4uft Citations

Near-atomic cryo-EM structure of the helical measles virus nucleocapsid.

Abstract

Measles is a highly contagious human disease. We used cryo-electron microscopy and single particle-based helical image analysis to determine the 4.3 Å resolution structure of the helical nucleocapsid formed by the folded domain of the Measles Virus nucleoprotein encapsidating an RNA. The resulting pseudoatomic model of the Measles Virus nucleocapsid offers important insights into the mechanism of the helical polymerisation of nucleocapsids of negative-strand RNA viruses, in particular via the exchange subdomains of the nucleoprotein.The structure reveals the mode of the nucleoprotein-RNA interaction and explains why each nucleoprotein of Measles Virus binds six nucleotides whereas the Respiratory Syncytial Virus nucleoprotein binds seven. It provides a rational basis for further analysis of Measles Virus replication and transcription, and reveals potential targets for drug design.

Reviews - 4uft mentioned but not cited (1)

  1. The Nucleoprotein and Phosphoprotein of Measles Virus. Guseva S, Milles S, Blackledge M, Ruigrok RWH. Front Microbiol 10 1832 (2019)

Articles - 4uft mentioned but not cited (2)

  1. Self-Assembly of Measles Virus Nucleocapsid-like Particles: Kinetics and RNA Sequence Dependence. Milles S, Jensen MR, Communie G, Maurin D, Schoehn G, Ruigrok RW, Blackledge M. Angew. Chem. Int. Ed. Engl. 55 9356-9360 (2016)
  2. Assembly and cryo-EM structures of RNA-specific measles virus nucleocapsids provide mechanistic insight into paramyxoviral replication. Desfosses A, Milles S, Jensen MR, Guseva S, Colletier JP, Maurin D, Schoehn G, Gutsche I, Ruigrok RWH, Blackledge M. Proc. Natl. Acad. Sci. U.S.A. (2019)


Reviews citing this publication (22)

  1. Computational modelling of flavivirus dynamics: The ins and outs. Huber RG, Marzinek JK, Boon PLS, Yue W, Bond PJ. Methods 185 28-38 (2021)
  2. Structural insights into RNA polymerases of negative-sense RNA viruses. Te Velthuis AJW, Grimes JM, Fodor E. Nat Rev Microbiol (2021)
  3. Epitranscriptomic marks: Emerging modulators of RNA virus gene expression. Netzband R, Pager CT. Wiley Interdiscip Rev RNA 11 e1576 (2020)
  4. Negri bodies and other virus membrane-less replication compartments. Nevers Q, Albertini AA, Lagaudrière-Gesbert C, Gaudin Y. Biochim Biophys Acta Mol Cell Res 1867 118831 (2020)
  5. Nucleocapsid Structure of Negative Strand RNA Virus. Luo M, Terrell JR, Mcmanus SA. Viruses 12 (2020)
