Cleavage and activation of the severe acute respiratory syndrome coronavirus spike protein by human airway trypsin-like protease

Journal of Virology

Volumn 85, Issue 24, 2011, Pages 13363-13372

  Bertram, Stephanie ^a,b   Glowacka, Ilona ^a   Müller, Marcel A ^c   Lavender, Hayley ^d   Gnirss, Kerstin ^a   Nehlmeier, Inga ^b   Niemeyer, Daniela ^c   He, Yuxian ^e   Simmons, Graham ^f   Drosten, Christian ^c   Soilleux, Elizabeth J ^d,g   Jahn, Olaf ^h   Steffen, Imke ^a,f   Pöhlmann, Stefan ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b GERMAN PRIMATE CENTER   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e INSTITUTE OF PATHOGEN BIOLOGY   (China)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^h MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; CATHEPSIN; CIS ACTING ELEMENT; TRANS ACTING FACTOR; TRANSMEMBRANE PROTEASE SERINE 2; TRYPTASE; TYPE II TRANSMEMBRANE SERINE PROTEASE; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS RECEPTOR; VIRUS SPIKE PROTEIN;

ARTICLE; BRONCHUS MUCOSA; CELL FUSION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MODIFICATION; HUMAN; HUMAN TISSUE; LUNG ALVEOLUS CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS ACTIVATION; VIRUS CELL INTERACTION; VIRUS EXPRESSION; VIRUS MUTATION; VIRUS SHEDDING; VIRUS TRANSMISSION; VIRUS VIRULENCE;

CELL LINE; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE GLYCOPROTEINS; PEPTIDYL-DIPEPTIDASE A; PROTEOLYSIS; RECEPTORS, VIRUS; SARS VIRUS; SERINE ENDOPEPTIDASES; VIRAL ENVELOPE PROTEINS;

SARS CORONAVIRUS;

EID: 84862908396     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05300-11     Document Type: Article

References (49)

