Murine coronavirus ubiquitin-like domain is important for papain-like protease stability and viral pathogenesis

Journal of Virology

Volumn 89, Issue 9, 2015, Pages 4907-4917

  Mielech, Anna M ^a   Deng, Xufang ^a   Chen, Yafang ^b   Kindler, Eveline ^c,d   Wheeler, Dorthea L ^e   Mesecar, Andrew D ^b   Thiel, Volker ^c,d   Perlman, Stanley ^e   Baker, Susan C ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b PURDUE UNIVERSITY   (United States)

^c Federal Institute of Virology and Immunology   (Switzerland)

^d UNIVERSITY OF BERN   (Switzerland)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 3; PAPAIN LIKE PROTEASE; PROTEINASE; UNCLASSIFIED DRUG; MUTANT PROTEIN; PEPTIDE HYDROLASE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STABILITY; FEMALE; HIGH TEMPERATURE; MALE; MOUSE; MURINE HEPATITIS CORONAVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; REVERSE GENETICS; TEMPERATURE SENSITIVITY; THERMOSTABILITY; UBIQUITIN LIKE DOMAIN; VIRUS ATTENUATION; VIRUS INACTIVATION; VIRUS MUTANT; VIRUS MUTATION; VIRUS PATHOGENESIS; VIRUS PLAQUE; VIRUS REPLICATION; VIRUS VIRULENCE; WILD TYPE; ANIMAL; ANIMAL HEPATITIS; C57BL MOUSE; CHEMISTRY; CORONAVIRUS INFECTION; ENZYMOLOGY; METABOLISM; MURINE HEPATITIS VIRUS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; TEMPERATURE; VIROLOGY;

CORONAVIRUS; MURINAE; MURINE HEPATITIS VIRUS; MUS;

ANIMALS; CORONAVIRUS INFECTIONS; DNA MUTATIONAL ANALYSIS; ENZYME STABILITY; FEMALE; HEPATITIS, VIRAL, ANIMAL; MICE, INBRED C57BL; MURINE HEPATITIS VIRUS; MUTANT PROTEINS; PEPTIDE HYDROLASES; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE; VIRUS REPLICATION;

EID: 84928549771     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00338-15     Document Type: Article

References (59)

