Methylation of translation elongation factor 1A by the METTL10-like See1 methyltransferase facilitates tombusvirus replication in yeast and plants

Virology

Volumn 448, Issue , 2014, Pages 43-54

  Li, Zhenghe ^a   Gonzalez, Paulina Alatriste ^a   Sasvari, Zsuzsanna ^a   Kinzy, Terri Goss ^b   Nagy, Peter D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Host factor; Methyltransferase; Nodaviruses; Plant; Posttranslational modification; Replication; Tomato bushy stunt virus; Tombusviruses; Translation elongation factor 1A; Virus host interaction; Yeast

Indexed keywords

ELONGATION FACTOR 1ALPHA; METHYLTRANSFERASE; SEE1 METHYLTRANSFERASE; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; CARNATION ITALIAN RINGSPOT VIRUS; CONTROLLED STUDY; NICOTIANA BENTHAMIANA; NODAVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN METHYLATION; SACCHAROMYCES CEREVISIAE; TOMBUSVIRUS; VIRUS REPLICATION;

EID: 84886266176     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.09.012     Document Type: Article

References (87)

1. Barajas D., Jiang Y., Nagy P.D. A unique role for the host ESCRT proteins in replication of tomato bushy stunt virus. PLoS Pathog. 2009, 5(12):e1000705.
2. Barajas D., Nagy P.D. Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology 2010, 397(2):358-368.
3. 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(9):6433-6444.
4. Blumenthal T., Young R.A., Brown S. Function and structure in phage Qbeta RNA replicase. Association of EF-Tu-Ts with the other enzyme subunits. J. Biol. Chem. 1976, 251(9):2740-2743.
5. Brinton M.A. Host factors involved in West Nile virus replication. Ann. N.Y. Acad. Sci. 2001, 951:207-219.
6. Carr-Schmid A., Durko N., Cavallius J., Merrick W.C., Kinzy T.G. Mutations in a GTP-binding motif of eukaryotic elongation factor 1A reduce both translational fidelity and the requirement for nucleotide exchange. J. Biol. Chem. 1999, 274(42):30297-30302.
7. Cavallius J., Popkie A.P., Merrick W.C. Site-directed mutants of post-translationally modified sites of yeast eEF1A using a shuttle vector containing a chromogenic switch. Biochim. Biophys. Acta 1997, 1350(3):345-358.
8. Cavallius J., Zoll W., Chakraburtty K., Merrick W.C. Characterization of yeast EF-1 alpha: non-conservation of post-translational modifications. Biochim. Biophys. Acta 1993, 1163(1):75-80.
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(1):403-413.
10. Cimarelli A., Luban J. Translation elongation factor 1-alpha interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 1999, 73(7):5388-5401.
11. Couttas T.A., Raftery M.J., Padula M.P., Herbert B.R., Wilkins M.R. Methylation of translation-associated proteins in Saccharomyces cerevisiae: identification of methylated lysines and their methyltransferases. Proteomics 2012, 12(7):960-972.
12. 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(18):10172-10187.
13. De Nova-Ocampo M., Villegas-Sepulveda N., del Angel R.M. Translation elongation factor-1alpha, La, and PTB interact with the 3' untranslated region of dengue 4 virus RNA. Virology 2002, 295(2):337-347.
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. Dinman J.D., Kinzy T.G. Translational misreading: mutations in translation elongation factor 1alpha differentially affect programmed ribosomal frameshifting and drug sensitivity. RNA 1997, 3(8):870-881.
16. Dreher T.W. Functions of the 3'-untranslated regions of positive strand rna viral genomes. Annu. Rev. Phytopathol. 1999, 37:151-174.
17. Fischle W., Tseng B.S., Dormann H.L., Ueberheide B.M., Garcia B.A., Shabanowitz J., Hunt D.F., Funabiki H., Allis C.D. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 2005, 438(7071):1116-1122.
18. Gietz R.D., Woods R.A. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 2002, 350:87-96.
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(9):772-778.
20. Gross S.R., Kinzy T.G. Improper organization of the actin cytoskeleton affects protein synthesis at initiation. Mol. Cell Biol. 2007, 27(5):1974-1989.
