The twenty-nine amino acid C-terminal cytoplasmic domain of poliovirus 3AB is critical for nucleic acid chaperone activity

RNA Biology

Volumn 7, Issue 6, 2010, Pages 820-829

  Gangaramani, Divya R ^a   Eden, Elizabeth L ^a   Shah, Manthan ^a   DeStefano, Jeffrey J ^a  

^a Bldg 142   (United States)

Author keywords

3AB; Nucleic acid chaperone; Picornavirus; Poliovirus; Virus replication

Indexed keywords

AMINO ACID; CHAPERONE; NUCLEIC ACID; PROTEIN 3AB; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; DNA TEMPLATE; GENE MUTATION; NONHUMAN; NUCLEIC ACID HYBRIDIZATION; POLIOMYELITIS VIRUS;

PICORNAVIRIDAE; POLIOVIRUS;

EID: 78751674527     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.7.6.13781     Document Type: Article

References (72)

1. Zuniga S, Sola I, Cruz JL, Enjuanes L. Role of RNA chaperones in virus replication. Virus Res 2009; 139:253-66.
2. Herschlag D. RNA chaperones and the RNA folding problem. J Biol Chem 1995; 270:20871-4.
3. Levin JG, Guo J, Ioulia R, Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acids Res Mol Biol 2005; 80:217-86.
4. Rajkowitsch L, Chen D, Stampfl S, Semrad K, Waldsich C, Mayer O, et al. RNA chaperones, RNA annealers and RNA helicases. RNA Biol 2007; 4:118-30.
5. Henriet S, Sinck L, Bec G, Gorelick RJ, Marquet R, Paillart JC. Vif is a RNA chaperone that could temporally regulate RNA dimerization and the early steps of HIV-1 reverse transcription. Nucleic Acids Res 2007; 35:5141-53.
6. Kuciak M, Gabus C, Ivanyi-Nagy R, Semrad K, Storchak R, Chaloin O, et al. The HIV-1 transcriptional activator Tat has potent nucleic acid chaperoning activities in vitro. Nucleic Acids Res 2008; 36:3389-400.
7. Rowley GL, Ma Q-F, Bathurst IC, Barr PJ, Kenyon GL. Stabilization and Activiation of Recombinant human Immunodeficiency Virus-1 Reverse Transcriptase-P66. Biochem Biophys Res Commun 1990; 167:673-9.
8. Cristofari G, Ivanyi-Nagy R, Gabus C, Boulant S, Lavergne JP, Penin F, et al. The hepatitis C virus Core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro. Nucleic Acids Res 2004; 32:2623-31.
9. Ivanyi-Nagy R, Lavergne JP, Gabus C, Ficheux D, Darlix JL. RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae. Nucleic Acids Res 2008; 36:712-25. (Pubitemid 351267229)
10. Zuniga S, Sola I, Moreno JL, Sabella P, Plana-Duran J, Enjuanes L. Coronavirus nucleocapsid protein is an RNA chaperone. Virology 2007; 357:215-27.
11. Mir MA, Panganiban AT. Characterization of the RNA chaperone activity of hantavirus nucleocapsid protein. J Virol 2006; 80:6276-85.
12. Huang ZS, Su WH, Wang JL, Wu HN. Selective strand annealing and selective strand exchange promoted by the N-terminal domain of hepatitis delta antigen. J Biol Chem 2003; 278:5685-93.
13. Destefano JJ, Titilope O. Poliovirus Protein 3AB Displays Nucleic Acid Chaperone and Helix-Destabilizing Activities. J Virol 2006; 80:1662-71.
14. Houghton M. In Fields BN, Knipe DM, Howley PM, (Eds.). Philidelphia: Lippincott-Raven 1996; 1:1035-58.
15. Towner JS, Ho TV, Semler BL. Determinants of membrane association for poliovirus protein 3AB. J Biol Chem 1996; 271:26810-8.
16. Hope DA, Diamond SE, Kirkegaard K. Genetic dissection of interaction between poliovirus 3D polymerase and viral protein 3AB. Journal of Virology 1997; 71:9490-8.
17. pol. J Virol 1995; 69:7169-79.
18. Li N, Cui ZQ, Wen JK, Zhang ZP, Wei HP, Zhou YF, et al. Live cell imaging of protein interactions in poliovirus RNA replication complex using fluorescence resonance energy transfer (FRET). Biochem Biophys Res Commun 2008; 368:489-94.
19. Yin J, Liu Y, Wimmer E, Paul AV. Complete protein linkage map between the P2 and P3 non-structural proteins of poliovirus. J Gen Virol 2007; 88:2259-67.
20. Strauss DM, Wuttke DS. Characterization of protein-protein interactions critical for poliovirus replication: analysis of 3AB and VPg binding to the RNA-dependent RNA polymerase. J Virol 2007; 81:6369-78.
21. pol with VPg and with genetic variants of 3AB. J Virol 1998; 72:6732-41.
22. Xiang W, Cuconati A, Paul AV, Cao X, Wimmer E. Molecular dissection of the multifunctional poliovirus RNA-binding protein 3AB. Rna 1995; 1:892-904.
23. Lama J, Sanz MA, Rodriguez PL. Role of 3AB protein in poliovirus genome replication. J Biol Chem 1995; 270:14430-8.
