Alfalfa mosaic virus coat protein bridges RNA and RNA-dependent RNA polymerase in vitro

Virology

Volumn 364, Issue 1, 2007, Pages 214-226

  Reichert, Vienna L ^a   Choi, Mehee ^a   Petrillo, Jessica E ^a   Gehrke, Lee ^a  

^a HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

Conformation; Positive strand RNA virus; Protein protein interactions; RNA dependent RNA polymerase; RNA protein interactions; Template selection; Viral RNA replication

Indexed keywords

PROTEIN AMV; UNCLASSIFIED DRUG; VIRUS PROTEIN;

3' UNTRANSLATED REGION; ALFALFA MOSAIC VIRUS; ANIMAL CELL; ARTICLE; IN VITRO STUDY; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA CONFORMATION; RNA REPLICATION;

ALFALFA MOSAIC VIRUS; BASE SEQUENCE; CAPSID PROTEINS; MACROMOLECULAR SUBSTANCES; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; RECOMBINANT PROTEINS; RNA REPLICASE; RNA, VIRAL; VIRUS REPLICATION;

ALFALFA MOSAIC VIRUS; RNA VIRUSES;

EID: 34249688279     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.02.026     Document Type: Article

References (61)

1. Ansel-McKinney P., and Gehrke L. 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 (1998) 767-785
2. Ansel-McKinney P., Scott S.W., Swanson M., Ge X., and Gehrke L. A plant viral coat protein RNA-binding consensus sequence contains a crucial arginine. EMBO J. 15 (1996) 5077-5084
3. Baer M., Houser F., Loesch-Fries L.S., and Gehrke L. Specific RNA binding by amino-terminal peptides of alfalfa mosaic virus coat protein. EMBO J. 13 (1994) 727-735
4. Blackwell J.L., and Brinton M.A. Translation elongation factor-1 alpha interacts with the 3′ stem-loop region of West Nile virus genomic RNA. J. Virol. 71 9 (1997) 6433-6444
5. Bol J.F. Alfalfa mosaic virus and ilarviruses: involvement of coat protein in multiple steps of the replication cycle. J. Gen. Virol. 82 (1999) 947-951
6. Bol J.F. Replication of alfamo- and ilarviruses: role of the coat protein. Annu. Rev. Phytopathol. 43 (2005) 39-62
7. Bol J.F., Van Vloten-Doting L., and Jaspars E.M.J. A functional equivalence of top component a RNA and coat protein in the initiation of infection by alfalfa mosaic virus. Virology 46 (1971) 73-85
8. Brown D., and Gold L. RNA replication by Q beta replicase: a working model. Proc. Natl. Acad. Sci. U.S.A. 93 21 (1996) 11558-11562
9. Chen J., Noueiry A., and Ahlquist P. Brome mosaic virus protein 1a recruits viral RNA 2 to RNA replication through a 5′ proximal RNA 2 signal. J. Virol. 75 7 (2001) 3207-3219
10. Degraaff M., Thorburn C., and Jaspars E.M.J. Interaction between RNA-dependent RNA polymerase of alfalfa mosaic virus and its template: oxidation of vicinal hydroxyl groups blocks in vitro RNA synthesis. Virology 213 2 (1995) 650-654
11. Degraaff M., Tveld M.R.M.I., and Jaspars E.M.J. In vitro evidence that the coat protein of alfalfa mosaic virus plays a direct role in the regulation of plus and minus RNA synthesis: implications for the life cycle of alfalfa mosaic virus. Virology 208 2 (1995) 583-589
12. Fechter P., Rudinger-Thirion J., Florentz C., and Giege R. Novel features in the tRNA-like world of plant viral RNAs. Cell. Mol. Life Sci. 58 11 (2001) 1547-1561
13. Fields B.N., Knipe D.M., and Howley P.M. Fields Virology. 3rd ed. 2 vols (1996), Lippincott-Raven, Philadelphia
14. Gamarnik A.V., and Andino R. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 12 15 (1998) 2293-2304
15. Gomila, R.C., Gehrke, L., in press. Biochemical approaches for characterizing RNA-protein complexes in preparation for high resolution structure analysis. In "Plant Virology Protocols", Vol. 2.
16. Gonsalves D., and Garnsey S.M. Functional equivalence of an RNA component and coat protein for infectivity of citrus leaf rugose virus. Virology 64 (1975) 25-31
17. Gonsalves D., and Garnsey S.M. Infectivity of heterologous RNA-protein mixtures from alfalfa mosaic, citrus leaf rugose, citrus variegation, and tobacco streak viruses. Virology 67 (1975) 319-326
