Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry

Journal of Virology

Volumn 86, Issue 12, 2012, Pages 6537-6545

  Kawase, Miyuki ^a   Shirato, Kazuya ^a   van der Hoek, Lia ^c   Taguchi, Fumihiro ^b   Matsuyama, Shutoku ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b NIPPON VETERINARY AND LIFE SCIENCE UNIVERSITY   (Japan)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

[1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; ANGIOTENSIN CONVERTING ENZYME 2; ANTIVIRUS AGENT; BAFILOMYCIN A1; CAMOSTAT MESILATE; CATHEPSIN L INHIBITOR; CYSTEINE PROTEINASE INHIBITOR; CYTOCHALASIN D; EPOXYSUCCINYL LEUCYLAMINDO 3 METHYLBUTANE ETHYL ESTER; GABEXATE MESILATE; LEUPEPTIN; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; BRONCHUS MUCOSA; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG PROTEIN BINDING; EPITHELIUM CELL; HUMAN; HUMAN CELL; INFECTION PREVENTION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS CELL INTERACTION; VIRUS ENTRY;

BRONCHI; CYSTEINE PROTEINASE INHIBITORS; DOWN-REGULATION; EPITHELIAL CELLS; HUMANS; SARS VIRUS; SERINE PROTEINASE INHIBITORS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS INTERNALIZATION;

CORONAVIRUS; SARS CORONAVIRUS;

EID: 84864018547     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00094-12     Document Type: Article

References (34)

1. 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.
2. Belouzard S, Madu I, Whittaker GR. 2010. Elastase-mediated activation of the severe acute respiratory syndrome coronavirus spike protein at discrete sites within the S2 domain. J. Biol. Chem. 285:22758 -22763.
3. Bertram S, et al. 2010. TMPRSS2 and TMPRSS4 facilitate trypsinindependent spread of influenza virus in Caco-2 cells. J. Virol. 84:10016- 10025.
4. Bertram S, 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.
5. Bertram S, Glowacka I, Steffen I, Kühl A, Pöhlmann S. 2010. Novel insights into proteolytic cleavage of influenza virus hemagglutinin. Rev. Med. Virol. 20:298 -310.
6. Bosch BJ, Bartelink W, Rottier PJM. 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, Freuer C, Steinmetzer T, Klenk H-D, Garten W. 2009. MDCK cells that express proteases TMPRSS2 and HAT provide a cell system to propagate influenza viruses in the absence of trypsin and to study cleavage of HA and its inhibition. Vaccine 27:6324-6329.
8. 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.
9. Böttcher-Friebertshäuser E, 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.
10. Böttcher-Friebertshäuser E, Stein DA, Klenk H-D, Garten W. 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.
11. Chaipan C, et al. 2009. Proteolytic activation of the 1918 influenza virus hemagglutinin. J. Virol. 83:3200 -3211.
12. Choi S-Y, Bertram S, Glowacka I, Park YW, Pöhlmann S. 2009. Type II transmembrane serine proteases in cancer and viral infections. Trends Mol. Med. 15:303-312.
13. Ding Y, et al. 2003. The clinical pathology of severe acute respiratory syndrome (SARS): a report from China. J. Pathol. 200:282-289.
14. Fukushi S, et al. 2005. Vesicular stomatitis virus pseudotyped with severe acute respiratory syndrome coronavirus spike protein. J. Gen. Virol. 86: 2269-2274.
15. 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.
16. Huang I-C, et al. 2006. SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J. Biol. Chem. 281:3198 -3203.
17. Kam Y-W, et al. 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. doi:10.1371/journal. pone.0007870.
18. Kawase M, Shirato K, Matsuyama S, Taguchi F. 2009. Proteasemediated entry via the endosome of human coronavirus 229E. J. Virol. 83:712-721.
19. 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.
20. 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.
21. Matsuyama S, Taguchi F. 2009. Two-step conformational changes in a coronavirus envelope glycoprotein mediated by receptor binding and proteolysis. J. Virol. 83:11133-11141.
22. Miyauchi K, Kim Y, Latinovic O, Morozov V, Melikyan GB. 2009. HIV enters cells via endocytosis and dynamin-dependent fusion with endosomes. Cell 137:433- 444.
23. Okumura Y, et al. 2010. Novel type II transmembrane serine proteases, MSPL and TMPRSS13, proteolytically activate membrane fusion activity of the hemagglutinin of highly pathogenic avian influenza viruses and induce their multicycle replication. J. Virol. 84:5089 -5096.
24. Paoloni-Giacobino A, Chen H, Peitsch MC, Rossier C, Antonarakis SE. 1997. Cloning of the TMPRSS2 gene, which encodes a novel serine protease with transmembrane, LDLRA, and SRCR domains and maps to 21q22.3. Genomics 44:309 -320.
25. Shirato K, Matsuyama S, Ujike M, Taguchi F. 2011. Role of proteases in the release of porcine epidemic diarrhea virus from infected cells. J. Virol. 85:7872-7880.
26. Shirogane Y, et al. 2008. Efficient multiplication of human metapneumovirus in Vero cells expressing the transmembrane serine protease TMPRSS2. J. Virol. 82:8942- 8946.
27. 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.
28. 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.
29. 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.
30. Simmons G, et al. 2004. Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoproteinmediated viral entry. Proc. Natl. Acad. Sci. U. S. A. 101:4240-4245.
31. Talukdar R, Tandon RK. 2008. Pancreatic stellate cells: new target in the treatment of chronic pancreatitis. J. Gastroenterol. Hepatol. 23:34-41.
32. To KF, Lo AWI. 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.
33. Watanabe R, et al. 2008. Entry from the cell surface of severe acute respiratory syndrome coronavirus with cleaved S protein as revealed by pseudotype virus bearing cleaved S protein. J. Virol. 82:11985-11991.
34. Yoshikawa T, et al. 2010. Dynamic innate immune responses of human bronchial epithelial cells to severe acute respiratory syndrome-associated coronavirus infection. PLoS One 5:e8729. doi:10.1371/journal. pone.0008729.