1887

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Volume 97, Issue 8

The contribution of the cytoplasmic retrieval signal of severe acute respiratory syndrome coronavirus to intracellular accumulation of S proteins and incorporation of S protein into virus-like particles Free

Abstract

The cytoplasmic tails of some coronavirus (CoV) spike (S) proteins contain an endoplasmic reticulum retrieval signal (ERRS) that can retrieve S proteins from the Golgi to the endoplasmic reticulum (ER); this process is thought to accumulate S proteins at the CoV budding site, the ER-Golgi intermediate compartment (ERGIC), and to facilitate S protein incorporation into virions. However, we showed previously that porcine epidemic diarrhoea CoV S proteins lacking the ERRS were efficiently incorporated into virions, similar to the original virus. Thus, the precise role of the ERRS in virus assembly remains unclear. Here, the roles of the S protein ERRS in severe acute respiratory syndrome CoV (SARS-CoV) intracellular trafficking and S incorporation into virus-like particles (VLPs) are described. Intracellular trafficking and indirect immunofluorescence analysis suggested that when M protein was present, wild-type S protein (wtS) could be retained in the pre- and post-medial Golgi compartments intracellularly and co-localized with M protein in the Golgi. In contrast, mutant S protein lacking the ERRS was distributed throughout the ER and only partially co-localized with M protein. Moreover, the intracellular accumulation of mutant S protein, particularly at the post-medial Golgi compartment, was significantly reduced compared with wtS. A VLP assay suggested that wtS that reached the post-medial compartment could be returned to the ERGIC for subsequent incorporation into VLPs, while mutant S protein could not. These results suggest that the ERRS of SARS-CoV contributes to intracellular S protein accumulation specifically in the post-medial Golgi compartment and to S protein incorporation into VLPs.

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Keyword(s): ER retrieval signal , severe acute respiratory syndrome coronavirus , spike protein , trafficking , virus assembly and virus-like particles
© 2016 The Authors
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2016-08-01
2024-04-26
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References

