Drug targets for rational design against emerging coronaviruses

Infectious Disorders - Drug Targets

Volumn 13, Issue 2, 2013, Pages 116-127

  Zhao, Qi ^a   Weber, Erin ^a   Yang, Haitao ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TIANJIN UNIVERSITY   (China)

Author keywords

Coronavirus; Main protease; Non structural proteins; Rational drug design; SARS; Virus entry; Virus host interaction

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; CORE PROTEIN; DIPEPTIDYL CARBOXYPEPTIDASE; IMMUNOPHILIN; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEINASE; RNA POLYMERASE; RUPINTRIVIR; TACROLIMUS; VIRUS SPIKE PROTEIN; CORONAVIRUS SPIKE GLYCOPROTEIN; DNA DIRECTED RNA POLYMERASE; PEPTIDE HYDROLASE;

CORONAVIRUS; DRUG DESIGN; DRUG TARGETING; ENZYME INHIBITION; HUMAN; LIFE CYCLE; NONHUMAN; REVIEW; RNA EDITING; SEVERE ACUTE RESPIRATORY SYNDROME; VIRUS CELL INTERACTION; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CORONAVIRIDAE; CORONAVIRUS INFECTIONS; DRUG DELIVERY SYSTEM; DRUG EFFECTS; METABOLISM; MOLECULAR GENETICS; MOLECULARLY TARGETED THERAPY; VIROLOGY;

AMINO ACID SEQUENCE; ANIMALS; CORONAVIRUS; CORONAVIRUS INFECTIONS; DNA-DIRECTED RNA POLYMERASES; DRUG DELIVERY SYSTEMS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR TARGETED THERAPY; PEPTIDE HYDROLASES; SPIKE GLYCOPROTEIN, CORONAVIRUS;

EID: 84882795091     PISSN: 18715265     EISSN: 18755852     Source Type: Journal    
DOI: 10.2174/18715265113139990024     Document Type: Review

References (156)

1. Pickett, B. E.; Greer, D. S.; Zhang, Y.; Stewart, L.; Zhou, L.; Sun, G., et al., Virus pathogen database and analysis resource (ViPR): a comprehensive bioinformatics database and analysis resource for the coronavirus research community. Viruses, 4(11), 3209-3226.
2. McIntosh, K.; Dees, J. H.; Becker, W. B.; Kapikian, A. Z.; Chanock, R. M., Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proc. Natl. Acad. Sci. U S A., 1967, 57(4), 933-9340.
3. Hamre, D.; Procknow, J.J. A new virus isolated from the human respiratory tract. Proc. Soc. Exp. Biol. Med. 1966, 121(1), 190-193.
4. van der Hoek, L.; Pyrc, K.; Jebbink, M. F.; Vermeulen-Oost, W.; Berkhout, R. J.; Wolthers, K. C., et al., Identification of a new human coronavirus. Nat. Med. 2004, 10(4), 368-373.
5. Esper, F.; Shapiro, E.D.; Weibel, C.; Ferguson, D.; Landry, M.L.; Kahn, J.S. Association between a novel human coronavirus and Kawasaki disease. J. Infect. Dis., 2005, 191(4), 499-502.
6. Woo, P.C.; Lau, S.K.; Chu, C.M.; Chan, K.H.; Tsoi, H.W.; Huang, Y. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol., 2005, 79(2), 884-895.
7. Drosten, C.; Gunther, S.; Preiser, W.; van der Werf, S.; Brodt, H. R.; Becker, S., et al., Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 2003, 348(20), 1967-1976.
8. van Boheemen, S.; de Graaf, M.; Lauber, C.; Bestebroer, T. M.; Raj, V. S.; Zaki, A. M. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio, 3(6).
9. Zaki, A. M.; van Boheemen, S.; Bestebroer, T. M.; Osterhaus, A. D.; Fouchier, R. A., Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med., 367(19), 1814-1820.
10. Guan, Y.; Zheng, B. J.; He, Y. Q.; Liu, X. L.; Zhuang, Z. X.; Cheung, C. L. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science, 2003, 302(5643), 276-278.
11. Dea, S.; Roy, R. S.; Begin, M. E., Bovine coronavirus isolation and cultivation in continuous cell lines. Am. J. Vet. Res., 1980, 41(1), 30-38.
12. O'Reilly, K. J.; Fishman, B.; Hitchcock, L. M., Feline infectious peritonitis: isolation of a coronavirus. Vet Rec., 1979, 104(15), 348.
13. Kamogawa, O.; Tomita, Y.; Kaneko, M.; Yamada, S.; Kubo, M.; Shimizu, M. Isolation of porcine respiratory coronavirus from pigs affected with porcine reproductive and respiratory syndrome. J. Vet. Med. Sci., 1996, 58(4), 385-388.
14. Kusanagi, K.; Kuwahara, H.; Katoh, T.; Nunoya, T.; Ishikawa, Y.; Samejima, T., et al., Isolation and serial propagation of porcine epidemic diarrhea virus in cell cultures and partial characterization of the isolate. J. Vet. Med. Sci., 1992, 54(2), 313-318.
