Coronavirus non-structural protein 16: Evasion, attenuation, and possible treatments

Virus Research

Volumn 194, Issue , 2014, Pages 191-199

  Menachery, Vineet D ^a   Debbink, Kari ^a,b   Baric, Ralph S ^a,b  

^a IL   (United States)

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

Author keywords

2'O Methyl transferase; 2'O MTase; CoV; MDA5; NSP16; SARS CoV

Indexed keywords

2' O METHYLTRANSFERASE; AURINTRICARBOXYLIC ACID; INTERFERON; LIVE VACCINE; MESSENGER RNA; METHYLTRANSFERASE; NONSTRUCTURAL PROTEIN 16; RNA VACCINE; S ADENOSYLHOMOCYSTEINE; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; SINEFUNGIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRAL PROTEIN;

ANTIVIRAL ACTIVITY; CATALYSIS; CORONAVIRUS; CORONAVIRUS INFECTION; DRUG EFFICACY; DRUG TARGETING; ENZYME ACTIVITY; HUMAN; IN VITRO STUDY; INFECTION PREVENTION; INNATE IMMUNITY; MOLECULAR RECOGNITION; NONHUMAN; PATHOGENESIS; REVIEW; RNA CAPPING; SARS CORONAVIRUS; VIRUS ATTENUATION; VIRUS CELL INTERACTION; VIRUS IMMUNITY; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE; ENZYMOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; PHYSIOLOGY; VIROLOGY;

CORONAVIRUS; SARS CORONAVIRUS;

CORONAVIRUS INFECTIONS; HUMANS; METHYLTRANSFERASES; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; SARS VIRUS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84920574962     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.09.009     Document Type: Review

References (57)

