Crystal structure of Middle East respiratory syndrome coronavirus helicase

PLoS Pathogens

Volumn 13, Issue 6, 2017, Pages

  Hao, Wei ^a   Wojdyla, Justyna Aleksandra ^b   Zhao, Rong ^a   Han, Ruiyun ^a   Das, Rajat ^c   Zlatev, Ivan ^c   Manoharan, Muthiah ^c   Wang, Meitian ^b   Cui, Sheng ^a  

^a INSTITUTE OF PATHOGEN BIOLOGY   (China)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c ALNYLAM PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; OLIGONUCLEOTIDE; SINGLE STRANDED RNA; DNA HELICASE;

ARTICLE; ATPASE ACTIVITY ASSAY; CENTRIFUGATION; CRYSTALLIZATION; DNA SEQUENCE; GENE SEQUENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HYDROLYSIS; MIDDLE EAST RESPIRATORY SYNDROME; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; SIZE EXCLUSION CHROMATOGRAPHY; CHEMISTRY; CORONAVIRUS INFECTION; ENZYMOLOGY; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; VIROLOGY;

CORONAVIRUS INFECTIONS; DNA HELICASES; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MODELS, MOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY;

EID: 85021844702     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006474     Document Type: Article

References (46)

1. Stadler K, Masignani V, Eickmann M, Becker S, Abrignani S, et al. (2003) SARS—beginning to understand a new virus. Nat Rev Microbiol1: 209–218. doi: 10.1038/nrmicro775 15035025
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 Med367: 1814–1820. doi: 10.1056/NEJMoa1211721 23075143
3. Kupferschmidt K, (2015) INFECTIOUS DISEASES. Amid panic, a chance to learn about MERS. Science348: 1183–1184. doi: 10.1126/science.348.6240.1183 26068815
4. Gorbalenya AE, Enjuanes L, Ziebuhr J, Snijder EJ, (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res117: 17–37. doi: 10.1016/j.virusres.2006.01.017 16503362
5. de Groot RJ, Cowley J.A., Enjuanes L,. (2012) Virus taxonomy: Elsevier Academic Press, Amsterdam.
6. Lauber C, Goeman JJ, Parquet Mdel C, Nga PT, Snijder EJ, et al. (2013) The footprint of genome architecture in the largest genome expansion in RNA viruses. PLoS Pathog9: e1003500. doi: 10.1371/journal.ppat.1003500 23874204
7. Lauber C, Ziebuhr J, Junglen S, Drosten C, Zirkel F, et al. (2012) Mesoniviridae: a proposed new family in the order Nidovirales formed by a single species of mosquito-borne viruses. Arch Virol157: 1623–1628. doi: 10.1007/s00705-012-1295-x 22527862
8. Adams MJ, King AM, Carstens EB, (2013) Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2013). Arch Virol158: 2023–2030. doi: 10.1007/s00705-013-1688-5 23580178
9. Perlman S, Netland J, (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol7: 439–450. doi: 10.1038/nrmicro2147 19430490
10. Cunha CB, Opal SM, (2014) Middle East respiratory syndrome (MERS): a new zoonotic viral pneumonia. Virulence5: 650–654. doi: 10.4161/viru.32077 25089913
11. Coleman CM, Frieman MB, (2014) Coronaviruses: important emerging human pathogens. J Virol88: 5209–5212. doi: 10.1128/JVI.03488-13 24600003
12. Thiel V, Ivanov KA, Putics A, Hertzig T, Schelle B, et al. (2003) Mechanisms and enzymes involved in SARS coronavirus genome expression. J Gen Virol84: 2305–2315. doi: 10.1099/vir.0.19424-0 12917450
13. Subissi L, Imbert I, Ferron F, Collet A, Coutard B, et al. (2014) SARS-CoV ORF1b-encoded nonstructural proteins 12–16: replicative enzymes as antiviral targets. Antiviral Res101: 122–130. doi: 10.1016/j.antiviral.2013.11.006 24269475
14. Subissi L, Posthuma CC, Collet A, Zevenhoven-Dobbe JC, Gorbalenya AE, et al. (2014) One severe acute respiratory syndrome coronavirus protein complex integrates processive RNA polymerase and exonuclease activities. Proc Natl Acad Sci U S A111: E3900–3909. doi: 10.1073/pnas.1323705111 25197083
15. Prentice E, McAuliffe J, Lu X, Subbarao K, Denison MR, (2004) Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J Virol78: 9977–9986. doi: 10.1128/JVI.78.18.9977-9986.2004 15331731
16. Singleton MR, Dillingham MS, Wigley DB, (2007) Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem76: 23–50. doi: 10.1146/annurev.biochem.76.052305.115300 17506634
17. Fairman-Williams ME, Guenther UP, Jankowsky E, (2010) SF1 and SF2 helicases: family matters. Curr Opin Struct Biol20: 313–324. doi: 10.1016/j.sbi.2010.03.011 20456941
18. Gorbalenya AE, Koonin EV, (1989) Viral proteins containing the purine NTP-binding sequence pattern. Nucleic Acids Res17: 8413–8440. 2555771
19. Jankowsky E, Fairman ME, (2007) RNA helicases—one fold for many functions. Curr Opin Struct Biol17: 316–324. doi: 10.1016/j.sbi.2007.05.007 17574830
20. Subramanya HS, Bird LE, Brannigan JA, Wigley DB, (1996) Crystal structure of a DExx box DNA helicase. Nature384: 379–383. doi: 10.1038/384379a0 8934527