15. Pensaert, M.; Callebaut, P.; Vergote, J., Isolation of a porcine respiratory, non-enteric coronavirus related to transmissible gastroenteritis. Vet. Q., 1986, 8(3), 257-261.
16. Liu, S.; Chen, J.; Kong, X.; Shao, Y.; Han, Z.; Feng, L. Isolation of avian infectious bronchitis coronavirus from domestic peafowl (Pavo cristatus) and teal (Anas). J. Gen. Virol., 2005, 86(Pt 3), 719-725.
17. Zanella, A.; Coaro, R.; Fabris, G.; Marchi, R.; Lavazza, A., Avian infectious bronchitis virus: isolation of an apparently new variant in Italy. Vet. Rec., 2000, 146 (7), 191-193.
18. Picault, J. P.; Drouin, P.; Guittet, M.; Bennejean, G.; Protais, J.; L'Hospitalier, R. Isolation, characterisation and preliminary cross-protection studies with a new pathogenic avian infectious bronchitis virus (strain PL-84084). Avian Pathol., 1986, 15(3), 367-383.
19. Hirai, K.; Shimakura, S., Isolation and characteristics of avian nephrosis-inducing infectious bronchitis virus (coronavirus). Nihon Juigaku Zasshi, 1971, 33(5), 209-216.
20. Chu, D. K.; Peiris, J. S.; Chen, H.; Guan, Y.; Poon, L. L., Genomic characterizations of bat coronaviruses (1A, 1B and HKU8) and evidence for co-infections in Miniopterus bats. J. Gen. Virol., 2008, 89(Pt 5), 1282-1287.
21. Muller, M. A.; Paweska, J. T.; Leman, P. A.; Drosten, C.; Grywna, K.; Kemp, A., et al., Coronavirus antibodies in African bat species. Emerg. Infect. Dis., 2007, 13(9), 1367-1370.
22. Wang, M.; Yan, M.; Xu, H.; Liang, W.; Kan, B.; Zheng, B., et al., SARS-CoV infection in a restaurant from palm civet. Emerg. Infect. Dis., 2005, 11(12), 1860-1865.
23. Song, H. D.; Tu, C. C.; Zhang, G. W.; Wang, S. Y.; Zheng, K.; Lei, L. C., Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. U S A., 2005, 102(7), 2430-2435.
24. Vengust, G.; Valencak, Z.; Bidovec, A., A serological survey of selected pathogens in wild boar in Slovenia. J. Vet. Med. B. Infect. Dis. Vet. Public Health, 2006, 53(1), 24-27.
25. Ostrowski, S.; Van Vuuren, M.; Lenain, D. M.; Durand, A., A serologic survey of wild felids from central west Saudi Arabia. J. Wildl. Dis., 2003, 39(3), 696-701.
26. Kimber, K. R.; Kollias, G. V.; Dubovi, E. J. Serologic survey of selected viral agents in recently captured wild North American river otters (Lontra canadensis). J. Zoo Wildl. Med., 2000, 31(2), 168-175.
27. Laurenson, K.; Van Heerden, J.; Stander, P.; Van Vuuren, M. J., Seroepidemiological survey of sympatric domestic and wild dogs (Lycaon pictus) in Tsumkwe District, north-eastern Namibia. Onderstepoort J. Vet. Res., 1997, 64(4), 313-316.
28. Foreyt, W. J.; Evermann, J. F., Serologic survey of canine coronavirus in wild coyotes in the western United States, 1972-1982. J. Wildl. Dis., 1985, 21(4), 428-430.
29. Iftimovici, R.; Mihail, A.; Iacobesco, V.; Popesco, A.; Mutiu, A.; Niculesco, R., et al., [Preliminary note on the circulation of some human respiratory viruses by wild birds] Arch. Inst. Pasteur Tunis, 1978, 55(3), 293-401.
30. Watanabe, Y.; Ibrahim, M. S.; Ikuta, K. Evolution and control of H5N1. A better understanding of the evolution and diversity of H5N1 flu virus and its host species in endemic areas could inform more efficient vaccination and control strategies. EMBO Rep., 14(2), 117-122.
31. Heikkinen, L. S.; Kazlauskas, A.; Melen, K.; Wagner, R.; Ziegler, T.; Julkunen, I., et al., Avian and 1918 Spanish influenza a virus NS1 proteins bind to Crk/CrkL Src homology 3 domains to activate host cell signaling. J. Biol. Chem., 2008, 283(9), 5719-5727.
32. Rest, J. S.; Mindell, D. P., SARS associated coronavirus has a recombinant polymerase and coronaviruses have a history of hostshifting. Infect. Genet. Evol., 2003, 3(3), 219-225.
33. Shi, Z.; Hu, Z., A review of studies on animal reservoirs of the SARS coronavirus. Virus Res., 2008, 133(1), 74-87.
34. Vijgen, L.; Keyaerts, E.; Moes, E.; Thoelen, I.; Wollants, E.; Lemey, P., et al., Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J. Virol., 2005, 79(3), 1595-1604.
35. Lu, G.; Liu, D. SARS-like virus in the Middle East: a truly batrelated coronavirus causing human diseases. Protein Cell, 3(11), 803-805.