1. Almazan F., Dediego M.L., Galan C., Escors D., Alvarez E., Ortego J., Sola I., Zuniga S., Alonso S., Moreno J.L., Nogales A., Capiscol C., Enjuanes L. Construction of a severe acute respiratory syndrome coronavirus infectious cDNA clone and a replicon to study coronavirus RNA synthesis. J. Virol. 2006, 80(21):10900-10906.
2. Becker M.M., Graham R.L., Donaldson E.F., Rockx B., Sims A.C., Sheahan T., Pickles R.J., Corti D., Johnston R.E., Baric R.S., Denison M.R. Synthetic recombinant bat SARS-like coronavirus is infectious in cultured cells and in mice. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(50):19944-19949.
3. Bolles M., Deming D., Long K., Agnihothram S., Whitmore A., Ferris M., Funkhouser W., Gralinski L., Totura A., Heise M., Baric R.S. A double-inactivated severe acute respiratory syndrome coronavirus vaccine provides incomplete protection in mice and induces increased eosinophilic proinflammatory pulmonary response upon challenge. J. Virol. 2011, 85(23):12201-12215.
4. Bouvet M., Debarnot C., Imbert I., Selisko B., Snijder E.J., Canard B., Decroly E. In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog. 2010, 6(4):e1000863.
5. Butchi N.B., Hinton D.R., Stohlman S.A., Kapil P., Fensterl V., Sen G.C., Bergmann C.C. Ifit2 deficiency results in uncontrolled neurotropic coronavirus replication and enhanced encephalitis via impaired alpha/beta interferon induction in macrophages. J. Virol. 2014, 88(2):1051-1064.
6. Chen Y., Cai H., Pan J., Xiang N., Tien P., Ahola T., Guo D. Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(9):3484-3489.
7. Chen Y., Su C., Ke M., Jin X., Xu L., Zhang Z., Wu A., Sun Y., Yang Z., Tien P., Ahola T., Liang Y., Liu X., Guo D. Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 2'-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog. 2011, 7(10):e1002294.
8. Corman V.M., Eckerle I., Bleicker T., Zaki A., Landt O., Eschbach-Bludau M., van Boheemen S., Gopal R., Ballhause M., Bestebroer T.M., Muth D., Muller M.A., Drexler J.F., Zambon M., Osterhaus A.D., Fouchier R.M., Drosten C. Detection of a novel human coronavirus by real-time reverse-transcription polymerase chain reaction. Euro Surveill. 2012, 17(39).
9. Daffis S., Szretter K.J., Schriewer J., Li J., Youn S., Errett J., Lin T.Y., Schneller S., Zust R., Dong H., Thiel V., Sen G.C., Fensterl V., Klimstra W.B., Pierson T.C., Buller R.M., Gale M., Shi P.Y., Diamond M.S. 2'-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 2010, 468(7322):452-456.
10. Debarnot C., Imbert I., Ferron F., Gluais L., Varlet I., Papageorgiou N., Bouvet M., Lescar J., Decroly E., Canard B. Crystallization and diffraction analysis of the SARS coronavirus nsp10-nsp16 complex. Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 2011, 67(Pt 3):404-408.
11. Decroly E., Debarnot C., Ferron F., Bouvet M., Coutard B., Imbert I., Gluais L., Papageorgiou N., Sharff A., Bricogne G., Ortiz-Lombardia M., Lescar J., Canard B. Crystal structure and functional analysis of the SARS-coronavirus RNA cap 2'-O-methyltransferase nsp10/nsp16 complex. PLoS Pathog. 2011, 7(5):e1002059.
12. Decroly E., Ferron F., Lescar J., Canard B. Conventional and unconventional mechanisms for capping viral mRNA. Nature reviews. Microbiology 2012, 10(1):51-65.
13. Decroly E., Imbert I., Coutard B., Bouvet M., Selisko B., Alvarez K., Gorbalenya A.E., Snijder E.J., Canard B. Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-2'O)-methyltransferase activity. J. Virol. 2008, 82(16):8071-8084.
14. Diamond M.S. IFIT1: a dual sensor and effector molecule that detects non-2'-O methylated viral RNA and inhibits its translation. Cytokine Growth Factor Rev. 2014, 10.1016/j.cytogfr.2014.05.002.
15. Donaldson E.F., Sims A.C., Deming D.J., Baric R.S. Mutational analysis of MHV-A59 replicase protein-nsp10. Adv. Exp. Med. Biol. 2006, 581:61-66.
16. Dong H., Zhang B., Shi P.Y. Flavivirus methyltransferase: a novel antiviral target. Antiviral Res. 2008, 80(1):1-10.
17. Edgar R., Domrachev M., Lash A.E. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30(1):207-210.
18. Feder M., Pas J., Wyrwicz L.S., Bujnicki J.M. Molecular phylogenetics of the RrmJ/fibrillarin superfamily of ribose 2'-O-methyltransferases. Gene 2003, 302(1-2):129-138.
19. Fensterl V., Wetzel J.L., Sen G.C. The interferon-induced protein, Ifit2, protects mice from infection of the peripheral nervous system by Vesicular stomatitis virus. J. Virol. 2014, 88(18):10303-10311. 10.1128/JVI.01341-14.
