Multifunctional roles for the N-terminal basic motif of Alfalfa mosaic virus coat protein: Nucleolar/cytoplasmic shuttling, modulation of RNA-binding activity, and virion formation

Molecular Plant-Microbe Interactions

Volumn 25, Issue 8, 2012, Pages 1093-1103

  Herranz, Mari Carmen ^a   Pallas, Vicente ^a   Aparicio, Frederic ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; COAT PROTEIN, ALFALFA MOSAIC VIRUS; KARYOPHERIN ALPHA; LYSINE;

AMINO ACID SEQUENCE; ARTICLE; CYTOPLASM; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOLUS; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; TOBACCO; VIRION; VIROLOGY; VIRUS REPLICATION;

ALPHA KARYOPHERINS; AMINO ACID SEQUENCE; CAPSID PROTEINS; CELL NUCLEOLUS; CYTOPLASM; LYSINE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TOBACCO; VIRION; VIRUS REPLICATION;

ALFALFA MOSAIC VIRUS;

EID: 84863592085     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-04-12-0079-R     Document Type: Article

References (63)

1. Ævarsson, A., Brazhnikov, E., Garber, M., Zherltonosova, J., Chirgadze, Y., Al-Karadaghi, S., Suensson, L. A., and Liljas, A. 1994. Three-dimensional structure of the ribosomal translocase: Elongation factor G from Thermus thermophilus. EMBO (Eur. Mol. Biol. Organ.) J. 13:3669-3677. (Pubitemid 24275012)
2. Ansel-McKinney, P., Scott, S. W., Swanson, M., Ge, X., and Gehrke, L. 1996. A plant viral coat protein RNA binding consensus sequence contains a crucial arginine. EMBO (Eur. Mol. Biol. Organ.) J. 15:5077-5084. (Pubitemid 26315818)
3. Aparicio, F., Vilar, M., Perez-Paya, E., and Pallas, V. 2003. The coat protein of Prunus necrotic ringspot virus specifically binds to and regulates the conformation of its genomic RNA. Virology 313:213-223. (Pubitemid 37013605)
4. Aparicio, F., Sánchez-Navarro, J., and Pallás, V. 2006. In vitro and in vivo mapping of the Prunus necrotic ringspot virus coat protein C-terminal dimerization domain by bimolecular fluorescence complementation. J. Gen. Virol. 87:1745-1750. (Pubitemid 43827230)
5. Asurmendi, S., Berg, R. H., Koo, J. C., and Beachy, R. N. 2004. Coat protein regulates formation of replication complexes during Tobacco mosaic virus infection. Proc. Natl. Acad. Sci. U. S. A. 101:1415-1420. (Pubitemid 38182703)
6. Baer, M., Houser, F., Loesch-Fries, L. S., and Gehrke, L. 1994. Specific RNA binding by amino-terminal peptides of alfalfa mosaic virus coat protein. EMBO (Eur. Mol. Biol. Organ.) J. 13:727-735. (Pubitemid 24050688)
7. Ballas, N., and Citovsky, V. 1997. Nuclear localization signal binding proteins from Arabidopsis mediates nuclear import of Agrobacterium-VirD2 protein. Proc. Natl. Acad. Sci. U. S. A. 94:10723-10728. (Pubitemid 27430801)
8. Bamunusinghe, D., Seo, J.-K., and Rao, A. L. N. 2011. Subcellular localization and rearrangement of endoplasmic reticulum by Brome mosaic virus capsid protein. J. Virol. 85:2953-2963.
9. Bhattacharjee, S., Lee, L.-Y., Oltmanns, H., Cao, H., Veena, Cuperus, J., and Stanton, B. G. 2008. IMPa-4, an Arabidopsis importin a isoform, is preferentially involved in agrobacterium-mediated plant transformation. Plant Cell 20:2661-2680. (Pubitemid 352844583)
10. Bol, J. F. 2005. Replication of alfamo-and ilarviruses: Role of the coat protein. Annu. Rev. Phytopathol. 43:39-62. (Pubitemid 41318864)
11. Boyne, J.-R., and Whitehouse, A. 2006. Nucleolar trafficking is essential for nuclear export of intronless herpesvirus mRNA. Proc. Natl. Acad. Sci. U. S. A. 103:15190-15195. (Pubitemid 44583186)
12. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W., and Baulcombe, D. C. 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO (Eur. Mol. Biol. Organ.) J. 17:6739-6746. (Pubitemid 28521807)
13. Canto, T., Uhrig, J. F., Swanson, M., Wright, K. M., and MacFarlane, S. A. 2006. Translocation of Tomato bushy stunt virus P19 protein into the nucleus by ALY proteins compromises its silencing suppressor activity. J. Virol. 80:9064-9072. (Pubitemid 44359980)
14. Chen, M. H., and Icenogle, J. P. 2004. Rubella virus capsid protein modulates viral genome replication and virus infectivity. J. Virol. 78:4314-4322. (Pubitemid 38437234)
15. Crivelli, G., Ciuffo, M., Genre, A., Masenga, V., and Turina, M. 2011 Reverse genetic analysis of ourmiaviruses reveals the nucleolar localization of the coat protein in Nicotiana benthamiana and unusual requirements for virion formation. J. Virol. 85:5091-5104.
16. Csorba, T., Pantaleo, V., and Burgyan, J. 2009. RNA silencing: An antiviral mechanism. Adv. Virus Res. 75:53-71.
17. De Graaff, M., Man In T'Veld, M. R., and Jaspars, E. M. 1995. 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 208:583-589.
18. Emmott, E., and Hiscox, J. A. 2009. Nucleolar targeting: The hub of the matter. EMBO (Eur. Mol. Biol. Organ.) Rep. 10:231-238.
19. Greco, A. 2009. Involvement of the nucleolus in replication of human viruses. Rev. Med. Virol. 19:201-214.
20. Guogas, L. M., Laforest, S. M., and Gehrke, L. 2005. Coat protein activation of Alfalfa mosaic virus replication is concentration dependent. J. Virol. 79:5752-5761. (Pubitemid 40548244)
21. Haupt, S., Stroganova, T., Ryabov, E., Kim, S. H., Fraser, G., Duncan, G., Mayo, M. A., Barker, H., and Taliansky, M. 2005. Nucleolar localization of Potato leafroll virus capsid proteins. J. Gen. Virol. 86:2891-2896. (Pubitemid 41410481)
22. He, S., Huang, K., Zhang, X., Yu, X., Huang, P., and An, C. 2011. The LSD1-type zinc finger motifs of Pisum sativa lsd1 are a novel nuclear localization signal and interact with importin alpha. PLoS One 6:e22131. Published online.
23. Hübner, S., Smith, H. M. S., Hu, W., Chan, C. K., Rihs, H.-P., Paschali, B. M., Raikhel, N. V., and Jans, D. A. 1999. Plant importin a binds nuclear localization sequences with high affinity and can mediate nuclear import independent of importin b. J. Biol. Chem. 274:22610-22617.
24. Kao, C. C., Ni, P., Hema, M., Huang, X., and Dragnea, B. 2011. The coat protein leads the way: An update on basic and applied studies with the Brome mosaic virus coat protein. Mol. Plant Pathol. 678:403-412.
25. Kim, S. H., MacFarlane, S., Kalinina, N. O., Rakitina, D., Ryabov, E. V., Gillespie, T., Haupt, S., Brown, J. W. S., and Taliansky, M. 2007a. Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc. Nat. Acad. Sci. U. S. A. 104:11115-11120. (Pubitemid 47175235)
26. Kim, S. H., Ryabov, E. V., Kalinina, N. O., Rakitina, D. V., Gillespie, T., MacFarlane, S., Haupt, S., Brown, J. W. S., and Taliansky, M. 2007b. Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO (Eur. Mol. Biol. Organ.) J. 26:2169-2179. (Pubitemid 46625803)
27. Krab, I. M., Caldwell, C., Gallie, R. D., and Bol, J. F. 2005. Coat protein enhances translational efficiency of Alfalfa mosaic virus RNAs and interacts with the eIF4G component of initiation factor eIF4F. J. Gen. Virol. 86:1841-1849. (Pubitemid 40766898)
