Poly(rC) binding proteins and the 5′ cloverleaf of uncapped poliovirus mRNA function during de novo assembly of polysomes

Journal of Virology

Volumn 82, Issue 12, 2008, Pages 5835-5846

  Kempf, Brian J ^a   Barton, David J ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTIC INITIATION FACTOR 4GI; EXONUCLEASE; INITIATION FACTOR 4G; MESSENGER RNA; NUCLEOTIDE; POLYADENYLIC ACID BINDING PROTEIN; RIBONUCLEOPROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL DIVISION; CELL SIZE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; HELA CELL; HUMAN; HUMAN CELL; KINETICS; MUTATION; OPEN READING FRAME; POLIOMYELITIS VIRUS; POLYSOME; PRIORITY JOURNAL; PROTEIN SECRETION; RIBOSOME; RNA TRANSLATION; TIME;

BINDING SITES; BINDING, COMPETITIVE; CELL-FREE SYSTEM; DNA, COMPLEMENTARY; HELA CELLS; HUMANS; KINETICS; NUCLEIC ACID CONFORMATION; PLASMIDS; POLIOVIRUS; POLY C; POLYRIBOSOMES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, RIBOSOMAL; RNA, VIRAL;

EUKARYOTA; POLIOVIRUS;

EID: 44949147279     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01513-07     Document Type: Article

References (66)

