Efficient translation of alfamovirus RNAs requires the binding of coat protein dimers to the 3′ termini of the viral RNAs Free

Abstract

The coat protein (CP) of (AMV) is required to initiate infection by the viral tripartite RNA genome whereas infection by the tripartite (BMV) genome is independent of CP. AMV CP stimulates translation of AMV RNA 50- to 100-fold. The 3′ untranslated region (UTR) of the AMV subgenomic CP messenger RNA 4 contains at least two CP binding sites. A CP binding site in the 3′-terminal 112 nucleotides of RNA 4 was found to be required for efficient translation of the RNA whereas an upstream binding site was not. Binding of CP to the AMV 3′ UTR induces a conformational change of the RNA but this change alone was not sufficient to stimulate translation. CP mutant R17A is unable to bind to the 3′ UTR and translation of RNA 4 encoding this mutant occurs at undetectable levels. Replacement of the 3′ UTR of this mutant RNA 4 by the 3′ UTR of BMV RNA 4 restored translation of R17A-CP to wild-type levels. Apparently, the BMV 3′ UTR stimulates translation independently of CP. AMV CP mutant N199 is defective in the formation of CP dimers and did not stimulate translation of RNA 4 although the mutant CP did bind to the 3′ UTR. The finding that N199-CP does not promote AMV infection corroborates the notion that the requirement of CP in the inoculum reflects its role in translation of the viral RNAs.

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2004-01-01
2024-03-29
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References