21. Huang T.S., Nagy P.D. Direct inhibition of tombusvirus plus-strand RNA synthesis by a dominant negative mutant of a host metabolic enzyme, glyceraldehyde-3-phosphate dehydrogenase, in yeast and plants. J. Virol. 2011, 85(17):9090-9102.
22. Jaag H.M., Lu Q., Schmitt M.E., Nagy P.D. Role of RNase MRP in viral RNA degradation and RNA recombination. J. Virol. 2011, 85(1):243-253.
23. Jiang Y., Serviene E., Gal J., Panavas T., Nagy P.D. Identification of essential host factors affecting tombusvirus RNA replication based on the yeast Tet promoters Hughes Collection. J. Virol. 2006, 80(15):7394-7404.
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(Pt. 12):2935-2943.
25. Jonczyk M., Pathak K.B., Sharma M., Nagy P.D. Exploiting alternative subcellular location for replication: tombusvirus replication switches to the endoplasmic reticulum in the absence of peroxisomes. Virology 2007, 362(2):320-330.
26. 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.
27. Kidmose R.T., Vasiliev N.N., Chetverin A.B., Andersen G.R., Knudsen C.R. Structure of the Qβ replicase, an RNA-dependent RNA polymerase consisting of viral and host proteins. Proc. Natl. Acad. Sci. 2010, 107(24):10884-10889.
28. Kou Y.H., Chou S.M., Wang Y.M., Chang Y.T., Huang S.Y., Jung M.Y., Huang Y.H., Chen M.R., Chang M.F., Chang S.C. Hepatitis C virus NS4A inhibits cap-dependent and the viral IRES-mediated translation through interacting with eukaryotic elongation factor 1A. J. Biomed. Sci. 2006, 13(6):861-874.
29. Kovalev N., Barajas D., Nagy P.D. Similar roles for yeast Dbp2 and Arabidopsis RH20 DEAD-box RNA helicases to Ded1 helicase in tombusvirus plus-strand synthesis. Virology 2012, 432(2):470-484.
30. Kovalev N., Pogany J., Nagy P.D. A Co-opted DEAD-Box RNA Helicase enhances tombusvirus plus-strand synthesis. PLoS Pathog. 2012, 8(2):e1002537.
31. Li Z., Barajas D., Panavas T., Herbst D.A., Nagy P.D. Cdc34p ubiquitin-conjugating enzyme is a component of the tombusvirus replicase complex and ubiquitinates p33 replication protein. J. Virol. 2008, 82(14):6911-6926.
32. Li Z., Nagy P.D. Diverse roles of host RNA binding proteins in RNA virus replication. RNA Biol. 2011, 8(2):305-315.
33. Li Z., Pogany J., Panavas T., Xu K., Esposito A.M., Kinzy T.G., Nagy P.D. Translation elongation factor 1A is a component of the tombusvirus replicase complex and affects the stability of the p33 replication co-factor. Virology 2009, 385(1):245-260.
34. Li Z., Pogany J., Tupman S., Esposito A.M., Kinzy T.G., Nagy P.D. Translation elongation factor 1A facilitates the assembly of the tombusvirus replicase and stimulates minus-strand synthesis. PLoS Pathog. 2010, 6(11):e1001175.
35. Lin J.Y., Mendu V., Pogany J., Qin J., Nagy P.D. The TPR Domain in the Host Cyp40-like cyclophilin binds to the viral replication protein and inhibits the assembly of the tombusviral replicase. PLoS Pathog. 2012, 8(2):e1002491.
36. Lipson R.S., Webb K.J., Clarke S.G. Two novel methyltransferases acting upon eukaryotic elongation factor 1A in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 2010, 500(2):137-143.
37. Martin-Granados C., Riechers S.P., Stahl U., Lang C. Absence of See1p, a widely conserved Saccharomyces cerevisiae protein, confers both deficient heterologous protein production and endocytosis. Yeast 2008, 25(12):871-877.
38. Mateyak M.K., Kinzy T.G. eEF1A: thinking outside the ribosome. J. Biol. Chem. 2010, 285(28):21209-21213.
39. Matsuda D., Yoshinari S., Dreher T.W. eEF1A binding to aminoacylated viral RNA represses minus strand synthesis by TYMV RNA-dependent RNA polymerase. Virology 2004, 321(1):47-56.
40. McCartney A.W., Greenwood J.S., Fabian M.R., White K.A., Mullen R.T. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 2005, 17(12):3513-3531.
41. Mendu V., Chiu M., Barajas D., Li Z., Nagy P.D. Cpr1 cyclophilin and Ess1 parvulin prolyl isomerases interact with the tombusvirus replication protein and inhibit viral replication in yeast model host. Virology 2010, 406(2):342-351.
