A chimeric virus-mouse model system for evaluating the function and inhibition of papain-like proteases of emerging coronaviruses

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 11825-11833

  Deng, Xufang ^a   Agnihothram, Sudhakar ^b   Mielech, Anna M ^a   Nichols, Daniel B ^a   Wilson, Michael W ^c   St John, Sarah E ^d   Larsen, Scott D ^c   Mesecar, Andrew D ^d   Lenschow, Deborah J ^e   Baric, Ralph S ^b   Baker, Susan C ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d PURDUE UNIVERSITY   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR; CELL PROTEIN; CYSTEINE; ENZYME INHIBITOR; GLYCOPROTEIN; PAPAIN; PAPAIN LIKE PROTEASE; PAPAIN LIKE PROTEASE INHIBITOR; PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; VIRUS ENZYME; PEPTIDE HYDROLASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOSAFETY; CATALYSIS; CHIMERA; CONTROLLED STUDY; CORONAVIRUS; CORONAVIRUS INFECTION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SUBSTRATE; GENE; GENE MUTATION; INTERFERON STIMULATED GENE 15; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SARS CORONAVIRUS; SINDBIS VIRUS; ANIMAL; CHLOROCEBUS AETHIOPS; DISEASE MODEL; ENZYMOLOGY; HAMSTER; METABOLISM; PHYSIOLOGY; VERO CELL LINE;

ANIMALS; CERCOPITHECUS AETHIOPS; CORONAVIRUS; CRICETINAE; DISEASE MODELS, ANIMAL; MICE; PAPAIN; PEPTIDE HYDROLASES; VERO CELLS;

EID: 84907429993     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01749-14     Document Type: Article

References (44)

1. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7:439-450. http://dx.doi.org/10.1038/nrmicro2147.
2. Song H-D, Tu C-C, Zhang G-W, Wang S-Y, Zheng K, Lei L-C, Chen Q-X, Gao Y-W, Zhou H-Q, Xiang H, Zheng H-J, Chern S-WW, Cheng F, Pan C-M, Xuan H, Chen S-J, Luo H-M, Zhou D-H, Liu Y-F, He J-F, Qin P-Z, Li L-H, Ren Y-Q, Liang W-J, Yu Y-D, Anderson L, Wang M, Xu R-H, Wu X-W, Zheng H-Y, Chen J-D, Liang G, Gao Y, Liao M, Fang L, Jiang L-Y, Li H, Chen F, Di B, He L-J, Lin J-Y, Tong S, Kong X, Du L, Hao P, Tang H, Bernini A, Yu X-J, Spiga O, Guo Z-M, Pan H-Y, He W-Z, Manuguerra J-C, Fontanet A, Danchin A, Niccolai N, Li Y-X, Wu C-I, Zhao G-P. 2005. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. U. S. A. 102:2430-2435. http://dx.doi.org/10.1073/pnas.0409608102.
3. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus ADME, Fouchier RAM. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367:1814-1820. http://dx.doi.org/10.1056/NEJMoa1211721.
4. Van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus ADME, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RAM. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. mBio 3:e00473-12. http://dx.doi.org/10.1128/mBio.00473-12.
5. Memish ZA, Cotten M, Meyer B, Watson SJ, Alsahafi AJ, Al Rabeeah AA, Corman VM, Sieberg A, Makhdoom HQ, Assiri A, Al Masri M, Aldabbagh S, Bosch B-J, Beer M, Müller MA, Kellam P, Drosten C. 2014. Human Infection with MERS coronavirus after exposure to infected camels, Saudi Arabia, 2013. Emerg. Infect. Dis. 20:1012-1015. http://dx.doi.org/10.3201/eid2006.140402.
6. Hemida MG, Chu DKW, Poon LLM, Perera RAPM, Alhammadi MA, Ng H-Y, Siu LY, Guan Y, Alnaeem A, Peiris M. 2014. MERS coronavirus in dromedary camel herd, Saudi Arabia. Infect. Dis. 20:1231-1234. http: //dx.doi.org/10.3201/eid2007.140571.
7. Azhar EI, El-Kafrawy SA, Farraj SA, Hassan AM, Al-Saeed MS, Hashem AM, Madani TA. 2014. Evidence for camel-to-human transmission of MERS coronavirus. N. Engl. J. Med. 370:2499-2505. http://dx.doi.org/10.1056/NEJMoa1401505.