  1. Baudoux P., Carrat C., Besnardeau L., Charley B., Laude H. 1998; Coronavirus pseudoparticles formed with recombinant M and E proteins induce alpha interferon synthesis by leukocytes. J Virol 72:8636–8643[PubMed]
     [Google Scholar]
  2. Bosch B. J., Martina B. E., Van Der Zee R., Lepault J., Haijema B. J., Versluis C., Heck A. J., de Groot R., Osterhaus A. D., Rottier P. J. 2004; Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc Natl Acad Sci U S A 101:8455–8460 [View Article][PubMed]
     [Google Scholar]
  3. Cavanagh D. 1981; Structural polypeptides of coronavirus IBV. J Gen Virol 53:93–103 [View Article][PubMed]
     [Google Scholar]
  4. Corse E., Machamer C. E. 2000; Infectious bronchitis virus E protein is targeted to the Golgi complex and directs release of virus-like particles. J Virol 74:4319–4326[PubMed] [CrossRef]
     [Google Scholar]
  5. Cosson P., Letourneur F. 1994; Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263:1629–1631 [CrossRef]
     [Google Scholar]
  6. de Groot R. J., Baker S. C., Baric R., Enjuanes L., Gorbalenya A. E., Holmes K. V., Perlman S., Poon L., Rottier P. J. M. et al. 2012 Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses: Family Coronaviridae Edited by King A., Adams M., Cartens E., Lefkowitz E. San Diego, CA: Academic Press;
     [Google Scholar]
  7. DeDiego M. L., Alvarez E., Almazán F., Rejas M. T., Lamirande E., Roberts A., Shieh W. J., Zaki S. R., Subbarao K., Enjuanes L. 2007; A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J Virol 81:1701–1713 [View Article][PubMed]
     [Google Scholar]
  8. Drosten C., Günther S., Preiser W., van der Werf S., Brodt H. R., Becker S., Rabenau H., Panning M., Kolesnikova L. et al. 2003; Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348:1967–1976 [View Article][PubMed]
     [Google Scholar]
  9. Fischer F., Stegen C. F., Masters P. S., Samsonoff W. A. 1998; Analysis of constructed E gene mutants of mouse hepatitis virus confirms a pivotal role for E protein in coronavirus assembly. J Virol 72:7885–7894[PubMed]
     [Google Scholar]
  10. Fouchier R. A., Kuiken T., Schutten M., van Amerongen G., van Doornum G. J., van den Hoogen B. G., Peiris M., Lim W., Stöhr K. et al. 2003; Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423:240 [View Article][PubMed]
     [Google Scholar]
  11. Heald-Sargent T., Gallagher T. 2012; Ready, set, fuse! The coronavirus spike protein and acquisition of fusion competence. Viruses 4:557–580 [View Article][PubMed]
     [Google Scholar]
  12. Hogue B. G., Brian D. A. 1986; Structural proteins of human respiratory coronavirus OC43. Virus Res 5:131–144[PubMed] [CrossRef]
     [Google Scholar]
  13. Horton M. R., Pease L. R. 1991; Recombination and mutagenesis of DNA-sequences using PCR. In Directed Mutagenesis: A Practical Approach , pp. 217–247 Edited by McPherson M. J. Oxford: Oxford University Press;
     [Google Scholar]
  14. Hsieh P. K., Chang S. C., Huang C. C., Lee T. T., Hsiao C. W., Kou Y. H., Chen I. Y., Chang C. K., Huang T. H. et al. 2005; Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent. J Virol 79:13848–13855 [View Article][PubMed]
     [Google Scholar]
  15. Huang Y., Yang Z. Y., Kong W. P., Nabel G. J. 2004; Generation of synthetic severe acute respiratory syndrome coronavirus pseudoparticles: implications for assembly and vaccine production. J Virol 78:12557–12565 [View Article][PubMed]
     [Google Scholar]
  16. King B., Brian D. A. 1982; Bovine coronavirus structural proteins. J Virol 42:700–707[PubMed]
     [Google Scholar]
  17. King B., Potts B. J., Brian D. A. 1985; Bovine coronavirus hemagglutinin protein. Virus Res 2:53–59[PubMed] [CrossRef]
     [Google Scholar]
  18. Klumperman J., Locker J. K., Meijer A., Horzinek M. C., Geuze H. J., Rottier P. J. 1994; Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J Virol 68:6523–6534[PubMed]
     [Google Scholar]
  19. Krijnse-Locker J., Ericsson M., Rottier P. J., Griffiths G. 1994; Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J Cell Biol 124:55–70[PubMed] [CrossRef]
     [Google Scholar]
  20. Ksiazek T. G., Erdman D., Goldsmith C. S., Zaki S. R., Peret T., Emery S., Tong S., Urbani C., Comer J. A. et al. 2003; A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953–1966 [View Article][PubMed]
     [Google Scholar]
  21. Kuo L., Masters P. S. 2002; Genetic evidence for a structural interaction between the carboxy termini of the membrane and nucleocapsid proteins of mouse hepatitis virus. J Virol 76:4987–4999[PubMed] [CrossRef]
     [Google Scholar]
  22. Lee M. C., Miller E. A., Goldberg J., Orci L., Schekman R. 2004; Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20:87–123 [View Article][PubMed]
     [Google Scholar]
  23. Li F. 2013; Receptor recognition and cross-species infections of SARS coronavirus. Antiviral Res 100:246–254 [View Article][PubMed]
     [Google Scholar]
  24. Lim K. P., Liu D. X. 2001; The missing link in coronavirus assembly. Retention of the avian coronavirus infectious bronchitis virus envelope protein in the pre-Golgi compartments and physical interaction between the envelope and membrane proteins. J Biol Chem 276:17515–17523 [View Article][PubMed]
     [Google Scholar]
  25. Lissenberg A., Vrolijk M. M., van Vliet A. L., Langereis M. A., de Groot-Mijnes J. D., Rottier P. J., de Groot R. J. 2005; Luxury at a cost? Recombinant mouse hepatitis viruses expressing the accessory hemagglutinin esterase protein display reduced fitness in vitro. J Virol 79:15054–15063 [View Article][PubMed]
     [Google Scholar]
  26. Lontok E., Corse E., Machamer C. E. 2004; Intracellular targeting signals contribute to localization of coronavirus spike proteins near the virus assembly site. J Virol 78:5913–5922 [View Article][PubMed]