24. pro with the 5′ and 3′ termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding. J Biol Chem 1994; 269:27004-14.
25. pro of poliovirus is essential for RNA replication. J Virol 1995; 69:3658-67.
26. Baron MH, Baltimore D. Anti-VPg antibody inhibition of the poliovirus replicase reaction and production of covalent complexes of VPg-related proteins and RNA. Cell 1982; 30:745-52.
27. Semler BL, Anderson CW, Hanecak R, Dorner LF, Wimmer E. A membrane-associated precursor to poliovirus VPg identified by immunoprecipitation with antibodies directed against a synthetic heptapeptide. Cell 1982; 28:405-12.
28. Takegami T, Kuhn RJ, Anderson CW, Wimmer E. Membrane-dependent uridylylation of the genomelinl\kerd protein PPg of poliovirus. Proc Natl Acad Sci USA 1983; 80:7447-51. (Pubitemid 14178020)
29. Takegami T, Semler BI, Anderson CW, Wimmer E. Membrane fractions active in poliovirus RNA replication contain VPg precursor polypeptides. Virology 1983; 128:33-47.
30. Paul AV, Boom JH, Filippov D, Wimmer E. Protein-primed RNA synthesis by purified RNA polymerase. Nature 1998; 393:280-4.
31. Paul AV, Rieder E, Kim DW, van Boom JH, Wimmer E. Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the In vitro uridylylation of VPg [In Process Citation]. J Virol 2000; 74:10359-70.
32. Fujita K, Krishnakumar SS, Franco D, Paul AV, London E, Wimmer E. Membrane topography of the hydrophobic anchor sequence of poliovirus 3A and 3AB proteins and the functional effect of 3A/3AB membrane association upon RNA replication. Biochemistry 2007; 46:5185-99.
33. Lyle JM, Clewell A, Richmond K, Richards OC, Hope DA, Schultz SC, et al. Similar structural basis for membrane localization and protein priming by an RNA-dependent RNA polymerase. J Biol Chem 2002; 277:16324-31.
34. Strauss DM, Glustrom LW, Wuttke DS. Towards an understanding of the poliovirus replication complex: the solution structure of the soluble domain of the poliovirus 3A protein. J Mol Biol 2003; 330:225-34.
35. pol. Stimulation of poly(U) synthesis in vitro by purified poliovirus protein 3AB. J Biol Chem 1994; 269:29173-81.
36. Richards OC, Ehrenfeld E. Effects of poliovirus 3AB protein on 3D polymerase-catalyzed reaction. J Biol Chem 1998; 273:12832-40.
37. Rodriguez-Wells V, Plotch SJ, DeStefano JJ. Primer-dependent synthesis by poliovirus RNA-dependent RNA polymerase (3D(pol)). Nucleic Acids Res 2001; 29:2715-24. (Pubitemid 32685034)
38. Andino R, Rieckhof GE, Achacoso PL, Baltimore D. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J 1993; 12:3587-98.
39. Andino R, Rieckhof GE, Baltimore D. A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA. Cell 1990; 63:369-80.
40. Rohll JB, Percy N, Ley R, Evans DJ, Almond JW, Barclay WS. The 5′-untranslated regions of picornavirus RNAs contain independent functional domains essential for RNA replication and translation. J Virol 1994; 68:4384-91.
41. Jackson RJ, Howell MT, Kaminski A. The novel mechanism of initiation of picornavirus RNA translation. Trends Biochem Sci 1990; 15:477-83.
42. Jang SK, Pestova TV, Hellen CU, Witherell GW, Wimmer E. Cap-independent translation of picornavirus RNAs: structure and function of the internal ribosomal entry site. Enzyme 1990; 44:292-309.
43. Agut H, Kean KM, Bellocq C, Fichot O, Girard M. Intratypic recombination of polioviruses: evidence for multiple crossing-over sites on the viral genome. J Virol 1987; 61:1722-5.
44. pol) is sufficient for template switching in vitro. J Biol Chem 1999; 274:2706-16.
45. Duggal R, Cuconati A, Gromeier M, Wimmer E. Genetic recombination of poliovirus in a cell-free system. Proc Natl Acad Sci USA 1997; 94:13786-91.
46. Duggal R, Wimmer E. Genetic recombination of poliovirus in vitro and in vivo: temperature-dependent alteration of crossover sites. Virology 1999; 258:30-41.
47. Gmyl AP, Belousov EV, Maslova SV, Khitrina EV, Chetverin AB, Agol VI. Nonreplicative RNA recombination in poliovirus. J Virol 1999; 73:8958-65.
48. Jarvis TC, Kirkegaard K. The polymerase in its labyrinth: mechanisms and implications of RNA recombination. Trends Genet 1991; 7:186-91.
49. Jarvis TC, Kirkegaard K. Poliovirus RNA recombination: mechanistic studies in the absence of selection. EMBO J 1992; 11:3135-45.
50. Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell 1986; 47:433-43.