28. Krichevsky, A., Kozlovsky, S. V., Gafni, Y., and Citovsky, V. 2006. Nuclear import and export of plant virus proteins and genomes. Mol. Plant Pathol. 7:131-146.
29. Kumar, A., Reddy, V. S., Yusibov, V., Chipman, P. R., Hata, Y., Fita, I., Fukuyama, K., Rossmann, M. G., Loesch-Fries, L. S., Baker, T. S., and Johnson, J. E. 1997. The structure of alfalfa mosaic virus capsid protein assembled as a T 5 1 icosahedral particle at 4.0-Å resolution. J. Virol. 71:7911-7916. (Pubitemid 27391742)
30. Kurita, K., Honda, K., Suzuma, S., Takamatsu, S., Nakamura, K., and Yamane, K. 1996. Identification of a region of Bacillus subtilis Ffh, a homologue of mammalian SRP54 protein, that is essential for binding to small cytoplasmic RNA. J. Biol. Chem. 271:13140-13146. (Pubitemid 26175892)
31. La Cour, T., Gupta, R., Rapacki, K., Skriver, K., Poulsen, F. M., and Brunak, S. 2003. NESbase version 1.0: A database of nuclear export signals. Nucleic Acids Res. 31:393-396. (Pubitemid 36150410)
32. Laemmli, U. K. 1970. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680-685.
33. Loesch-Fries, L. S., Halk, E. L., Nelson, S. E., and Krahn, K. J. 1985. Human leukocyte interferon does not inhibit alfalfa mosaic virus in protoplasts or tobacco tissue. Virology 143:626-629. (Pubitemid 15035311)
34. Neeleman, L., van der Kuil, A. C., and Bol, J. F. 1991. Role of alfalfa mosaic virus coat protein gene in symptom formation. Virology 181:687-698.
35. Neeleman, L., Linthorst, H. J. M., and Bol, J. F. 2004. Efficient translation of alfamovirus RNAs requires the binding of coat protein dimers to the 3' termini of the viral RNAs. J. Gen. Virol. 85:231-240. (Pubitemid 38128888)
36. Pallas, V., and Garcia, J. A. 2011. How do plant viruses induce disease? Interactions and interference with host components. J. Gen Virol. 92:2691-2705.
37. Pallas, V., Mas, P., and Sanchez-Navarro, J. A. 1998. Detection of plant RNA viruses by nonisotopic dot-blot hybridization. Methods Mol. Biol. 81:461-468.
38. Qi, D., Omarov, R. T., and Scholthof, K. B. G. 2008. The complex subcellular distribution of satellite panicum mosaic virus capsid protein reflects its multifunctional role during infection. Virology 376:154-164.
39. Quadt R., Rosdorff H. J. M., Hunt T. W., and Jaspars, E. M. J. 1991. Analysis of the protein composition of alfalfa mosaic virus RNA-dependent RNA polymerase. Virology 182:309-315.
40. Rajamaki, M. L., and Valkonen, J. P. T. 2009. Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana species. Plant Cell 21:2485-2502.
41. Rao, A. L., and Grantham G. L. 1996. Molecular studies on bromovirus capsid protein. II. Functional analysis of the amino-terminal argininerich motif and its role in encapsidation, movement, and pathology. Virology 226:294-305. (Pubitemid 27025809)
42. Reichert, V. L., Choi, M., Petrillo, J. E., and Gehrke, L. 2007. Alfalfa mosaic virus coat protein bridges RNA and RNA-dependent RNA polymerase in vitro. Virology 364:214-226. (Pubitemid 46829283)
43. Reusken, C. B. E. M., Neeleman, L., and Bol, J. F. 1994. The 3'-untranslated region of alfalfa mosaic virus RNA 3 contains at least two independent binding sites for viral coat protein. Nucleic Acids Res. 22:1346-1353.
44. Roy, A., Kucukural, A., and Zhang, Y. 2010. I-TASSER: A unified platform for automated protein structure and function prediction. Nat. Protocols 5:725-738.
