Proteolytic activation of the SARS-coronavirus spike protein: Cutting enzymes at the cutting edge of antiviral research

Antiviral Research

Volumn 100, Issue 3, 2013, Pages 605-614

  Simmons, Graham ^a   Zmora, Pawel ^b   Gierer, Stefanie ^b   Heurich, Adeline ^b   Pöhlmann, Stefan ^b  

^a BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^b GERMAN PRIMATE CENTER   (Germany)

Author keywords

Cathepsin L; MERS; Protease; SARS; Spike protein; TMPRSS2

Indexed keywords

[1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; ANTIPARASITIC AGENT; ANTIVIRUS AGENT; BAFILOMYCIN; CAMOSTAT MESILATE; CATHEPSIN; CATHEPSIN L; ELASTASE; LEUPEPTIN; PROTEINASE; SERINE PROTEINASE; VIRUS PROTEIN; VITRONECTIN; ANGIOTENSIN CONVERTING ENZYME 2; CORONAVIRUS SPIKE GLYCOPROTEIN; DIPEPTIDYL CARBOXYPEPTIDASE; MEMBRANE PROTEIN; S PROTEIN, SEVERE ACUTE RESPIRATORY SYNDROME CORONAVIRUS; TMPRSS2 PROTEIN, HUMAN;

ANTIVIRAL ACTIVITY; CELL SURFACE; CONFORMATIONAL TRANSITION; CORONAVIRUS; DISEASE SURVEILLANCE; ENDOSOME; ENZYME ACTIVATION; HUMAN; MEMBRANE FUSION; NONHUMAN; PANDEMIC; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PUBLIC HEALTH; REVIEW; SARS CORONAVIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS INFECTIVITY; VIRUS TRANSMISSION; BIOLOGICAL MODEL; COMMUNICABLE DISEASE; CORONAVIRUS INFECTION; ENZYMOLOGY; LUNG; METABOLISM; PATHOLOGY; PHYSIOLOGY; VIROLOGY; VIRUS ENTRY; VIRUS REPLICATION; MERS; SPIKE PROTEIN; TMPRSS2;

ANIMALIA; SARS CORONAVIRUS;

CATHEPSINS; COMMUNICABLE DISEASES, EMERGING; CORONAVIRUS INFECTIONS; ENDOSOMES; HUMANS; LUNG; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PEPTIDYL-DIPEPTIDASE A; PROTEOLYSIS; SARS VIRUS; SERINE ENDOPEPTIDASES; SERINE PROTEASES; SEVERE ACUTE RESPIRATORY SYNDROME; SPIKE GLYCOPROTEIN, CORONAVIRUS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

CATHEPSIN L; MERS; PROTEASE; SARS; SPIKE PROTEIN; TMPRSS2;

EID: 84886731880     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.09.028     Document Type: Review

References (106)

