Ribosomal protein P0 promotes potato virus a infection and functions in viral translation together with VPg and eIF(iso)4E

Journal of Virology

Volumn 87, Issue 8, 2013, Pages 4302-4312

  Hafrén, Anders ^a   Eskelin, Katri ^a   Mäkinen, Kristiina ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTIC INITIATION FACTOR (ISO) 4E; INITIATION FACTOR 4E; PROTEIN VPG; RIBOSOME PROTEIN; RIBOSOME PROTEIN P0; RIBOSOME PROTEIN P1; RIBOSOME PROTEIN P2; RIBOSOME PROTEIN P3; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; POTATO VIRUS A INFECTION; POTYVIRUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PURIFICATION; RNA DEGRADATION; RNA TRANSLATION; VIRAL PLANT DISEASE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

EUKARYOTIC INITIATION FACTOR-4E; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; POTYVIRUS; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; SEQUENCE ANALYSIS, DNA; TOBACCO; VIRAL PROTEINS;

POTATO VIRUS A;

EID: 84875800979     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03198-12     Document Type: Article

References (71)

1. Bushell M, Sarnow P. 2002. Hijacking the translation apparatus by RNA viruses. J. Cell Biol. 158:395-399.
2. Dreher TW, Miller WA. 2006. Translational control in positive strand RNA plant viruses. Virology 344:185-197.
3. Lloyd RE. 2006. Translational control by viral proteinases. Virus Res. 119:76-88.
4. Thompson SR, Sarnow P. 2003. Enterovirus 71 contains a type I IRES element that functions when eukaryotic initiation factor eIF4G is cleaved. Virology 315:259-266.
5. Park HS, Himmelbach A, Browning KS, Hohn T, Ryabova LA. 2001. A plant viral "reinitiation" factor interacts with the host translational machinery. Cell 106:723-733.
6. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT. 2003. Host factors in positive-strand RNA virus genome replication. J. Virol. 77: 8181-8186.
7. Blumenthal T, Carmichael GG. 1979. RNA replication: function and structure of Qbeta-replicase. Annu. Rev. Biochem. 48:525-548.
8. Li Z, Pogany J, Tupman S, Esposito AM, Kinzy TG, Nagy PD. 2010. Translation elongation factor 1A facilitates the assembly of the tombusvirus replicase and stimulates minus-strand synthesis. PLoS Pathog. 6:e1001175. doi:10.1371/journal.ppat.1001175.
9. Osman TA, Buck KW. 1997. The tobacco mosaic virus RNA polymerase complex contains a plant protein related to the RNA-binding subunit of yeast eIF-3. J. Virol. 71:6075-6082.
10. Quadt R, Kao CC, Browning KS, Hershberger RP, Ahlquist P. 1993. Characterization of a host protein associated with brome mosaic virus RNA-dependentRNApolymerase. Proc. Natl. Acad. Sci. U. S. A. 90:1498-1502.
11. Taylor DN, Carr JP. 2000. The GCD10 subunit of yeast eIF-3 binds the methyltransferase-like domain of the 126 and 183 kDa replicase proteins of tobacco mosaic virus in the yeast two-hybrid system. J. Gen. Virol. 81:1587-1591.
12. Mizumoto H, Iwakawa HO, Kaido M, Mise K, Okuno T. 2006. Capindependent translation mechanism of red clover necrotic mosaic virus RNA2 differs from that of RNA1 and is linked to RNA replication. J. Virol. 80:3781-3791.
13. Sanz MA, Castello A, Carrasco L. 2007. Viral translation is coupled to transcription in Sindbis virus-infected cells. J. Virol. 81:7061-7068.
14. Sanz MA, Castello A, Ventoso I, Berlanga JJ, Carrasco L. 2009. Dual mechanism for the translation of subgenomic mRNA from Sindbis virus in infected and uninfected cells. PLoS One 4:e4772. doi:10.1371/journal .pone.0004772.
15. Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363-374.
16. Beauchemin C, Boutet N, Laliberte JF. 2007. Visualization of the interaction between the precursors of VPg, the viral protein linked to the genome of turnip mosaic virus, and the translation eukaryotic initiation factor iso 4E in planta. J. Virol. 81:775-782.
17. Beauchemin C, Laliberte JF. 2007. The poly(A) binding protein is internalized in virus-induced vesicles or redistributed to the nucleolus during turnip mosaic virus infection. J. Virol. 81:10905-10913.
18. Thivierge K, Cotton S, Dufresne PJ, Mathieu I, Beauchemin C, Ide C, Fortin MG, Laliberte JF. 2008. Eukaryotic elongation factor 1A interacts with turnip mosaic virus RNA-dependent RNA polymerase and VPg-Pro in virus-induced vesicles. Virology 377:216-225.
19. Dufresne PJ, Thivierge K, Cotton S, Beauchemin C, Ide C, Ubalijoro E, Laliberte JF, Fortin MG. 2008. Heat shock 70 protein interaction with turnip mosaic virus RNA-dependent RNA polymerase within virusinduced membrane vesicles. Virology 374:217-227.
20. Wang A, Krishnaswamy S. 2012. Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol. Plant Pathol. 13:795-803.
21. Gonzalo P, Reboud JP. 2003. The puzzling lateral flexible stalk of the ribosome. Biol. Cell 95:179-193.
22. Wool IG, Chan YL, Gluck A, Suzuki K. 1991. The primary structure of rat ribosomal proteins P0, P1, and P2 and a proposal for a uniform nomenclature for mammalian and yeast ribosomal proteins. Biochimie 73: 861-870.
23. Bailey-Serres J, Vangala S, Szick K, Lee CH. 1997. Acidic phosphoprotein complex of the 60S ribosomal subunit of maize seedling roots. Components and changes in response to flooding. Plant Physiol. 114:1293-1305.
24. Szick K, Springer M, Bailey-Serres J. 1998. Evolutionary analyses of the 12-kDa acidic ribosomal P-proteins reveal a distinct protein of higher plant ribosomes. Proc. Natl. Acad. Sci. U. S. A. 95:2378-2383.
25. Sanchez-Madrid F, Vidales FJ, Ballesta JP. 1981. Effect of phosphorylation on the affinity of acidic proteins from Saccharomyces cerevisiae for the ribosomes. Eur. J. Biochem. 114:609-613.
26. Tsurugi K, Ogata K. 1985. Evidence for the exchangeability of acidic ribosomal proteins on cytoplasmic ribosomes in regenerating rat liver. J. Biochem. 98:1427-1431.
27. Zinker S, Warner JR. 1976. The ribosomal proteins of Saccharomyces cerevisiae. Phosphorylated and exchangeable proteins. J. Biol. Chem. 251: 1799-1807.
28. Aruna K, Chakraborty T, Rao PN, Santos C, Ballesta JP, Sharma S.2005. Functional complementation of yeast ribosomal P0 protein with Plasmodium falciparum P0. Gene 357:9-17.
29. Kouyanou S, Santos C, Koliaraki V, Ballesta JP. 2003. Protein BmP0 from the silkworm Bombyx mori can be assembled and is functional in the Saccharomyces cerevisiae ribosomal stalk in the absence of the acidic P1 and P2 proteins. Gene 314:173-179.
30. Rodriguez-Gabriel MA, Remacha M, Ballesta JP. 2000. The RNA interacting domain but not the protein interacting domain is highly conserved in ribosomal protein P0. J. Biol. Chem. 275:2130-2136.
31. Remacha M, Jimenez-Diaz A, Bermejo B, Rodriguez-Gabriel MA, Guarinos E, Ballesta JP. 1995. Ribosomal acidic phosphoproteins P1 and P2 are not required for cell viability but regulate the pattern of protein expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:4754-4762.