1. Peiris JS, Guan Y, Yuen KY. 2004. Severe acute respiratory syndrome. Nat Med 10:S88-S97. http://dx.doi.org/10.1038/nm1143.
2. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 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.
3. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad SciUSA 102:14040-14045. http://dx.doi.org/10.1073/pnas.0506735102.
4. Poon LL, Chu DK, Chan KH, Wong OK, Ellis TM, Leung YH, Lau SK, Woo PC, Suen KY, Yuen KY, Guan Y, Peiris JS. 2005. Identification of a novel coronavirus in bats. J Virol 79:2001-2009. http://dx.doi.org/10.1128/JVI.79.4.2001-2009.2005.
5. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev 7:439-450. http://dx.doi.org/10.1038/nrmicro2147.
6. Dominguez SR, O'Shea TJ, Oko LM, Holmes KV. 2007. Detection of group 1 coronaviruses in bats in North America. Emerg Infect Dis 13: 1295-1300. http://dx.doi.org/10.3201/eid1309.070491.
7. Woo PC, Lau SK, Huang Y, Yuen KY. 2009. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med 234:1117-1127. http://dx.doi.org/10.3181/0903-MR-94.
8. Ge X-Y, Li J-L, Yang X-L, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang Y-J, Luo C-M, Tan B, Wang N, Zhu Y, Crameri G, Zhang S-Y, Wang L-F, Daszak P, Shi Z-L. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:535-538. http://dx.doi.org/10.1038/nature12711.
9. Briese T, Mishra N, Jain K, Zalmout IS, Jabado OJ, Karesh WB, Daszak P, Mohammed OB, Alagaili AN, Lipkin WI. 2014. Middle East respiratory syndrome coronavirus quasispecies that include homologues of human isolates revealed through whole-genome analysis and virus cultured from dromedary camels in Saudi Arabia. mBio 5:e01146-14. http://dx.doi.org/10.1128/mBio.01146-14.
10. Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA, Cummings DA, 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, KSA MERS-CoV Investigation Team. 2013. Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med 369(5):407-416. http://dx.doi.org/10.1056/NEJMoa1306742.
11. Guery B, Poissy J, El Mansouf L, Sejourne C, Ettahar N, Lemaire X, Vuotto F, Goffard A, Behillil S, Enouf V, Caro V, Mailles A, Che D, Manuguerra JC, Mathieu D, Fontanet A, van der Werf S, MERS-CoV Study Group. 2013. Clinical features and viral diagnosis of two cases of infection with Middle East respiratory syndrome coronavirus: a report of nosocomial transmission. Lancet 381:2265-2272. http://dx.doi.org/10.1016/S0140-6736(13)60982-4.
12. Cotten M, Watson SJ, Zumla AI, Makhdoom HQ, Palser AL, Ong SH, Al Rabeeah AA, Alhakeem RF, Assiri A, Al-Tawfiq JA, Albarrak A, Barry M, Shibl A, Alrabiah FA, Hajjar S, Balkhy HH, Flemban H, Rambaut A, Kellam P, Memish ZA. 2014. Spread, circulation, and evolution of the Middle East respiratory syndrome coronavirus. mBio 5:e01062-13. http://dx.doi.org/10.1128/mBio.01062-13.
13. Chiu SS, Chan KH, Chu KW, Kwan SW, Guan Y, Poon LL, Peiris JS. 2005. Human coronavirus NL63 infection and other coronavirus infections in children hospitalized with acute respiratory disease in Hong Kong, China. Clin Infect Dis 40:1721-1729. http://dx.doi.org/10.1086/430301.
14. Esper F, Weibel C, Ferguson D, Landry ML, Kahn JS. 2006. Coronavirus HKU1 infection in the United States. Emerg Infect Dis 12:775-779. http://dx.doi.org/10.3201/eid1205.051316.
15. Van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, 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.
16. Vabret A, Mourez T, Gouarin S, Petitjean J, Freymuth F. 2003. An outbreak of coronavirus OC43 respiratory infection in Normandy, France. Clin Infect Dis 36:985-989. http://dx.doi.org/10.1086/374222.
17. Lau SK, Li KS, Tsang AK, Lam CS, Ahmed S, Chen H, Chan KH, Woo PC, Yuen KY. 2013. Genetic characterization of betacoronavirus lineage C viruses in bats reveals marked sequence divergence in the spike protein of pipistrellus bat coronavirus HKU5 in Japanese pipistrelle: implications for the origin of the novel Middle East respiratory syndrome coronavirus. J Virol 87:8638-8650. http://dx.doi.org/10.1128/JVI.01055-13.
18. Mielech AM, Chen Y, Mesecar AD, Baker SC. 2014. Nidovirus papainlike proteases: multifunctional enzymes with protease, deubiquitinating and deISGylating activities. Virus Res 194:184-190. http://dx.doi.org/10.1016/j.virusres.2014.01.025.
19. Weiss SR, Leibowitz JL. 2011. Coronavirus pathogenesis. Adv Virus Res 81:85-164. http://dx.doi.org/10.1016/B978-0-12-385885-6.00009-2.
