Clinical isolates of human coronavirus 229E bypass the endosome for cell entry

Journal of Virology

Volumn 91, Issue 1, 2017, Pages

  Shirato, Kazuya ^a   Kanou, Kazuhiko ^a   Kawase, Miyuki ^a   Matsuyama, Shutoku ^a  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Cathepsin; Coronavirus; Endosomes; TMPRSS2

Indexed keywords

CATHEPSIN L; PROTEINASE; TRANSMEMBRANE PROTEASE SERINE 2; UNCLASSIFIED DRUG; VIRUS SPIKE PROTEIN; CORONAVIRUS SPIKE GLYCOPROTEIN; CTSL1 PROTEIN, HUMAN; PROTEINASE INHIBITOR; SERINE PROTEINASE; TMPRSS2 PROTEIN, HUMAN;

AIRWAY EPITHELIUM CELL; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; ENDOSOME; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN CORONAVIRUS 229E; NONHUMAN; PRIORITY JOURNAL; PSEUDOTYPING; STRAIN DIFFERENCE; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS STRAIN; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CELL MEMBRANE; COMMON COLD; CORONAVIRUS INFECTION; DRUG EFFECTS; ENDOCYTOSIS; EPITHELIUM CELL; EVOLUTION; GENETICS; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MUTATION; RESPIRATORY MUCOSA; SEQUENCE ALIGNMENT; VIROLOGY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BIOLOGICAL EVOLUTION; CATHEPSIN L; CELL MEMBRANE; COMMON COLD; CORONAVIRUS 229E, HUMAN; CORONAVIRUS INFECTIONS; ENDOCYTOSIS; ENDOSOMES; EPITHELIAL CELLS; HELA CELLS; HUMANS; IMMUNE EVASION; MUTATION; PROTEASE INHIBITORS; RESPIRATORY MUCOSA; SEQUENCE ALIGNMENT; SERINE ENDOPEPTIDASES; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRUS INTERNALIZATION;

EID: 85008173902     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01387-16     Document Type: Article

References (36)