20. Fett C., DeDiego M.L., Regla-Nava J.A., Enjuanes L., Perlman S. Complete protection against severe acute respiratory syndrome coronavirus-mediated lethal respiratory disease in aged mice by immunization with a mouse-adapted virus lacking E protein. J. Virol. 2013, 87(12):6551-6559.
21. Frieman M.B., Chen J., Morrison T.E., Whitmore A., Funkhouser W., Ward J.M., Lamirande E.W., Roberts A., Heise M., Subbarao K., Baric R.S. SARS-CoV pathogenesis is regulated by a STAT1 dependent but a type I, II and III interferon receptor independent mechanism. PLoS Pathog. 2010, 6(4):e1000849.
22. Ge X.Y., Li J.L., Yang X.L., Chmura A.A., Zhu G., Epstein J.H., Mazet J.K., 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. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 2013, 503(7477):535-538.
23. Graham R.L., Becker M.M., Eckerle L.D., Bolles M., Denison M.R., Baric R.S. A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nat. Med. 2012, 18(12):1820-1826.
24. Graham R.L., Donaldson E.F., Baric R.S. A decade after SARS: strategies for controlling emerging coronaviruses. Nat. Rev. Microbiol. 2013, 11(12):836-848.
25. Habjan M., Hubel P., Lacerda L., Benda C., Holze C., Eberl C.H., Mann A., Kindler E., Gil-Cruz C., Ziebuhr J., Thiel V., Pichlmair A. Sequestration by IFIT1 impairs translation of 2'O-unmethylated capped RNA. PLoS Pathog. 2013, 9(10):e1003663.
26. He B., Zhang Y., Xu L., Yang W., Yang F., Feng Y., Xia L., Zhou J., Zhen W., Feng Y., Guo H., Zhang H., Tu C. Identification of diverse alphacoronaviruses and genomic characterization of a novel severe acute respiratory syndrome-like coronavirus from bats in china. J. Virol. 2014, 88(12):7070-7082.
27. He R., Adonov A., Traykova-Adonova M., Cao J., Cutts T., Grudesky E., Deschambaul Y., Berry J., Drebot M., Li X. Potent and selective inhibition of SARS coronavirus replication by aurintricarboxylic acid. Biochem. Biophys. Res. Commun. 2004, 320(4):1199-1203.
28. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., Schlee M., Endres S., Hartmann G. 5'-Triphosphate RNA is the ligand for RIG-I. Science 2006, 314(5801):994-997.
29. Huang Y.W., Dickerman A.W., Pineyro P., Li L., Fang L., Kiehne R., Opriessnig T., Meng X.J. Origin, evolution, and genotyping of emergent porcine epidemic diarrhea virus strains in the United States. MBio 2013, 4(5). e00737-00713.
30. Hyde J.L., Gardner C.L., Kimura T., White J.P., Liu G., Trobaugh D.W., Huang C., Tonelli M., Paessler S., Takeda K., Klimstra W.B., Amarasinghe G.K., Diamond M.S. A viral RNA structural element alters host recognition of nonself RNA. Science 2014, 343(6172):783-787.
31. Imbert I., Snijder E.J., Dimitrova M., Guillemot J.C., Lecine P., Canard B. The SARS-Coronavirus PLnc domain of nsp3 as a replication/transcription scaffolding protein. Virus Res. 2008, 133(2):136-148.
32. 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.
33. Ivanov K.A., Ziebuhr J. Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5'-triphosphatase activities. J. Virol. 2004, 78(14):7833-7838.
34. Josset L., Menachery V.D., Gralinski L.E., Agnihothram S., Sova P., Carter V.S., Yount B.L., Graham R.L., Baric R.S., Katze M.G. Cell host response to infection with novel human coronavirus EMC predicts potential antivirals and important differences with SARS coronavirus. MBio 2013, 4(3). e00165-00113.
35. Ke M., Chen Y., Wu A., Sun Y., Su C., Wu H., Jin X., Tao J., Wang Y., Ma X., Pan J.A., Guo D. 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. 2012, 167(2):322-328.
36. Kim W.K., Jain D., Sanchez M.D., Koziol-White C.J., Matthews K., Ge M.Q., Haczku A., Panettieri R.A., Frieman M.B., Lopez C.B. Deficiency of melanoma differentiation-associated protein 5 results in exacerbated chronic postviral lung inflammation. Am. J. Respir. Crit. Care Med. 2014, 189(4):437-448.
37. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J.H., Wang H., Crameri G., Hu Z., Zhang H., Zhang J., McEachern J., Field H., Daszak P., Eaton B.T., Zhang S., Wang L.-F. Bats are natural reservoirs of SARS-like coronaviruses. Science 2005, 310(5748):676-679.
38. Lugari A., Betzi S., Decroly E., Bonnaud E., Hermant A., Guillemot J.C., Debarnot C., Borg J.P., Bouvet M., Canard B., Morelli X., Lecine P. Molecular mapping of the RNA Cap 2'-O-methyltransferase activation interface between severe acute respiratory syndrome coronavirus nsp10 and nsp16. J. Biol. Chem. 2010, 285(43):33230-33241.
39. Ma Y., Wei Y., Zhang X., Zhang Y., Cai H., Zhu Y., Shilo K., Oglesbee M., Krakowka S., Whelan S.P., Li J. mRNA cap methylation influences pathogenesis of vesicular stomatitis virus in vivo. J. Virol. 2014, 88(5):2913-2926.