36. Balboni, A.; Gallina, L.; Palladini, A.; Prosperi, S.; Battilani, M., A real-time PCR assay for bat SARS-like coronavirus detection and its application to Italian greater horseshoe bat faecal sample surveys. Sci. World J., 2012, 989514.
37. Woo, P. C.; Lau, S. K.; Huang, Y.; Yuen, K. Y. Coronavirus diversity, phylogeny and interspecies jumping. Exp. Biol. Med. (Maywood), 2009, 234(10), 1117-1127.
38. Lavi, E.; Fishman, P. S.; Highkin, M. K.; Weiss, S. R., Limbic encephalitis after inhalation of a murine coronavirus. Lab Invest., 1988, 58(1), 31-36.
39. Johnson-Lussenburg, C. M.; Zheng, Q. Coronavirus and multiple sclerosis: results of a case/control longitudinal serological study. Adv. Exp. Med. Biol., 1987, 218, 421-429.
40. Kern, P.; Muller, G.; Schmitz, H.; Racz, P.; Meigel, W.; Riethmuller, G., et al., Detection of coronavirus-like particles in homosexual men with acquired immunodeficiency and related lymphadenopathy syndrome. Klin Wochenschr, 1985, 63(2), 68-72.
41. Akerlund, A.; Greiff, L.; Andersson, M.; Bende, M.; Alkner, U.; Persson, C. G., Mucosal exudation of fibrinogen in coronavirus induced common colds. Acta Otolaryngol., 1993, 113(5), 642-648.
42. Bende, M.; Barrow, I.; Heptonstall, J.; Higgins, P. G.; Al-Nakib, W.; Tyrrell, D. A., et al., Changes in human nasal mucosa during experimental coronavirus common colds. Acta Otolaryngol, 1989, 107 (3-4), 262-269.
43. Turner, R. B.; Felton, A.; Kosak, K.; Kelsey, D. K.; Meschievitz, C. K., Prevention of experimental coronavirus colds with intranasal alpha-2b interferon. J. Infect. Dis., 1986, 154(3), 443-447.
44. Reed, S. E., The behaviour of recent isolates of human respiratory coronavirus in vitro and in volunteers: evidence of heterogeneity among 229E-related strains. J. Med. Virol., 1984, 13(2), 179-192.
45. Hendley, J.O.; Fishburne, H.B.; Gwaltney, J.M. Jr., Coronavirus infections in working adults. Eight-year study with 229 E and OC 43. Am. Rev. Respir. Dis., 1972, 105 (5), 805-811.
46. Greenberg, S. B. Rhinovirus and coronavirus infections. Semin. Respir. Crit. Care Med., 2007, 28(2), 182-192.
47. Lim, M. K., Bird flu: pandemic flu preparation: an unheeded lesson from SARS. BMJ 2006, 332 (7546), 913.
48. Cherry, J. D., The chronology of the 2002-2003 SARS mini pandemic. Paediatr.Respir. Rev., 2004, 5 (4), 262-269.
49. Cherry, J. D.; Krogstad, P., SARS: the first pandemic of the 21st century. Pediatr. Res., 2004, 56 (1), 1-5.
50. Verma, I. M., SARS: fear of global pandemic. Mol Ther 2003, 7 (6), 711.
51. Cyranoski, D.; Abbott, A., Apartment complex holds clues to pandemic potential of SARS. Nature, 2003, 423 (6935), 3-4.
52. Pascoe, N., A pandemic flu: not if, but when. SARS was the wake-up call we slept through. Tex Nurs., 2006, 80(1), 6-10.
53. Ng, S. M.; Chan, T. H.; Chan, C. L.; Lee, A. M.; Yau, J. K.; Chan, C. H. Group debriefing for people with chronic diseases during the SARS pandemic: Strength-Focused and Meaning-Oriented Approach for Resilience and Transformation (SMART). Community Ment. Health J., 2006, 42(1), 53-63.
54. Webster, P., Canada strengthens pandemic plan in wake of SARS. Lancet, 2004, 363 (9409), 628.
55. Enserink, M., Breakthrough of the year. SARS: a pandemic prevented. Science, 2003, 302 (5653), 2045.
56. Shortridge, K. F., SARS exposed, pandemic influenza lurks. Lancet, 2003, 361 (9369), 1649.
57. Yang, H.; Xie, W.; Xue, X.; Yang, K.; Ma, J.; Liang, W., et al., Design of wide-spectrum inhibitors targeting coronavirus main proteases. PLoS Biol., 2005, 3(10), e324.
58. Pfefferle, S.; Schopf, J.; Kogl, M.; Friedel, C. C.; Muller, M. A, Carbajo-Lozoya, J., et al., The SARS-coronavirus-host interactome: identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog., 7 (10), e1002331.
59. O'Keefe, B. R.; Giomarelli, B.; Barnard, D. L.; Shenoy, S. R.; Chan, P. K.; McMahon, J. B., et al., Broad-spectrum in vitro activity and in vivo efficacy of the antiviral protein griffithsin against emerging viruses of the family Coronaviridae. J. Virol., 84 (5), 2511-21.
60. Kim, Y.; Lovell, S.; Tiew, K. C.; Mandadapu, S. R.; Alliston, K. R.; Battaile, K. P., et al., Broad-spectrum antivirals against 3C or 3C-like proteases of picornaviruses, noroviruses, and coronaviruses. J. Virol., 86 (21), 11754-11762.