32. Remacha M, Jimenez-Diaz A, Santos C, Briones E, Zambrano R, Rodriguez Gabriel MA, Guarinos E, Ballesta JP. 1995. Proteins P1, P2, and P0, components of the eukaryotic ribosome stalk. New structural and functional aspects. Biochem. Cell Biol. 73:959-968.
33. Huang C, Mandava CS, Sanyal S. 2010. The ribosomal stalk plays a key role in IF2-mediated association of the ribosomal subunits. J. Mol. Biol. 399:145-153.
34. Martinez-Azorin F, Remacha M, Ballesta JP. 2008. Functional characterization of ribosomal P1/P2 proteins in human cells. Biochem. J. 413: 527-534.
35. Hafren A, Hofius D, Ronnholm G, Sonnewald U, Makinen K. 2010. HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant Cell 22:523-535.
36. Williams AJ, Werner-Fraczek J, Chang IF, Bailey-Serres J. 2003. Regulated phosphorylation of 40S ribosomal protein S6 in root tips of maize. Plant Physiol. 132:2086-2097.
37. Eskelin K, Suntio T, Hyvarinen S, Hafren A, Makinen K. 2010. Renilla luciferase-based quantitation of potato virus A infection initiated with Agrobacterium infiltration of N. benthamiana leaves. J. Virol. Methods 164:101-110.
38. Curtis MD, Grossniklaus U. 2003. A gateway cloning vector set for highthroughput functional analysis of genes in planta. Plant Physiol. 133:462-469.
39. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T. 2007. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104:34-41.
40. Eskelin K, Hafren A, Rantalainen KI, Makinen K. 2011. Potyviral VPg enhances viralRNAtranslation and inhibits reportermRNAtranslation in planta. J. Virol. 85:9210-9221.
41. Helliwell C, Waterhouse P. 2003. Constructs and methods for highthroughput gene silencing in plants. Methods 30:289-295.
42. Johansen LK, Carrington JC. 2001. Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol. 126:930-938.
43. Elkon K, Skelly S, Parnassa A, Moller W, Danho W, Weissbach H, Brot N. 1986. Identification and chemical synthesis of a ribosomal protein antigenic determinant in systemic lupus erythematosus. Proc. Natl. Acad. Sci. U. S. A. 83:7419-7423.
44. Szick-Miranda K, Bailey-Serres J. 2001. Regulated heterogeneity in 12- kDa P-protein phosphorylation and composition of ribosomes in maize (Zea mays L.). J. Biol. Chem. 276:10921-10928.
45. Santos C, Ballesta JP. 1994. Ribosomal protein P0, contrary to phosphoproteins P1 and P2, is required for ribosome activity and Saccharomyces cerevisiae viability. J. Biol. Chem. 269:15689-15696.
46. Dunoyer P, Thomas C, Harrison S, Revers F, Maule A. 2004. A cysteinerich plant protein potentiates potyvirus movement through an interaction with the virus genome-linked protein VPg. J. Virol. 78:2301-2309.
47. Borden KL, CampbellDwyer EJ, Carlile GW, Djavani M, Salvato MS. 1998. Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins. J. Virol. 72:3819-3826.
48. Lo KY, Li Z, Bussiere C, Bresson S, Marcotte EM, Johnson AW. 2010. Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol. Cell 39:196-208.
49. Krokowski D, Tchorzewski M, Boguszewska A, McKay AR, Maslen SL, Robinson CV, Grankowski N. 2007. Elevated copy number of L-A virus in yeast mutant strains defective in ribosomal stalk. Biochem. Biophys. Res. Commun. 355:575-580.
50. Funkhouser AW, Schultz DE, Lemon SM, Purcell RH, Emerson SU. 1999. Hepatitis A virus translation is rate-limiting for virus replication in MRC-5 cells. Virology 254:268-278.
51. Simoes EA, Sarnow P. 1991. An RNA hairpin at the extreme 5= end of the poliovirus RNA genome modulates viral translation in human cells. J. Virol. 65:913-921.
