1sh2 › Citations

Crystal structure of norwalk virus polymerase reveals the carboxyl terminus in the active site cleft.

Ng KK, Pendás-Franco N, Rojo J, Boga JA, Machín A, Alonso JM, Parra F
J Biol Chem 279 16638-45 (2004)
Related entries: 1sh0, 1sh3

Cited: 88 times
EuropePMC logo PMID: 14764591

Abstract

Norwalk virus is a major cause of acute gastroenteritis for which effective treatments are sorely lacking. To provide a basis for the rational design of novel antiviral agents, the main replication enzyme in Norwalk virus, the virally encoded RNA-dependent RNA polymerase (RdRP), has been expressed in an enzymatically active form, and its structure has been crystallographically determined both in the presence and absence of divalent metal cations. Although the overall fold of the enzyme is similar to that seen previously in the RdRP from rabbit hemorrhagic disease virus, the carboxyl terminus, surprisingly, is located in the active site cleft in five independent copies of the protein in three distinct crystal forms. The location of this carboxyl-terminal segment appears to interfere with the binding of double-stranded RNA in the active site cleft and may play a role in the initiation of RNA synthesis or mediate interactions with accessory replication proteins.

Reviews - 1sh2 mentioned but not cited (2)

  1. Antiviral targets of human noroviruses. Prasad BV, Shanker S, Muhaxhiri Z, Deng L, Choi JM, Estes MK, Song Y, Palzkill T, Atmar RL. Curr Opin Virol 18 117-125 (2016)
  2. Recent Advances in the Discovery of Norovirus Therapeutics. Kim Y, Galasiti Kankanamalage AC, Chang KO, Groutas WC. J Med Chem 58 9438-9450 (2015)

Articles - 1sh2 mentioned but not cited (1)

  1. RNA-Dependent RNA Polymerases of Both Virulent and Benign Rabbit Caliciviruses Induce Striking Rearrangement of Golgi Membranes. Urakova N, Strive T, Frese M. PLoS One 12 e0169913 (2017)


Reviews citing this publication (22)

  1. The epidemiologic and clinical importance of norovirus infection. Atmar RL, Estes MK. Gastroenterol Clin North Am 35 275-90, viii (2006)
  2. Noroviruses everywhere: has something changed? Estes MK, Prasad BV, Atmar RL. Curr Opin Infect Dis 19 467-474 (2006)
  3. Structure-function relationships among RNA-dependent RNA polymerases. Ng KK, Arnold JJ, Cameron CE. Curr Top Microbiol Immunol 320 137-156 (2008)
  4. Norovirus protein structure and function. Hardy ME. FEMS Microbiol Lett 253 1-8 (2005)
  5. The flavivirus polymerase as a target for drug discovery. Malet H, Massé N, Selisko B, Romette JL, Alvarez K, Guillemot JC, Tolou H, Yap TL, Vasudevan S, Lescar J, Canard B. Antiviral Res 80 23-35 (2008)
  6. A Structure-Function Diversity Survey of the RNA-Dependent RNA Polymerases From the Positive-Strand RNA Viruses. Jia H, Gong P. Front Microbiol 10 1945 (2019)
  7. RNA synthetic mechanisms employed by diverse families of RNA viruses. McDonald SM. Wiley Interdiscip Rev RNA 4 351-367 (2013)
  8. Role of motif B loop in allosteric regulation of RNA-dependent RNA polymerization activity. Garriga D, Ferrer-Orta C, Querol-Audí J, Oliva B, Verdaguer N. J Mol Biol 425 2279-2287 (2013)
  9. Fidelity Variants and RNA Quasispecies. Bordería AV, Rozen-Gagnon K, Vignuzzi M. Curr Top Microbiol Immunol 392 303-322 (2016)
  10. Structure and function of RNA replication. Ortín J, Parra F. Annu Rev Microbiol 60 305-326 (2006)
  11. Antiviral strategies to control calicivirus infections. Rohayem J, Bergmann M, Gebhardt J, Gould E, Tucker P, Mattevi A, Unge T, Hilgenfeld R, Neyts J. Antiviral Res 87 162-178 (2010)
  12. Structure(s), function(s), and inhibition of the RNA-dependent RNA polymerase of noroviruses. Deval J, Jin Z, Chuang YC, Kao CC. Virus Res 234 21-33 (2017)
  13. A structural view of the RNA-dependent RNA polymerases from the Flavivirus genus. Lu G, Gong P. Virus Res 234 34-43 (2017)
  14. Packaging of Genomic RNA in Positive-Sense Single-Stranded RNA Viruses: A Complex Story. Comas-Garcia M. Viruses 11 E253 (2019)
  15. Calicivirus RNA-Dependent RNA Polymerases: Evolution, Structure, Protein Dynamics, and Function. Smertina E, Urakova N, Strive T, Frese M. Front Microbiol 10 1280 (2019)
  16. Viruses in Rodent Colonies: Lessons Learned from Murine Noroviruses. Karst SM, Wobus CE. Annu Rev Virol 2 525-548 (2015)
  17. Human Norovirus Proteins: Implications in the Replicative Cycle, Pathogenesis, and the Host Immune Response. Campillay-Véliz CP, Carvajal JJ, Avellaneda AM, Escobar D, Covián C, Kalergis AM, Lay MK. Front Immunol 11 961 (2020)
  18. The uncoupling of catalysis and translocation in the viral RNA-dependent RNA polymerase. Shu B, Gong P. RNA Biol 14 1314-1319 (2017)
  19. Structure and Function of Caliciviral RNA Polymerases. Lee JH, Chung MS, Kim KH. Viruses 9 E329 (2017)
  20. Current tools for norovirus drug discovery. Weerasekara S, Prior AM, Hua DH. Expert Opin Drug Discov 11 529-541 (2016)
  21. Structural organization of viral RNA-dependent RNA polymerases. Shatskaya GS, Dmitrieva TM. Biochemistry (Mosc) 78 231-235 (2013)
  22. Calicivirus Non-structural Proteins: Potential Functions in Replication and Host Cell Manipulation. Smertina E, Hall RN, Urakova N, Strive T, Frese M. Front Microbiol 12 712710 (2021)