8. Perera RA, Wang P, Gomaa MR, El-Shesheny R, Kandeil A, Bagato O, Siu LY, Shehata MM, Kayed AS, Moatasim Y, Li M, Poon LL, Guan Y, Webby RJ, Ali MA, Peiris JS, Kayali G. 2013. Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralisation assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Euro Surveill. 18:pii=20574. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20574.
9. Reusken CBEM, Haagmans BL, Müller MA, Gutierrez C, Godeke G-J, Meyer B, Muth D, Raj VS, Smits-De Vries L, Corman VM, Drexler J-F, Smits SL, El Tahir YE, De Sousa R, van Beek J, Nowotny N, van Maanen K, Hidalgo-Hermoso E, Bosch B-J, Rottier P, Osterhaus A, Gortázar-Schmidt C, Drosten C, Koopmans MPG. 2013. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect. Dis. 13:859-866. http://dx.doi.org/10.1016/S1473-3099(13)70164-6.
10. Memish ZA, Zumla AI, Al-Hakeem RF, Al-Rabeeah AA, Stephens GM. 2013. Family cluster of Middle East respiratory syndrome coronavirus infections. N. Engl. J. Med. 368:2487-2494. http://dx.doi.org/10.1056 /NEJMoa1303729.
11. Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA, Cummings DAT, Alabdullatif ZN, Assad M, Almulhim A, Makhdoom H, Madani H, Alhakeem R, Al-Tawfiq JA, Cotten M, Watson SJ, Kellam P, Zumla AI, Memish ZA. 2013. Hospital outbreak of Middle East respiratory syndrome coronavirus. N. Engl. J. Med. 369:407-416. http://dx.doi.org/10.1056/NEJMoa1306742.
12. Cotten M, Watson SJ, Kellam P, Al-Rabeeah AA, Makhdoom HQ, Assiri A, Al-Tawfiq JA, Alhakeem RF, Madani H, AlRabiah FA, Al Hajjar S, Al-Nassir WN, Albarrak A, Flemban H, Balkhy HH, Alsubaie S, Palser AL, Gall A, Bashford-Rogers R, Rambaut A, Zumla AI, Memish ZA. 2013. Transmission and evolution of the Middle East respiratory syndrome coronavirus in Saudi Arabia: a descriptive genomic study. Lancet 382:1993-2002. http://dx.doi.org/10.1016/S0140-6736(13) 61887-5.
13. Ratia K, Pegan S, Takayama J, Sleeman K, Coughlin M, Baliji S, Chaudhuri R, Fu W, Prabhakar BS, Johnson ME, Baker SC, Ghosh AK, Mesecar AD. 2008. A noncovalent class of papain-like protease/deubiquitinase inhibitors blocks SARS virus replication. Proc. Natl. Acad. Sci. U. S. A. 105:16119-16124. http://dx.doi.org/10.1073/pnas.0805240105.
14. Lindner HA, Fotouhi-Ardakani N, Lytvyn V, Lachance P, Sulea T, Ménard R. 2005. The papain-like protease from the severe acute respiratory syndrome coronavirus is a deubiquitinating enzyme. J. Virol. 79: 15199-15208. http://dx.doi.org/10.1128/JVI.79.24.15199-15208.2005.
15. Barretto N, Jukneliene D, Ratia K, Chen Z, Mesecar AD, Baker SC. 2005. The papain-like protease of severe acute respiratory syndrome coronavirus has deubiquitinating activity. J. Virol. 79:15189-15198. http://dx.doi.org/10.1128/JVI.79.24.15189-15198.2005.
16. Ratia K, Saikatendu KS, Santarsiero BD, Barretto N, Baker SC, Stevens RC, Mesecar AD. 2006. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc. Natl. Acad. Sci. U. S. A. 103:5717-5722. http://dx.doi.org/10.1073/pnas.0510851103.
17. Frieman M, Ratia K, Johnston RE, Mesecar AD, Baric RS. 2009. Severe acute respiratory syndrome coronavirus papain-like protease ubiquitinlike domain and catalytic domain regulate antagonism of IRF3 and NFkappaB signaling. J. Virol. 83:6689-6705. http://dx.doi.org/10.1128/JVI.02220-08.
18. Clementz M, Chen Z, Banach BS, Wang Y, Sun L, Ratia K, Baez-Santos YM, Wang J, Takayama J, Ghosh AK, Li K, Mesecar AD, Baker SC. 2010. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J. Virol. 84:4619-4629. http://dx.doi.org/10.1128/JVI.02406-09.