61. Cavanagh, D., Coronavirus IBV: structural characterization of the spike protein. J Gen Virol 1983, 64 (Pt 12), 2577-83.
62. Bonilla, P. J.; Pinon, J. L.; Hughes, S.; Weiss, S. R., Characterization of the leader papain-like protease of MHV-A59. Adv. Exp. Med. Biol., 1995, 380, 423-430.
63. Lu, Y.; Lu, X.; Denison, M. R., Identification and characterization of a serine-like proteinase of the murine coronavirus MHV-A59. J. Virol., 1995, 69(6), 3554-3559.
64. von Grotthuss, M.; Wyrwicz, L. S.; Rychlewski, L., mRNA cap-1 methyltransferase in the SARS genome. Cell, 2003, 113 (6), 701-2.
65. Prentice, E.; McAuliffe, J.; Lu, X.; Subbarao, K.; Denison, M. R., Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J. Virol., 2004, 78 (18), 9977-86.
66. Pachuk, C. J.; Bredenbeek, P. J.; Zoltick, P. W.; Spaan, W. J.; Weiss, S. R., Molecular cloning of the gene encoding the putative polymerase of mouse hepatitis coronavirus, strain A59. Virology, 1989, 171 (1), 141-148.
67. Imbert, I.; Guillemot, J. C.; Bourhis, J. M.; Bussetta, C.; Coutard, B.; Egloff, M. P., et al., A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J., 2006, 25 (20), 4933-42.
68. Ivanov, K. A.; Thiel, V.; Dobbe, J. C.; van der Meer, Y.; Snijder, E. J.; Ziebuhr, J., Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J. Virol., 2004, 78(11), 5619-5632.
69. Tanaka, T.; Kamitani, W.; DeDiego, M. L.; Enjuanes, L.; Matsuura, Y., Severe acute respiratory syndrome coronavirus nsp1 facilitates efficient propagation in cells through a specific translational shutoff of host mRNA. J. Virol., 86(20), 11128-11137.
70. Kamitani, W.; Huang, C.; Narayanan, K.; Lokugamage, K. G.; Makino, S., A two-pronged strategy to suppress host protein synthesis by SARS coronavirus Nsp1 protein. Nat. Struct. Mol. Biol., 2009, 16(11), 1134-1140.
71. Delmas, B.; Gelfi, J.; Sjostrom, H.; Noren, O.; Laude, H., Further characterization of aminopeptidase-N as a receptor for coronaviruses. Adv. Exp. Med. Biol., 1993, 342, 293-8.
72. Schultze, B.; Herrler, G., Recognition of cellular receptors by bovine coronavirus. Arch. Virol., 1994, 9, 451-9.
73. Li, D.; Cavanagh, D., Coronavirus IBV-induced membrane fusion occurs at near-neutral pH. Arch. Virol., 1992, 122 (3-4), 307-316.
74. Laude, H., Background paper. Mapping epitopes on coronavirus glycoproteins. Adv. Exp. Med. Biol., 1990, 276, 139-142.
75. Li, F.; Li, W.; Farzan, M.; Harrison, S. C., Structure of SARS coronavirus spike receptor-binding domain complexed with receptor. Science, 2005, 309(5742), 1864-1868.
76. Li, W.; Moore, M. J.; Vasilieva, N.; Sui, J.; Wong, S. K.; Berne, M. A., et al., Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature, 2003, 426(6965), 450-454.
77. Ishii, K.; Hasegawa, H.; Nagata, N.; Ami, Y.; Fukushi, S.; Taguchi, F., et al., Neutralizing antibody against severe acute respiratory syndrome (SARS)-coronavirus spike is highly effective for the protection of mice in the murine SARS model. Microbiol. Immunol., 2009, 53(2), 75-82.
78. Hua, R. H.; Wu, D. L.; Tong, G. Z.; Wang, Y. F.; Tian, Z. J.; Zhou, Y. J., [Identification of mimotope peptides which bind to the SARS-CoV spike protein specific monoclonal antibody 2C5 with phage-displayed peptides library] Sheng Wu Gong Cheng Xue Bao, 2006, 22 (5), 701-6.
79. Yu, X. F.; Liang, L. H.; She, M.; Liao, X. L.; Gu, J.; Li, Y. H., et al., Production of a monoclonal antibody against SARS-CoV spike protein with single intrasplenic immunization of plasmid DNA. Immunol. Lett., 2005, 100(2), 177-181.
80. Bisht, H.; Roberts, A.; Vogel, L.; Subbarao, K.; Moss, B., Neutralizing antibody and protective immunity to SARS coronavirus infection of mice induced by a soluble recombinant polypeptide containing an N-terminal segment of the spike glycoprotein. Virology, 2005, 334(2), 160-165.
81. Zhang, Y.; Yang, F.; Li, Y. H.; Li, W. H.; Tu, X. M.; Wei, Q. [Potent neutralization antibody elicited in mice by SARS-associated coronavirus spike protein S1 domain] Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi, 2004, 18 (3), 258-560.