45. Ryabov, E. V., Kim, S. H., and Taliansky, M. E. 2004. Identification of a nuclear localization signal and nuclear export signal of the umbraviral long-distance RNA movement protein. J. Gen. Virol. 85:1329-1333. (Pubitemid 38659797)
46. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
47. Sanchez-Navarro, J. A., and Bol, J. F. 2001. Role of the Alfalfa mosaic virus movement protein and coat protein in virus transport. Mol. Plant-Microbe Interact. 14:1051-1062. (Pubitemid 32818293)
48. Sanchez-Navarro, J. A., and Pallas, V. 1997. Evolutionary relationships in the ilarviruses: Nucleotide sequence of prunus necrotic ringspot virus RNA 3. Arch. Virol. 142:749-763. (Pubitemid 27185680)
49. Sanchez-Navarro, J. A., Miglino, R., Ragozzino, A., and Bol, J. F. 2001. Engineering of Alfalfa mosaic virus RNA 3 into an expression vector. Arch. Virol. 146:923-939. (Pubitemid 32477405)
50. Scholthof, H. B. 2005. Plant virus transport: Motions of functional equivalence. Trends Plant Sci. 10:376-382. (Pubitemid 41059665)
51. Semashko, M. A., Rakitina, D. V., González, I., Canto, T., Kalinina, N. O., and Taliansky, M. E. 2012. Movement protein of hordeivirus interacts in vitro and in vivo with coilin, a major structural protein of Cajal bodies. Dokl. Biochem. Biophysics. 44:57-60.
52. Sharma, P., and Ikegami, M. 2009. Characterization of signals that dictate nuclear/nucleolar and cytoplasmic shuttling of the capsid protein of Tomato leaf curl Java virus associated with DNAb satellite. Virus Res. 144:145-153.
53. Taliansky, M. E., Brown, J. W. S., Rajamaki, M. L., Valkonen, J. P. T., and Kalinina, N. O. 2010. Involvement of the plant nucleolus in virus and viroid infections: Parallels with animal pathosystems. Adv. Virus Res. 77:119-158.
54. Taschner, P. E., Van der Kuyl, A. C., Neeleman, L., and Bol, J. F. 1991. Replication of an incomplete alfalfa mosaic virus genome in plants transformed with viral replicase genes. Virology 181:445-450.
55. Tenllado, F., and 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. (Pubitemid 30131968)
56. Van der Vossen E. A. G., Neeleman L., and Bol, J. F. 1994. Early and late functions of alfalfa mosaic virus coat protein can be mutated separately. Virology 202:891-903. (Pubitemid 24254903)
57. Van der Vossen, E. A. G., Reusken, B. E. M., and Bol, J. F. 1996. Cis-preferential stimulation of alfalfa mosaic virus RNA 3 accumulation by the viral coat protein a. Virology 220:163-70. (Pubitemid 26202350)
58. Vanpeltheerschap, H., Verbeek, H., Slot, J. W., and Vanvlotendoting, L. 1987. The location of coat protein and viral RNAs of alfalfa mosaicvirus in infected tobacco leaves and protoplasts. Virology 160:297-300.
59. Wang, Y., Tzfira, T., Gaba, V., Citovsky, V., Palukaitis, P., and Gal-On, A. 2004. Functional analysis of the Cucumber mosaic virus 2b protein: Pathogenicity and nuclear localization. J. Gen. Virol. 85:3135-3147. (Pubitemid 39360058)
60. Yusibov, V. M., and 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.
61. Yusibov, V., and Loesch-Fries, L. S. 1998. Functional significance of three basic n terminal amino acids of alfalfa mosaic virus coat protein. Virology 242:1-5. (Pubitemid 28396352)
62. Zhang, Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinf. 9:40.
63. Zhang, Y. J., Zhang, X. F., Niu, S. F., Han, C. G., Yu, J. L., and Li, D. W. 2011. Nuclear localization of Beet black scorch virus capsid protein and its interaction with importin alpha. Virus Res. 155:307-315.