Untranslated regions of diverse plant viral RNAs vary greatly in translation enhancement efficiency

BMC Biotechnology

Volumn 12, Issue , 2012, Pages

  Fan, Qiuling ^a,b   Treder, Krzysztof ^a   Miller, W A ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CELL DEATH; COSTS; PLANT CELL CULTURE; PLANTS (BOTANY); PROTEINS; TOBACCO;

BARLEY YELLOW DWARF VIRUS; CAP-INDEPENDENT TRANSLATION; ENHANCEMENT EFFICIENCY; PROTEIN EXPRESSIONS; TOBACCO MOSAIC VIRUS; TOMATO BUSHY STUNT VIRUS; UNTRANSLATED REGIONS; VIRAL EXPRESSION VECTOR;

VIRUSES;

LUCIFERASE; MESSENGER RNA; UNCAPPED RNA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANGIOSPERM; ARTICLE; CONTROLLED STUDY; DEFECTIVE VIRUS; DICOTYLEDON; GENE EXPRESSION; GENE MAPPING; LUTEOVIRUS; MONOCOT; NONHUMAN; OAT; PLANT CELL; PLANT VIRUS; PROTOPLAST; REPORTER GENE; RNA CAPPING; RNA SEQUENCE; RNA STABILITY; RNA TRANSLATION; TOBACCO MOSAIC VIRUS; TOMATO BUSHY STUNT VIRUS; WHEAT GERM; GENETICS; METABOLISM; PROTEIN SYNTHESIS; TOBACCO; TOBAMOVIRUS; TOMBUSVIRUS; VIRUS GENOME; WHEAT;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; AVENA SATIVA; GENES, REPORTER; GENOME, VIRAL; LUTEOVIRUS; PLANT CELLS; PROTEIN BIOSYNTHESIS; PROTOPLASTS; RNA, MESSENGER; RNA, VIRAL; TOBACCO; TOBACCO NECROSIS SATELLITE VIRUS; TOBAMOVIRUS; TOMBUSVIRUS; TRITICUM;

EID: 84860511213     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-12-22     Document Type: Article

References (52)