42. Mine A., Okuno T. Composition of plant virus RNA replicase complexes. Curr. Opin. Virol. 2012, 2(6):669-675.
43. Nagy P.D. Yeast as a model host to explore plant virus-host interactions. Annu. Rev. Phytopathol. 2008, 46:217-242.
44. Nagy P.D. The roles of host factors in tombusvirus RNA recombination. Adv. Virus Res. 2011, 81:63-84.
45. Nagy P.D., Barajas D., Pogany J. Host factors with regulatory roles in tombusvirus replication. Curr. Opin. Virol. 2012, 2(6):685-692.
46. Nagy P.D., Pogany J. Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 2006, 344(1):211-220.
47. Nagy P.D., Pogany J. Multiple roles of viral replication proteins in plant RNA virus replication. Methods Mol. Biol. 2008, 451:55-68.
48. Nagy P.D., Pogany J. Global genomics and proteomics approaches to identify host factors as targets to induce resistance against tomato bushy stunt virus. Adv. Virus Res. 2010, 76:123-177.
49. Nagy P.D., Pogany J. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 2012, 10(2):137-149.
50. Nishikiori M., Dohi K., Mori M., Meshi T., Naito S., Ishikawa M. Membrane-bound tomato mosaic virus replication proteins participate in RNA synthesis and are associated with host proteins in a pattern distinct from those that are not membrane bound. J. Virol. 2006, 80(17):8459-8468.
51. Ozturk S.B., Vishnu M.R., Olarewaju O., Starita L.M., Masison D.C., Kinzy T.G. Unique classes of mutations in the Saccharomyces cerevisiae G-protein translation elongation factor 1A suppress the requirement for guanine nucleotide exchange. Genetics 2006, 174(2):651-663.
52. Panavas T., Hawkins C.M., Panaviene Z., Nagy P.D. The role of the p33:p33/p92 interaction domain in RNA replication and intracellular localization of p33 and p92 proteins of Cucumber necrosis tombusvirus. Virology 2005, 338(1):81-95.
53. Panavas T., Nagy P.D. Yeast as a model host to study replication and recombination of defective interfering RNA of Tomato bushy stunt virus. Virology 2003, 314(1):315-325.
54. Panavas T., Serviene E., Brasher J., Nagy P.D. Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc. Natl. Acad. Sci. USA 2005, 102(20):7326-7331.
55. Panaviene Z., Nagy P.D. Mutations in the RNA-binding domains of tombusvirus replicase proteins affect RNA recombination in vivo. Virology 2003, 317(2):359-372.
56. Panaviene Z., Panavas T., Nagy P.D. Role of an internal and two 3'-terminal RNA elements in assembly of tombusvirus replicase. J. Virol. 2005, 79(16):10608-10618.
57. Panaviene Z., Panavas T., Serva S., Nagy P.D. Purification of the cucumber necrosis virus replicase from yeast cells: role of coexpressed viral RNA in stimulation of replicase activity. J. Virol. 2004, 78(15):8254-8263.
58. Pathak K.B., Jiang Z., Ochanine V., Sharma M., Pogany J., Nagy P.D. Characterization of dominant-negative and temperature-sensitive mutants of tombusvirus replication proteins affecting replicase assembly. Virology 2013, 437(1):48-61.
59. Pathak K.B., Pogany J., Nagy P.D. Non-template functions of the viral RNA in plant RNA virus replication. Curr. Opin. Virol. 2011, 1(5):332-338.
60. Pathak K.B., Pogany J., Xu K., White K.A., Nagy P.D. Defining the roles of cis-Acting RNA elements in tombusvirus replicase assembly in vitro. J. Virol. 2012, 86(1):156-171.
61. Pathak K.B., Sasvari Z., Nagy P.D. The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology 2008, 379(2):294-305.
62. Pogany J., Nagy P.D. p33-Independent activation of a truncated p92 RNA-dependent RNA polymerase of tomato bushy stunt virus in yeast cell-free extract. J. Virol. 2012, 86(22):12025-12038.
63. Pogany J., Panavas T., Serviene E., Nawaz-Ul-Rehman M.S., Nagy P.D. A high-throughput approach for studying virus replication in yeast. Current Protocols in Microbiology 2010, 19. (16J.1.1-16J.1.15).
64. Pogany J., Stork J., Li Z., Nagy P.D. In vitro assembly of the tomato bushy stunt virus replicase requires the host Heat shock protein 70. Proc. Natl. Acad. Sci. USA 2008, 105(50):19956-19961.