40. Martin J.L., McMillan F.M. SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol. 2002, 12(6):783-793.
41. Menachery V.D., Eisfeld A.J., Schafer A., Josset L., Sims A.C., Proll S., Fan S., Li C., Neumann G., Tilton S.C., Chang J., Gralinski L.E., Long C., Green R., Williams C.M., Weiss J., Matzke M.M., Webb-Robertson B.J., Schepmoes A.A., Shukla A.K., Metz T.O., Smith R.D., Waters K.M., Katze M.G., Kawaoka Y., Baric R.S. Pathogenic influenza viruses and coronaviruses utilize similar and contrasting approaches to control interferon-stimulated gene responses. MBio 2014, 5(3). e01174-01114.
42. Menachery V.D., Yount B.L., Josset L., Gralinski L.E., Scobey T., Agnihothram S., Katze M.G., Baric R.S. Attenuation and restoration of severe acute respiratory syndrome coronavirus mutant lacking 2'-o-methyltransferase activity. J. Virol. 2014, 88(8):4251-4264.
43. Myong S., Cui S., Cornish P.V., Kirchhofer A., Gack M.U., Jung J.U., Hopfner K.P., Ha T. Cytosolic viral sensor RIG-I is a 5'-triphosphate-dependent translocase on double-stranded RNA. Science 2009, 323(5917):1070-1074.
44. Nicholls J., Dong X.-P., Jiang G., Peiris M. SARS: clinical virology and pathogenesis. Respirology 2003, 8(Suppl.):6-8.
45. Page C., Goicochea L., Matthews K., Zhang Y., Klover P., Holtzman M.J., Hennighausen L., Frieman M. Induction of alternatively activated macrophages enhances pathogenesis during severe acute respiratory syndrome coronavirus infection. J. Virol. 2012, 86(24):13334-13349.
46. Pan J., Peng X., Gao Y., Li Z., Lu X., Chen Y., Ishaq M., Liu D., Dediego M.L., Enjuanes L., Guo D. Genome-wide analysis of protein-protein interactions and involvement of viral proteins in SARS-CoV replication. PLoS ONE 2008, 3(10):e3299.
47. Perlman S., Netland J. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 2009, 7(6):439-450.
48. Pichlmair A., Lassnig C., Eberle C.A., Gorna M.W., Baumann C.L., Burkard T.R., Burckstummer T., Stefanovic A., Krieger S., Bennett K.L., Rulicke T., Weber F., Colinge J., Muller M., Superti-Furga G. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat. Immunol. 2011, 12(7):624-630.
49. Sawicki S.G., Sawicki D.L., Younker D., Meyer Y., Thiel V., Stokes H., Siddell S.G. Functional and genetic analysis of coronavirus replicase-transcriptase proteins. PLoS Pathog. 2005, 1(4):e39.
50. Sheahan T., Morrison T.E., Funkhouser W., Uematsu S., Akira S., Baric R.S., Heise M.T. MyD88 is required for protection from lethal infection with a mouse-adapted SARS-CoV. PLoS Pathog. 2008, 4(12):e1000240.
51. Sheahan T., Whitmore A., Long K., Ferris M., Rockx B., Funkhouser W., Donaldson E., Gralinski L., Collier M., Heise M., Davis N., Johnston R., Baric R.S. Successful vaccination strategies that protect aged mice from lethal challenge from influenza virus and heterologous severe acute respiratory syndrome coronavirus. J. Virol. 2011, 85(1):217-230.
52. Sims A.C., Tilton S.C., Menachery V.D., Gralinski L.E., Schafer A., Matzke M.M., Webb-Robertson B.J., Chang J., Luna M.L., Long C.E., Shukla A.K., Bankhead A.R., Burkett S.E., Zornetzer G., Tseng C.T., Metz T.O., Pickles R., McWeeney S., Smith R.D., Katze M.G., Waters K.M., Baric R.S. Release of severe acute respiratory syndrome coronavirus nuclear import block enhances host transcription in human lung cells. J. Virol. 2013, 87(7):3885-3902.
53. Snijder E.J., Bredenbeek P.J., Dobbe J.C., Thiel V., Ziebuhr J., Poon L.L., Guan Y., Rozanov M., Spaan W.J., Gorbalenya A.E. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol. 2003, 331(5):991-1004.
54. von Grotthuss M., Wyrwicz L.S., Rychlewski L. mRNA cap-1 methyltransferase in the SARS genome. Cell 2003, 113(6):701-702.
55. Zhang Y., Wei Y., Zhang X., Cai H., Niewiesk S., Li J. Rational design of human metapneumovirus live attenuated vaccine candidates by inhibiting viral messenger RNA cap methyltransferase. J. Virol. 2014, 88(19):11411-11429. 10.1128/JVI.00876-14.
56. Zust R., Cervantes-Barragan L., Habjan M., Maier R., Neuman B.W., Ziebuhr J., Szretter K.J., Baker S.C., Barchet W., Diamond M.S., Siddell S.G., Ludewig B., Thiel V. 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. 2011, 12(2):137-143.
57. Zust R., Dong H., Li X.F., Chang D.C., Zhang B., Balakrishnan T., Toh Y.X., Jiang T., Li S.H., Deng Y.Q., Ellis B.R., Ellis E.M., Poidinger M., Zolezzi F., Qin C.F., Shi P.Y., Fink K. Rational design of a live attenuated dengue vaccine: 2'O-methyl-transferase mutants are highly attenuated and immunogenic in mice and macaques. PLoS Pathog. 2013, 9(8):e1003521.