82. Struck, A. W.; Axmann, M.; Pfefferle, S.; Drosten, C.; Meyer, B., A hexapeptide of the receptor-binding domain of SARS corona virus spike protein blocks viral entry into host cells via the human receptor ACE2. Antiviral. Res., 94(3), 288-296.
83. Raj, V. S.; Mou, H.; Smits, S. L.; Dekkers, D. H.; Muller, M. A.; Dijkman, R., et al., Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature, 495 (7440), 251-254.
84. Kliger, Y.; Levanon, E. Y., Cloaked similarity between HIV-1 and SARS-CoV suggests an anti-SARS strategy. BMC Microbiol., 2003, 3, 20.
85. Xu, Y.; Lou, Z.; Liu, Y.; Pang, H.; Tien, P.; Gao, G. F., et al., Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem., 2004, 279(47), 49414-9.
86. Xu, Y.; Liu, Y.; Lou, Z.; Qin, L.; Li, X.; Bai, Z., et al., Structural basis for coronavirus-mediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J. Biol. Chem., 2004, 279 (29), 30514-22.
87. Su, S. B.; Gong, W. H.; Gao, J. L.; Shen, W. P.; Grimm, M. C.; Deng, X., et al., T20/DP178, an ectodomain peptide of human immunodeficiency virus type 1 gp41, is an activator of human phagocyte N-formyl peptide receptor. Blood, 1999, 93(11), 3885-92.
88. Lawless, M. K.; Barney, S.; Guthrie, K. I.; Bucy, T. B.; Petteway, S. R., Jr.; Merutka, G., HIV-1 membrane fusion mechanism: structural studies of the interactions between biologically-active peptides from gp41. Biochemistry, 1996, 35 (42), 13697-708.
89. Bosch, B. J.; Martina, B. E.; Van Der Zee, R.; Lepault, J.; Haijema, B. J.; Versluis, C., et al., Severe acute respiratory syndrome coronavirus (SARS-CoV) infection inhibition using spike protein heptad repeat-derived peptides. Proc. Natl. Acad. Sci. U S A., 2004, 101 (22), 8455-60.
90. Liu, S.; Xiao, G.; Chen, Y.; He, Y.; Niu, J.; Escalante, C. R., et al., Interaction between heptad repeat 1 and 2 regions in spike protein of SARS-associated coronavirus: implications for virus fusogenic mechanism and identification of fusion inhibitors. Lancet, 2004, 363 (9413), 938-947.
91. Xu, Y.; Zhu, J.; Liu, Y.; Lou, Z.; Yuan, F.; Cole, D. K., et al., Characterization of the heptad repeat regions, HR1 and HR2, and design of a fusion core structure model of the spike protein from severe acute respiratory syndrome (SARS) coronavirus. Biochemistry, 2004, 43(44), 14064-71.
92. Ni, L.; Zhu, J.; Zhang, J.; Yan, M.; Gao, G. F.; Tien, P., Design of recombinant protein-based SARS-CoV entry inhibitors targeting the heptad-repeat regions of the spike protein S2 domain. Biochem Biophys Res Commun 2005, 330 (1), 39-45.
93. Bosch, B. J.; Rossen, J. W.; Bartelink, W.; Zuurveen, S. J.; de Haan, C. A.; Duquerroy, S., et al., Coronavirus escape from heptad repeat 2 (HR2)-derived peptide entry inhibition as a result of mutations in the HR1 domain of the spike fusion protein. J. Virol., 2008, 82 (5), 2580-2585.
94. Tsai, J. C.; de Groot, L.; Pinon, J. D.; Iacono, K. T.; Phillips, J. J.; Seo, S. H., et al., Amino acid substitutions within the heptad repeat domain 1 of murine coronavirus spike protein restrict viral antigen spread in the central nervous system. Virology, 2003, 312(2), 369-380.
95. Chu, L. H.; Chan, S. H.; Tsai, S. N.; Wang, Y.; Cheng, C. H.; Wong, K. B., et al., Fusion core structure of the severe acute respiratory syndrome coronavirus (SARS-CoV): in search of potent SARS-CoV entry inhibitors. J. Cell Biochem., 2008, 104(6), 2335-2347.
96. Lu, X.; Lu, Y.; Denison, M. R., Intracellular and in vitro-translated 27-kDa proteins contain the 3C-like proteinase activity of the coronavirus MHV-A59. Virology, 1996, 222 (2), 375-82.
97. Ziebuhr, J.; Herold, J.; Siddell, S. G., Characterization of a human coronavirus (strain 229E) 3C-like proteinase activity. J. Virol., 1995, 69 (7), 4331-4338.
98. Denison, M. R.; Kim, J. C.; Ross, T., Inhibition of coronavirus MHV-A59 replication by proteinase inhibitors. Adv Exp Med Biol 1995, 380, 391-7.
99. Baker, S. C.; Yokomori, K.; Dong, S.; Carlisle, R.; Gorbalenya, A. E.; Koonin, E. V., et al., Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J. Virol., 1993, 67 (10), 6056-63.
100. Liu, D. X.; Brierley, I.; Brown, T. D., Identification of a trypsin-like serine proteinase domain encoded by ORF 1a of the coronavirus IBV. Adv. Exp. Med. Biol., 1995, 380, 405-411.