1. A.O. Adedeji, W. Severson, C. Jonsson, K. Singh, S.R. Weiss, and S.G. Sarafianos Novel inhibitors of severe acute respiratory syndrome coronavirus entry that act by three distinct mechanisms J. Virol. 87 2013 8017 8028
2. K.K. Ang, J. Ratnam, J. Gut, J. Legac, E. Hansell, Z.B. Mackey, K.M. Skrzypczynska, A. Debnath, J.C. Engel, P.J. Rosenthal, J.H. McKerrow, M.R. Arkin, and A.R. Renslo Mining a cathepsin inhibitor library for new antiparasitic drug leads PLoS. Negl. Trop. Dis. 5 2011 e1023
3. A. Annan, H.J. Baldwin, V.M. Corman, S.M. Klose, M. Owusu, E.E. Nkrumah, E.K. Badu, P. Anti, O. Agbenyega, B. Meyer, S. Oppong, Y.A. Sarkodie, E.K. Kalko, P.H. Lina, E.V. Godlevska, C. Reusken, A. Seebens, F. Gloza-Rausch, P. Vallo, M. Tschapka, C. Drosten, and J.F. Drexler Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe Emerg. Infect. Dis. 19 2013 456 459
4. T.M. Antalis, T.H. Bugge, and Q. Wu Membrane-anchored serine proteases in health and disease Prog. Mol. Biol. Transl. Sci. 99 2011 1 50
5. M. Backovic, and T.S. Jardetzky Class III viral membrane fusion proteins Adv. Exp. Med. Biol. 714 2011 91 101
6. J. Baron, C. Tarnow, D. Mayoli-Nussle, E. Schilling, D. Meyer, M. Hammami, F. Schwalm, T. Steinmetzer, Y. Guan, W. Garten, H.D. Klenk, and E. Bottcher-Friebertshauser Matriptase, HAT, and TMPRSS2 activate the hemagglutinin of H9N2 influenza A viruses J. Virol. 87 2013 1811 1820
7. A. Beaulieu, E. Gravel, A. Cloutier, I. Marois, E. Colombo, A. Desilets, C. Verreault, R. Leduc, E. Marsault, and M.V. Richter Matriptase proteolytically activates influenza virus and promotes multicycle replication in the human airway epithelium J. Virol. 87 2013 4237 4251
8. S. Belouzard, V.C. Chu, and G.R. Whittaker Activation of the SARS coronavirus spike protein via sequential proteolytic cleavage at two distinct sites Proc. Natl. Acad. Sci. USA 106 2009 5871 5876
9. S. Belouzard, I. Madu, and G.R. Whittaker Elastase-mediated activation of the severe acute respiratory syndrome coronavirus spike protein at discrete sites within the S2 domain J. Biol. Chem. 285 2010 22758 22763
10. S. Belouzard, J.K. Millet, B.N. Licitra, and G.R. Whittaker Mechanisms of coronavirus cell entry mediated by the viral spike protein Viruses 4 2012 1011 1033
11. S. Bertram, R. Dijkman, M. Habjan, A. Heurich, S. Gierer, I. Glowacka, K. Welsch, M. Winkler, H. Schneider, H. Hofmann-Winkler, V. Thiel, and S. Pöhlmann TMPRSS2 activates the human coronavirus 229E for cathepsin-independent host cell entry and is expressed in viral target cells in the respiratory epithelium J. Virol. 87 2013 6150 6160
12. S. Bertram, I. Glowacka, P. Blazejewska, E. Soilleux, P. Allen, S. Danisch, I. Steffen, S.Y. Choi, Y. Park, H. Schneider, K. Schughart, and S. Pöhlmann TMPRSS2 and TMPRSS4 facilitate trypsin-independent spread of influenza virus in Caco-2 cells J. Virol. 84 2010 10016 10025
13. S. Bertram, I. Glowacka, M.A. Muller, H. Lavender, K. Gnirss, I. Nehlmeier, D. Niemeyer, Y. He, G. Simmons, C. Drosten, E.J. Soilleux, O. Jahn, I. Steffen, and S. Pöhlmann Cleavage and activation of the severe acute respiratory syndrome coronavirus spike protein by human airway trypsin-like protease J. Virol. 85 2011 13363 13372
14. S. Bertram, I. Glowacka, I. Steffen, A. Kuhl, and S. Pöhlmann Novel insights into proteolytic cleavage of influenza virus hemagglutinin Rev. Med. Virol. 20 2010 298 310
