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Noncatalytic ions direct the RNA-dependent RNA polymerase of bacterial double-stranded RNA virus ϕ6 from de novo initiation to elongation.

Wright S, Poranen MM, Bamford DH, Stuart DI, Grimes JM
J Virol 86 2837-49 (2012)
Related entries: 4a8f, 4a8k, 4a8m, 4a8o, 4a8q, 4a8w, 4a8y

Cited: 26 times
EuropePMC logo PMID: 22205747

Abstract

RNA-dependent RNA polymerases (RdRps) are key to the replication of RNA viruses. A common divalent cation binding site, distinct from the positions of catalytic ions, has been identified in many viral RdRps. We have applied biochemical, biophysical, and structural approaches to show how the RdRp from bacteriophage ϕ6 uses the bound noncatalytic Mn(2+) to facilitate the displacement of the C-terminal domain during the transition from initiation to elongation. We find that this displacement releases the noncatalytic Mn(2+), which must be replaced for elongation to occur. By inserting a dysfunctional Mg(2+) at this site, we captured two nucleoside triphosphates within the active site in the absence of Watson-Crick base pairing with template and mapped movements of divalent cations during preinitiation. These structures refine the pathway from preinitiation through initiation to elongation for the RNA-dependent RNA polymerization reaction, explain the role of the noncatalytic divalent cation in 6 RdRp, and pinpoint the previously unresolved Mn(2+)-dependent step in replication.

Reviews - 4a8s mentioned but not cited (1)

  1. Cystoviral RNA-directed RNA polymerases: Regulation of RNA synthesis on multiple time and length scales. Alphonse S, Ghose R. Virus Res 234 135-152 (2017)

Articles - 4a8s mentioned but not cited (2)

  1. Noncatalytic ions direct the RNA-dependent RNA polymerase of bacterial double-stranded RNA virus ϕ6 from de novo initiation to elongation. Wright S, Poranen MM, Bamford DH, Stuart DI, Grimes JM. J Virol 86 2837-2849 (2012)
  2. Evidence for a non-catalytic ion-binding site in multiple RNA-dependent RNA polymerases. Mönttinen HA, Ravantti JJ, Poranen MM. PLoS One 7 e40581 (2012)


Reviews citing this publication (3)

  1. RNA Dependent RNA Polymerases: Insights from Structure, Function and Evolution. Venkataraman S, Prasad BVLS, Selvarajan R. Viruses 10 E76 (2018)
  2. Common and unique features of viral RNA-dependent polymerases. te Velthuis AJ. Cell Mol Life Sci 71 4403-4420 (2014)
  3. Structural Studies of Bacteriophage Φ6 and Its Transformations during Its Life Cycle. Heymann JB. Viruses 15 2404 (2023)

Articles citing this publication (20)