101. Tibbles, K. W.; Brierley, I.; Cavanagh, D.; Brown, T. D., Characterization in vitro of an autocatalytic processing activity associated with the predicted 3C-like proteinase domain of the coronavirus avian infectious bronchitis virus. J. Virol., 1996, 70 (3), 1923-1930.
102. Lim, K. P.; Liu, D. X., Characterization of the two overlapping papain-like proteinase domains encoded in gene 1 of the coronavirus infectious bronchitis virus and determination of the C-terminal cleavage site of an 87-kDa protein. Virology, 1998, 245 (2), 303-312.
103. Dong, S.; Baker, S. C., Determinants of the p28 cleavage site recognized by the first papain-like cysteine proteinase of murine coronavirus. Virology, 1994, 204 (2), 541-9.
104. Ziebuhr, J.; Heusipp, G.; Seybert, A.; Siddell, S. G., Substrate specificity of the human coronavirus 229E 3C-like proteinase. Adv. Exp. Med. Biol., 1998, 440, 115-20.
105. Liu, D. X.; Shen, S.; Xu, H. Y.; Wang, S. F., Proteolytic mapping of the coronavirus infectious bronchitis virus 1b polyprotein: evidence for the presence of four cleavage sites of the 3C-like proteinase and identification of two novel cleavage products. Virology 1998, 246 (2), 288-297.
106. Ziebuhr, J.; Siddell, S. G., Processing of the human coronavirus 229E replicase polyproteins by the virus-encoded 3C-like proteinase: identification of proteolytic products and cleavage sites common to pp1a and pp1ab. J. Virol., 1999, 73 (1), 177-85.
107. Du, Q. S.; Wang, S. Q.; Zhu, Y.; Wei, D. Q.; Guo, H.; Sirois, S., et al., Polyprotein cleavage mechanism of SARS CoV Mpro and chemical modification of the octapeptide. Peptides, 2004, 25 (11), 1857-64.
108. Ziebuhr, J.; Bayer, S.; Cowley, J. A.; Gorbalenya, A. E., The 3C-like proteinase of an invertebrate nidovirus links coronavirus and potyvirus homologs. J. Virol., 2003, 77 (2), 1415-26.
109. Zhong, N.; Zhang, S.; Xue, F.; Kang, X.; Zou, P.; Chen, J., et al., C-terminal domain of SARS-CoV main protease can form a 3D domain-swapped dimer. Protein Sci., 2009, 18 (4), 839-844.
110. Zheng, K.; Ma, G.; Zhou, J.; Zen, M.; Zhao, W.; Jiang, Y., et al., Insight into the activity of SARS main protease: Molecular dynamics study of dimeric and monomeric form of enzyme. Proteins, 2007, 66 (2), 467-79.
111. Goetz, D. H.; Choe, Y.; Hansell, E.; Chen, Y. T.; McDowell, M.; Jonsson, C. B. Substrate specificity profiling and identification of a new class of inhibitor for the major protease of the SARS coronavirus. Biochemistry, 2007, 46 (30), 8744-52.
112. Zhu, L.; George, S.; Schmidt, M. F.; Al-Gharabli, S. I.; Rademann, J.; Hilgenfeld, R., Peptide aldehyde inhibitors challenge the substrate specificity of the SARS-coronavirus main protease. Antiviral Res., 92(2), 204-212.
113. Taranto, A. G.; Carvalho, P.; Avery, M. A., QM/QM studies for Michael reaction in coronavirus main protease (3CL Pro). J. Mol. Graph Model, 2008, 27(3), 275-285.
114. Verschueren, K. H.; Pumpor, K.; Anemuller, S.; Chen, S.; Mesters, J. R.; Hilgenfeld, R., A structural view of the inactivation of the SARS coronavirus main proteinase by benzotriazole esters. Chem. Biol., 2008, 15(6), 597-606.
115. Xue, X.; Yu, H.; Yang, H.; Xue, F.; Wu, Z.; Shen, W., et al., Structures of two coronavirus main proteases: implications for substrate binding and antiviral drug design. J. Virol., 2008, 82(5), 2515-2527.
116. Zhao, Q.; Li, S.; Xue, F.; Zou, Y.; Chen, C.; Bartlam, M. Structure of the main protease from a global infectious human coronavirus, HCoV-HKU1. J. Virol., 2008, 82(17), 8647-8655.
117. Kim, Y.; Mandadapu, S. R.; Groutas, W. C.; Chang, K. O., Potent inhibition of feline coronaviruses with peptidyl compounds targeting coronavirus 3C-like protease. Antiviral Res., 97 (2), 161-168.
118. Bacha, U.; Barrila, J.; Gabelli, S. B.; Kiso, Y.; Mario Amzel, L.; Freire, E., Development of broad-spectrum halomethyl ketone inhibitors against coronavirus main protease 3CL(pro). Chem. Biol. Drug Des., 2008, 72(1), 34-49.
119. Patick, A. K.; Binford, S. L.; Brothers, M. A.; Jackson, R. L.; Ford, C. E.; Diem, M. D., et al., In vitro antiviral activity of AG7088, a potent inhibitor of human rhinovirus 3C protease. Antimicrob. Agents Chemother., 1999, 43(10), 2444-50.
