Translation elongation factor 1B (eEF1B) is an essential host factor for Tobacco mosaic virus infection in plants

Virology

Volumn 439, Issue 2, 2013, Pages 105-114

  Hwang, JeeNa ^a   Oh, Chang Sik ^b   Kang, Byoung Cheorl ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

Author keywords

Eukaryotic translation elongation factor 1A; Eukaryotic translation elongation factor 1B; Host factor; Tobacco mosaic virus; Virus resistance

Indexed keywords

COAT PROTEIN; ELONGATION FACTOR 1ALPHA; ELONGATION FACTOR 1BETA; HOST FACTOR; MESSENGER RNA; METHYLTRANSFERASE; RNA POLYMERASE; VIRUS RNA;

ARTICLE; CAPSICUM ANNUUM; CONTROLLED STUDY; ELONGATION FACTOR 1ALPHA GENE; ELONGATION FACTOR 1BETA GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SILENCING; GENETIC CODE; IN VIVO STUDY; NICOTIANA BENTHAMIANA; NONHUMAN; PLANT GENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TOBACCO MOSAIC VIRUS; VIRAL PLANT DISEASE; VIRUS REPLICATION; VIRUS RESISTANCE;

GENE SILENCING; HOST-PATHOGEN INTERACTIONS; PEPTIDE ELONGATION FACTORS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RNA REPLICASE; TOBACCO; TOBACCO MOSAIC VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EUKARYOTA; NICOTIANA BENTHAMIANA; TOBACCO MOSAIC VIRUS;

EID: 84875803943     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.02.004     Document Type: Article

References (66)