52. Cherry S, Doukas T, Armknecht S, Whelan S, Wang H, Sarnow P, Perrimon N. 2005. Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev. 19:445-452.
53. Basso J, Dallaire P, Charest PJ, Devantier Y, Laliberte JF. 1994. Evidence for an internal ribosome entry site within the 5= non-translated region of turnip mosaic potyvirus RNA. J. Gen. Virol. 75(Part 11):3157-3165.
54. Gallie DR. 2001. Cap-independent translation conferred by the 5= leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J. Virol. 75:12141-12152.
55. Niepel M, Gallie DR. 1999. Identification and characterization of the functional elements within the tobacco etch virus 5= leader required for cap-independent translation. J. Virol. 73:9080-9088.
56. Yang C, Zhang C, Dittman JD, Whitham SA. 2009. Differential requirement of ribosomal protein S6 by plant RNA viruses with different translation initiation strategies. Virology 390:163-173.
57. Martin MT, Garcia JA. 1991. Plum pox potyvirus RNA replication in a crude membrane fraction from infected Nicotiana clevelandii leaves. J. Gen. Virol. 72(Part 4):785-790.
58. Schaad MC, Jensen PE, Carrington JC. 1997. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum- targeted viral protein. EMBO J. 16:4049-4059.
59. Carvalho CM, Santos AA, Pires SR, Rocha CS, Saraiva DI, Machado JP, Mattos EC, Fietto LG, Fontes EP. 2008. Regulated nuclear trafficking of rpL10A mediated by NIK1 represents a defense strategy of plant cells against virus. PLoS Pathog. 4:e1000247. doi:10.1371/journal.ppat.1000247.
60. Brendel C, Rehbein M, Kreienkamp HJ, Buck F, Richter D, Kindler S. 2004. Characterization of Staufen 1 ribonucleoprotein complexes. Biochem. J. 384:239-246.
61. Jonson L, Vikesaa J, Krogh A, Nielsen LK, Hansen T, Borup R, Johnsen AH, Christiansen J, Nielsen FC. 2007. Molecular composition of IMP1 ribonucleoprotein granules. Mol. Cell. Proteomics 6:798-811.
62. Yacoub A, Kelley MR, Deutsch WA. 1996. Drosophila ribosomal protein PO contains apurinic/apyrimidinic endonuclease activity. Nucleic Acids Res. 24:4298-4303.
63. Huang TS, Wei T, Laliberte JF, Wang A. 2010. A host RNA helicase-like protein, AtRH8, interacts with the potyviral genome-linked protein, VPg, associates with the virus accumulation complex, and is essential for infection. Plant Physiol. 152:255-266.
64. Grangeon R, Cotton S, Laliberte JF. 2010. A model for the biogenesis of turnip mosaic virus replication factories. Commun. Integr. Biol. 3:363-365.
65. Cotton S, Grangeon R, Thivierge K, Mathieu I, Ide C, Wei T, Wang A, Laliberte JF. 2009. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 83:10460-10471.
66. Vuorinen AL, Gammelgard E, Auvinen P, Somervuo P, Dere S, Valkonen JPT. 2010. Factors underpinning the responsiveness and higher levels of virus resistance realised in potato genotypes carrying virusspecific R genes. Ann. Appl. Biol. 157:229-241.
67. Leonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberte JF. 2004. Interaction of VPg-Pro of turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J. Gen. Virol. 85:1055-1063.
68. Khan MA, Miyoshi H, Gallie DR, Goss DJ. 2008. Potyvirus genomelinked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J. Biol. Chem. 283:1340-1349.
69. Coller J, Parker R. 2004. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 73:861-890.
70. Jacobson A, Peltz SW. 1996. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem. 65:693-739.
71. Beckham CJ, Parker R. 2008. P bodies, stress granules, and viral life cycles. Cell Host Microbe 3:206-212.