Articles citing this publication (63)

  1. Crystal structure of the dengue virus RNA-dependent RNA polymerase catalytic domain at 1.85-angstrom resolution. Yap TL, Xu T, Chen YL, Malet H, Egloff MP, Canard B, Vasudevan SG, Lescar J. J Virol 81 4753-4765 (2007)
  2. Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. Thompson AA, Peersen OB. EMBO J 23 3462-3471 (2004)
  3. Genetic and Epidemiologic Trends of Norovirus Outbreaks in the United States from 2013 to 2016 Demonstrated Emergence of Novel GII.4 Recombinant Viruses. Cannon JL, Barclay L, Collins NR, Wikswo ME, Castro CJ, Magaña LC, Gregoricus N, Marine RL, Chhabra P, Vinjé J. J Clin Microbiol 55 2208-2221 (2017)
  4. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. Arnold JJ, Vignuzzi M, Stone JK, Andino R, Cameron CE. J Biol Chem 280 25706-25716 (2005)
  5. The structure of a birnavirus polymerase reveals a distinct active site topology. Pan J, Vakharia VN, Tao YJ. Proc Natl Acad Sci U S A 104 7385-7390 (2007)
  6. X-ray crystallographic structure of the Norwalk virus protease at 1.5-A resolution. Zeitler CE, Estes MK, Venkataram Prasad BV. J Virol 80 5050-5058 (2006)
  7. Structure-based inhibition of Norovirus RNA-dependent RNA polymerases. Mastrangelo E, Pezzullo M, Tarantino D, Petazzi R, Germani F, Kramer D, Robel I, Rohayem J, Bolognesi M, Milani M. J Mol Biol 419 198-210 (2012)
  8. Activation mechanism of a noncanonical RNA-dependent RNA polymerase. Garriga D, Navarro A, Querol-Audí J, Abaitua F, Rodríguez JF, Verdaguer N. Proc Natl Acad Sci U S A 104 20540-20545 (2007)
  9. Structural and functional characterization of sapovirus RNA-dependent RNA polymerase. Fullerton SW, Blaschke M, Coutard B, Gebhardt J, Gorbalenya A, Canard B, Tucker PA, Rohayem J. J Virol 81 1858-1871 (2007)
  10. De novo initiation of RNA synthesis by the arterivirus RNA-dependent RNA polymerase. Beerens N, Selisko B, Ricagno S, Imbert I, van der Zanden L, Snijder EJ, Canard B. J Virol 81 8384-8395 (2007)
  11. Stabilization of poliovirus polymerase by NTP binding and fingers-thumb interactions. Thompson AA, Albertini RA, Peersen OB. J Mol Biol 366 1459-1474 (2007)
  12. Crystal structure of complete rhinovirus RNA polymerase suggests front loading of protein primer. Appleby TC, Luecke H, Shim JH, Wu JZ, Cheney IW, Zhong W, Vogeley L, Hong Z, Yao N. J Virol 79 277-288 (2005)
  13. Inhibition of norovirus replication by the nucleoside analogue 2'-C-methylcytidine. Rocha-Pereira J, Jochmans D, Dallmeier K, Leyssen P, Cunha R, Costa I, Nascimento MS, Neyts J. Biochem Biophys Res Commun 427 796-800 (2012)
  14. Norovirus proteinase-polymerase and polymerase are both active forms of RNA-dependent RNA polymerase. Belliot G, Sosnovtsev SV, Chang KO, Babu V, Uche U, Arnold JJ, Cameron CE, Green KY. J Virol 79 2393-2403 (2005)
  15. Binding of 2'-amino-2'-deoxycytidine-5'-triphosphate to norovirus polymerase induces rearrangement of the active site. Zamyatkin DF, Parra F, Machín A, Grochulski P, Ng KK. J Mol Biol 390 10-16 (2009)