1. Ahlquist P., Noueiry A.O., Lee W.M., Kushner D.B., Dye B.T. Host factors in positive-strand RNA virus genome replication. J. Virol. 2003, 77:8181-8186.
2. Ala-Poikela M., Goytia E., Haikonen T., Rajamäki M.L., Valkonen J.P. Helper component proteinase of the genus Potyvirus is an interaction partner of translation initiation factors eIF(iso)4E and eIF4E and contains a 4E binding motif. J. Virol. 2011, 85:6784-6794.
3. Ashby J.A., Stevenson C.E., Jarvis G.E., Lawson D.M., Maule A.J. Structure-based mutational analysis of eIF4E in relation to sbm1 resistance to pea seed-borne mosaic virus in pea. PLoS One 2011, 6:e15873.
4. Asurmendi S., Berg R.H., Koo J.C., Beachy R.N. Coat protein regulates formation of replication complexes during tobacco mosaic virus infection. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(5):1415-1420.
5. Bastin M., Hall T.C. Interaction of elongation-factor 1 with aminoacylated Brome mosaic virus and transfer RNAs. J. Virol. 1976, 20:117-122.
6. Blackwell J.L., Brinton M.A. Translation elongation factor-1 alpha interacts with the 3' stem-loop region of West Nile virus genomic RNA. J. Virol. 1997, 71:6433-6444.
7. Blumenthal T., Carmichael G.G. RNA replication function and structure of Qbeta-replicase. Annu. Rev. Biochem. 1979, 48:525-548.
8. Charron C., Nicolai M., Gallois J.L., Robaglia C., Moury B., Palloix A., Caranta C. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J. 2008, 54:56-68.
9. Chuang S.M., Chen L., Lambertson D., Anand M., Kinzy T.G., Madura K. Proteasome-mediated degradation of cotranslationally damaged proteins involves translation elongation factor 1A. Mol. Cell Biol. 2005, 25:403-413.
10. Cotton S., Grangeon R., Thivierge K., Mathieu I., Ide C., Wei T.Y., Wang A.M., Laliberte J.F. Turnip mosaic virus RNA replication complex vesicles are mobile, align with microfilaments, and are each derived from a single viral genome. J. Virol. 2009, 83:10460-10471.
11. Davis W.G., Blackwell J.L., Shi P.Y., Brinton M.A. Interaction between the cellular protein eEF1A and the 3'-terminal stem-loop of West Nile virus genomic RNA facilitates viral minus-strand RNA synthesis. J. Virol. 2007, 81:10172-10187.
12. De Nova-Ocampo M., Villegas-Sepuveda N., del Angel R.M. Translation elongation factor-1 alpha, La, and PTB interact with the 3' untranslated region of dengue 4 virus RNA. Virology 2002, 295:337-347.
13. Diaz-Pendon J.A., Truniger V., Nieto C., Garcia-Mas J., Bendahmane A., Aranda M.A. Advances in understanding recessive resistance to plant viruses. Mol. Plant Pathol. 2004, 5:223-233.
14. Dinesh-Kumar S.P., Anandalakshmi R., Marathe R., Schiff M., Liu Y. Virus-induced gene silencing. Methods Mol. Biol. 2003, 236:287-294.
15. Dong Y., Burch-Smith T.M., Liu Y., Mamillapalli P., Dinesh-Kumar S.P. A ligation-independent cloning tobacco rattle virus vector for high-throughput virus-induced gene silencing identifies roles for NbMADS4-1 and -2 in floral development. Plant Physiol. 2007, 145:1161-1170.
16. Dufresne P.J., Thivierge K., Cotton S., Beauchemin C., Ide C., Ubalijoro E., Laliberte J.F., Fortin M.G. Heat shock 70 protein interaction with Turnip mosaic virus RNA-dependent RNA polymerase within virus-induced membrane vesicles. Virology 2008, 374:217-227.
17. Earley K.W., Haag J.R., Pontes O., Opper K., Juehne T., Song K., Pikaard C.S. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 2006, 45(4):616-629.
18. Gao Z., Johansen E., Eyers S., Thomas C.L., Noel Ellis T.H., Maule A.J. The potyvirus recessive resistance gene, sbm1, identifies a novel role for translation initiation factor eIF4E in cell-to-cell trafficking. Plant J. 2004, 40:376-385.
19. Gross S.R., Kinzy T.G. Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol. 2005, 12:772-778.
20. Harris K.S., Xiang W., Alexander L., Lane W.S., Paul A.V., Wimmer E. Interaction of poliovirus polypeptide 3CDpro with the 5' and 3' termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding. J. Biol. Chem. 1994, 269:27004-27014.
21. Ishibashi K., Nishikiori M., Ishikawa M. Interactions between tobamovirus replication proteins and cellular factors: their impacts on virus multiplication. Mol. Plant Microbe Interact. 2010, 23(11):1413-1419.
22. Ishikawa M., Meshi T., Motoyoshi F., Takamatsu N., Okada Y. In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus. Nucleic Acids Res. 1986, 14(21):8291-8305. 1986.
