Different residues in the SARS-CoV spike protein determine cleavage and activation by the host cell protease TMPRSS2

PLoS ONE

Volumn 12, Issue 6, 2017, Pages

  Reinke, Lennart Michel ^a   Spiegel, Martin ^a,b   Plegge, Teresa ^a   Hartleib, Anika ^a   Nehlmeier, Inga ^a   Gierer, Stefanie ^a   Hoffmann, Markus ^a   Hofmann Winkler, Heike ^a   Winkler, Michael ^a   Pöhlmann, Stefan ^a  

^a GERMAN PRIMATE CENTER   (Germany)

^b BRANDENBURG MEDICAL SCHOOL THEODOR FONTANE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; SERINE PROTEINASE; TRYPSIN; VITRONECTIN; CORONAVIRUS SPIKE GLYCOPROTEIN; S PROTEIN, SEVERE ACUTE RESPIRATORY SYNDROME CORONAVIRUS; TMPRSS2 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BETACORONAVIRUS; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE MUTATION; GLYCOSYLATION; GOLGI COMPLEX; HOST CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MEMBRANE FUSION; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MUTAGENESIS; NONHUMAN; PROTEIN CLEAVAGE; SARS CORONAVIRUS; SEQUENCE ANALYSIS; TARGET CELL; VIRUS ACTIVATION; VIRUS ENTRY; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; METABOLISM; MUTATION; PROTEIN TRANSPORT;

HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MUTATION; PROTEIN TRANSPORT; SERINE ENDOPEPTIDASES; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRUS INTERNALIZATION;

EID: 85021064427     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0179177     Document Type: Article

References (33)