15. S. Bertram, A. Heurich, H. Lavender, S. Gierer, S. Danisch, P. Perin, J.M. Lucas, P.S. Nelson, S. Pöhlmann, and E.J. Soilleux Influenza and SARS-coronavirus activating proteases TMPRSS2 and HAT are expressed at multiple sites in human respiratory and gastrointestinal tracts PLoS One 7 2012 e35876
16. M.L. Biniossek, D.K. Nagler, C. Becker-Pauly, and O. Schilling Proteomic identification of protease cleavage sites characterizes prime and non-prime specificity of cysteine cathepsins B, L, and S J. Proteome Res. 10 2011 5363 5373
17. B.J. Bosch, W. Bartelink, and P.J. Rottier 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 2008 8887 8890
18. E. Böttcher-Friebertshauser, C. Freuer, F. Sielaff, S. Schmidt, M. Eickmann, J. Uhlendorff, T. Steinmetzer, H.D. Klenk, and W. Garten Cleavage of influenza virus hemagglutinin by airway proteases TMPRSS2 and HAT differs in subcellular localization and susceptibility to protease inhibitors J. Virol. 84 2010 5605 5614
19. E. Böttcher-Friebertshauser, H.D. Klenk, and W. Garten Activation of influenza viruses by proteases from host cells and bacteria in the human airway epithelium Pathog. Dis. doi 2013 10.1111/2049-632X.12053
20. E. Böttcher-Friebertshauser, D.A. Stein, H.D. Klenk, and W. Garten 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 2011 1554 1562
21. E. Böttcher, T. Matrosovich, M. Beyerle, H.D. Klenk, W. Garten, and M. Matrosovich Proteolytic activation of influenza viruses by serine proteases TMPRSS2 and HAT from human airway epithelium J. Virol. 80 2006 9896 9898 (Pubitemid 44435664)
22. R. Boycott, H.D. Klenk, and M. Ohuchi Cell tropism of influenza virus mediated by hemagglutinin activation at the stage of virus entry Virology 203 1994 313 319 (Pubitemid 24261758)
23. C. Chaipan, D. Kobasa, S. Bertram, I. Glowacka, I. Steffen, T.S. Tsegaye, M. Takeda, T.H. Bugge, S. Kim, Y. Park, A. Marzi, and S. Pöhlmann Proteolytic activation of the 1918 influenza virus hemagglutinin J. Virol. 83 2009 3200 3211
24. K. Chandran, N.J. Sullivan, U. Felbor, S.P. Whelan, and J.M. Cunningham Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection Science 308 2005 1643 1645 (Pubitemid 40807517)
25. H.A. Chapman, R.J. Riese, and G.P. Shi Emerging roles for cysteine proteases in human biology Annu. Rev. Physiol. 59 1997 63 88 (Pubitemid 27142435)
26. V.C. Cheng, S.K. Lau, P.C. Woo, and K.Y. Yuen Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection Clin. Microbiol. Rev. 20 2007 660 694 (Pubitemid 47623772)
27. S.S. Chiu, K.H. Chan, K.W. Chu, S.W. Kwan, Y. Guan, L.L. Poon, and J.S. Peiris Human coronavirus NL63 infection and other coronavirus infections in children hospitalized with acute respiratory disease in Hong Kong, China Clin. Infect. Dis. 40 2005 1721 1729 (Pubitemid 40803500)
28. K.E. Follis, J. York, and J.H. Nunberg Furin cleavage of the SARS coronavirus spike glycoprotein enhances cell-cell fusion but does not affect virion entry Virology 350 2006 358 369 (Pubitemid 43928105)
29. S. Gierer, S. Bertram, F. Kaup, F. Wrensch, A. Heurich, A. Kramer-Kuhl, K. Welsch, M. Winkler, B. Meyer, C. Drosten, U. Dittmer, T. von Hahn, G. Simmons, H. Hofmann, and S. Pöhlmann 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 2013 5502 5511