  6. Receptor-mediated cell entry of paramyxoviruses: Mechanisms, and consequences for tropism and pathogenesis. Navaratnarajah CK, Generous AR, Yousaf I, Cattaneo R. J Biol Chem 295 2771-2786 (2020)
  7. Solid-State NMR for Studying the Structure and Dynamics of Viral Assemblies. Lecoq L, Fogeron ML, Meier BH, Nassal M, Böckmann A. Viruses 12 (2020)
  8. Bipartite promoters and RNA editing of paramyxoviruses and filoviruses. le Mercier P, Kolakofsky D. RNA 25 279-285 (2019)
  9. Virus-Receptor Interactions: Structural Insights For Oncolytic Virus Development. Jayawardena N, Burga LN, Poirier JT, Bostina M. Oncolytic Virother 8 39-56 (2019)
  10. Measles virus: Background and oncolytic virotherapy. Bhattacharjee S, Yadava PK. Biochem Biophys Rep 13 58-62 (2018)
  11. Modulation of Measles Virus NTAIL Interactions through Fuzziness and Sequence Features of Disordered Binding Sites. Bignon C, Troilo F, Gianni S, Longhi S. Biomolecules 9 (2018)
  12. Electron Cryomicroscopy of Viruses at Near-Atomic Resolutions. Kaelber JT, Hryc CF, Chiu W. Annu Rev Virol 4 287-308 (2017)
  13. How order and disorder within paramyxoviral nucleoproteins and phosphoproteins orchestrate the molecular interplay of transcription and replication. Longhi S, Bloyet LM, Gianni S, Gerlier D. Cell. Mol. Life Sci. 74 3091-3118 (2017)
  14. Multiscale molecular dynamics simulation approaches to the structure and dynamics of viruses. Huber RG, Marzinek JK, Holdbrook DA, Bond PJ. Prog. Biophys. Mol. Biol. 128 121-132 (2017)
  15. Polymerases of paramyxoviruses and pneumoviruses. Fearns R, Plemper RK. Virus Res. 234 87-102 (2017)
  16. Structure and organization of paramyxovirus particles. Cox RM, Plemper RK. Curr Opin Virol 24 105-114 (2017)
  17. Dissecting Virus Infectious Cycles by Cryo-Electron Microscopy. Lee KK, Gui L. PLoS Pathog. 12 e1005625 (2016)
  18. Host-Pathogen Interactions in Measles Virus Replication and Anti-Viral Immunity. Jiang Y, Qin Y, Chen M. Viruses 8 (2016)
  19. Organization, Function, and Therapeutic Targeting of the Morbillivirus RNA-Dependent RNA Polymerase Complex. Sourimant J, Plemper RK. Viruses 8 (2016)
  20. The principle of conformational signaling. Tompa P. Chem Soc Rev 45 4252-4284 (2016)
  21. Towards a structural understanding of RNA synthesis by negative strand RNA viral polymerases. Reguera J, Gerlach P, Cusack S. Curr. Opin. Struct. Biol. 36 75-84 (2016)
  22. Structural disorder within paramyxoviral nucleoproteins. Longhi S. FEBS Lett. 589 2649-2659 (2015)