1. Hilgenfeld R, Peiris M. (2013) From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses. Antiviral Res 100: 286–295. https://doi.org/10.1016/j.antiviral.2013.08.015 PMID: 24012996
2. Poon LL, Guan Y, Nicholls JM, Yuen KY, Peiris JS. (2004) The aetiology, origins, and diagnosis of severe acute respiratory syndrome. Lancet Infect Dis 4: 663–671. https://doi.org/10.1016/S1473-3099 (04)01172-7 PMID: 15522678
3. Zaki AM, van BS, Bestebroer TM, Osterhaus AD, Fouchier RA. (2012) Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367: 1814–1820. https://doi.org/10.1056/ NEJMoa1211721 PMID: 23075143
4. Zumla A, Hui DS, Perlman S. (2015) Middle East respiratory syndrome. Lancet 386: 995–1007. https://doi.org/10.1016/S0140-6736(15)60454-8 PMID: 26049252
5. Belouzard S, Millet JK, Licitra BN, Whittaker GR. (2012) Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses 4: 1011–1033. https://doi.org/10.3390/v4061011 PMID: 22816037
6. Hofmann H, Pöhlmann S. (2004) Cellular entry of the SARS coronavirus. Trends Microbiol 12: 466–472. https://doi.org/10.1016/j.tim.2004.08.008 PMID: 15381196
7. Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, et al. (2003) Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426: 450–454. https://doi.org/10.1038/nature02145 PMID: 14647384
8. Li W, Choe H, Farzan M. (2006) Insights from the association of SARS-CoV S-protein with its receptor, ACE2. Adv Exp Med Biol 581: 209–218. https://doi.org/10.1007/978-0-387-33012-9_36 PMID: 17037532
9. Millet JK, Whittaker GR. (2015) Host cell proteases: Critical determinants of coronavirus tropism and pathogenesis. Virus Res 202: 120–134. https://doi.org/10.1016/j.virusres.2014.11.021 PMID: 25445340
10. Simmons G, Zmora P, Gierer S, Heurich A, Pöhlmann S. (2013) Proteolytic activation of the SARS-coronavirus spike protein: cutting enzymes at the cutting edge of antiviral research. Antiviral Res 100: 605–614. https://doi.org/10.1016/j.antiviral.2013.09.028 PMID: 24121034
11. Simmons G, Gosalia DN, Rennekamp AJ, Reeves JD, Diamond SL, Bates P. (2005) Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci U S A 102: 11876–11881. https://doi.org/10.1073/pnas.0505577102 PMID: 16081529
12. Glowacka I, Bertram S, Müller MA, Allen P, Soilleux E, Pfefferle S, et al. (2011) Evidence that TMPRSS2 activates the severe acute respiratory syndrome coronavirus spike protein for membrane fusion and reduces viral control by the humoral immune response. J Virol 85: 4122–4134. https://doi.org/10.1128/JVI.02232-10 PMID: 21325420
13. Matsuyama S, Nagata N, Shirato K, Kawase M, Takeda M, Taguchi F. (2010) Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J Virol 84: 12658–12664. https://doi.org/10.1128/JVI.01542-10 PMID: 20926566
14. Shulla A, Heald-Sargent T, Subramanya G, Zhao J, Perlman S, Gallagher T. (2011) A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J Virol 85: 873–882. https://doi.org/10.1128/JVI.02062-10 PMID: 21068237
15. Zhou Y, Vedantham P, Lu K, Agudelo J, Carrion R Jr., Nunneley JW, et al. (2015) Protease inhibitors targeting coronavirus and filovirus entry. Antiviral Res 116: 76–84. https://doi.org/10.1016/j.antiviral.2015.01.011 PMID: 25666761
16. Hatesuer B, Bertram S, Mehnert N, Bahgat MM, Nelson PS, Pohlmann S, et al. (2013) Tmprss2 is essential for influenza H1N1 virus pathogenesis in mice. PLoS Pathog 9: e1003774. https://doi.org/10.1371/journal.ppat.1003774 PMID: 24348248
17. Sakai K, Ami Y, Tahara M, Kubota T, Anraku M, Abe M, et al. (2014) The host protease TMPRSS2 plays a major role in in vivo replication of emerging H7N9 and seasonal influenza viruses. J Virol 88: 5608–5616. https://doi.org/10.1128/JVI.03677-13 PMID: 24600012
18. Tarnow C, Engels G, Arendt A, Schwalm F, Sediri H, Preuss A, et al. (2014) TMPRSS2 is a host factor that is essential for pneumotropism and pathogenicity of H7N9 influenza A virus in mice. J Virol 88: 4744–4751. https://doi.org/10.1128/JVI.03799-13 PMID: 24522916
19. Cheng Z, Zhou J, To KK, Chu H, Li C, Wang D, et al. (2015) Identification of TMPRSS2 as a Susceptibility Gene for Severe 2009 Pandemic A(H1N1) Influenza and A(H7N9) Influenza. J Infect Dis.
20. Simmons G, Bertram S, Glowacka I, Steffen I, Chaipan C, Agudelo J, et al. (2011) Different host cell proteases activate the SARS-coronavirus spike-protein for cell-cell and virus-cell fusion. Virology 413: 265–274. https://doi.org/10.1016/j.virol.2011.02.020 PMID: 21435673
21. Bertram S, Glowacka I, Muller MA, Lavender H, Gnirss K, Nehlmeier I, et al. (2011) Cleavage and activation of the severe acute respiratory syndrome coronavirus spike protein by human airway trypsin-like protease. J Virol 85: 13363–13372. https://doi.org/10.1128/JVI.05300-11 PMID: 21994442
22. Belouzard S, Chu VC, Whittaker GR. (2009) Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc Natl Acad Sci U S A 106: 5871–5876. https://doi.org/10.1073/pnas.0809524106 PMID: 19321428
23. Simmons G, Reeves JD, Grogan CC, Vandenberghe LH, Baribaud F, Whitbeck JC, et al. (2003) DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305: 115–123. PMID: 12504546
24. Wrensch F, Winkler M, Pöhlmann S. (2014) IFITM proteins inhibit entry driven by the MERS-coronavirus spike protein: evidence for cholesterol-independent mechanisms. Viruses 6: 3683–3698. https://doi.org/10.3390/v6093683 PMID: 25256397
25. Niwa H, Yamamura K, Miyazaki J. (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193–199. PMID: 1660837
26. Kremers GJ, Goedhart J, van Munster EB, Gadella TW Jr. (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Forster radius. Biochemistry 45: 6570–6580. https://doi.org/10.1021/bi0516273 PMID: 16716067
27. de Jong AS, Visch HJ, de MF, van Dommelen MM, Swarts HG, Luyten T, et al. (2006) The coxsackie-virus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi. J Biol Chem 281: 14144–14150. https://doi.org/10.1074/jbc. M511766200 PMID: 16540472
28. Plegge T, Hofmann-Winkler H, Spiegel M, Pöhlmann S. (2016) Evidence that Processing of the Severe Fever with Thrombocytopenia Syndrome Virus Gn/Gc Polyprotein Is Critical for Viral Infectivity and Requires an Internal Gc Signal Peptide. PLoS One 11: e0166013. https://doi.org/10.1371/journal.pone.0166013 PMID: 27855227
29. Follis KE, York J, Nunberg JH. (2006) Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry. Virology 350: 358–369. https://doi.org/10.1016/j.virol.2006.02.003 PMID: 16519916
30. Kam YW, Okumura Y, Kido H, Ng LF, Bruzzone R, Altmeyer R. (2009) Cleavage of the SARS coronavirus spike glycoprotein by airway proteases enhances virus entry into human bronchial epithelial cells in vitro. PLoS One 4: e7870. https://doi.org/10.1371/journal.pone.0007870 PMID: 19924243
31. Bosch BJ, Bartelink W, Rottier PJ. (2008) Cathepsin L functionally cleaves the severe acute respiratory syndrome coronavirus class I fusion protein upstream of rather than adjacent to the fusion peptide. J Virol 82: 8887–8890. https://doi.org/10.1128/JVI.00415-08 PMID: 18562523
32. Böttcher-Friebertshauser E, Freuer C, Sielaff F, Schmidt S, Eickmann M, Uhlendorff J, et al. (2010) Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors. J Virol 84: 5605–5614. https://doi.org/10.1128/JVI.00140-10 PMID: 20237084
33. Peitsch C, Klenk HD, Garten W, Böttcher-Friebertshauser E. (2014) Activation of influenza A viruses by host proteases from swine airway epithelium. J Virol 88: 282–291. https://doi.org/10.1128/JVI.01635-13 PMID: 24155384