30. I. Glowacka, S. Bertram, P. Herzog, S. Pfefferle, I. Steffen, M.O. Muench, G. Simmons, H. Hofmann, T. Kuri, F. Weber, J. Eichler, C. Drosten, and S. Pöhlmann Differential downregulation of ACE2 by the spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus NL63 J. Virol. 84 2010 1198 1205
31. I. Glowacka, S. Bertram, M.A. Muller, P. Allen, E. Soilleux, S. Pfefferle, I. Steffen, T.S. Tsegaye, Y. He, K. Gnirss, D. Niemeyer, H. Schneider, C. Drosten, and S. Pöhlmann 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 2011 4122 4134
32. K. Gnirss, A. Kuhl, C. Karsten, I. Glowacka, S. Bertram, F. Kaup, H. Hofmann, and S. Pöhlmann Cathepsins B and L activate Ebola but not Marburg virus glycoproteins for efficient entry into cell lines and macrophages independent of TMPRSS2 expression Virology 424 2012 3 10
33. G.J. Gorse, T.Z. O'Connor, S.L. Hall, J.N. Vitale, and K.L. Nichol Human coronavirus and acute respiratory illness in older adults with chronic obstructive pulmonary disease J. Infect. Dis. 199 2009 847 857
34. Y. Guan, B.J. Zheng, Y.Q. He, X.L. Liu, Z.X. Zhuang, C.L. Cheung, S.W. Luo, P.H. Li, L.J. Zhang, Y.J. Guan, K.M. Butt, K.L. Wong, K.W. Chan, W. Lim, K.F. Shortridge, K.Y. Yuen, J.S. Peiris, and L.L. Poon Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China Science 302 2003 276 278 (Pubitemid 37248756)
35. S. Haga, N. Nagata, T. Okamura, N. Yamamoto, T. Sata, N. Yamamoto, T. Sasazuki, and Y. Ishizaka TACE antagonists blocking ACE2 shedding caused by the spike protein of SARS-CoV are candidate antiviral compounds Antiviral Res. 85 2010 551 555
36. S. Haga, N. Yamamoto, C. Nakai-Murakami, Y. Osawa, K. Tokunaga, T. Sata, N. Yamamoto, T. Sasazuki, and Y. Ishizaka Modulation of TNF-alpha-converting enzyme by the spike protein of SARS-CoV and ACE2 induces TNF-alpha production and facilitates viral entry Proc. Natl. Acad. Sci. USA 105 2008 7809 7814 (Pubitemid 351872720)
37. B.S. Hamilton, D.W. Gludish, and G.R. Whittaker Cleavage activation of the human-adapted influenza virus subtypes by matriptase reveals both subtype and strain specificities J. Virol. 86 2012 10579 10586
38. I. Hamming, W. Timens, M.L. Bulthuis, A.T. Lely, G.J. Navis, and H. van Goor Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis J. Pathol. 203 2004 631 637 (Pubitemid 38714099)
39. S.C. Harrison Viral membrane fusion Nat. Struct. Mol. Biol. 15 2008 690 698 (Pubitemid 351932011)
40. T. Heald-Sargent, and T. Gallagher Ready, set, fuse! The coronavirus spike protein and acquisition of fusion competence Viruses 4 2012 557 580
41. H. Hofmann, K. Hattermann, A. Marzi, T. Gramberg, M. Geier, M. Krumbiegel, S. Kuate, K. Uberla, M. Niedrig, and S. Pöhlmann S protein of severe acute respiratory syndrome-associated coronavirus mediates entry into hepatoma cell lines and is targeted by neutralizing antibodies in infected patients J. Virol. 78 2004 6134 6142 (Pubitemid 38715911)
42. H. Hofmann, and S. Pöhlmann Cellular entry of the SARS coronavirus Trends Microbiol. 12 2004 466 472 (Pubitemid 39286125)
43. H. Hofmann, G. Simmons, A.J. Rennekamp, C. Chaipan, T. Gramberg, E. Heck, M. Geier, A. Wegele, A. Marzi, P. Bates, and S. Pöhlmann Highly conserved regions within the spike proteins of human coronaviruses 229E and NL63 determine recognition of their respective cellular receptors J. Virol. 80 2006 8639 8652 (Pubitemid 44384874)