23. Jenner C.E., Nellist C.F., Barker G.C., Walsh J.A. Turnip mosaic virus (TuMV) is able to use alleles of both eIF4E and eIF(iso)4E from multiple loci of the diploid Brassica rapa. Mol. Plant Microbe Interact. 2010, 23(11):1498-1505.
24. Johnson C.M., Perez D.R., French R., Merrick W.C., Donis R.O. The NS5A protein of bovine viral diarrhoea virus interacts with the alpha subunit of translation elongation factor-1. J. Gen. Virol. 2001, 82:2935-2943.
25. Joshi R.L., Ravel J.M., Haenni A.L. Interaction of turnip yellow mosaic virus Val-RNA with eukaryotic elongation factor EF-1 [alpha]. Search for a function. EMBO J. 1986, 5(6):1143-1148.
26. Kang B.C., Yeam I., Frantz J.D., Murphy J.F., Jahn M.M. The pvr1 locus in Capsicum encodes a translation initiation factor eIF4E that interacts with Tobacco etch virus VPg. Plant J. 2005, 42:392-405.
27. Kang B.C., Yeam I., Jahn M.M. Genetics of plant virus resistance. Annu. Rev. Phytopathol. 2005, 43:581-621.
28. Kanyuka K., Mcgrann G., Alhudaib K., Hariri D., Adams M.J. Biological and sequence analysis of a novel European isolate of Barley mild mosaic virus that overcomes the barley rym5 resistance gene. Arch. Virol. 2004, 149:1469-1480.
29. Kawakami S., Watanabe Y., Beachy R.N. Tobacco mosaic virus infection spreads cell to cell as intact replication complexes. Proc. Natl. Acad. Sci. U.S.A. 2004, 101(16):6291-6296.
30. Kidmose R.T., Vasiliev N.N., Chetverin A.B., Andersen G.R., Knudsen C.R. Structure of the Qbeta replicase, an RNA-dependent RNA polymerase consisting of viral and host proteins. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:10884-10889.
31. Knapp E., Danyluk G.M., Achor D., Lewandowski D.J. A bipartite Tobacco mosaic virus-defective RNA (dRNA) system to study the role of the N-terminal methyl transferase domain in cell-to-cell movement of dRNAs. Virology 2005, 341(1):47-58.
32. Le Sourd F., Boulben S., Le Bouffant R., Cormier P., Morales J., Belle R., Mulner-Lorillon O. eEF1B: at the dawn of the 21st century. Biochim. Biophys. Acta-Gene Struct. Expression 2006, 1759:13-31.
33. Leonard S., Plante D., Wittmann S., Daigneault N., Fortin M.G., Laliberte J.F. Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J. Virol. 2000, 74:7730-7737.
34. Lewandowski D.J., Dawson W.O. Functions of the 126- and 183-kDa proteins of tobacco mosaic virus. Virology 2000, 271(1):90-98.
35. Ling K.S., Harris K.R., Meyer J.D., Levi A., Guner N., Wehner T.C., Bendahmane A., Havey M.J. Non-synonymous single nucleotide polymorphisms in the watermelon eIF4E gene are closely associated with resistance to zucchini yellow mosaic virus. Theor. Appl. Genet. 2009, 120:191-200.
36. Liu J.Z., Blancaflor E.B., Nelson R.S. The Tobacco mosaic virus 126-kilodalton protein, a constituent of the virus replication complex, alone or within the complex aligns with and traffics along microfilaments. Plant Physiol. 2005, 138:1853-1865.
37. Liu Y., Schiff M., Dinesh-Kumar S.P. Involvement of MEK1 MAPKK, NTF6MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J. 2004, 38:800-809.
38. Lozan-Duran R., Rosas-Diaz T., Luna A.P., Bejarano E.R. Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS One 2011, 6(7):e22383.
39. Lu R., Martin-Hernandez A.M., Peart J.R., Malcuit I., Baulcombe D.C. Virus-induced gene silencing in plants. Methods 2003, 30:296-303.
40. Más P., Beachy R.N. Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J. Cell Biol. 1999, 147(5):945-958.
41. Matsuda D., Bauer L., Tinnesand K., Dreher T.W. Expression of the two nested overlapping reading frames of turnip yellow mosaic virus RNA is enhanced by a 5' cap and by 5' and 3' viral sequences. J. Virol. 2004, 78:9325-9335.
42. Matsuda D., Dreher T.W. The tRNA-like structure of Turnip yellow mosaic virus RNA is a 3'-translational enhancer. Virology 2004, 321:36-46.
43. Mazier M., Flamain F., Nicolaï M., Sarnette V., Caranta C. Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS One 2011, 6(12):e29595.
44. Miller S., Krijnse-Locker J. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 2008, 6(5):363-374.
45. Nagy P.D., Pogany J. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 2011, 10(2):137-149.
46. Nicaise V., German-Retana S., Sanjuan R., Dubrana M.P., Mazier M., Maisonneuve B., Candresse T., Caranta C., LeGall O. The eukaryotic translation initiation factor 4E controls lettuce susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol. 2003, 132:1272-1282.