1. Hamre D, Procknow JJ. 1966. A new virus isolated from the human respiratory tract. Proc Soc Exp Biol Med 121:190-193. https://doi.org/10.3181/00379727-121-30734.
2. Shirato K, Kawase M, Watanabe O, Hirokawa C, Matsuyama S, Nishimura H, Taguchi F. 2012. Differences in neutralizing antigenicity between laboratory and clinical isolates of HCoV-229E isolated in Japan in 2004-2008 depend on the S1 region sequence of the spike protein. J Gen Virol 93:1908-1917. https://doi.org/10.1099/vir.0.043117-0.
3. Chibo D, Birch C. 2006. Analysis of human coronavirus 229E spike and nucleoprotein genes demonstrates genetic drift between chronologically distinct strains. J Gen Virol 87:1203-1208. https://doi.org/10.1099/vir.0.81662-0.
4. Owusu M, Annan A, Corman VM, Larbi R, Anti P, Drexler JF, Agbenyega O, Adu-Sarkodie Y, Drosten C. 2014. Human coronaviruses associated with upper respiratory tract infections in three rural areas of Ghana. PLoS One 9:e99782. https://doi.org/10.1371/journal.pone.0099782.
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. https://doi.org/10.1002/rmv.657.
6. White JM, Delos SE, Brecher M, Schornberg K. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit Rev Biochem Mol Biol 43:189-219. https://doi.org/10.1080/10409230802058320.
7. 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.
8. 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. https://doi.org/10.1074/jbc.M110.103275.
9. Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM. 2005. Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308:1643-1645. https://doi.org/10.1126/science.1110656.
10. Matsuyama S, Ujike M, Morikawa S, Tashiro M, Taguchi F. 2005. Proteasemediated enhancement of severe acute respiratory syndrome coronavirus infection. Proc Natl Acad Sci U S A 102:12543-12547. https://doi.org/10.1073/pnas.0503203102.
11. Millet JK, Whittaker GR. 2014. Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc Natl Acad Sci U S A 111:15214-15219. https://doi.org/10.1073/pnas.1407087111.
12. 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.
13. Simmons G, Reeves JD, Rennekamp AJ, Amberg SM, Piefer AJ, Bates P. 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. https://doi.org/10.1073/pnas.0306446101.
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.
15. Bertram S, Dijkman R, Habjan M, Heurich A, Gierer S, Glowacka I, Welsch K, Winkler M, Schneider H, Hofmann-Winkler H, Thiel V, Pöhlmann S. 2013 TMPRSS2 activates the human coronavirus 229E for cathepsinindependent host cell entry and is expressed in viral target cells in the respiratory epithelium. J Virol 87:6150-6160. https://doi.org/10.1128/JVI.03372-12.
16. Kawase M, Shirato K, Matsuyama S, Taguchi F. 2009. Protease-mediated entry via the endosome of human coronavirus 229E. J Virol 83:712-721. https://doi.org/10.1128/JVI.01933-08.
17. 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. https://doi.org/10.1016/j.cell.2009.02.046.
18. Zhou Y, Vedantham P, Lu K, Agudelo J, Carrion R, Nunneley JW, Barnard D, Pöhlmann S, McKerrow JH, Renslo AR, Simmons G. 2015. Protease inhibitors targeting coronavirus and filovirus entry. Antiviral Res 116: 76-84. https://doi.org/10.1016/j.antiviral.2015.01.011.
19. Madu IG, Roth SL, Belouzard S, Whittaker GR. 2009. Characterization of a highly conserved domain within the severe acute respiratory syndrome coronavirus spike protein S2 domain with characteristics of a viral fusion peptide. J Virol 83:7411-7421. https://doi.org/10.1128/JVI.00079-09.
20. Misasi J, Chandran K, Yang J-Y, Considine B, Filone CM, Cote M, Sullivan N, Fabozzi G, Hensley L, Cunningham J. 2012. Filoviruses require endosomal cysteine proteases for entry but exhibit distinct protease preferences. J Virol 86:3284-3292. https://doi.org/10.1128/JVI.06346-11.
21. Pyrc K, Sims AC, Dijkman R, Jebbink M, Long C, Deming D, Donaldson E, Vabret A, Baric R, van der Hoek L, Pickles R. 2010. Culturing the unculturable: human coronavirus HKU1 infects, replicates, and produces progeny virions in human ciliated airway epithelial cell cultures. J Virol 84:11255-11263. https://doi.org/10.1128/JVI.00947-10.
22. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. 2005. Welldifferentiated human airway epithelial cell cultures. Methods Mol Med 107:183-206.
23. Walls AC, Tortorici MA, Bosch B-J, Frenz B, Rottier PJM, DiMaio F, Rey F, Veesler D. 2016. Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531:114-117. https://doi.org/10.1038/nature16988.
24. Kirchdoerfer RN, Cottrell CA, Wang N, Pallesen J, Yassine HM, Turner HL, Corbett KS, Graham BS, McLellan JS, Ward AB. 2016. Pre-fusion structure of a human coronavirus spike protein. Nature 531:118-121. https://doi.org/10.1038/nature17200.
25. Blasius AL, Beutler B. 2010. Intracellular Toll-like receptors. Immunity 32:305-315. https://doi.org/10.1016/j.immuni.2010.03.012.
26. Jensen S, Thomsen AR. 2012. Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. J Virol 86:2900-2910. https://doi.org/10.1128/JVI.05738-11.
27. 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. https://doi.org/10.1128/JVI.00959-09.
28. Gierer S, Bertram S, Kaup F, Wrensch F, Heurich A, Krämer-Kühl A, Welsch K, Winkler M, Meyer B, Drosten C, Dittmer U, von Hahn T, Simmons G, Hofmann H, Pöhlmann S. 2013. The spike protein of the emerging betacoronavirus EMC uses a novel coronavirus receptor for entry, can be activated by TMPRSS2, and is targeted by neutralizing antibodies. J Virol 87:5502-5511. https://doi.org/10.1128/JVI.00128-13.
29. Yamaya M, Shimotai Y, Hatachi Y, Lusamba Kalonji N, Tando Y, Kitajima Y, Matsuo K, Kubo H, Nagatomi R, Hongo S, Homma M, Nishimura H. 2015 The serine protease inhibitor camostat inhibits influenza virus replication and cytokine production in primary cultures of human tracheal epithelial cells. Pulm Pharmacol Ther 33:66-74. https://doi.org/10.1016/j.pupt.2015.07.001.
30. Kawase M, Shirato K, van der Hoek L, Taguchi F, Matsuyama S. 2012. Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry. J Virol 86:6537-6545. https://doi.org/10.1128/JVI.00094-12.
31. Yamamoto M, Matsuyama S, Li X, Takeda M, Kawaguchi Y, Inoue J, Matsuda Z. Identification of nafamostat as a potent inhibitor of Middle East respiratory syndrome (MERS) corona virus S-mediated membrane fusion using the split protein-based cell-cell fusion assay. Antimicrob Agents Chemother, in press.
32. Talukdar R, Tandon RK. 2008. Pancreatic stellate cells: new target in the treatment of chronic pancreatitis. J Gastroenterol Hepatol 23:34-41.
33. Adler G, Rausch U, Weidenbach F, Arnold R, Kern HF. 1984. General and selective inhibition of pancreatic enzyme discharge using a proteinase inhibitor (FOY-305). Klin Wochenschr 62:406-411. https://doi.org/10.1007/BF01742297.
34. Shirato K, Kawase M, Matsuyama S. 2013. Middle East respiratory syndrome coronavirus infection mediated by the transmembrane serine protease TMPRSS2. J Virol 87:12552-12561. https://doi.org/10.1128/JVI.01890-13.
35. 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 21q223. Genomics 44:309-320. https://doi.org/10.1006/geno.1997.4845.
36. Baker D, Sali A. 2001. Protein structure prediction and structural genomics. Science 294:93-96. https://doi.org/10.1126/science.1065659.