44. K.V. Holmes Coronaviruses D. Knipe, Fields Virology 2001 Lippincott, Wiliams & Wilkins Philadelphia 1187 1203
45. I.C. Huang, B.J. Bosch, F. Li, W. Li, K.H. Lee, S. Ghiran, N. Vasilieva, T.S. Dermody, S.C. Harrison, P.R. Dormitzer, M. Farzan, P.J. Rottier, and H. Choe SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells J. Biol. Chem. 281 2006 3198 3203 (Pubitemid 43845930)
46. Y. Imai, K. Kuba, S. Rao, Y. Huan, F. Guo, B. Guan, P. Yang, R. Sarao, T. Wada, H. Leong-Poi, M.A. Crackower, A. Fukamizu, C.C. Hui, L. Hein, S. Uhlig, A.S. Slutsky, C. Jiang, and J.M. Penninger Angiotensin-converting enzyme 2 protects from severe acute lung failure Nature 436 2005 112 116 (Pubitemid 40966195)
47. A. Jean, C. Quach, A. Yung, and M. Semret Severity and outcome associated with human coronavirus OC43 infections among children Pediatr. Infect. Dis. J. 32 2013 325 329
48. M. Jevsnik, T. Ursic, N. Zigon, L. Lusa, U. Krivec, and M. Petrovec Coronavirus infections in hospitalized pediatric patients with acute respiratory tract disease BMC Infect. Dis. 12 2012 365
49. D. Jia, M. Taguchi, and M. Otsuki Preventive and therapeutic effects of the protease inhibitor camostat on pancreatic fibrosis and atrophy in CCK-1 receptor-deficient rats Pancreas 30 2005 54 61 (Pubitemid 40070627)
50. H.P. Jia, D.C. Look, P. Tan, L. Shi, M. Hickey, L. Gakhar, M.C. Chappell, C. Wohlford-Lenane, and P.B. McCray Jr. Ectodomain shedding of angiotensin converting enzyme 2 in human airway epithelia Am. J. Physiol Lung Cell Mol. Physiol. 297 2009 L84 L96
51. Y.W. Kam, Y. Okumura, H. Kido, L.F. Ng, R. Bruzzone, and R. Altmeyer Cleavage of the SARS coronavirus spike glycoprotein by airway proteases enhances virus entry into human bronchial epithelial cells in vitro PLoS One 4 2009 e7870
52. M. Kawase, K. Shirato, S. Matsuyama, and F. Taguchi Protease-mediated entry via the endosome of human coronavirus 229E J. Virol. 83 2009 712 721
53. M. Kawase, K. Shirato, L. van der Hoek, F. Taguchi, and S. Matsuyama Simultaneous treatment of human bronchial epithelial cells with serine and cysteine protease inhibitors prevents severe acute respiratory syndrome coronavirus entry J. Virol. 86 2012 6537 6545
54. H. Kido, Y. Okumura, H. Yamada, T.Q. Le, and M. Yano Proteases essential for human influenza virus entry into cells and their inhibitors as potential therapeutic agents Curr. Pharm. Des. 13 2007 405 414 (Pubitemid 46477761)
55. T.S. Kim, C. Heinlein, R.C. Hackman, and P.S. Nelson Phenotypic analysis of mice lacking the TMPRSS2-encoded protease Mol. Cell Biol. 26 2006 965 975 (Pubitemid 43146490)
56. C. Kooi, M. Cervin, and R. Anderson Differentiation of acid-pH-dependent and -nondependent entry pathways for mouse hepatitis virus Virology 180 1991 108 119
57. K. Kuba, Y. Imai, S. Rao, H. Gao, F. Guo, B. Guan, Y. Huan, P. Yang, Y. Zhang, W. Deng, L. Bao, B. Zhang, G. Liu, Z. Wang, M. Chappell, Y. Liu, D. Zheng, A. Leibbrandt, T. Wada, A.S. Slutsky, D. Liu, C. Qin, C. Jiang, and J.M. Penninger A crucial role of angiotensin converting enzyme 2 (ACE2) in SARS coronavirus-induced lung injury Nat. Med. 11 2005 875 879 (Pubitemid 41161120)