120. Matthews, D. A.; Dragovich, P. S.; Webber, S. E.; Fuhrman, S. A.; Patick, A. K.; Zalman, L. S., et al., Structure-assisted design of mechanism-based irreversible inhibitors of human rhinovirus 3C protease with potent antiviral activity against multiple rhinovirus serotypes. Proc. Natl. Acad. Sci. U S A., 1999, 96(20), 11000-7.
121. Binford, S. L.; Maldonado, F.; Brothers, M. A.; Weady, P. T.; Zalman, L. S.; Meador, J. W., 3rd, Conservation of amino acids in human rhinovirus 3C protease correlates with broad-spectrum antiviral activity of rupintrivir, a novel human rhinovirus 3C protease inhibitor. Antimicrob. Agents Chemother., 2005, 49(2), 619-626.
122. Herold, J.; Gorbalenya, A. E.; Thiel, V.; Schelle, B.; Siddell, S. G., Proteolytic processing at the amino terminus of human coronavirus 229E gene 1-encoded polyproteins: identification of a papain-like proteinase and its substrate. J. Virol., 1998, 72(2), 910-8.
123. Wojdyla, J. A.; Manolaridis, I.; van Kasteren, P. B.; Kikkert, M.; Snijder, E. J.; Gorbalenya, A. E. Papain-like protease 1 from transmissible gastroenteritis virus: crystal structure and enzymatic activity toward viral and cellular substrates. J. Virol., 84 (19), 10063-10073.
124. Clementz, M. A.; Chen, Z.; Banach, B. S.; Wang, Y.; Sun, L.; Ratia, K., et al., Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J. Virol., 84 (9), 4619-29.
125. Li, S. W.; Lai, C. C.; Ping, J. F.; Tsai, F. J.; Wan, L.; Lin, Y. J. Severe acute respiratory syndrome coronavirus papain-like protease suppressed alpha interferon-induced responses through downregulation of extracellular signal-regulated kinase 1-mediated signalling pathways. J. Gen. Virol., 92 (Pt 5), 1127-40.
126. Chaudhuri, R.; Tang, S.; Zhao, G.; Lu, H.; Case, D. A.; Johnson, M. E., Comparison of SARS and NL63 papain-like protease binding sites and binding site dynamics: inhibitor design implications. J. Mol. Biol., 414 (2), 272-288.
127. Ghosh, A. K.; Takayama, J.; Rao, K. V.; Ratia, K.; Chaudhuri, R.; Mulhearn, D. C., et al., Severe acute respiratory syndrome coronavirus papain-like novel protease inhibitors: design, synthesis, protein-ligand X-ray structure and biological evaluation. J. Med. Chem., 53 (13), 4968-4979.
128. Pan, J.; Peng, X.; Gao, Y.; Li, Z.; Lu, X.; Chen, Y., et al., Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication. PLoS One 2008, 3 (10), e3299.
129. te Velthuis, A. J.; van den Worm, S. H.; Snijder, E. J., The SARS-coronavirus nsp7+nsp8 complex is a unique multimeric RNA polymerase capable of both de novo initiation and primer extension. Nucleic Acids Res., 40 (4), 1737-47.
130. Li, S.; Zhao, Q.; Zhang, Y.; Bartlam, M.; Li, X.; Rao, Z., New nsp8 isoform suggests mechanism for tuning viral RNA synthesis. Protein Cell, 1 (2), 198-204.
131. te Velthuis, A. J.; Arnold, J. J.; Cameron, C. E.; van den Worm, S. H.; Snijder, E. J., The RNA polymerase activity of SARS-coronavirus nsp12 is primer dependent. Nucleic Acids Res., 38 (1), 203-14.
132. Azzi, A.; Lin, S. X., Human SARS-coronavirus RNA-dependent RNA polymerase: activity determinants and nucleoside analogue inhibitors. Proteins, 2004, 57 (1), 12-4.
133. te Velthuis, A. J.; van den Worm, S. H.; Sims, A. C.; Baric, R. S.; Snijder, E. J.; van Hemert, M. J., Zn(2+) inhibits coronavirus and arterivirus RNA polymerase activity in vitro and zinc ionophores block the replication of these viruses in cell culture. PLoS Pathog., 6 (11), e1001176.
134. Xu, X.; Liu, Y.; Weiss, S.; Arnold, E.; Sarafianos, S. G.; Ding, J., Molecular model of SARS coronavirus polymerase: implications for biochemical functions and drug design. Nucleic Acids Res., 2003, 31 (24), 7117-30.
135. Adedeji, A. O.; Singh, K.; Sarafianos, S. G., Structural and biochemical basis for the difference in the helicase activity of two different constructs of SARS-CoV helicase. Cell Mol. Biol., (Noisyle-grand) 58 (1), 114-21.
136. Adedeji, A. O.; Marchand, B.; Te Velthuis, A. J.; Snijder, E. J.; Weiss, S.; Eoff, R. L., et al., Mechanism of nucleic acid unwinding by SARS-CoV helicase. PLoS One 7 (5), e36521.