19. Ghosh AK, Takayama J, Rao KV, Ratia K, Chaudhuri R, Mulhearn DC, Lee H, Nichols DB, Baliji S, Baker SC, Johnson ME, Mesecar AD. 2010. Severe acute respiratory syndrome coronavirus papain-like novel protease inhibitors: design, synthesis, protein-ligand X-ray structure and biological evaluation. J. Med. Chem. 53:4968-4979. http://dx.doi.org/10.1021 /jm1004489.
20. Roberts A, Deming D, Paddock CD, Cheng A, Yount B, Vogel L, Herman BD, Sheahan T, Heise M, Genrich GL, Zaki SR, Baric R, Subbarao K. 2007. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog. 3:e5. http://dx.doi.org/10.1371/journal.ppat.0030005.
21. Day CW, Baric R, Cai SX, Frieman M, Kumaki Y, Morrey JD, Smee DF, Barnard DL. 2009. A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. Virology 395: 210-222. http://dx.doi.org/10.1016/j.virol.2009.09.023.
22. McCray PB, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L, Shi L, Netland J, Jia HP, Halabi C, Sigmund CD, Meyerholz DK, Kirby P, Look DC, Perlman S. 2007. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J. Virol. 81:813-821. http://dx.doi.org/10.1128/JVI.02012-06.
23. Tseng C-TK, Huang C, Newman P, Wang N, Narayanan K, Watts DM, Makino S, Packard MM, Zaki SR, Chan T-S, Peters CJ. 2007. Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human angiotensin-converting enzyme 2 virus receptor. J. Virol. 81: 1162-1173. http://dx.doi.org/10.1128/JVI.01702-06.
24. Munster VJ, de Wit E, Feldmann H. 2013. Pneumonia from human coronavirus in a macaque model. N. Engl. J. Med. 368:1560-1562. http: //dx.doi.org/10.1056/NEJMc1215691.
25. De Wit E, Rasmussen AL, Falzarano D, Bushmaker T, Feldmann F, Brining DL, Fischer ER, Martellaro C, Okumura A, Chang J, Scott D, Benecke AG, Katze MG, Feldmann H, Munster VJ. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 110:16598-16603. http://dx.doi.org/10.1073/pnas.1310744110.
26. Coleman CM, Matthews KL, Goicochea L, Frieman MB. 2013. Wild type and innate immune deficient mice are not susceptible to the Middle East Respiratory Syndrome Coronavirus. J. Gen. Virol. 95:408-412. http://dx.doi.org/10.1099/vir.0.060640-0.
27. De Wit E, Prescott J, Baseler L, Bushmaker T, Thomas T, Lackemeyer MG, Martellaro C, Milne-Price S, Haddock E, Haagmans BL, Feldmann H, Munster VJ. 2013. The Middle East respiratory syndrome coronavirus (MERS-CoV) does not replicate in Syrian hamsters. PLoS One 8:e69127. http://dx.doi.org/10.1371/journal.pone.0069127.
28. Raj VS, Mou H, Smits SL, Dekkers DHW, Müller MA, Dijkman R, Muth D, Demmers JAA, Zaki A, Fouchier RAM, Thiel V, Drosten C, Rottier PJM, Osterhaus ADME, Bosch BJ, Haagmans BL. 2013. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495:251-254. http://dx.doi.org/10.1038 /nature12005.
29. Zhao J, Li K, Wohlford-Lenane C, Agnihothram SS, Fett C, Zhao J, Gale MJ, Baric RS, Enjuanes L, Gallagher T, McCray PB, Perlman S. 2014. Rapid generation of a mouse model for Middle East respiratory syndrome. Proc. Natl. Acad. Sci. U. S. A. 111:4970-4975. http://dx.doi.org/10.1073 /pnas.1323279111.
30. Agnihothram S, Yount BL, Donaldson EF, Huynh J, Menachery VD, Gralinski LE, Graham RL, Becker MM, Tomar S, Scobey TD, Osswald HL, Whitmore A, Gopal R, Ghosh AK, Mesecar A, Zambon M, Heise M, Denison MR, Baric RS. 2014. A mouse model for Betacoronavirus subgroup 2c using a bat coronavirus strain HKU5 variant. mBio 5:e00047-14. http://dx.doi.org/10.1128/mBio.00047-14.