21. Korolev S, Hsieh J, Gauss GH, Lohman TM, Waksman G, (1997) Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell90: 635–647. 9288744
22. Singleton MR, Wigley DB, (2002) Modularity and specialization in superfamily 1 and 2 helicases. J Bacteriol184: 1819–1826. doi: 10.1128/JB.184.7.1819-1826.2002 11889086
23. Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM, (1988) A novel superfamily of nucleoside triphosphate-binding motif containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett235: 16–24. 2841153
24. Cheng Z, Muhlrad D, Lim MK, Parker R, Song H, (2007) Structural and functional insights into the human Upf1 helicase core. EMBO J26: 253–264. doi: 10.1038/sj.emboj.7601464 17159905
25. Deng Z, Lehmann KC, Li X, Feng C, Wang G, et al. (2014) Structural basis for the regulatory function of a complex zinc-binding domain in a replicative arterivirus helicase resembling a nonsense-mediated mRNA decay helicase. Nucleic Acids Res42: 3464–3477. doi: 10.1093/nar/gkt1310 24369429
26. Chakrabarti S, Jayachandran U, Bonneau F, Fiorini F, Basquin C, et al. (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol Cell41: 693–703. doi: 10.1016/j.molcel.2011.02.010 21419344
27. Ziebuhr J, (2005) The coronavirus replicase. Curr Top Microbiol Immunol287: 57–94. 15609509
28. Lehmann KC, Snijder EJ, Posthuma CC, Gorbalenya AE, (2015) What we know but do not understand about nidovirus helicases. Virus Res202: 12–32. doi: 10.1016/j.virusres.2014.12.001 25497126
29. Ivanov KA, Thiel V, Dobbe JC, van der Meer Y, Snijder EJ, et al. (2004) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J Virol78: 5619–5632. doi: 10.1128/JVI.78.11.5619-5632.2004 15140959
30. Adedeji AO, Lazarus H, (2016) Biochemical Characterization of Middle East Respiratory Syndrome Coronavirus Helicase. mSphere1.
31. Adedeji AO, Marchand B, Te Velthuis AJ, Snijder EJ, Weiss S, et al. (2012) Mechanism of nucleic acid unwinding by SARS-CoV helicase. PLoS One7: e36521. doi: 10.1371/journal.pone.0036521 22615777
32. Seybert A, Posthuma CC, van Dinten LC, Snijder EJ, Gorbalenya AE, et al. (2005) A complex zinc finger controls the enzymatic activities of nidovirus helicases. J Virol79: 696–704. doi: 10.1128/JVI.79.2.696-704.2005 15613297
33. Zhang R, Li Y, Cowley TJ, Steinbrenner AD, Phillips JM, et al. (2015) The nsp1, nsp13, and M proteins contribute to the hepatotropism of murine coronavirus JHM.WU. J Virol89: 3598–3609. doi: 10.1128/JVI.03535-14 25589656
34. Clerici M, Mourao A, Gutsche I, Gehring NH, Hentze MW, et al. (2009) Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J28: 2293–2306. doi: 10.1038/emboj.2009.175 19556969
35. Seybert A, Hegyi A, Siddell SG, Ziebuhr J, (2000) The human coronavirus 229E superfamily 1 helicase has RNA and DNA duplex-unwinding activities with 5'-to-3' polarity. RNA6: 1056–1068. 10917600
36. Lee NR, Kwon HM, Park K, Oh S, Jeong YJ, et al. (2010) Cooperative translocation enhances the unwinding of duplex DNA by SARS coronavirus helicase nsP13. Nucleic Acids Res38: 7626–7636. doi: 10.1093/nar/gkq647 20671029
37. Wachter A, Hartmann L, (2014) NMD: nonsense-mediated defense. Cell Host Microbe16: 273–275. doi: 10.1016/j.chom.2014.08.015 25211070
38. Hu Z, Yan C, Liu P, Huang Z, Ma R, et al. (2013) Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science341: 172–175. doi: 10.1126/science.1236381 23765277
39. Zlatev I, Lackey JG, Zhang L, Dell A, McRae K, et al. (2013) Automated parallel synthesis of 5'-triphosphate oligonucleotides and preparation of chemically modified 5'-triphosphate small interfering RNA. Bioorg Med Chem21: 722–732. doi: 10.1016/j.bmc.2012.11.043 23260577
40. Zlatev I, Manoharan M, Vasseur JJ, Morvan F (2012) Solid-phase chemical synthesis of 5'-triphosphate DNA, RNA, and chemically modified oligonucleotides. Curr Protoc Nucleic Acid Chem Chapter 1: Unit1 28.
41. Vonrhein C, Blanc E, Roversi P, Bricogne G, (2007) Automated structure solution with autoSHARP. Methods Mol Biol364: 215–230. doi: 10.1385/1-59745-266-1:215 17172768
42. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr66: 486–501. doi: 10.1107/S0907444910007493 20383002
43. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr66: 213–221. doi: 10.1107/S0907444909052925 20124702
44. Cui S, Eisenacher K, Kirchhofer A, Brzozka K, Lammens A, et al. (2008) The C-terminal regulatory domain is the RNA 5'-triphosphate sensor of RIG-I. Mol Cell29: 169–179. doi: 10.1016/j.molcel.2007.10.032 18243112
45. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res32: 1792–1797. doi: 10.1093/nar/gkh340 15034147
46. Robert X, Gouet P, (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res42: W320–324. doi: 10.1093/nar/gku316 24753421