18. Guogas L.M., Filman D.J., Hogle J.M., and Gehrke L. Cofolding organizes alfalfa mosaic virus RNA and coat protein for replication. Science 306 5704 (2004) 2108-2111
19. Guogas L., Laforest S., and Gehrke L. The activation of replication by alfalfa mosaic virus coat protein is concentration dependent. J. Virol. 79 9 (2005) 5752-5761
20. Houser-Scott F., Baer M.L., Liem Jr. K.F., Cai J.M., and Gehrke L. Nucleotide sequence and structural determinants of specific binding of coat protein or coat protein peptides to the 3′ untranslated region of alfalfa mosaic virus RNA 4. J. Virol. 68 (1994) 2194-2205
21. Houwing C.J., and Jaspars E.M.J. Coat protein binds to the 3′-terminal part of RNA 4 of alfalfa mosaic virus. Biochemistry 17 (1978) 2927-2933
22. Houwing C., and Jaspars E.M.J. Coat protein blocks the in vitro transcription of the virion RNAs of alfalfa mosaic virus. FEBS Lett. 209 (1986) 284-288
23. Houwing C.J., and Jaspars E.M. 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 1 (2000) 13-35
24. Jaspars E.M. Genome activation in alfamo- and ilarviruses. Arch. Virol. 144 5 (1999) 843-863
25. Kao C.C., and Sun J.H. Initiation of minus-strand RNA synthesis by the brome mosaic virus RNA-dependent RNA polymerase: use of oligoribonucleotide primers. J. Virol. 70 10 (1996) 6826-6830
26. Kao C.C., Yang X., Kline A., Wang Q.M., Barket D., and Heinz B.A. Template requirements for RNA synthesis by a recombinant hepatitis C virus RNA-dependent RNA polymerase. J. Virol. 74 23 (2000) 11121-11128
27. Kao C.C., Singh P., and Ecker D.J. De novo initiation of viral RNA-dependent RNA synthesis. Virology 287 2 (2001) 251-260
28. Krab I.M., Caldwell C., Gallie D.R., and Bol J.F. Coat protein enhances translational efficiency of alfalfa mosaic virus RNAs and interacts with the eIF4G component of initiation factor eIF4F. J. Gen. Virol. 86 Pt. 6 (2005) 1841-1849
29. Kruseman J., Kraal B., Jaspars E.M.J., Bol J.F., Brederode F., and Veldstra H. Molecular weight of the coat protein of alfalfa mosaic virus. Biochemistry 10 3 (1971) 447-455
30. Laforest S.M., and Gehrke L. Spatial determinants of the alfalfa mosaic virus coat protein binding site. RNA 10 1 (2004) 48-58
31. Lai M.M. Cellular factors in the transcription and replication of viral RNA genomes: a parallel to DNA-dependent RNA transcription. Virology 244 1 (1998) 1-12
32. Lohmann V., Korner F., Herian U., and Bartenschlager R. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J. Virol. 71 11 (1997) 8416-8428
33. Maizels N., and Weiner A.M. Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc. Natl. Acad. Sci. U.S.A. 91 15 (1994) 6729-6734
34. Maizels N., and Weiner A.M. The genomic tag hypothesis: what molecular fossils tell us about the evolution of tRNA. In: Gesteland R., Cech T.R., and Atkins J. (Eds). The RNA World. 2nd ed. (1999), Cold Spring Harbor Press, Cold Spring Harbor 79-111
35. Miller W.A., Bujarski J.J., Dreher T.W., and Hall T.C. Minus-strand initiation by brome mosaic virus replicase within the 3′ tRNA-like structure of native and modified templates. J. Mol. Biol. 187 (1986) 537-546
36. Nagy P.D., Carpenter C.D., and Simon A.E. A novel 3′-end repair mechanism in an RNA virus. Proc. Natl. Acad. Sci. U.S.A. 94 4 (1997) 1113-1118
37. Neeleman L., and Bol J.F. cis-Acting functions of alfalfa mosaic virus proteins involved in replication and encapsidation of viral RNA. Virology 254 2 (1999) 324-333
38. Neeleman L., Olsthoorn R.C., Linthorst H.J., and Bol J.F. Translation of a nonpolyadenylated viral RNA is enhanced by binding of viral coat protein or polyadenylation of the RNA. Proc. Natl. Acad. Sci. U.S.A. 98 25 (2001) 14286-14291
39. Neeleman L., Linthorst H.J., and Bol J.F. Efficient translation of alfamovirus RNAs requires the binding of coat protein dimers to the 3′ termini of the viral RNAs. J. Gen. Virol. 85 Pt. 1 (2004) 231-240