  16. The active form of the norovirus RNA-dependent RNA polymerase is a homodimer with cooperative activity. Högbom M, Jäger K, Robel I, Unge T, Rohayem J. J Gen Virol 90 281-291 (2009)
  17. The structure of bovine viral diarrhea virus RNA-dependent RNA polymerase and its amino-terminal domain. Choi KH, Gallei A, Becher P, Rossmann MG. Structure 14 1107-1113 (2006)
  18. Distinct conformations of a putative translocation element in poliovirus polymerase. Sholders AJ, Peersen OB. J Mol Biol 426 1407-1419 (2014)
  19. Structural basis of substrate specificity and protease inhibition in Norwalk virus. Muhaxhiri Z, Deng L, Shanker S, Sankaran B, Estes MK, Palzkill T, Song Y, Prasad BV. J Virol 87 4281-4292 (2013)
  20. Nucleotidylylation of the VPg protein of a human norovirus by its proteinase-polymerase precursor protein. Belliot G, Sosnovtsev SV, Chang KO, McPhie P, Green KY. Virology 374 33-49 (2008)
  21. Mutational evidence for a structural model of the Lassa virus RNA polymerase domain and identification of two residues, Gly1394 and Asp1395, that are critical for transcription but not replication of the genome. Hass M, Lelke M, Busch C, Becker-Ziaja B, Günther S. J Virol 82 10207-10217 (2008)
  22. Structural explanation for the role of Mn2+ in the activity of phi6 RNA-dependent RNA polymerase. Poranen MM, Salgado PS, Koivunen MR, Wright S, Bamford DH, Stuart DI, Grimes JM. Nucleic Acids Res 36 6633-6644 (2008)
  23. Nonnucleoside inhibitors of norovirus RNA polymerase: scaffolds for rational drug design. Eltahla AA, Lim KL, Eden JS, Kelly AG, Mackenzie JM, White PA. Antimicrob Agents Chemother 58 3115-3123 (2014)
  24. Naphthalene-sulfonate inhibitors of human norovirus RNA-dependent RNA-polymerase. Tarantino D, Pezzullo M, Mastrangelo E, Croci R, Rohayem J, Robel I, Bolognesi M, Milani M. Antiviral Res 102 23-28 (2014)
  25. Structures of the compact helical core domains of feline calicivirus and murine norovirus VPg proteins. Leen EN, Kwok KY, Birtley JR, Simpson PJ, Subba-Reddy CV, Chaudhry Y, Sosnovtsev SV, Green KY, Prater SN, Tong M, Young JC, Chung LM, Marchant J, Roberts LO, Kao CC, Matthews S, Goodfellow IG, Curry S. J Virol 87 5318-5330 (2013)
  26. Crystal structures of murine norovirus-1 RNA-dependent RNA polymerase in complex with 2-thiouridine or ribavirin. Alam I, Lee JH, Cho KJ, Han KR, Yang JM, Chung MS, Kim KH. Virology 426 143-151 (2012)
  27. Crystal structures of murine norovirus-1 RNA-dependent RNA polymerase. Lee JH, Alam I, Han KR, Cho S, Shin S, Kang S, Yang JM, Kim KH. J Gen Virol 92 1607-1616 (2011)
  28. 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)
  29. 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)
  30. Highly similar structural frames link the template tunnel and NTP entry tunnel to the exterior surface in RNA-dependent RNA polymerases. Lang DM, Zemla AT, Zhou CL. Nucleic Acids Res 41 1464-1482 (2013)
  31. Murine norovirus-1 3Dpol exhibits RNA-dependent RNA polymerase activity and nucleotidylylates on Tyr of the VPg. Han KR, Choi Y, Min BS, Jeong H, Cheon D, Kim J, Jee Y, Shin S, Yang JM. J Gen Virol 91 1713-1722 (2010)
