  PubMed Central  Google Scholar 

  17. M. Lenassi, G. Cagney, M. Liao, T. Vaupotic, K. Bartholomeeusen, Y. Cheng, N.J. Krogan, A. Plemenitas, B.M. Peterlin, Traffic 11, 110–122 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. R. Madrid, K. Janvier, D. Hitchin, J. Day, S. Coleman, C. Noviello, J. Bouchet, A. Benmerah, J. Guatelli, S. Benichou, J. Biol. Chem. 280, 5032–5044 (2005)

    Article  CAS  PubMed  Google Scholar 

  19. J. Klibi, T. Niki, A. Riedel, C. Pioche-Durieu, S. Souquere, E. Rubinstein, S. Le Moulec, J. Guigay, M. Hirashima, F. Guemira, D. Adhikary, J. Mautner, P. Busson, Blood 113, 957–1966 (2009)

    Article  Google Scholar 

  20. F.J. Verweij, M.A. van Eijndhoven, E.S. Hopmans, T. Vendrig, T. Wurdinger, E. Cahir-McFarland, E. Kieff, D. Geerts, R. van der Kant, J. Neefjes, J.M. Middeldorp, D.M. Pegtel, EMBO J. 30, 2115–2129 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. D.G. Meckes Jr, Kh Shair, A.R. Marquitz, C.-P. Kung, R.H. Edwards, N. Raab-Traub, Proc. Natl. Acad. Sci. US A 23, 20370–20375 (2010)

    Article  Google Scholar 

  22. F.L. Cosset, M. Dreux, J. Hepatol. 60, 674–675 (2014)

    Article  PubMed  Google Scholar 

  23. F. Masciopinto, C. Giovani, S. Campagnoli, L. Galli-Stampino, P. Colombatto, M. Brunetto, T.S.B. Yen, M. Houghton, P. Pileri, S. Abrignani, Eur. J. Immunol. 34, 2834–2842 (2004)

    Article  CAS  PubMed  Google Scholar 

  24. V. Ramakrishnaiah, C. Thumann, I. Fofana, F. Habersetzer, Q. Pan, P.E. de Ruiter, R. Willemsen, J.A.A. Demmers, V. Stalin Raj, G. Jenster, J. Kwekkeboom, H.W. Tilanus, B.L. Haagmans, T.F. Baumert, L.J.W. van der Laan, L.J. van der Laan, Proc. Natl. Acad. Sci. USA 110, 13109–13113 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. S.M. Robinson, G. Tsueng, J. Sin, V. Mangale, S. Rahawi, L.L. McIntyre, W. Williams, N. Kha, C. Cruz, B.M. Hancock, D.P. Nguyen, M.R. Sayen, B.J. Hilton, K.S. Doran, A.M. Segall, R. Wolkowicz, C.T. Cornell, J.L. Whitton, R.A. Gottlieb, R. Feuer, PLoS Pathog. 10, e1004045 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  26. Nj Schmidt, E.H. Lennette, H.H. Ho, J. Infect. Dis. 129, 304–309 (1974)

    Article  CAS  PubMed  Google Scholar 

  27. J.M. Bible, P. Pantelidis, P.K.S. Chan, C.Y.W. Tong, C.Y. Tong, Rev. Med. Virol. 17, 371–379 (2007)

    Article  CAS  PubMed  Google Scholar 

  28. P.C. McMinn, FEMS Microbiol. Rev. 26, 91–107 (2002)

    Article  CAS  PubMed  Google Scholar 

  29. L.-X. Mao, Chin J Clin Lab Sci 28, 327–329 (2010)

    CAS  Google Scholar 

  30. I. Wada, D. Rindress, P.H. Cameron, W.J. Ou, J.J. Doherty 2nd, D. Louvard, A.W. Bell, D. Dignard, D.Y. Thomas, J.J. Bergeron, J. Biol. Chem. 266, 19599–19610 (1991)

    CAS  PubMed  Google Scholar 

  31. P. Gastaminza, K.A. Dryden, B. Boyd, M.R. Wood, M. Law, M. Yeager, F.V. Chisari, J. Virol. 84, 10999–11009 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by Health Science and Technology Support Program of Zhenjiang (Grant No. SHW2015014), Jiangsu Province “333” Project.

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Correspondence to Lingxiang Mao or Huaxi Xu.

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The authors declare no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Edited by Paul Schnitzler.

Lingxiang Mao and Jing Wu contributed equally to this work.

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Mao, L., Wu, J., Shen, L. et al. Enterovirus 71 transmission by exosomes establishes a productive infection in human neuroblastoma cells. Virus Genes 52, 189–194 (2016). https://doi.org/10.1007/s11262-016-1292-3

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