1. Andino, R., G. E. Rieckhof, P. L. Achacoso, and D. Baltimore. 1993. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA. EMBO J. 12:3587-3598.
2. Andrei, M. A., D. Ingelfinger, R. Heintzmann, T. Achsel, R. Rivera-Pomar, and R. Luhrmann. 2005. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11:717-727.
3. Barton, D. J., and J. B. Flanegan. 1993. Coupled translation and replication of poliovirus RNA in vitro: synthesis of functional 3D polymerase and infectious virus. J. Virol. 67:822-831.
4. Barton, D. J., and J. B. Flanegan. 1997. Synchronous replication of poliovirus RNA: initiation of negative-strand RNA synthesis requires the guanidine-inhibited activity of protein 2C. J. Virol. 71:8482-8489.
5. Barton, D. J., B. J. Morasco, and J. B. Flanegan. 1996. Assays for poliovirus polymerase, 3D(Pol), and authentic RNA replication in HeLa S10 extracts. Methods Enzymol. 275:35-57.
6. Barton, D. J., B. J. Morasco, and J. B. Flanegan. 1999. Translating ribosomes inhibit poliovirus negative-strand RNA synthesis. J. Virol. 73:10104-10112.
7. Barton, D. J., B. J. O'Donnell, and J. B. Flanegan. 2001. 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J. 20:1439-1448.
8. Blyn, L. B., K. M. Swiderek, O. Richards, D. C. Stahl, B. L. Semler, and E. Ehrenfeld. 1996. Poly(rC) binding protein 2 binds to stem-loop IV of the poliovirus RNA 5′ noncoding region: identification by automated liquid chromatography-tandem mass spectrometry. Proc. Natl. Acad. Sci. USA 93:11115-11120.
9. Blyn, L. B., J. S. Towner, B. L. Semler, and E. Ehrenfeld. 1997. Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J. Virol. 71:6243-6246.
10. Coller, J., and R. Parker. 2004. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73:861-890.
11. Collis, P. S., B. J. O'Donnell, D. J. Barton, J. A. Rogers, and J. B. Flanegan. 1992. Replication of poliovirus RNA and subgenomic RNA transcripts in transfected cells. J. Virol. 66:6480-6488.
12. Cougot, N., S. Babajko, and B. Seraphin. 2004. Cytoplasmic foci are sites of mRNA decay in human cells. J. Cell Biol. 165:31-40.
13. Fenger-Gron, M., C. Fillman, B. Norrild, and J. Lykke-Andersen. 2005. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol. Cell 20:905-915.
14. Fillman, C., and J. Lykke-Andersen. 2005. RNA decapping inside and outside of processing bodies. Curr. Opin. Cell Biol. 17:326-331.
15. Gamarnik, A. V., and R. Andino. 2000. Interactions of viral protein 3CD and poly(rC) binding protein with the 5′ untranslated region of the poliovirus genome. J. Virol. 74:2219-2226.
16. Gamarnik, A. V., and R. Andino. 1997. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3:882-892.
17. Gherzi, R., K. Y. Lee, P. Briata, D. Wegmuller, C. Moroni, M. Karin, and C. Y. Chen. 2004. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell 14:571-583.
18. Gradi, A., Y. V. Svitkin, H. Imataka, and N. Sonenberg. 1998. Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl. Acad. Sci. USA 95:11089-11094.
19. Hammond, M. L., and L. H. Bowman. 1988. Insulin stimulates the translation of ribosomal proteins and the transcription of rDNA in mouse myoblasts. J. Biol. Chem. 263:17785-17791.
20. Hentze, M. W. 1997. eIF4G: a multipurpose ribosome adapter? Science 275:500-501.
21. Herold, J., and R. Andino. 2001. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell 7:581-591.
22. Hewlett, M. J., J. K. Rose, and D. Baltimore. 1976. 5′-terminal structure of poliovirus polyribosomal RNA is pUp. Proc. Natl. Acad. Sci. USA 73:327-330.
23. Imataka, H., A. Gradi, and N. Sonenberg. 1998. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:7480-7489.
24. Ingelfinger, D., D. J. Arndt-Jovin, R. Luhrmann, and T. Achsel. 2002. The human LSm1-7 proteins colocalize with the mRNA-degrading enzymes Dcp1/2 and Xrnl in distinct cytoplasmic foci. RNA 8:1489-1501.
25. pro is a multifunctional protein that regulates the stability, translation and replication of poliovirus RNA. Virology 345:346-357.
26. Pro increases viral mRNA stability and polysome stability coordinately in time with cleavage of eIF4G. J. Virol. 82:5847-5859.
27. Kuyumcu-Martinez, N. M., M. Joachims, and R. E. Lloyd. 2002. Efficient cleavage of ribosome-associated poly(A)-binding protein by enterovirus 3C protease. J. Virol. 76:2062-2074.
28. Kuyumcu-Martinez, N. M., M. E. Van Eden, P. Younan, and R. E. Lloyd. 2004. Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol. Cell. Biol. 24:1779-1790.
29. Lloyd, R. E. 2006. Translational control by viral proteinases. Virus Res. 119:76-88.
30. Lyons, T., K. E. Murray, A. W. Roberts, and D. J. Barton. 2001. Poliovirus 5′-terminal cloverleaf RNA is required in cis for VPg uridylylation and the initiation of negative-strand RNA synthesis. J. Virol. 75:10696-106708.
31. Makeyev, A. V., and S. A. Liebhaber. 2002. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA 8:265-278.
32. Molla, A., A. V. Paul, and E. Wimmer. 1991. Cell-free, de novo synthesis of poliovirus. Science 254:1647-1651.
33. Morasco, B. J., N. Sharma, J. Parilla, and J. B. Flanegan. 2003. Poliovirus cre(2C)-dependent synthesis of VPgpUpU is required for positive- but not negative-strand RNA synthesis. J. Virol. 77:5136-5144.
34. Morino, S., H. Imataka, Y. V. Svitkin, T. V. Pestova, and N. Sonenberg. 2000. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol. Cell. Biol. 20:468-477.
35. Murray, K. E., and D. J. Barton. 2003. Poliovirus CRE-dependent VPg uridylylation is required for positive-strand RNA synthesis but not for negative-strand RNA synthesis. J. Virol. 77:4739-4750.