Articles citing this publication (37)

  1. Crystal Structure of the Measles Virus Nucleoprotein Core in Complex with an N-Terminal Region of Phosphoprotein. Guryanov SG, Liljeroos L, Kasaragod P, Kajander T, Butcher SJ. J. Virol. 90 2849-2857 (2016)
  2. A Druggable Pocket at the Nucleocapsid/Phosphoprotein Interaction Site of Human Respiratory Syncytial Virus. Ouizougun-Oubari M, Pereira N, Tarus B, Galloux M, Lassoued S, Fix J, Tortorici MA, Hoos S, Baron B, England P, Desmaële D, Couvreur P, Bontems F, Rey FA, Eléouët JF, Sizun C, Slama-Schwok A, Duquerroy S. J. Virol. 89 11129-11143 (2015)
  3. Measles virus nucleo- and phosphoproteins form liquid-like phase-separated compartments that promote nucleocapsid assembly. Guseva S, Milles S, Jensen MR, Salvi N, Kleman JP, Maurin D, Ruigrok RWH, Blackledge M. Sci Adv 6 eaaz7095 (2020)
  4. Nucleocapsid assembly in pneumoviruses is regulated by conformational switching of the N protein. Renner M, Bertinelli M, Leyrat C, Paesen GC, Saraiva de Oliveira LF, Huiskonen JT, Grimes JM. Elife 5 e12627 (2016)
  5. Modulation of Re-initiation of Measles Virus Transcription at Intergenic Regions by PXD to NTAIL Binding Strength. Bloyet LM, Brunel J, Dosnon M, Hamon V, Erales J, Gruet A, Lazert C, Bignon C, Roche P, Longhi S, Gerlier D. PLoS Pathog. 12 e1006058 (2016)
  6. Structure and assembly of the Ebola virus nucleocapsid. Wan W, Kolesnikova L, Clarke M, Koehler A, Noda T, Becker S, Briggs JAG. Nature 551 394-397 (2017)
  7. Structural Disorder within Paramyxoviral Nucleoproteins and Phosphoproteins in Their Free and Bound Forms: From Predictions to Experimental Assessment. Habchi J, Longhi S. Int J Mol Sci 16 15688-15726 (2015)
  8. Cryo-EM structure of the Ebola virus nucleoprotein-RNA complex at 3.6 Å resolution. Sugita Y, Matsunami H, Kawaoka Y, Noda T, Wolf M. Nature 563 137-140 (2018)
  9. Promotion of virus assembly and organization by the measles virus matrix protein. Ke Z, Strauss JD, Hampton CM, Brindley MA, Dillard RS, Leon F, Lamb KM, Plemper RK, Wright ER. Nat Commun 9 1736 (2018)
  10. The structurally disordered paramyxovirus nucleocapsid protein tail domain is a regulator of the mRNA transcription gradient. Cox RM, Krumm SA, Thakkar VD, Sohn M, Plemper RK. Sci Adv 3 e1602350 (2017)
  11. A key role for the carboxy-terminal tail of the murine coronavirus nucleocapsid protein in coordination of genome packaging. Kuo L, Koetzner CA, Masters PS. Virology 494 100-107 (2016)
  12. Comparison of the efficiency of different newcastle disease virus reverse genetics systems. Liu H, de Almeida RS, Gil P, Albina E. J. Virol. Methods 249 111-116 (2017)
  13. An ultraweak interaction in the intrinsically disordered replication machinery is essential for measles virus function. Milles S, Jensen MR, Lazert C, Guseva S, Ivashchenko S, Communie G, Maurin D, Gerlier D, Ruigrok RWH, Blackledge M. Sci Adv 4 eaat7778 (2018)
  14. Binding of RNA by the Nucleoproteins of Influenza Viruses A and B. Labaronne A, Swale C, Monod A, Schoehn G, Crépin T, Ruigrok RW. Viruses 8 (2016)
  15. Releasing the Genomic RNA Sequestered in the Mumps Virus Nucleocapsid. Severin C, Terrell JR, Zengel JR, Cox R, Plemper RK, He B, Luo M. J. Virol. 90 10113-10119 (2016)
  16. Structural characterization by transmission electron microscopy and immunoreactivity of recombinant Hendra virus nucleocapsid protein expressed and purified from Escherichia coli. Pearce LA, Yu M, Waddington LJ, Barr JA, Scoble JA, Crameri GS, McKinstry WJ. Protein Expr Purif 116 19-29 (2015)
  17. Synthesis of human parainfluenza virus 2 nucleocapsid protein in yeast as nucleocapsid-like particles and investigation of its antigenic structure. Bulavaitė A, Lasickienė R, Vaitiekaitė A, Sasnauskas K, Žvirblienė A. Appl. Microbiol. Biotechnol. 100 4523-4534 (2016)