  1. Molecular basis for nucleotide conservation at the ends of the dengue virus genome. Selisko B, Potisopon S, Agred R, Priet S, Varlet I, Thillier Y, Sallamand C, Debart F, Vasseur JJ, Canard B. PLoS Pathog 8 e1002912 (2012)
  2. Signatures of Nucleotide Analog Incorporation by an RNA-Dependent RNA Polymerase Revealed Using High-Throughput Magnetic Tweezers. Dulin D, Arnold JJ, van Laar T, Oh HS, Lee C, Perkins AL, Harki DA, Depken M, Cameron CE, Dekker NH. Cell Rep 21 1063-1076 (2017)
  3. Plate tectonics of virus shell assembly and reorganization in phage φ8, a distant relative of mammalian reoviruses. El Omari K, Sutton G, Ravantti JJ, Zhang H, Walter TS, Grimes JM, Bamford DH, Stuart DI, Mancini EJ. Structure 21 1384-1395 (2013)
  4. Backtracking behavior in viral RNA-dependent RNA polymerase provides the basis for a second initiation site. Dulin D, Vilfan ID, Berghuis BA, Poranen MM, Depken M, Dekker NH. Nucleic Acids Res 43 10421-10429 (2015)
  5. RNA-dependent RNA polymerase of Japanese encephalitis virus binds the initiator nucleotide GTP to form a mechanistically important pre-initiation state. Surana P, Satchidanandam V, Nair DT. Nucleic Acids Res 42 2758-2773 (2014)
  6. Initiation of RNA Polymerization and Polymerase Encapsidation by a Small dsRNA Virus. Collier AM, Lyytinen OL, Guo YR, Toh Y, Poranen MM, Tao YJ. PLoS Pathog 12 e1005523 (2016)
  7. Characterization of a nodavirus replicase revealed a de novo initiation mechanism of RNA synthesis and terminal nucleotidyltransferase activity. Wang Z, Qiu Y, Liu Y, Qi N, Si J, Xia X, Wu D, Hu Y, Zhou X. J Biol Chem 288 30785-30801 (2013)
  8. Factors affecting de novo RNA synthesis and back-priming by the respiratory syncytial virus polymerase. Noton SL, Aljabr W, Hiscox JA, Matthews DA, Fearns R. Virology 462-463 318-327 (2014)
  9. Probing, by self-assembly, the number of potential binding sites for minor protein subunits in the procapsid of double-stranded RNA bacteriophage Φ6. Sun X, Bamford DH, Poranen MM. J Virol 86 12208-12216 (2012)
  10. Temperature controlled high-throughput magnetic tweezers show striking difference in activation energies of replicating viral RNA-dependent RNA polymerases. Seifert M, van Nies P, Papini FS, Arnold JJ, Poranen MM, Cameron CE, Depken M, Dulin D. Nucleic Acids Res 48 5591-5602 (2020)
  11. Flock house virus RNA polymerase initiates RNA synthesis de novo and possesses a terminal nucleotidyl transferase activity. Wu W, Wang Z, Xia H, Liu Y, Qiu Y, Liu Y, Hu Y, Zhou X. PLoS One 9 e86876 (2014)
  12. Structure of a VP1-VP3 complex suggests how birnaviruses package the VP1 polymerase. Bahar MW, Sarin LP, Graham SC, Pang J, Bamford DH, Stuart DI, Grimes JM. J Virol 87 3229-3236 (2013)
  13. Annotating Protein Functional Residues by Coupling High-Throughput Fitness Profile and Homologous-Structure Analysis. Du Y, Wu NC, Jiang L, Zhang T, Gong D, Shu S, Wu TT, Sun R. mBio 7 e01801-16 (2016)
  14. The C-terminal priming domain is strongly associated with the main body of bacteriophage ϕ6 RNA-dependent RNA polymerase. Sarin LP, Wright S, Chen Q, Degerth LH, Stuart DI, Grimes JM, Bamford DH, Poranen MM. Virology 432 184-193 (2012)
  15. Hydrophobic and charged residues in the C-terminal arm of hepatitis C virus RNA-dependent RNA polymerase regulate initiation and elongation. Cherry AL, Dennis CA, Baron A, Eisele LE, Thommes PA, Jaeger J. J Virol 89 2052-2063 (2015)
  16. Structure of the RNA-directed RNA polymerase from the cystovirus φ12. Ren Z, C Franklin M, Ghose R. Proteins 81 1479-1484 (2013)
  17. Methyl Relaxation Measurements Reveal Patterns of Fast Dynamics in a Viral RNA-Directed RNA Polymerase. Alphonse S, Bhattacharya S, Wang H, Ghose R. Biochemistry 54 5828-5838 (2015)
  18. Controlled Disassembly and Purification of Functional Viral Subassemblies Using Asymmetrical Flow Field-Flow Fractionation (AF4). Eskelin K, Poranen MM. Viruses 10 E579 (2018)
  19. Single-molecule measurements of viral ssRNA packaging. Hanhijärvi KJ, Ziedaite G, Bamford DH, Hæggström E, Poranen MM. RNA 23 119-129 (2017)
  20. RNA-Dependent RNA Polymerase from Heterobasidion RNA Virus 6 Is an Active Replicase In Vitro. Levanova AA, Vainio EJ, Hantula J, Poranen MM. Viruses 13 1738 (2021)


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