36. Murray, K. E., A. W. Roberts, and D. J. Barton. 2001. Poly(rC) binding proteins mediate poliovirus mRNA stability. RNA 7:1126-1141.
37. Murray, K. E., B. P. Steil, A. W. Roberts, and D. J. Barton. 2004. Replication of poliovirus RNA with complete internal ribosome entry site deletions. J. Virol. 78:1393-1402.
38. Newbury, S. F. 2006. Control of mRNA stability in eukaryotes. Biochem. Soc. Trans. 34:30-34.
39. Nomoto, A., N. Kitamura, F. Golini, and E. Wimmer. 1977. The 5′-terminal structures of poliovirion RNA and poliovirus mRNA differ only in the genome-linked protein VPg. Proc. Natl. Acad. Sci. USA 74:5345-5349.
40. Nomoto, A., Y. F. Lee, and E. Wimmer. 1976. The 5′ end of poliovirus mRNA is not capped with m7G(5′)ppp(5′)Np. Proc. Natl. Acad. Sci. USA 73:375-380.
41. Novak, J. E., and K. Kirkegaard. 1994. Coupling between genome translation and replication in an RNA virus. Genes Dev. 8:1726-1737.
42. Ochs, K., A. Zeller, L. Saleh, G. Bassili, Y. Song, A. Sonntag, and M. Niepmann. 2003. Impaired binding of standard initiation factors mediates poliovirus translation attenuation. J. Virol. 77:115-122.
43. Ohlmann, T., M. Rau, V. M. Pain, and S. J. Morley. 1996. The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J. 15:1371-1382.
44. Palacios, R., R. D. Palmiter, and R. T. Schimke. 1972. Identification and isolation of ovalbumin-synthesizing polysomes. I. Specific binding of 125 I-anti-ovalbumin to polysomes. J. Biol. Chem. 247:2316-2321.
45. Parker, R., and H. Song. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11:121-127.
46. Parsley, T. B., J. S. Towner, L. B. Blyn, E. Ehrenfeld, and B. L. Semler. 1997. Poly(rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA 3:1124-1134.
47. Pelletier, J., G. Kaplan, V. R. Racaniello, and N. Sonenberg. 1988. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5′ noncoding region. Mol. Cell. Biol. 8:1103-1112.
48. Penman, S., K. Scherrer, Y. Becker, and J. E. Darnell. 1963. Polyribosomes in normal and poliovirus-infected HeLa cells and their relationship to messenger-RNA. Proc. Natl. Acad. Sci. USA 49:654-662.
49. Prevot, D., J. L. Darlix, and T. Ohlmann. 2003. Conducting the initiation of protein synthesis: the role of eIF4G. Biol. Cell 95:141-156.
50. Prevot, D., D. Decimo, C. H. Herbreteau, F. Roux, J. Garin, J. L. Darlix, and T. Ohlmann. 2003. Characterization of a novel RNA-binding region of eIF4GI critical for ribosomal scanning. EMBO J. 22:1909-1921.
51. Ruan, H., C. Y. Brown, and D. R. Morris. 1997. Analysis of ribosome loading onto mRNA species: implications for translational control, p. 305-321. In J. D. Richter (ed.), mRNA formation and function. Academic Press, New York, NY.
52. Scharff, M. D., A. J. Shatkin, and L. Levintow. 1963. Association of newly formed viral protein with specific polyribosomes. Proc. Natl. Acad. Sci. USA 50:686-694.
53. Sharma, N., B. J. O'Donnell, and J. B. Flanegan. 2005. 3′-Terminal sequence in poliovirus negative-strand templates is the primary cis-acting element required for VPgpUpU-primed positive-strand initiation. J. Virol. 79:3565-3577.
54. Sheth, U., and R. Parker. 2003. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300:805-808.
55. Soto Rifo, R., E. P. Ricci, D. Decimo, O. Moncorge, and T. Ohlmann. 2007. Back to basics: the untreated rabbit reticulocyte lysate as a competitive system to recapitulate cap/poly(A) synergy and the selective advantage of IRES-driven translation. Nucleic Acids Res. 35:e121.
56. Summers, D. F., and J. V. Maizel, Jr. 1967. Disaggregation of HeLa cell polysomes after infection with poliovirus. Virology 31:550-552.
57. Summers, D. F., J. V. Maizel, Jr., and J. E. Darnell, Jr. 1967. The decrease in size and synthetic activity of poliovirus polysomes late in the infectious cycle. Virology 31:427-435.
58. Svitkin, Y. V., and N. Sonenberg. 2003. Cell-free synthesis of encephalomyocarditis virus. J. Virol. 77:6551-6555.
59. Svitkin, Y. V., and N. Sonenberg. 2004. An efficient system for cap- and poly(A)-dependent translation in vitro. Methods Mol. Biol. 257:155-170.
60. Thoma, C., A. Ostareck-Lederer, and M. W. Hentze. 2004. A poly(A) tail-responsive in vitro system for cap- or IRES-driven translation from HeLa cells. Methods Mol. Biol. 257:171-180.
61. Todd, S., J. S. Towner, and B. L. Semler. 1997. Translation and replication properties of the human rhinovirus genome in vivo and in vitro. Virology 229:90-97.
62. Trono, D., R. Andino, and D. Baltimore. 1988. An RNA sequence of hundreds of nucleotides at the 5′ end of poliovirus RNA is involved in allowing viral protein synthesis. J. Virol. 62:2291-2299.
63. van Hoof, A., P. A. Frischmeyer, H. C. Dietz, and R. Parker. 2002. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295:2262-2264.
64. van Hoof, A., and R. Parker. 2002. Messenger RNA degradation: beginning at the end. Curr. Biol. 12:R285-R287.
65. van Ooij, M. J., D. A. Vogt, A. Paul, C. Castro, J. Kuijpers, F. J. van Kuppeveld, C. E. Cameron, E. Wimmer, R. Andino, and W. J. Melchers. 2006. Structural and functional characterization of the coxsackievirus B3 CRE(2C): role of CRE(2C) in negative- and positive-strand RNA synthesis. J. Gen. Virol. 87:103-113.
66. Wang, X., and S. A. Liebhaber. 1996. Complementary change in cis determinants and trans factors in the evolution of an mRNP stability complex. EMBO J. 15:5040-5051.