58. D.W. Lambert, M. Yarski, F.J. Warner, P. Thornhill, E.T. Parkin, A.I. Smith, N.M. Hooper, and A.J. Turner Tumor necrosis factor-alpha convertase (ADAM17) mediates regulated ectodomain shedding of the severe-acute respiratory syndrome-coronavirus (SARS-CoV) receptor, angiotensin-converting enzyme-2 (ACE2) J. Biol. Chem. 280 2005 30113 30119 (Pubitemid 41216188)
59. S.K. Lau, P.C. Woo, K.S. Li, Y. Huang, H.W. Tsoi, B.H. Wong, S.S. Wong, S.Y. Leung, K.H. Chan, and K.Y. Yuen Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats Proc. Natl. Acad. Sci. USA 102 2005 14040 14045 (Pubitemid 41377699)
60. H. Laude, K. Van Reeth, and M. Pensaert Porcine respiratory coronavirus: molecular features and virus-host interactions Vet. Res. 24 1993 125 150
61. M. Leslie Infectious diseases. Drug developers finally take aim at a neglected disease Science 333 2011 933 935
62. F. Li Receptor recognition and cross-species infections of SARS coronavirus Antiviral Res. 100 2013 246 254
63. F. Li, W. Li, M. Farzan, and S.C. Harrison Structure of SARS coronavirus spike receptor-binding domain complexed with receptor LI2005 Science 309 2005 1864 1868 (Pubitemid 41325098)
64. W. Li, M.J. Moore, N. Vasilieva, J. Sui, S.K. Wong, M.A. Berne, M. Somasundaran, J.L. Sullivan, K. Luzuriaga, T.C. Greenough, H. Choe, and M. Farzan Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus Nature 426 2003 450 454 (Pubitemid 37490132)
65. W. Li, Z. Shi, M. Yu, W. Ren, C. Smith, J.H. Epstein, H. Wang, G. Crameri, Z. Hu, H. Zhang, J. Zhang, J. McEachern, H. Field, P. Daszak, B.T. Eaton, S. Zhang, and L.F. Wang Bats are natural reservoirs of SARS-like coronaviruses Science 310 2005 676 679 (Pubitemid 41528160)
66. W. Li, S.K. Wong, F. Li, J.H. Kuhn, I.C. Huang, H. Choe, and M. Farzan Animal origins of the severe acute respiratory syndrome coronavirus: insight from ACE2-S-protein interactions J. Virol. 80 2006 4211 4219
67. I.G. Madu, S.L. Roth, S. Belouzard, and G.R. Whittaker 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 2009 7411 7421
68. A. Marzi, T. Reinheckel, and H. Feldmann Cathepsin B & L are not required for ebola virus replication PLoS Negl. Trop. Dis. 6 2012 e1923
69. P.S. Masters The molecular biology of coronaviruses Adv. Virus Res. 66 2006 193 292 (Pubitemid 44107834)
70. S. Matsuyama, N. Nagata, K. Shirato, M. Kawase, M. Takeda, and F. Taguchi Efficient activation of the severe acute respiratory syndrome coronavirus spike protein by the transmembrane protease TMPRSS2 J. Virol. 84 2010 12658 12664
71. S. Matsuyama, M. Ujike, S. Morikawa, M. Tashiro, and F. Taguchi Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection Proc. Natl. Acad. Sci. USA 102 2005 12543 12547 (Pubitemid 41266395)
72. D. Meyer, F. Sielaff, M. Hammami, E. Bottcher-Friebertshauser, W. Garten, and T. Steinmetzer Identification of the first synthetic inhibitors of the type II transmembrane serine protease TMPRSS2 suitable for inhibition of influenza virus activation Biochem. J. 452 2013 331 343
73. J. Misasi, K. Chandran, J.Y. Yang, B. Considine, C.M. Filone, M. Cote, N. Sullivan, G. Fabozzi, L. Hensley, and J. Cunningham Filoviruses require endosomal cysteine proteases for entry but exhibit distinct protease preferences J. Virol. 86 2012 3284 3292
74. T.C. Nash, and M.J. Buchmeier Entry of mouse hepatitis virus into cells by endosomal and nonendosomal pathways Virology 233 1997 1 8 (Pubitemid 27348763)