47. Nieto C., Piron F., Dalmais M., Marco C.F., Moriones E., Gómez-Guillamón M.L., Truniger V., Gómez P., Garcia-Mas J., Aranda M.A., Bendahmane A. EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol. 2007, 7:34.
48. Oh C.S., Martin G.B. Tomato 14-3-3 protein TFT7 interacts with a MAP kinase kinase to regulate immunity-associated programmed cell death mediated by diverse disease resistance proteins. J. Biol. Chem. 2011, 286(16):14129-14136.
49. Piron F., Nicolaï M., Minoïa S., Piednoir E., Moretti A., Salgues A., Zamir D., Caranta C., Bendahmane A. An induced mutation in tomato eIF4E leads to immunity to two potyviruses. PloS One 2010, 5(6):e11313.
50. Rodnina M.V., Wintermeyer W. Recent mechanistic insights into eukaryotic ribosomes. Curr. Opin. Cell Biol. 2009, 21:435-443.
51. Ruffel S., Gallois J.L., Lesage M.L., Caranta C. The recessive potyvirus resistance gene pot-1 is the tomato orthologue of the pepper pvr2-eIF4E gene. Mol. Genet. Genomics 2005, 274:346-353.
52. Ruffel S., Gallois J.L., Moury B., Robaglia C., Palloix A., Caranta C. Simultaneous mutations in translation initiation factors eIF4E and eIF4E are required to prevent Pepper veinal mottle virus infection of pepper. J. Gen. Virol. 2006, 87:2089-2098.
53. Saito T., Hosokawa D., Meshi T., Okada Y. Immunocytochemical localization of the 130K and 180K proteins (putative replicase components) of tobacco mosaic virus. Virology 1987, 160(2):477-481.
54. Sasvari Z., Izotova L., Kinzy T.G., Nagy P.D. Synergistic roles of eukaryotic translation elongation factors 1Bγ and 1A in stimulation of tombusvirus minus-strand synthesis. PLoS Pathog. 2011, 7(12):e1002438.
55. Stein N., Perovic D., Kumlehn J., Pellio B., Stracke S., Streng S., Ordon F., Graner A. The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J. 2005, 42:912-922.
56. Takeshita D., Tomita K. Assembly of QΒ viral RNA polymerase with host translational elongation factors EF-Tu and -Ts. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15733-15738.
57. Thivierge K., Cotton S., Dufresne P.J., Mathieu I., Beauchemin C., Ide C., Fortin M.G., Laliberte J.F. Eukaryotic elongation factor 1A interacts with Turnip mosaic virus RNA-dependent RNA polymerase and VPg-Pro in virus-induced vesicles. Virology 2008, 377:216-225.
58. Truniger V., Aranda M.A. Recessive resistance to plant viruses. Adv. Virus Res. 2009, 75:119-159.
59. Wang A., Krishnaswamy S. Eukaryotic translation initiation factor 4E-mediated recessive resistance to plant viruses and its utility in crop improvement. Mol. Plant Pathol. 2012, 13:795-803.
60. Watanabe T., Honda A., Iwata A., Ueda S., Hibi T., Ishihama A. Isolation from tobacco mosaic virus-infected tobacco of a solubilized template-specific RNA-dependent RNA polymerase containing a 126K/183K protein heterodimer. J. Virol. 1999, 73(4):2633-2640.
61. Xu G., Li S., Xie K., Zhang Q., Wang Y., Tang Y., Liu D., Hong Y., He C., Liu Y. Plant ERD2-like proteins function as endoplasmic reticulum luminal protein receptors and participate in programmed cell death during innate immunity. Plant J. 2012, 72:57-69.
62. Yang C., Zhang C., Dittman J.D., Whitham S.A. Differential requirement of ribosomal protein S6 by plant RNA viruses with different translation initiation strategies. Virology 2009, 390:163-173.
63. Yamaji Y., Kobayashi T., Hamada K., Sakurai K., Yoshii A., Suzuki M., Namba S., Hibi T. In vivo interaction between Tobacco mosaic virus RNA-dependent RNA polymerase and host translation elongation factor 1A. Virology 2006, 347:100-108.
64. Yamaji Y., Sakurai K., Hamada K., Komatsu K., Ozeki J., Yoshida A., Yoshii A., Shimizu T., Namba S., Hibi T. Significance of eukaryotic translation elongation factor 1A in Tobacco mosaic virus infection. Arch. Virol. 2010, 155:263-268.
65. Yeam I., Cavatorta J.R., Ripoll D.R., Kang B.C., Jahn M.M. Functional dissection of naturally occurring amino acid substitutions in eIF4E that confers recessive potyvirus resistance in plants. Plant Cell 2007, 19:2913-2928.
66. Zeenko V.V., Ryabova L.A., Spirin A.S., Rothnie H.M., Hess D., Browning K.S., Hohn T. Eukaryotic elongation factor 1A interacts with the upstream pseudoknot domain in the 3' untranslated region of tobacco mosaic virus RNA. J. Virol. 2002, 76:5678-5691.