  32. Comparison of the replication properties of murine and human calicivirus RNA-dependent RNA polymerases. Bull RA, Hyde J, Mackenzie JM, Hansman GS, Oka T, Takeda N, White PA. Virus Genes 42 16-27 (2011)
  33. Poliovirus polymerase residue 5 plays a critical role in elongation complex stability. Hobdey SE, Kempf BJ, Steil BP, Barton DJ, Peersen OB. J Virol 84 8072-8084 (2010)
  34. Human norovirus genogroup II recombinants in Thailand, 2009-2014. Phumpholsup T, Chieochansin T, Vongpunsawad S, Vuthitanachot V, Payungporn S, Poovorawan Y. Arch Virol 160 2603-2609 (2015)
  35. Norovirus RNA-dependent RNA polymerase is phosphorylated by an important survival kinase, Akt. Eden JS, Sharpe LJ, White PA, Brown AJ. J Virol 85 10894-10898 (2011)
  36. Structure of a murine norovirus NS6 protease-product complex revealed by adventitious crystallisation. Leen EN, Baeza G, Curry S. PLoS One 7 e38723 (2012)
  37. 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)
  38. Structure and function of the c-myc DNA-unwinding element-binding protein DUE-B. Kemp M, Bae B, Yu JP, Ghosh M, Leffak M, Nair SK. J Biol Chem 282 10441-10448 (2007)
  39. Residues Arg283, Arg285, and Ile287 in the nucleotide binding pocket of bovine viral diarrhea virus NS5B RNA polymerase affect catalysis and fidelity. Curti E, Jaeger J. J Virol 87 199-207 (2013)
  40. Isolation and characterization of a new Vesivirus from rabbits. Martín-Alonso JM, Skilling DE, González-Molleda L, del Barrio G, Machín A, Keefer NK, Matson DO, Iversen PL, Smith AW, Parra F. Virology 337 373-383 (2005)
  41. PPNDS inhibits murine Norovirus RNA-dependent RNA-polymerase mimicking two RNA stacking bases. Croci R, Tarantino D, Milani M, Pezzullo M, Rohayem J, Bolognesi M, Mastrangelo E. FEBS Lett 588 1720-1725 (2014)
  42. A nucleobase-binding pocket in a viral RNA-dependent RNA polymerase contributes to elongation complex stability. Shi W, Ye HQ, Deng CL, Li R, Zhang B, Gong P. Nucleic Acids Res 48 1392-1405 (2020)
  43. Expression of the murine norovirus (MNV) ORF1 polyprotein is sufficient to induce apoptosis in a virus-free cell model. Herod MR, Salim O, Skilton RJ, Prince CA, Ward VK, Lambden PR, Clarke IN. PLoS One 9 e90679 (2014)
  44. Repurposing of rutin for the inhibition of norovirus replication. Chéron N, Yu C, Kolawole AO, Shakhnovich EI, Wobus CE. Arch Virol 160 2353-2358 (2015)
  45. Subgenomic promoter recognition by the norovirus RNA-dependent RNA polymerases. Lin X, Thorne L, Jin Z, Hammad LA, Li S, Deval J, Goodfellow IG, Kao CC. Nucleic Acids Res 43 446-460 (2015)
  46. Significance of the C-terminal amino acid residue in mengovirus RNA-dependent RNA polymerase. Dmitrieva TM, Alexeevski AV, Shatskaya GS, Tolskaya EA, Gmyl AP, Khitrina EV, Agol VI. Virology 365 79-91 (2007)
  47. Structure of a backtracked state reveals conformational changes similar to the state following nucleotide incorporation in human norovirus polymerase. Zamyatkin D, Rao C, Hoffarth E, Jurca G, Rho H, Parra F, Grochulski P, Ng KK. Acta Crystallogr D Biol Crystallogr 70 3099-3109 (2014)