137. Bhardwaj, K.; Sun, J.; Holzenburg, A.; Guarino, L. A.; Kao, C. C., RNA recognition and cleavage by the SARS coronavirus endoribonuclease. J. Mol. Biol., 2006, 361 (2), 243-56.
138. Xu, X.; Zhai, Y.; Sun, F.; Lou, Z.; Su, D.; Xu, Y., et al., New antiviral target revealed by the hexameric structure of mouse hepatitis virus nonstructural protein nsp15. J. Virol., 2006, 80 (16), 7909-17.
139. Xu, L. H.; Huang, M.; Fang, S. G.; Liu, D. X., Coronavirus infection induces DNA replication stress partly through interaction of its nonstructural protein 13 with the p125 subunit of DNA polymerase delta. J. Biol. Chem., 286 (45), 39546-59.
140. Yu, M. S.; Lee, J.; Lee, J. M.; Kim, Y.; Chin, Y. W.; Jee, J. G., et al., Identification of myricetin and scutellarein as novel chemical inhibitors of the SARS coronavirus helicase, nsP13. Bioorg. Med. Chem. Lett., 22 (12), 4049-54.
141. Decroly, E.; Debarnot, C.; Ferron, F.; Bouvet, M.; Coutard, B.; Imbert, I., et al., Crystal structure and functional analysis of the SARS-coronavirus RNA cap 2'-O-methyltransferase nsp10/nsp16 complex. PLoS Pathog., 7 (5), e1002059.
142. Chen, Y.; Su, C.; Ke, M.; Jin, X.; Xu, L.; Zhang, Z., et al., Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 2'-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog., 7 (10), e1002294.
143. Bouvet, M.; Debarnot, C.; Imbert, I.; Selisko, B.; Snijder, E. J.; Canard, B., et al., In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog., 6 (4), e1000863.
144. Lugari, A.; Betzi, S.; Decroly, E.; Bonnaud, E.; Hermant, A.; Guillemot, J. C., et al., Molecular mapping of the RNA Cap 2'-O-methyltransferase activation interface between severe acute respiratory syndrome coronavirus nsp10 and nsp16. J. Biol. Chem., 285(43), 33230-41.
145. Ke, M.; Chen, Y.; Wu, A.; Sun, Y.; Su, C.; Wu, H., et al., Short peptides derived from the interaction domain of SARS coronavirus nonstructural protein nsp10 can suppress the 2'-O-methyltransferase activity of nsp10/nsp16 complex. Virus Res., 167 (2), 322-8.
146. Narayanan, K.; Huang, C.; Lokugamage, K.; Kamitani, W.; Ikegami, T.; Tseng, C. T., Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J. Virol., 2008, 82(9), 4471-4479.
147. Wathelet, M. G.; Orr, M.; Frieman, M. B.; Baric, R. S., Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J. Virol., 2007, 81(21), 11620-11633.
148. auregui, A. R.; Savalia, D.; Lowry, V. K.; Farrell, C. M.; Wathelet, M. G., Identification of Residues of SARS-CoV nsp1 That Differentially Affect Inhibition of Gene Expression and Antiviral Signaling. PLoS One, 8(4), e62416.
149. Carbajo-Lozoya, J.; Muller, M. A.; Kallies, S.; Thiel, V.; Drosten, C.; von Brunn, A., Replication of human coronaviruses SARS-CoV, HCoV-NL63 and HCoV-229E is inhibited by the drug FK506. Virus Res., 165 (1), 112-117.
150. no150/no Lokugamage, K. G.; Narayanan, K.; Huang, C.; Makino, S., Severe acute respiratory syndrome coronavirus protein nsp1 is a novel eukaryotic translation inhibitor that represses multiple steps of translation initiation. J. Virol., 86(24), 13598-13608.
151. no151/no Huang, C.; Lokugamage, K. G.; Rozovics, J. M.; Narayanan, K.; Semler, B. L.; Makino, S., SARS coronavirus nsp1 protein induces template-dependent endonucleolytic cleavage of mRNAs: viral mRNAs are resistant to nsp1-induced RNA cleavage. PLoS Pathog., 7 (12), e1002433.
152. no152/no Ma, X. Z.; Bartczak, A.; Zhang, J.; Khattar, R.; Chen, L.; Liu, M. F., et al., Proteasome inhibition in vivo promotes survival in a lethal murine model of severe acute respiratory syndrome. J. Virol., 84(23), 12419-28.
153. Plewczynski, D.; Hoffmann, M.; von Grotthuss, M.; Ginalski, K.; Rychewski, L., In silico prediction of SARS protease inhibitors by virtual high throughput screening. Chem. Biol. Drug Des., 2007, 69 (4), 269-279.
154. Lin, C. W.; Tsai, F. J.; Tsai, C. H.; Lai, C. C.; Wan, L.; Ho, T. Y., et al., Anti-SARS coronavirus 3C-like protease effects of Isatis indigotica root and plant-derived phenolic compounds. Antiviral Res., 2005, 68(1), 36-42.
155. Sievers, F.; Wilm, A.; Dineen, D.; Gibson, T. J.; Karplus, K.; Li, W., et al., Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 539.
156. Galtier, N.; Gouy, M.; Gautier, C., Seaview and Phylo_Win: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci., 1996, 12 (6), 543-8.