  18. The Unstructured Paramyxovirus Nucleocapsid Protein Tail Domain Modulates Viral Pathogenesis through Regulation of Transcriptase Activity. Thakkar VD, Cox RM, Sawatsky B, da Fontoura Budaszewski R, Sourimant J, Wabbel K, Makhsous N, Greninger AL, von Messling V, Plemper RK. J. Virol. 92 (2018)
  19. The glutamic residue at position 402 in the C-terminus of Newcastle disease virus nucleoprotein is critical for the virus. Yu X, Cheng J, He Z, Li C, Song Y, Xue J, Yang H, Zhang R, Zhang G. Sci Rep 7 17471 (2017)
  20. A Polyamide Inhibits Replication of Vesicular Stomatitis Virus by Targeting RNA in the Nucleocapsid. Gumpper RH, Li W, Castañeda CH, Scuderi MJ, Bashkin JK, Luo M. J. Virol. 92 (2018)
  21. Extensive editing of cellular and viral double-stranded RNA structures accounts for innate immunity suppression and the proviral activity of ADAR1p150. Pfaller CK, Donohue RC, Nersisyan S, Brodsky L, Cattaneo R. PLoS Biol. 16 e2006577 (2018)
  22. Measles Virus Forms Inclusion Bodies with Properties of Liquid Organelles. Zhou Y, Su JM, Samuel CE, Ma D. J. Virol. 93 (2019)
  23. Structural Description of the Nipah Virus Phosphoprotein and Its Interaction with STAT1. Jensen MR, Yabukarski F, Communie G, Condamine E, Mas C, Volchkova V, Tarbouriech N, Bourhis JM, Volchkov V, Blackledge M, Jamin M. Biophys J 118 2470-2488 (2020)
  24. Structural dissection of human metapneumovirus phosphoprotein using small angle x-ray scattering. Renner M, Paesen GC, Grison CM, Granier S, Grimes JM, Leyrat C. Sci Rep 7 14865 (2017)
  25. A paramyxovirus-like model for Ebola virus bipartite promoters. Gutsche I, le Mercier P, Kolakofsky D. PLoS Pathog 16 e1008972 (2020)
  26. Bipartite interface of the measles virus phosphoprotein X domain with the large polymerase protein regulates viral polymerase dynamics. Du Pont V, Jiang Y, Plemper RK. PLoS Pathog. 15 e1007995 (2019)
  27. Complementary Mutations in the N and L Proteins for Restoration of Viral RNA Synthesis. Li W, Gumpper RH, Uddin Y, Schmidt-Krey I, Luo M. J. Virol. 92 (2018)
  28. High resolution cryo-EM structure of the helical RNA-bound Hantaan virus nucleocapsid reveals its assembly mechanisms. Arragain B, Reguera J, Desfosses A, Gutsche I, Schoehn G, Malet H. Elife 8 (2019)
  29. In vitro trackable assembly of RNA-specific nucleocapsids of the respiratory syncytial virus. Gao Y, Cao D, Ahn HM, Swain A, Hill S, Ogilvie C, Kurien M, Rahmatullah T, Liang B. J. Biol. Chem. 295 883-895 (2020)
  30. On the helical arrangements of protein molecules. Dauter Z, Jaskolski M. Protein Sci. 27 643-652 (2018)
  31. Regulation of measles virus gene expression by P protein coiled-coil properties. Bloyet LM, Schramm A, Lazert C, Raynal B, Hologne M, Walker O, Longhi S, Gerlier D. Sci Adv 5 eaaw3702 (2019)
  32. Self-capping of nucleoprotein filaments protects the Newcastle disease virus genome. Song X, Shan H, Zhu Y, Hu S, Xue L, Chen Y, Ding W, Niu T, Gu J, Ouyang S, Shen QT, Liu ZJ. Elife 8 (2019)
  33. The control of paramyxovirus genome hexamer length and mRNA editing. Matsumoto Y, Ohta K, Kolakofsky D, Nishio M. RNA 24 461-467 (2018)
  34. The effects of codon usage on the formation of secondary structures of nucleocapsid protein of peste des petits ruminants virus. Ma XX, Wang YN, Cao XA, Li XR, Liu YS, Zhou JH, Cai XP. Genes Genomics 40 905-912 (2018)
  35. The structure of the nucleoprotein of Influenza D shows that all Orthomyxoviridae nucleoproteins have a similar NPCORE, with or without a NPTAIL for nuclear transport. Donchet A, Oliva J, Labaronne A, Tengo L, Miloudi M, C A Gerard F, Mas C, Schoehn G, W H Ruigrok R, Ducatez M, Crépin T. Sci Rep 9 600 (2019)
  36. Unusual, stable replicating viruses generated from mumps virus cDNA clones. Bamford C, Wignall-Fleming E, Sreenu VB, Randall R, Duprex P, Rima B. PLoS ONE 14 e0219168 (2019)
  37. Viral evolution identifies a regulatory interface between paramyxovirus polymerase complex and nucleocapsid that controls replication dynamics. Sourimant J, Thakkar VD, Cox RM, Plemper RK. Sci Adv 6 eaaz1590 (2020)