  1. Ansel-McKinney P., Gehrke L. 1998; RNA determinants of a specific RNA-coat protein peptide interaction in alfalfa mosaic virus: conservation of homologous features in ilarvirus RNAs. J Mol Biol 278:767–785
    [Google Scholar]
  2. Ansel-McKinney P., Scott S. W., Swanson M., Ge X., Gehrke L. 1996; A plant viral coat protein RNA binding consensus sequence contains a crucial arginine. EMBO J 15:5077–5084
    [Google Scholar]
  3. Baer M., Houser F., Loesch-Fries L. S., Gehrke L. 1994; Specific RNA binding by amino-terminal peptides of alfalfa mosaic virus coat protein. EMBO J 13:727–735
    [Google Scholar]
  4. Bol J. F. 1999; Alfalfa mosaic virus and ilarviruses: involvement of coat protein in multiple steps of the replication cycle. J Gen Virol 80:1089–1102
    [Google Scholar]
  5. Bol J. F. 2003; Alfalfa mosaic virus: coat protein-dependent initiation of infection. Mol Plant Pathol 4:1–8
    [Google Scholar]
  6. Browning K. S. 1996; The plant translational apparatus. Plant Mol Biol 32:107–144
    [Google Scholar]
  7. Choi J., Loesch-Fries L. S. 1999; Effect of C-terminal mutations of alfalfa mosaic virus coat protein on dimer formation and assembly in vitro . Virology 260:182–189
    [Google Scholar]
  8. Choi J., Kim B.-S., Zhao X., Loesch-Fries S. 2003; The importance of alfalfa mosaic virus coat protein dimers in the initiation of replication. Virology 305:44–49
    [Google Scholar]
  9. Gallie D. R. 1991; The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev 5:2108–2116
    [Google Scholar]
  10. Gallie D. R. 2001; Cap-independent translation conferred by the 5′ leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J Virol 75:12141–12152
    [Google Scholar]
  11. Gallie D. R., Kobayashi M. 1994; The role of the 3′-untranslated region of non-polyadenylated plant viral mRNAs in regulating translational efficiency. Gene 142:159–165
    [Google Scholar]
  12. Guo L., Allen E. M., Miller W. A. 2001; Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell 7:1103–1109
    [Google Scholar]
  13. Hann L., Webb A. C., Cai J.-M., Gehrke L. 1997; Identification of a competitive translation determinant in the 3′ untranslated region of alfalfa mosaic virus coat protein mRNA. Mol Cell Biol 17:2005–2013
    [Google Scholar]
  14. Houser-Scott F., Baer M. L., Liem K. F., Cai J.-M., Gehrke L. 1994; Nucleotide sequence and structural determinants of specific binding of coat protein or coat protein peptides to the 3′ untranslation region of alfalfa mosaic virus RNA 4. J Virol 68:2194–2205
    [Google Scholar]
  15. Houser-Scott F., Ansel-McKinney P., Cai J.-M., Gehrke L. 1997; In vitro genetic selection analysis of alfalfa mosaic virus coat protein binding to 3′-terminal AUGC repeats in the viral RNAs. J Virol 71:2310–2319
    [Google Scholar]
  16. Houwing C. J., Jaspars E. M. J. 1982; Coat protein binding sites in nucleation complexes of alfalfa mosaic virus RNA 4. Biochemistry 21:3408–3414
    [Google Scholar]
  17. Houwing C. J., Jaspars E. M. J. 2000; Activation of the alfalfa mosaic virus genome by viral coat protein in non-transgenic plants and protoplasts. The protection model biochemically tested. Arch Virol 145:13–35
    [Google Scholar]
  18. Imataka H., Gradi A., Sonenberg N. 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
    [Google Scholar]
  19. Jaspars E. M. J. 1999; Genome activation in alfamo- and ilarviruses. Arch Virol 144:843–863
    [Google Scholar]
  20. Jobling S. A., Gehrke L. 1987; Enhanced translation of chimeric messenger RNAs containing a plant viral untranslated leader sequence. Nature 325:622–625
    [Google Scholar]
  21. Langereis K., Neeleman L., Bol J. F. 1986; Biologically active transcripts of cloned DNA of coat protein messenger of two plant viruses. Plant Mol Biol 6:281–288
    [Google Scholar]
  22. Le H., Tanguay R. L., Balasta M. L., Wei C.-C., Browning K. S., Metz A. M., Goss D. J., Gallie D. R. 1997; Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A) binding and increase its RNA binding activity. J Biol Chem 272:16247–16255
    [Google Scholar]
  23. Le H., Browning K. S., Gallie D. R. 2000; The phosphorylation state of poly(A)-binding protein specifies its binding to poly(A) RNA and its interaction with eukaryotic initiation factor (eIF) 4F, eIFiso4F, and eIF4B. J Biol Chem 275:17452–17462
    [Google Scholar]
  24. Ling J., Morley S. J., Pain V. M., Marzluff W. F., Gallie D. R. 2002; The histone 3′-terminal stem–loop-binding protein enhances translation through a functional and physical interaction with eukaryotic initiation factor 4G (eIF4G) and eIF3. Mol Cell Biol 22:7853–7867
    [Google Scholar]
  25. Neeleman L., Bol J. F. 1999; Cis-acting functions of alfalfa mosaic virus proteins involved in replication and encapsidation of viral RNA. Virology 254:324–333
    [Google Scholar]
  26. Neeleman L., van der Kuyl A. C., Bol J. F. 1991; Role of alfalfa mosaic virus coat protein gene in symptom formation. Virology 181:687–693
    [Google Scholar]
  27. Neeleman L., Olsthoorn R. C. L., Linthorst H. J. M., Bol J. F. 2001; Translation of a nonpolyadenylated RNA is enhanced by binding of viral coat protein or polyadenylation of the RNA. Proc Natl Acad Sci U S A 98:14286–14291
    [Google Scholar]
  28. Olsthoorn R. C. L., Bol J. F. 2002; Role of an essential triloop hairpin and flanking structures in the 3′ untranslated region of alfalfa mosaic virus RNA in in vitro transcription. J Virol 76:8747–8756
    [Google Scholar]
  29. Olsthoorn R. C. L., Mertens S., Brederode F. T., Bol J. F. 1999; A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. EMBO J 18:4856–4864
    [Google Scholar]
  30. Reusken C. B. E. M., Bol J. F. 1996; Structural elements of the 3′-terminal coat protein binding site in alfalfa mosaic virus RNAs. Nucleic Acids Res 24:2660–2665
    [Google Scholar]
  31. Reusken C. B. E. M., Neeleman L., Bol J. F. 1994; The 3′-untranslated region of alfalfa mosaic virus RNA 3 contains at least two independent binding sites for coat protein. Nucleic Acids Res 22:1346–1353
    [Google Scholar]
  32. Svitkin Y. V., Imataka H., Khalghpour K., Kahvejian A., Liebig H. D., Sonenberg N. 2001; Poly(A)-binding protein interaction with eIF-4G stimulates picornavirus IRES-dependent translation. RNA 7:1743–1752
    [Google Scholar]
  33. Tarun S. Z., Sachs A. B. 1996; Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J 15:7168–7177
    [Google Scholar]
  34. Tenllado F., Bol J. F. 2000; Genetic dissection of the multiple functions of alfalfa mosaic virus coat protein in viral RNA replication, encapsidation, and movement. Virology 268:29–40
    [Google Scholar]
  35. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350–4354
    [Google Scholar]
  36. van der Vossen E. A. G., Neeleman L., Bol J. F. 1994; Early and late functions of alfalfa mosaic virus coat protein can be mutated separately. Virology 202:891–903
    [Google Scholar]
  37. van Rossum C. M. A., Reusken C. B. E. M., Brederode F. Th., Bol J. F. 1997; The 3′ untranslated region of alfalfa mosaic virus RNA 3 contains a core promoter for minus-strand RNA synthesis and an enhancer element. J Gen Virol 78:3045–3049
    [Google Scholar]
  38. Vende P., Piron M., Castagne N., Poncet D. 2000; Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA-3′ end. J Virol 74:7064–7071
    [Google Scholar]
  39. Vlot A. C., Neeleman L., Linthorst H. J. M., Bol J. F. 2000; Role of the 3′-untranslated regions of alfalfa mosaic virus RNAs in the formation of a transiently expressed replicase in plants and in the assembly of virions. J Virol 75:6440–6449
    [Google Scholar]
  40. Wilkie G. S., Dickson K. S., Gray N. K. 2003; Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci 28:182–188
    [Google Scholar]
  41. Yusibov V. M., Loesch-Fries L. S. 1995; N-terminal basic amino acids of alfalfa mosaic virus coat protein involved in the initiation of infection. Virology 208:405–407
    [Google Scholar]
  42. Zuidema D., Jaspars E. M. J. 1984; Comparative investigations on the coat protein binding sites of the genomic RNAs of alfalfa mosaic and tobacco streak viruses. Virology 135:43–52
    [Google Scholar]
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