20. Hurst KR, Ye R, Goebel SJ, Jayaraman P, Masters PS. 2010. An interaction between the nucleocapsid protein and a component of the replicase-transcriptase complex is crucial for the infectivity of coronavirus genomic RNA. J Virol 84:10276-10288. http://dx.doi.org/10.1128/JVI.01287-10.
21. Hurst KR, Koetzner CA, Masters PS. 2013. Characterization of a critical interaction between the coronavirus nucleocapsid protein and nonstructural protein 3 of the viral replicase-transcriptase complex. J Virol 87: 9159-9172. http://dx.doi.org/10.1128/JVI.01275-13.
22. Ziebuhr J, Thiel V, Gorbalenya AE. 2001. The autocatalytic release of a putative RNA virus transcription factor from its polyprotein precursor involves two paralogous papain-like proteases that cleave the same peptide bond. J Biol Chem 276:33220-33232. http://dx.doi.org/10.1074/jbc. M104097200.
23. Graham RL, Denison MR. 2006. Replication of murine hepatitis virus is regulated by papain-like proteinase 1 processing of nonstructural proteins 1, 2, and 3. J Virol 80:11610-11620. http://dx.doi.org/10.1128/JVI.01428-06.
24. Kanjanahaluethai A, Baker SC. 2000. Identification of mouse hepatitis virus papain-like proteinase 2 activity. J Virol 74:7911-7921. http://dx.doi.org/10.1128/JVI.74.17.7911-7921.2000.
25. Lindner HA, Fotouhi-Ardakani N, Lytvyn V, Lachance P, Sulea T, Menard 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.
26. 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.
27. Clementz MA, 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.
28. Devaraj SG, Wang N, Chen Z, Tseng M, Barretto N, Lin R, Peters CJ, Tseng CT, Baker SC, Li K. 2007. Regulation of IRF-3-dependent innate immunity by the papain-like protease domain of the severe acute respiratory syndrome coronavirus. J Biol Chem 282:32208-32221. http://dx.doi.org/10.1074/jbc. M704870200.
29. 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.
30. Mielech AM, Kilianski A, Baez-Santos YM, Mesecar AD, Baker SC. 2014. MERS-CoV papain-like protease has deISGylating and deubiquitinating activities. Virology 450-451:64-70. http://dx.doi.org/10.1016/j.virol.2013.11.040.
31. Xing Y, Chen J, Tu J, Zhang B, Chen X, Shi H, Baker SC, Feng L, Chen Z. 2013. The papain-like protease of porcine epidemic diarrhea virus negatively regulates type I interferon pathway by acting as a viral deubiquitinase. J Gen Virol 94:1554-1567. http://dx.doi.org/10.1099/vir.0.051169-0.
32. Yang H, Yang M, Ding Y, Liu Y, Lou Z, Zhou Z, Sun L, Mo L, Ye S, Pang H, Gao GF, Anand K, Bartlam M, Hilgenfeld R, Rao Z. 2003. The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc Natl Acad Sci USA 100: 13190-13195. http://dx.doi.org/10.1073/pnas.1835675100.
33. Zheng D, Chen G, Guo B, Cheng G, Tang H. 2008. PLP2, a potent deubiquitinase from murine hepatitis virus, strongly inhibits cellular type I interferon production. Cell Res 18:1105-1113. http://dx.doi.org/10.1038/cr.2008.294.
34. Frieman M, Basu D, Matthews K, Taylor J, Jones G, Pickles R, Baric R, Engel DA. 2011. Yeast based small molecule screen for inhibitors of SARS-CoV. PLoS One 6:e28479. http://dx.doi.org/10.1371/journal.pone.0028479.
35. 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 USA 105:16119-16124. http://dx.doi.org/10.1073/pnas.0805240105.
36. 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 USA 103:5717-5722. http://dx.doi.org/10.1073/pnas.0510851103.
37. Lei J, Mesters JR, Drosten C, Anemüller S, Ma Q, Hilgenfeld R. 2014. Crystal structure of the papain-like protease of MERS coronavirus reveals unusual, potentially druggable active-site features. Antiviral Res 109:72-82. http://dx.doi.org/10.1016/j.antiviral.2014.06.011.
38. Yount B, Denison MR, Weiss SR, Baric RS. 2002. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J Virol 76:11065-11078. http://dx.doi.org/10.1128/JVI.76.21.11065-11078.2002.
39. Kilianski A, Mielech AM, Deng X, Baker SC. 2013. Assessing activity and inhibition of Middle East respiratory syndrome coronavirus papain-like and 3C-like proteases using luciferase-based biosensors. J Virol 87:11955-11962. http://dx.doi.org/10.1128/JVI.02105-13.
40. Yount B, Curtis KM, Fritz EA, Hensley LE, Jahrling PB, Prentice E, Denison MR, Geisbert TW, Baric RS. 2003. Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. Proc Natl Acad Sci USA 100:12995-13000. http://dx.doi.org/10.1073/pnas.1735582100.
41. Báez-Santos YM, Barraza SJ, Wilson MW, Agius MP, 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.