  48. Identification of a Broad-Spectrum Viral Inhibitor Targeting a Novel Allosteric Site in the RNA-Dependent RNA Polymerases of Dengue Virus and Norovirus. Yi D, Li Q, Pang L, Wang Y, Zhang Y, Duan Z, Liang C, Cen S. Front Microbiol 11 1440 (2020)
  49. Primer-independent initiation of RNA synthesis by SeMV recombinant RNA-dependent RNA polymerase. Govind K, Savithri HS. Virology 401 280-292 (2010)
  50. 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)
  51. Genetic characterization of norovirus GII.4 variants circulating in Canada using a metagenomic technique. Petronella N, Ronholm J, Suresh M, Harlow J, Mykytczuk O, Corneau N, Bidawid S, Nasheri N. BMC Infect Dis 18 521 (2018)
  52. Norovirus RNA-dependent RNA polymerase: A computational study of metal-binding preferences. Shaik MM, Bhattacharjee N, Feliks M, Ng KK, Field MJ. Proteins 85 1435-1445 (2017)
  53. Development of a Gaussia luciferase-based human norovirus protease reporter system: cell type-specific profile of Norwalk virus protease precursors and evaluation of inhibitors. Qu L, Vongpunsawad S, Atmar RL, Prasad BV, Estes MK. J Virol 88 10312-10326 (2014)
  54. A Motif in the F Homomorph of Rabbit Haemorrhagic Disease Virus Polymerase Is Important for the Subcellular Localisation of the Protein and Its Ability to Induce Redistribution of Golgi Membranes. Urakova N, Warden AC, White PA, Strive T, Frese M. Viruses 9 E202 (2017)
  55. 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)
  56. Identification of amino acids within norovirus polymerase involved in RNA binding and viral replication. Han KR, Alhatlani BY, Cho S, Lee JH, Hosmillo M, Goodfellow IG, Kim KH, Yang JM. J Gen Virol 98 1311-1315 (2017)
  57. Molecular characterization of a novel cryptic virus infecting pigeonpea plants. Kumar S, Subbarao BL, Kumari R, Hallan V. PLoS One 12 e0181829 (2017)
  58. Letter RNA-dependent RNA polymerase: Addressing Zika outbreak by a phylogeny-based drug target study. Stephen P, Lin SX. Chem Biol Drug Des 91 322-327 (2018)
  59. Application of Molecular Dynamics Simulations to the Design of Nucleotide Inhibitors Binding to Norovirus Polymerase. Freedman H, Kundu J, Tchesnokov EP, Law JLM, Nieman JA, Schinazi RF, Tyrrell DL, Gotte M, Houghton M. J Chem Inf Model 60 6566-6578 (2020)
  60. Substrate recognition by norovirus polymerase: microsecond molecular dynamics study. Maláč K, Barvík I. J Comput Aided Mol Des 27 373-388 (2013)
  61. Complete Genome Sequence, Molecular Characterization and Phylogenetic Relationships of a Temminck's Stint Calicivirus: Evidence for a New Genus within Caliciviridae Family. Matsvay A, Dyachkova M, Sai A, Burskaia V, Artyushin I, Shipulin G. Microorganisms 10 1540 (2022)
  62. Effect of intramolecular hydrogen-bond formation on the molecular conformation of amino acids. Giubertoni G, Sofronov OO, Bakker HJ. Commun Chem 3 84 (2020)
  63. Mapping human norovirus antigens during infection reveals the breadth of the humoral immune response. Su L, Huang W, Neill FH, Estes MK, Atmar RL, Palzkill T. NPJ Vaccines 8 87 (2023)


Quick links