31. Frias-Staheli N, Giannakopoulos NV, Kikkert M, Taylor SL, Bridgen A, Paragas J, Richt JA, Rowland RR, Schmaljohn CS, Lenschow DJ, Snijder EJ, García-Sastre A, Virgin HW. 2007. Ovarian tumor domaincontaining viral proteases evade ubiquitin-and ISG15-dependent innate immune responses. Cell Host Microbe 2:404-416. http://dx.doi.org/10.1016/j.chom.2007.09.014.
32. Lenschow DJ, Giannakopoulos NV, Gunn LJ, Johnston C, Guin AKO, Schmidt RE, Levine B, Virgin HW, IV. 2005. Identification of interferonstimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79:13974-13983. http://dx.doi.org/10.1128/JVI.79.22.13974-13983.2005.
33. Skaug B, Chen ZJ. 2010. Emerging role of ISG15 in antiviral immunity. Cell 143:187-190. http://dx.doi.org/10.1016/j.cell.2010.09.033.
34. Nicholson B, Leach CA, Goldenberg SJ, Francis DM, Kodrasov MP, Tian X, Shanks J, Sterner DE, Bernal A, Mattern MR, Wilkinson KD, Butt TR. 2008. Characterization of ubiquitin and ubiquitin-like-protein isopeptidase activities. Protein Sci. 17:1035-1043. http://dx.doi.org/10.1110/ps.083450408.
35. Kilianski A, Mielech A, Deng X, Baker SC. 2013. Assessing activity and inhibition of MERS-CoV papain-like and 3C-like proteases using luciferase-based biosensors. J. Virol. 87:11955-11962. http://dx.doi.org/10.1128/JVI.02105-13.
36. Baez-Santos YM, Barraza SJ, Wilson MW, Agius M, Mielech AM, Davis NM, Baker SC, Larsen SD, Mesecar AD. 2014. X-Ray structural and biological evaluation of a series of potent and highly selective inhibitors of human coronavirus papain-like proteases. J. Med. Chem. 57:2393-2412. http://dx.doi.org/10.1021/jm401712t.
37. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, Osiak A, Levine B, Schmidt RE, Garci A, Leib DA, Pekosz A, Knobeloch K, Horak I, Whiting HV, IV. 2007. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. U. S. A. 104:1371-1376. http://dx.doi.org/10.1073/pnas.0607038104.
38. Ma X-Z, Bartczak A, Zhang J, He W, Shalev I, Smil D, Chen L, Phillips J, Feld JJ, Selzner N, Levy G, McGilvray I. 2014. Protein interferonstimulated gene 15 conjugation delays but does not overcome coronavirus proliferation in a model of fulminant hepatitis. J. Virol. 88:6195-6204. http://dx.doi.org/10.1128/JVI.03801-13.
39. Cong X-L, Lo M-C, Reuter BA, Yan M, Fan J-B, Zhang D-E. 2012. Usp18 promotes conventional CD11b+ dendritic cell development. J. Immunol. 188:4776-4781. http://dx.doi.org/10.4049/jimmunol.1101609.
40. Lu G, Hu Y, Wang Q, Qi J, Gao F, Li Y, Zhang Y, Zhang W, Yuan Y, Bao J, Zhang B, Shi Y, Yan J, Gao GF. 2013. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500:227-231. http://dx.doi.org/10.1038/nature12328.
41. Chen Y, Rajashankar KR, Yang Y, Agnihothram SS, Liu C, Lin Y-L, Baric RS, Li F. 2013. Crystal structure of the receptor-binding domain from newly emerged Middle East respiratory syndrome coronavirus. J. Virol. 87:10777-10783. http://dx.doi.org/10.1128/JVI.01756-13.
42. Fouchier RAM, Hartwig NG, Bestebroer TM, Niemeyer B, de Jong JC, Simon JH, Osterhaus ADME. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. U. S. A. 101:6212-6216. http://dx.doi.org/10.1073/pnas.0400762101.
43. Van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJM, Wolthers KC, Wertheim-van Dillen PME, Kaandorp J, Spaargaren J, Berkhout B. 2004. Identification of a new human coronavirus. Nat. Med. 10:368-373. http://dx.doi.org/10.1038/nm1024.
44. Woo PCY, Lau SKP, Chu C, Chan K, Tsoi H, Huang Y, Wong BHL, Poon RWS, Cai JJ, Luk W, Poon LLM, Wong SSY, Guan Y, Peiris JSM, Yuen K. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895. http://dx.doi.org/10.1128/JVI.79.2.884-895.2005.