42. Zhu X, Ménard R, Sulea T. 2007. High incidence of ubiquitin-like domains in human ubiquitin-specific proteases. Proteins 69:1-7. http://dx.doi.org/10.1002/prot.21546.
43. Faesen AC, Luna-Vargas MPA, Sixma TK. 2012. The role of UBL domains in ubiquitin-specific proteases. Biochem Soc Trans 40:539-545. http://dx.doi.org/10.1042/BST20120004.
44. Hu M, Li P, Song L, Jeffrey PD, Chenova TA, Wilkinson KD, Cohen RE, Shi Y. 2005. Structure and mechanisms of the proteasome-associated deubiquitinating enzyme USP14. EMBO J 24:3747-3756. http://dx.doi.org/10.1038/sj.emboj.7600832.
45. Faesen AC, Dirac AMG, Shanmugham A, Ovaa H, Perrakis A, Sixma TK. 2011. Mechanism of USP7/HAUSP activation by its C-terminal ubiquitin-like domain and allosteric regulation by GMP-synthetase. Mol Cell 44:147-159. http://dx.doi.org/10.1016/j.molcel.2011.06.034.
46. Zhao L, Jha BK, Wu A, Elliott R, Ziebuhr J, Gorbalenya AE, Silverman RH, Weiss SR. 2012. Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe 11:607-616. http://dx.doi.org/10.1016/j.chom.2012.04.011.
47. Zhao L, Rose KM, Elliott R, Van Rooijen N, Weiss SR. 2011. Cell-typespecific type I interferon antagonism influences organ tropism of murine coronavirus. J Virol 85:10058-10068. http://dx.doi.org/10.1128/JVI.05075-11.
48. Zhang R, Li Y, Cowley TJ, Steinbrenner A, Phillips JM, Yount BL, Baric RS, Weiss SR. 14 January 2015. The nsp1, nsp13, andMproteins contribute to the hepatotropism of murine coronavirus JHM.WU. J Virol http://dx.doi.org/10.1128/JVI.03535-14.
49. Bailey-Elkin BA, Knaap RCM, Johnson GG, Dalebout TJ, Ninaber DK, van Kasteren PB, Bredenbeek PJ, Snijder EJ, Kikkert M, Mark BL. 2014. Crystal structure of the Middle East respiratory syndrome coronavirus (MERS-CoV) papain-like protease bound to ubiquitin facilitates targeted disruption of deubiquitinating activity to demonstrate its role in innate immune suppression. J Biol Chem 289:34667-34682. http://dx.doi.org/10.1074/jbc. M114.609644.
50. Van Kasteren PB, Bailey-Elkin BA, James TW, Ninaber DK, Beugeling C, Khajehpour M, Snijder EJ, Mark BL, Kikkert M. 2013. Deubiquitinase function of arterivirus papain-like protease 2 suppresses the innate immune response in infected host cells. Proc Natl Acad Sci USA 110: E838-E847. http://dx.doi.org/10.1073/pnas.1218464110.
51. Lei L, Ying S, Baojun L, Yi Y, Xiang H, Wenli S, Zounan S, Deyin G, Qingyu Z, Jingmei L, Guohui C. 2013. Attenuation of mouse hepatitis virus by deletion of the LLRKxGxKG region of Nsp1. PLoS One 8:e61166. http://dx.doi.org/10.1371/journal.pone.0061166.
52. Zust R, Cervantes-Barragan L, Kuri T, Blakqori G, Weber F, Ludewig B, Thiel V. 2007. Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog 3:e109. http://dx.doi.org/10.1371/journal.ppat.0030109.
53. Wathelet MG, Orr M, Frieman MB, Baric RS. 2007. Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81:11620-11633. http://dx.doi.org/10.1128/JVI.00702-07.
54. Eriksson KK, Cervantes-Barragán L, Ludewig B, Thiel V. 2008. Mouse hepatitis virus liver pathology is dependent on ADP-ribose-1″-phosphatase, a viral function conserved in the alpha-like supergroup. J Virol 82:12325-12334. http://dx.doi.org/10.1128/JVI.02082-08.
55. Kuri T, Eriksson KK, Putics A, Züst R, Snijder EJ, Davidson AD, Siddell SG, Thiel V, Ziebuhr J, Weber F. 2011. The ADP-ribose-1″-monophosphatase domains of severe acute respiratory syndrome coronavirus and human coronavirus 229E mediate resistance to antiviral interferon responses. J Gen Virol 92:1899-1905. http://dx.doi.org/10.1099/vir.0.031856-0.
56. Fehr AR, Athmer J, Channappanavar R, Phillips JM, Meyerholz DK, Perlman S. 2015. The NSP3 macrodomain promotes virulence in mice with coronavirus-induced encephalitis. J Virol 89:1523-1536. http://dx.doi.org/10.1128/JVI.02596-14.
57. Graham RL, Becker MM, Eckerle LD, Bolles M, Denison MR, Baric RS. 2012. A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nat Med 18:1820-1826. http://dx.doi.org/10.1038/nm.2972.
58. Zust R, Cervantes-Barragan L, Habjan M, Maier R, Neuman BW, Ziebuhr J, Szretter KJ, Baker SC, Barchet W, Diamond MS, Siddell SG, Ludewig B, Thiel V. 2011. Ribose 2'-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat Immunol 12:137-143. http://dx.doi.org/10.1038/ni.1979.
59. Menachery VD, Yount BL, Josset L, Gralinski LE, Scobey T, Agnihothram S, Katze MG, Baric RS. 2014. Attenuation and restoration of SARS-CoV mutant lacking 2' O methyltransferase activity. J Virol 88: 4251-4264. http://dx.doi.org/10.1128/JVI.03571-13.