51. Nagy PD, Simon AE. New insights into the mechanisms of RNA recombination. Virology 1997; 235:1-9. (Pubitemid 27380801)
52. Pierangeli A, Bucci M, Forzan M, Pagnotti P, Equestre M, Perez Bercoff R. 'Primer alignment-and-extension': a novel mechanism of viral RNA recombination responsible for the rescue of inactivated poliovirus cDNA clones. J Gen Virol 1999; 80:1889-97.
53. Romanova LI, Blinov VM, Tolskaya EA, Viktorova EG, Kolesnikova MS, Guseva EA, et al. The primary structure of crossover regions of intertypic poliovirus recombinants: a model of recombination between RNA genomes. Virology 1986; 155:202-13.
54. Simon AE. Replication, recombination and symptom-modulation properties of the satellite RNAs of turnip crinkle virus. Curr Top Microbiol Immunol 1999; 239:19-36.
55. Tolskaya EA, Romanova LI, Blinov VM, Viktorova EG, Sinyakov AN, Kolesnikova MS, et al. Studies on the recombination between RNA genomes of poliovirus: the primary structure and nonrandom distribution of crossover regions in the genomes of intertypic poliovirus recombinants. Virology 1987; 161:54-61.
56. Darlix JL, Vincent A, Gabus C, de Rocquigny H, Roques B. Trans-activation of the 5′ to 3′ viral DNA strand transfer by nucleocapsid protein during reverse transcription of HIV1 RNA. C R Acad Sci III 1993; 316:763-71.
57. Allain B, Lapadat-Tapolsky M, Berlioz C, Darlix JL. Transactivation of the minus-strand DNA transfer by nucleocapsid protein during reverse transcription of the retroviral genome. EMBO J 1994; 13:973-81.
58. Peliska JA, Balasubramanian S, Giedroc DP, Benkovic SJ. Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity. Biochemistry 1994; 33:13817-23.
59. You JC, McHenry CS. Human immunodeficiency virus nucleocapsid protein accelerates strand transfer of the terminally redundant sequences involved in reverse transcription. J Biol Chem 1994; 269:31491-5.
60. DeStefano JJ. Human immunodeficiency virus nucleocapsid protein stimulates strand transfer from internal regions of heteropolymeric RNA templates. Arch Virol 1995; 140:1775-89.
61. Rodriguez-Rodriguez L, Tsuchihashi Z, Fuentes GM, Bambara RA, Fay PJ. Influence of human immunodeficiency virus nucleocapsid protein on synthesis and strand transfer by the reverse transcriptase in vitro. J Biol Chem 1995; 270:15005-11.
62. Cameron CE, Ghosh M, Le Grice SF, Benkovic SJ. Mutations in HIV reverse transcriptase which alter RNase H activity and decrease strand transfer efficiency are suppressed by HIV nucleocapsid protein. Proc Natl Acad Sci USA 1997; 94:6700-5.
63. Guo J, Henderson LE, Bess J, Kane B, Levin JG. Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA. J Virol 1997; 71:5178-88.
64. Heath MJ, Derebail SS, Gorelick RJ, DeStefano JJ. Differing roles of the N-terminal and C-terminal zinc fingers in HIV-1 nucleocapsid protein enhanced nucleic acid annealing. J Biol Chem 2003; 278:30755-63.
65. Anthony RM, Destefano JJ. In vitro synthesis of long DNA products in reactions with HIV-RT and nucleocapsid protein. J Mol Biol 2007; 365:310-24.
66. Narayanan N, Gorelick RJ, DeStefano JJ. Structure/function mapping of amino acids in the N-terminal zinc finger of the human immunodeficiency virus type 1 nucleocapsid protein: residues responsible for nucleic acid helix destabilizing activity. Biochemistry 2006; 45:12617-28.
67. Tanchou V, Delaunay T, Bodeus M, Roques B, Darlix JL, Benarous R. Conformational changes between human immunodeficiency virus type 1 nucleocapsid protein NCp7 and its precursor NCp15 as detected by anti-NCp7 monoclonal antibodies. J Gen Virol 1995; 76:2457-66.
68. Schein CH, Oezguen N, van der Heden van Noort GJ, Filippov DV, Paul A, Kumar E, et al. NMR solution structure of poliovirus uridylylated peptide linked to the genome (VPgpU). Peptides 2008.
69. Schein CH, Oezguen N, Volk DE, Garimella R, Paul A, Braun W. NMR structure of the viral peptide linked to the genome (VPg) of poliovirus. Peptides 2006; 27:1676-84.
70. You JC, McHenry CS. HIV nucleocapsid protein. Expression in Escherichia coli, purification and characterization. J Biol Chem 1993; 268:16519-27.
71. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406-15. (Pubitemid 37442169)
72. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual. 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press 2001.