75. Y. Okumura, E. Takahashi, M. Yano, M. Ohuchi, T. Daidoji, T. Nakaya, E. Bottcher, W. Garten, H.D. Klenk, and H. Kido 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 2010 5089 5096
76. G.Y. Oudit, Z. Kassiri, C. Jiang, P.P. Liu, S.M. Poutanen, J.M. Penninger, and J. Butany SARS-coronavirus modulation of myocardial ACE2 expression and inflammation in patients with SARS Eur. J. Clin. Invest. 39 2009 618 625
77. J.S. Peiris, Y. Guan, and K.Y. Yuen Severe acute respiratory syndrome Nat. Med. 10 2004 S88 S97
78. P. Pietschmann, U. Foger-Samwald, W. Sipos, and M. Rauner The role of cathepsins in osteoimmunology Crit. Rev. Eukaryot. Gene Expr. 23 2013 11 26
79. R.K. Plemper Cell entry of enveloped viruses Curr. Opin. Virol. 1 2011 92 100
80. Z. Qiu, S.T. Hingley, G. Simmons, C. Yu, J. Das Sarma, P. Bates, and S.R. Weiss Endosomal proteolysis by cathepsins is necessary for murine coronavirus mouse hepatitis virus type 2 spike-mediated entry J. Virol. 80 2006 5768 5776 (Pubitemid 43849155)
81. T. Reinheckel, J. Deussing, W. Roth, and C. Peters Towards specific functions of lysosomal cysteine peptidases: phenotypes of mice deficient for cathepsin B or cathepsin L Biol. Chem. 382 2001 735 741 (Pubitemid 32631710)
82. B. Rockx, T. Baas, G.A. Zornetzer, B. Haagmans, T. Sheahan, M. Frieman, M.D. Dyer, T.H. Teal, S. Proll, J. van den Brand, R. Baric, and M.G. Katze Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection J. Virol. 83 2009 7062 7074
83. P.P. Shah, T. Wang, R.L. Kaletsky, M.C. Myers, J.E. Purvis, H. Jing, D.M. Huryn, D.C. Greenbaum, A.B. Smith 3rd, P. Bates, and S.L. Diamond 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 2010 319 324
84. Y. Shirogane, M. Takeda, M. Iwasaki, N. Ishiguro, H. Takeuchi, Y. Nakatsu, M. Tahara, H. Kikuta, and Y. Yanagi Efficient multiplication of human metapneumovirus in Vero cells expressing the transmembrane serine protease TMPRSS2 J. Virol. 82 2008 8942 8946
85. A. Shulla, T. Heald-Sargent, G. Subramanya, J. Zhao, S. Perlman, and T. Gallagher A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry J. Virol. 85 2011 873 882
86. G. Simmons, S. Bertram, I. Glowacka, I. Steffen, C. Chaipan, J. Agudelo, K. Lu, A.J. Rennekamp, H. Hofmann, P. Bates, and S. Pöhlmann Different host cell proteases activate the SARS-coronavirus spike-protein for cell-cell and virus-cell fusion Virology 413 2011 265 274
87. G. Simmons, D.N. Gosalia, A.J. Rennekamp, J.D. Reeves, S.L. Diamond, and P. Bates Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry Proc. Natl. Acad. Sci. USA 102 2005 11876 11881 (Pubitemid 41170818)
88. G. Simmons, J.D. Reeves, A.J. Rennekamp, S.M. Amberg, A.J. Piefer, and P. Bates Characterization of severe acute respiratory syndrome-associated coronavirus (SARS-CoV) spike glycoprotein-mediated viral entry Proc. Natl. Acad. Sci. USA 101 2004 4240 4245 (Pubitemid 38405913)
89. K. Stadler, and R. Rappuoli SARS: understanding the virus and development of rational therapy Curr. Mol. Med. 5 2005 677 697 (Pubitemid 41824230)
90. I. Steffen, N.M. Liss, B.S. Schneider, J.N. Fair, C.Y. Chiu, and G. Simmons Characterization of the Bas-Congo virus glycoprotein and its function in pseudotyped viruses J. Virol. 87 2013 9558 9568