40. Olsthoorn R.C., Mertens S., Brederode F.T., and Bol J.F. A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. EMBO J. 18 17 (1999) 4856-4864
41. Olsthoorn R.C., Haasnoot P.C., and Bol J.F. Similarities and differences between the subgenomic and minus-strand promoters of an RNA plant virus. J. Virol. 78 8 (2004) 4048-4053
42. Petrillo J.E., Rocheleau G., Kelley-Clarke B., and Gehrke L. Evaluation of the conformational switch model for coat protein function in alfalfa mosaic virus replication. J. Virol. 79 9 (2005) 5743-5751
43. Pogany J., White K.A., and Nagy P.D. Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J. Virol. 79 8 (2005) 4859-4869
44. Quadt R., Rosdorff H.J.M., Hunt T.W., and Jaspars E.M.J. Analysis of the protein composition of alfalfa mosaic virus RNA-dependent RNA polymerase. Virology 182 1 (1991) 309-315
45. Rao A.L.N., Dreher T.W., Marsh L.E., and Hall T.C. Telomeric function of the tRNA-like structure of brome mosaic virus RNA. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 5335-5339
46. Reusken C.B.E.M., Neeleman L., and Bol J.F. The 3′-untranslated region of alfalfa mosaic virus RNA 3 contains at least two independent binding sites for viral coat protein. Nucleic Acids Res. 22 8 (1994) 1346-1353
47. Reusken C.B.E.M., Neeleman L., Brederode F.T., and Bol J.F. Mutations in coat protein binding sites of alfalfa mosaic virus RNA 3 affect subgenomic RNA 4 accumulation and encapsidation of viral RNAs. J. Virol. 71 11 (1997) 8385-8391
48. Rocheleau G., Petrillo J., Guogas L., and Gehrke L. Degenerate in vitro genetic selection reveals mutations that diminish alfalfa mosaic virus RNA replication without affecting coat protein binding. J. Virol. 78 15 (2004) 8036-8046
49. Schwartz M., Chen J., Lee W.M., Janda M., and Ahlquist P. Alternate, virus-induced membrane rearrangements support positive-strand RNA virus genome replication. Proc. Natl. Acad. Sci. U.S.A. 101 31 (2004) 11263-11268
50. Stork J., Panaviene Z., and Nagy P.D. Inhibition of in vitro RNA binding and replicase activity by phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus. Virology 343 1 (2005) 79-92
51. Taschner P.E.M., Vanderkuyl A.C., Neeleman L., and Bol J.F. Replication of an incomplete alfalfa mosaic virus genome in plants transformed with viral replicase genes. Virology 181 2 (1991) 445-450
52. Van Der Heijden M.W., Carette J.E., Reinhoud P.J., Haegi A., and Bol J.F. Alfalfa mosaic virus replicase proteins P1 and P2 interact and colocalize at the vacuolar membrane. J. Virol. 75 4 (2001) 1879-1887
53. van Dijk A.A., Makeyev E.V., and Bamford D.H. Initiation of viral RNA-dependent RNA polymerization. J. Gen. Virol. 85 Pt. 5 (2004) 1077-1093
54. van Rossum C.M., Reusken C.B., Brederode F.T., and Bol J.F. 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 Pt. 11 (1997) 3045-3049
55. van Vloten-Doting L. Coat protein is required for infectivity of tobacco streak virus: biological equivalence of the coat proteins of tobacco streak and alfalfa mosaic virus. Virology 65 (1975) 215-225
56. van der Kuyl A.C., Neeleman L., and Bol J.F. Role of alfalfa mosaic virus coat protein in regulation of the balance between viral plus and minus strand RNA synthesis. Virology 185 (1991) 496-499
57. Vlot A.C., Neeleman L., Linthorst H.J., and Bol J.F. 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 14 (2001) 6440-6449
58. Weiner A.M., and Maizels N. tRNA-like structures tag the 3′ ends of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 7383-7387
59. Yang Y., Rijnbrand R., Watowich S., and Lemon S.M. Genetic evidence for an interaction between a picornaviral cis-acting RNA replication element and 3CD protein. J. Biol. Chem. 279 13 (2004) 12659-12667
60. Zuidema D., Bierhuizen M.F.A., Cornelissen B.J.C., Bol J.F., and Jaspars E.M.J. Coat protein binding sites on RNA 1 of alfalfa mosaic virus. Virology 125 (1983) 361-369
61. Zuker M., and Jacobson A.B. Using reliability information to annotate RNA secondary structures. RNA 4 6 (1998) 669-679