     [Google Scholar]
  27. Machamer C. E., Mentone S. A., Rose J. K., Farquhar M. G. 1990; The E1 glycoprotein of an avian coronavirus is targeted to the cis Golgi complex. Proc Natl Acad Sci U S A 87:6944–6948[PubMed] [CrossRef]
     [Google Scholar]
  28. Masters P. S. 2006; The molecular biology of coronaviruses. Adv Virus Res 66:193–292 [View Article][PubMed]
     [Google Scholar]
  29. Matsuyama S., Ujike M., Morikawa S., Tashiro M., Taguchi F. 2005; Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection. Proc Natl Acad Sci U S A 102:12543–12547 [View Article][PubMed]
     [Google Scholar]
  30. McBride C. E., Li J., Machamer C. E. 2007; The cytoplasmic tail of the severe acute respiratory syndrome coronavirus spike protein contains a novel endoplasmic reticulum retrieval signal that binds COPI and promotes interaction with membrane protein. J Virol 81:2418–2428 [View Article][PubMed]
     [Google Scholar]
  31. Narayanan K., Maeda A., Maeda J., Makino S. 2000; Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells. J Virol 74:8127–8134[PubMed] [CrossRef]
     [Google Scholar]
  32. Nguyen V. P., Hogue B. G. 1997; Protein interactions during coronavirus assembly. J Virol 71:9278–9284[PubMed]
     [Google Scholar]
  33. Ohnishi K., Sakaguchi M., Kaji T., Akagawa K., Taniyama T., Kasai M., Tsunetsugu-Yokota Y., Oshima M., Yamamoto K. et al. 2005; Immunological detection of severe acute respiratory syndrome coronavirus by monoclonal antibodies. Jpn J Infect Dis 58:88–94[PubMed]
     [Google Scholar]
  34. Opstelten D. J., Raamsman M. J., Wolfs K., Horzinek M. C., Rottier P. J. 1995; Envelope glycoprotein interactions in coronavirus assembly. J Cell Biol 131:339–349[PubMed] [CrossRef]
     [Google Scholar]
  35. Rota P. A., Oberste M. S., Monroe S. S., Nix W. A., Campagnoli R., Icenogle J. P., Penaranda S., Bankamp B., Maher K. 2003; Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394–1399 [CrossRef]
     [Google Scholar]
  36. Schwegmann-Wessels C., Al-Falah M., Escors D., Wang Z., Zimmer G., Deng H., Enjuanes L., Naim H. Y., Herrler G. 2004; A novel sorting signal for intracellular localization is present in the S protein of a porcine coronavirus but absent from severe acute respiratory syndrome-associated coronavirus. J Biol Chem 279:43661–43666 [View Article][PubMed]
     [Google Scholar]
  37. Shirato K., Maejima M., Matsuyama S., Ujike M., Miyazaki A., Takeyama N., Ikeda H., Taguchi F. 2011; Mutation in the cytoplasmic retrieval signal of porcine epidemic diarrhea virus spike (S) protein is responsible for enhanced fusion activity. Virus Res 161:188–193 [View Article][PubMed]
     [Google Scholar]
  38. Siu Y. L., Teoh K. T., Lo J., Chan C. M., Kien F., Escriou N., Tsao S. W., Nicholls J. M., Altmeyer R. et al. 2008; The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles. J Virol 82:11318–11330 [View Article][PubMed]
     [Google Scholar]
  39. Tooze J., Tooze S., Warren G. 1984; Replication of coronavirus MHV-A59 in sac- cells: determination of the first site of budding of progeny virions. Eur J Cell Biol 33:281–293[PubMed]
     [Google Scholar]
  40. Ujike M., Taguchi F. 2015; Incorporation of spike and membrane glycoproteins into coronavirus virions. Viruses 7:1700–1725 [View Article][PubMed]
     [Google Scholar]
  41. Ujike M., Huang C., Shirato K., Matsuyama S., Makino S., Taguchi F. 2012; Two palmitylated cysteine residues of the severe acute respiratory syndrome coronavirus spike (S) protein are critical for S incorporation into virus-like particles, but not for M-S co-localization. J Gen Virol 93:823–828 [View Article][PubMed]
     [Google Scholar]
  42. Ujike M., Nishikawa H., Otaka A., Yamamoto N., Yamamoto N., Matsuoka M., Kodama E., Fujii N., Taguchi F. 2008; Heptad repeat-derived peptides block protease-mediated direct entry from the cell surface of severe acute respiratory syndrome coronavirus but not entry via the endosomal pathway. J Virol 82:588–592 [View Article][PubMed]
     [Google Scholar]
  43. Vennema H., Godeke G. J., Rossen J. W., Voorhout W. F., Horzinek M. C., Opstelten D. J., Rottier P. J. 1996; Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J 15:2020–2028[PubMed]
     [Google Scholar]
  44. Wege H., Wege H., Nagashima K., ter Meulen V. 1979; Structural polypeptides of the murine coronavirus JHM. J Gen Virol 42:37–47 [View Article][PubMed]
     [Google Scholar]
  45. Winter C., Schwegmann-Wessels C., Neumann U., Herrler G. 2008; The spike protein of infectious bronchitis virus is retained intracellularly by a tyrosine motif. J Virol 82:2765–2771 [View Article][PubMed]
     [Google Scholar]
  46. Woo P. C., Lau S. K., Lam C. S., Lau C. C., Tsang A. K., Lau J. H., Bai R., Teng J. L., Tsang C. C. et al. 2012; Discovery of seven novel mammalian and avian coronaviruses in the genus Deltacoronavirus supports bat coronaviruses as the gene source of Alphacoronavirus and Betacoronavirus and avian coronaviruses as the gene source of Gammacoronavirus and Deltacoronavirus . J Virol 86:3995–4008 [View Article][PubMed]
     [Google Scholar]
  47. Youn S., Collisson E. W., Machamer C. E. 2005; Contribution of trafficking signals in the cytoplasmic tail of the infectious bronchitis virus spike protein to virus infection. J Virol 79:13209–13217 [View Article][PubMed]
     [Google Scholar]
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The contribution of the cytoplasmic retrieval signal of severe acute respiratory syndrome coronavirus to intracellular accumulation of S proteins and incorporation of S protein into virus-like particles
J. Gen. Virol. 97, 1853 (2016); https://doi.org/10.1099/jgv.0.000494
/content/journal/jgv/10.1099/jgv.0.000494
/content/journal/jgv/10.1099/jgv.0.000494
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