1. Beaufort, N., et al. 2007. The human airway trypsin-like protease modulates the urokinase receptor (uPAR, CD87) structure and functions. Am. J. Physiol. Lung Cell. Mol. Physiol. 292:L1263-L1272.
2. Belouzard, S., V. C. Chu, and G. R. Whittaker. 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.
3. Bergeron, E., et al. 2005. Implication of proprotein convertases in the processing and spread of severe acute respiratory syndrome coronavirus. Biochem. Biophys. Res. Commun. 326:554-563.
4. Bertram, S., et al. 2010. TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells. J. Virol. 84:10016-10025.
5. Bertram, S., I. Glowacka, I. Steffen, A. Kuhl, and S. Pöhlmann. 2010. Novel insights into proteolytic cleavage of influenza virus hemagglutinin. Rev. Med. Virol. 20:298-310.
6. Bosch, B. J., W. Bartelink, and P. J. Rottier. 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.
7. Böttcher, E., et al. 2006. Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium. J. Virol. 80:9896-9898.
8. Böttcher-Friebertshauser, E., D. A. Stein, H. D. Klenk, and W. Garten. 2011. Inhibition of influenza virus infection in human airway cell cultures by an antisense peptide-conjugated morpholino oligomer targeting the hemagglutinin- activating protease TMPRSS2. J. Virol. 85:1554-1562.
9. Chaipan, C., et al. 2009. Proteolytic activation of the 1918 influenza virus hemagglutinin. J. Virol. 83:3200-3211.
10. Choi, S. Y., S. Bertram, I. Glowacka, Y. W. Park, and S. Pöhlmann. 2009. Type II transmembrane serine proteases in cancer and viral infections. Trends Mol. Med. 15:303-312.
11. Connor, R. I., B. K. Chen, S. Choe, and N. R. Landau. 1995. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935-944.
12. Gao, F., et al. 2003. Codon usage optimization of HIV type 1 subtype C gag, pol, env, and nef genes: in vitro expression and immune responses in DNAvaccinated mice. AIDS Res. Hum. Retroviruses 19:817-823.
13. Glowacka, I., et al. 2010. Differential downregulation of ACE2 by the spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus NL63. J. Virol. 84:1198-1205.
14. Glowacka, I., 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.
15. Guan, Y., et al. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:276-278.
16. Hamming, I., et al. 2004. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. J. Pathol. 203:631-637.
17. He, Y., et al. 2004. Identification of immunodominant sites on the spike protein of severe acute respiratory syndrome (SARS) coronavirus: implication for developing SARS diagnostics and vaccines. J. Immunol. 173:4050-4057.
18. Hofmann, H., et al. 2004. Susceptibility to SARS coronavirus S proteindriven infection correlates with expression of angiotensin converting enzyme 2 and infection can be blocked by soluble receptor. Biochem. Biophys. Res. Commun. 319:1216-1221.
19. Hofmann, H., et al. 2004. S protein of severe acute respiratory syndromeassociated coronavirus mediates entry into hepatoma cell lines and is targeted by neutralizing antibodies in infected patients. J. Virol. 78:6134-6142.
20. Hofmann, H., and S. Pöhlmann. 2004. Cellular entry of the SARS coronavirus. Trends Microbiol. 12:466-472.
21. Hofmann, H., et al. 2006. Highly conserved regions within the spike proteins of human coronaviruses 229E and NL63 determine recognition of their respective cellular receptors. J. Virol. 80:8639-8652.
22. Imai, Y., et al. 2005. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 436:112-116.
23. Jahn, O., D. Hesse, M. Reinelt, and H. D. Kratzin. 2006. Technical innovations for the automated identification of gel-separated proteins by MALDITOF mass spectrometry. Anal. Bioanal. Chem. 386:92-103.
24. Jung, H., et al. 2008. TMPRSS4 promotes invasion, migration and metastasis of human tumor cells by facilitating an epithelial-mesenchymal transition. Oncogene 27:2635-2647.
25. Kuba, K., et al. 2005. A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury. Nat. Med. 11:875-879.
26. Kuiken, T., et al. 2003. Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362:263-270.
27. Lau, S. K., et al. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. U. S. A. 102:14040-14045.
28. Li, W., et al. 2003. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426:450-454.
29. Li, W., et al. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676-679.
30. Matsuyama, S., et al. 2010. Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2. J. Virol. 84:12658-12664.
31. Mossel, E. C., et al. 2008. SARS-CoV replicates in primary human alveolar type II cell cultures but not in type I-like cells. Virology 372:127-135.
32. Peiris, J. S., Y. Guan, and K. Y. Yuen. 2004. Severe acute respiratory syndrome. Nat. Med. 10:S88-S97.
33. Peiris, J. S., K. Y. Yuen, A. D. Osterhaus, and K. Stohr. 2003. The severe acute respiratory syndrome. N. Engl. J. Med. 349:2431-2441.
34. Pulford, K., et al. 1997. Detection of anaplastic lymphoma kinase (ALK) and nucleolar protein nucleophosmin (NPM)-ALK proteins in normal and neoplastic cells with the monoclonal antibody ALK1. Blood 89:1394-1404.
35. Scott, H. S., et al. 2001. Insertion of beta-satellite repeats identifies a transmembrane protease causing both congenital and childhood onset autosomal recessive deafness. Nat. Genet. 27:59-63.
36. Shah, P. P., et al. 2010. A small-molecule oxocarbazate inhibitor of human cathepsin L blocks severe acute respiratory syndrome and Ebola pseudotype virus infection into human embryonic kidney 293T cells. Mol. Pharmacol. 78:319-324.
37. Shirogane, Y., et al. 2008. Efficient multiplication of human metapneumovirus in Vero cells expressing the transmembrane serine protease TMPRSS2. J. Virol. 82:8942-8946.
38. Shulla, A., et al. 2011. A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J. Virol. 85:873-882.
39. Simmons, G., et al. 2011. Different host cell proteases activate the SARScoronavirus spike-protein for cell-cell and virus-cell fusion. Virology 413: 265-274.
40. Simmons, G., et al. 2005. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc. Natl. Acad. Sci. U. S. A. 102:11876-11881.
41. Simmons, G., et al. 2003. DC-SIGN and DC-SIGNR bind Ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305:115-123.
42. Simmons, G., et al. 2004. Characterization of severe acute respiratory syndrome- associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry. Proc. Natl. Acad. Sci. U. S. A. 101:4240-4245.
43. Stadler, K., et al. 2003. SARS-beginning to understand a new virus. Nat. Rev. Microbiol. 1:209-218.
44. Takahashi, M., et al. 2001. Localization of human airway trypsin-like protease in the airway: an immunohistochemical study. Histochem. Cell Biol. 115:181-187.
45. Tedoldi, S., et al. 2006. Jaw1/LRMP, a germinal centre-associated marker for the immunohistological study of B-cell lymphomas. J. Pathol. 209:454-463.
46. To, K. F., and A. W. Lo. 2004. Exploring the pathogenesis of severe acute respiratory syndrome (SARS): the tissue distribution of the coronavirus (SARS-CoV) and its putative receptor, angiotensin-converting enzyme 2 (ACE2). J. Pathol. 203:740-743.
47. To, K. F., et al. 2004. Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases. J. Pathol. 202:157-163.
48. Wang, H., et al. 2008. SARS coronavirus entry into host cells through a novel clathrin- and caveolae-independent endocytic pathway. Cell Res. 18:290-301.
49. Wysocka, M., et al. 2010. Substrate specificity and inhibitory study of human airway trypsin-like protease. Bioorg. Med. Chem. 18:5504-5509.