65. Qanungo K.R., Shaji D., Mathur M., Banerjee A.K. Two RNA polymerase complexes from vesicular stomatitis virus-infected cells that carry out transcription and replication of genome RNA. Proc. Natl. Acad. Sci. USA 2004, 101(16):5952-5957.
66. Sasikumar A.N., Perez W.B., Kinzy T.G. The many roles of the eukaryotic elongation factor 1 complex. Wiley Interdiscip. Rev. RNA 2012, 3(4):543-555.
67. Sasvari Z., Izotova L., Kinzy T.G., Nagy P.D. Synergistic roles of eukaryotic translation elongation factors 1Bgamma and 1A in stimulation of tombusvirus minus-strand synthesis. PLoS Pathog. 2011, 7(12):e1002438.
68. Serva S., Nagy P.D. Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J. Virol. 2006, 80(5):2162-2169.
69. Serviene E., Jiang Y., Cheng C.P., Baker J., Nagy P.D. Screening of the yeast yTHC collection identifies essential host factors affecting tombusvirus RNA recombination. J. Virol. 2006, 80(3):1231-1241.
70. Serviene E., Shapka N., Cheng C.P., Panavas T., Phuangrat B., Baker J., Nagy P.D. Genome-wide screen identifies host genes affecting viral RNA recombination. Proc. Natl. Acad. Sci. USA 2005, 102(30):10545-10550.
71. Shah Nawaz-Ul-Rehman M., Martinez-Ochoa N., Pascal H., Sasvari Z., Herbst C., Xu K., Baker J., Sharma M., Herbst A., Nagy P.D. Proteome-wide overexpression of host proteins for identification of factors affecting tombusvirus RNA replication: an inhibitory role of protein kinase C. J. Virol. 2012, 86(17):9384-9395.
72. Shah Nawaz-Ul-Rehman M., Reddisiva Prasanth K., Baker J., Nagy P.D. Yeast screens for host factors in positive-strand RNA virus replication based on a library of temperature-sensitive mutants. Methods 2013, 59(2):207-216.
73. Stork J., Kovalev N., Sasvari Z., Nagy P.D. RNA chaperone activity of the tombusviral p33 replication protein facilitates initiation of RNA synthesis by the viral RdRp in vitro. Virology 2011, 409(2):338-347.
74. Takeshita D., Tomita K. Assembly of Qβ viral RNA polymerase with host translational elongation factors EF-Tu and -Ts. Proc. Natl. Acad. Sci. 2010, 107(36):15733-15738.
75. 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(1):216-225.
76. Venter P.A., Schneemann A. Recent insights into the biology and biomedical applications of Flock House virus. Cell Mol. Life Sci. 2008, 65(17):2675-2687.
77. Wang R.Y., Nagy P.D. Tomato bushy stunt virus co-opts the RNA-binding function of a host metabolic enzyme for viral genomic RNA synthesis. Cell Host Microbe 2008, 3(3):178-187.
78. Wang R.Y., Stork J., Nagy P.D. A key role for heat shock protein 70 in the localization and insertion of tombusvirus replication proteins to intracellular membranes. J. Virol. 2009, 83(7):3276-3287.
79. Wang R.Y., Stork J., Pogany J., Nagy P.D. A temperature sensitive mutant of heat shock protein 70 reveals an essential role during the early steps of tombusvirus replication. Virology 2009, 394(1):28-38.
80. Warren K., Wei T., Li D., Qin F., Warrilow D., Lin M.H., Sivakumaran H., Apolloni A., Abbott C.M., Jones A., Anderson J.L., Harrich D. Eukaryotic elongation factor 1 complex subunits are critical HIV-1 reverse transcription cofactors. Proc. Natl. Acad. Sci. USA 2012, 109(24):9587-9592.
81. Weber-Lotfi F., Dietrich A., Russo M., Rubino L. Mitochondrial targeting and membrane anchoring of a viral replicase in plant and yeast cells. J. Virol. 2002, 76(20):10485-10496.
82. White K.A., Nagy P.D. Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog. Nucleic Acid Res. Mol. Biol. 2004, 78:187-226.
83. Xu K., Huang T.S., Nagy P.D. Authentic in vitro replication of two tombusviruses in isolated mitochondrial and endoplasmic reticulum membranes. J. Virol. 2012, 86(23):12779-12794.
84. Xu K., Nagy P.D. Dissecting virus-plant interactions through proteomics approaches. Curr. Proteomics 2010, 7(4):316-327.
85. 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(1):100-108.
86. 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(2):263-268.
87. 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(11):5678-5691.