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

Journal of General Virology

Volumn 85, Issue 1, 2004, Pages 231-240

  Neeleman, Lyda ^a   Linthorst, Huub J M ^a   Bol, John F ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; DIMER; MESSENGER RNA; MUTANT PROTEIN; VIRUS RNA;

3' UNTRANSLATED REGION; ALFAMOVIRUS; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; IN VIVO STUDY; INOCULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA TRANSLATION; VIRUS INFECTION; WILD TYPE;

3' UNTRANSLATED REGIONS; ALFALFA MOSAIC VIRUS; ANIMALS; BASE SEQUENCE; CAPSID PROTEINS; DIMERIZATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BIOSYNTHESIS; RABBITS; RETICULOCYTES; RNA, VIRAL;

ALFALFA MOSAIC VIRUS; ALFAMOVIRUS; BROME MOSAIC VIRUS; BROMUS; MEDICAGO SATIVA; RNA VIRUSES;

EID: 1642462833     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.19581-0     Document Type: Article

References (42)

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.
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.
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.
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.
5. Bol, J. F. (2003). Alfalfa mosaic virus: coat protein-dependent initiation of infection. Mol Plant Pathol 4, 1-8.
6. Browning, K. S. (1996). The plant translational apparatus. Plant Mol Biol 32, 107-144.
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.
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.
9. Gallie, D. R. (1991). The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev 5, 2108-2116.
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.
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.
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.
13. Hann, L., Webb, A. C., Cal, 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.
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.
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.
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.
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.
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.
19. Jaspars, E. M. J. (1999). Genome activation in alfamo- and ilarviruses. Arch Virol 144, 843-863.
20. Jobling, S. A. & Gehrke, L. (1987). Enhanced translation of chimeric messenger RNAs containing a plant viral untranslated leader sequence. Nature 325, 622-625.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.