91. K.F. To, J.H. Tong, P.K. Chan, F.W. Au, S.S. Chim, K.C. Chan, J.L. Cheung, E.Y. Liu, G.M. Tse, A.W. Lo, Y.M. Lo, and H.K. Ng Tissue and cellular tropism of the coronavirus associated with severe acute respiratory syndrome: an in-situ hybridization study of fatal cases J. Pathol. 202 2004 157 163 (Pubitemid 38208652)
92. L. van der Hoek, K. Pyrc, M.F. Jebbink, W. Vermeulen-Oost, R.J. Berkhout, K.C. Wolthers, P.M. Wertheim-van Dillen, J. Kaandorp, J. Spaargaren, and B. Berkhout Identification of a new human coronavirus Nat. Med. 10 2004 368 373 (Pubitemid 38508514)
93. O. Vasiljeva, T. Reinheckel, C. Peters, D. Turk, V. Turk, and B. Turk Emerging roles of cysteine cathepsins in disease and their potential as drug targets Curr. Pharm. Des. 13 2007 387 403 (Pubitemid 46477760)
94. L.F. Wang, and B.T. Eaton Bats, civets and the emergence of SARS Curr. Top. Microbiol. Immunol. 315 2007 325 344
95. P. Wang, J. Chen, A. Zheng, Y. Nie, X. Shi, W. Wang, G. Wang, M. Luo, H. Liu, L. Tan, X. Song, Z. Wang, X. Yin, X. Qu, X. Wang, T. Qing, M. Ding, and H. Deng Expression cloning of functional receptor used by SARS coronavirus Biochem. Biophys. Res. Commun. 315 2004 439 444 (Pubitemid 38183125)
96. B.A. Wevers, and L. van der Hoek Recently discovered human coronaviruses Clin. Lab. Med. 29 2009 715 724
97. A.C. Wong, R.G. Sandesara, N. Mulherkar, S.P. Whelan, and K. Chandran A forward genetic strategy reveals destabilizing mutations in the Ebolavirus glycoprotein that alter its protease dependence during cell entry J. Virol. 84 2010 163 175
98. S.K. Wong, W. Li, M.J. Moore, H. Choe, and M. Farzan A 193-amino acid fragment of the SARS coronavirus S protein efficiently binds angiotensin-converting enzyme 2 J. Biol. Chem. 279 2004 3197 3201 (Pubitemid 38140552)
99. P.C. Woo, S.K. Lau, C.M. Chu, K.H. Chan, H.W. Tsoi, Y. Huang, B.H. Wong, R.W. Poon, J.J. Cai, W.K. Luk, L.L. Poon, S.S. Wong, Y. Guan, J.S. Peiris, and K.Y. Yuen Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia J. Virol. 79 2005 884 895 (Pubitemid 40053872)
100. World-Health-Organization, 2013. Novel coronavirus infection - update. http://www.who.int/csr/don/2013-09-07/en/index.html.
101. Z.Y. Yang, Y. Huang, L. Ganesh, K. Leung, W.P. Kong, O. Schwartz, K. Subbarao, and G.J. Nabel PH-dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN J. Virol. 78 2004 5642 5650 (Pubitemid 38661651)
102. A.M. Zaki, S. van Boheemen, T.M. Bestebroer, A.D. Osterhaus, and R.A. Fouchier Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia N. Engl. J. Med. 367 2012 1814 1820
103. O.P. Zhirnov, M.R. Ikizler, and P.F. Wright Cleavage of influenza a virus hemagglutinin in human respiratory epithelium is cell associated and sensitive to exogenous antiproteases J. Virol. 76 2002 8682 8689 (Pubitemid 34864063)
104. O.P. Zhirnov, H.D. Klenk, and P.F. Wright Aprotinin and similar protease inhibitors as drugs against influenza Antiviral Res. 92 2011 27 36
105. Y. Zhou, J. Agudelo, K. Lu, D.H. Goetz, E. Hansell, Y.T. Chen, W.R. Roush, J. McKerrow, C.S. Craik, S.M. Amberg, and G. Simmons Inhibitors of SARS-CoV entry - identification using an internally-controlled dual envelope pseudovirion assay Antiviral Res. 92 2011 187 194
106. Y. Zhou, and G. Simmons Development of novel entry inhibitors targeting emerging viruses Expert Rev. Anti Infect. Ther. 10 2012 1129 1138