1. Schneider RJ, Mohr I. Translation initiation and viral tricks. Trends Biochem Sci 2003, 28:130-136. 10.1016/S0968-0004(03)00029-X, 12633992.
2. Jackson RJ, Hellen CU, Pestova TV. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 2010, 11:113-127. 10.1038/nrm2838, 20094052.
3. Kneller EL, Rakotondrafara AM, Miller WA. Cap-independent translation of plant viral RNAs. Virus Res 2006, 119:63-75. 10.1016/j.virusres.2005.10.010, 1880899, 16360925.
4. Dreher TW, Miller WA. Translational control in positive strand RNA plant viruses. Virology 2006, 344:185-197. 10.1016/j.virol.2005.09.031, 1847782, 16364749.
5. Walsh D, Mohr I. Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol 2011, 9:860-875. 10.1038/nrmicro2655, 22002165.
6. Nicholson BL, White KA. 3′ cap-independent translation enhancers of positive-strand RNA plant viruses. Curr Opin Virol 2011, 1:373-380. 10.1016/j.coviro.2011.10.002, 22440838.
7. Gazo BM, Murphy P, Gatchel JR, Browning KS. A novel interaction of Cap-binding protein complexes eukaryotic initiation factor (eIF) 4 F and eIF(iso)4 F with a region in the 3′-untranslated region of satellite tobacco necrosis virus. J Biol Chem 2004, 279:13584-13592. 10.1074/jbc.M311361200, 14729906.
8. Treder K, Pettit Kneller EL, Allen EM, Wang Z, Browning KS, Miller WA. The 3′ cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 2008, 14:134-147. 2151041, 18025255.
9. Nicholson BL, Wu B, Chevtchenko I, White KA. Tombusvirus recruitment of host translational machinery via the 3′ UTR. RNA 2010, 16:1402-1419. 10.1261/rna.2135210, 2885689, 20507975.
10. Browning KS. Plant translation initiation factors: it is not easy to be green. Biochem Soc Trans 2004, 32:589-591.
11. Guo L, Allen E, Miller WA. Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell 2001, 7:1103-1109. 10.1016/S1097-2765(01)00252-0, 11389856.
12. Fabian MR, White KA. 5′-3′ RNA-RNA interaction facilitates cap- and poly(A) tail-independent translation of tomato bushy stunt virus mRNA: a potential common mechanism for Tombusviridae. J Biol Chem 2004, 279:28862-28872. 10.1074/jbc.M401272200, 15123633.
13. Rakotondrafara AM, Polacek C, Harris E, Miller WA. Oscillating kissing stem-loop interactions mediate 5′ scanning-dependent translation by a viral 3′-cap-independent translation element. RNA 2006, 12:1893-1906. 10.1261/rna.115606, 1581982, 16921068.
14. Fabian MR, White KA. Analysis of a 3′-translation enhancer in a tombusvirus: a dynamic model for RNA-RNA interactions of mRNA termini. RNA 2006, 12:1304-1314. 10.1261/rna.69506, 1484428, 16682565.
15. Gallie DR, Walbot V. RNA pseudoknot domain of tobacco mosaic virus can functionally substitute for a poly(A) tail in plant and animal cells. Genes Dev 1990, 4:1149-1157. 10.1101/gad.4.7.1149, 1976569.
16. Shen R, Miller WA. Structures required for poly(A) tail-independent translation overlap with, but are distinct from, cap-independent translation and RNA replication signals at the 3′ end of Tobacco necrosis virus RNA. Virology 2007, 358:448-458. 10.1016/j.virol.2006.08.054, 1995077, 17023016.
17. Shen R, Miller WA. The 3′ untranslated region of tobacco necrosis virus RNA contains a barley yellow dwarf virus-like cap-independent translation element. J Virol 2004, 78:4655-4664. 10.1128/JVI.78.9.4655-4664.2004, 387721, 15078948.
18. Guo L, Allen E, Miller WA. Structure and function of a cap-independent translation element that functions in either the 3′ or the 5′ untranslated region. RNA 2000, 6:1808-1820. 10.1017/S1355838200001539, 1370050, 11142380.
19. Meulewaeter F, van Lipzig R, Gultyaev AP, Pleij CW, Van Damme D, Cornelissen M, van Eldik G. Conservation of RNA structures enables TNV and BYDV 5′ and 3′ elements to cooperate synergistically in cap-independent translation. Nucleic Acids Res 2004, 32:1721-1730. 10.1093/nar/gkh338, 390335, 15020708.
20. Meulewaeter F, Van Montagu M, Cornelissen M. Features of the autonomous function of the translational enhancer domain of satellite tobacco necrosis virus. RNA 1998, 4:1347-1356. 10.1017/S135583829898092X, 1369708, 9814756.
21. Danthinne X, Seurinck J, Meulewaeter F, Van Montagu M, Cornelissen M. The 3′ untranslated region of satellite tobacco necrosis virus RNA stimulates translation in vitro. Mol Cell Biol 1993, 13:3340-3349. 359791, 8497255.
22. Timmer RT, Benkowski LA, Schodin D, Lax SR, Metz AM, Ravel JM, Browning KS. The 5′ and 3′ untranslated regions of satellite tobacco necrosis virus RNA affect translational efficiency and dependence on a 5′ cap structure. J Biol Chem 1993, 268:9504-9510.
23. van Lipzig R, Gultyaev AP, Pleij CW, van Montagu M, Cornelissen M, Meulewaeter F. The 5′ and 3′ extremities of the satellite tobacco necrosis virus translational enhancer domain contribute differentially to stimulation of translation. RNA 2002, 8:229-236. 10.1017/S1355838202018071, 1370248, 11924567.
24. Nicholson BL, White KA. Context-influenced cap-independent translation of Tombusvirus mRNAs in vitro. Virology 2008, 380:203-212. 10.1016/j.virol.2008.08.003, 18775547.
25. Sarawaneeyaruk S, Iwakawa HO, Mizumoto H, Murakami H, Kaido M, Mise K, Okuno T. Host-dependent roles of the viral 5′ untranslated region (UTR) in RNA stabilization and cap-independent translational enhancement mediated by the 3′ UTR of Red clover necrotic mosaic virus RNA1. Virology 2009, 391:107-118. 10.1016/j.virol.2009.05.037, 19577782.
26. Meulewaeter F, Danthinne X, Van Montagu M, Cornelissen M. 5′- and 3′-sequences of satellite tobacco necrosis virus RNA promoting translation in tobacco [published erratum appears in Plant J 1998, 15:153-154]. Plant J 1998, 14:169-176. 10.1046/j.1365-313X.1998.00104.x, 9628014.
27. Ivanov PA, Karpova OV, Skulachev MV, Tomashevskaya OL, Rodionova NP, Dorokhov Yu L, Atabekov JG. A tobamovirus genome that contains an internal ribosome entry site functional in vitro. Virology 1997, 232:32-43. 10.1006/viro.1997.8525, 9185586.
28. Dorokhov YL, Skulachev MV, Ivanov PA, Zvereva SD, Tjulkina LG, Merits A, Gleba YY, Hohn TJ, Atabekov JG. Polypurine (A)-rich sequences promote cross-kingdom conservation of internal ribosome entry. Proc Natl Acad Sci USA 2002, 99:5301-5306. 10.1073/pnas.082107599, 122764, 11959981.
29. Gallie DR, Walbot V. Identification of the motifs within the tobacco mosaic virus 5′-leader responsible for enhancing translation. Nucleic Acids Res 1992, 20:4631-4638. 10.1093/nar/20.17.4631, 334194, 1408765.
30. Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TM. The 5′-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res 1987, 15:3257-3273. 10.1093/nar/15.8.3257, 340728, 3575095.
31. Streatfield SJ. Approaches to achieve high-level heterologous protein production in plants. Plant Biotech J 2007, 5:2-15.
32. Dorokhov YL, Ivanov PA, Novikov VK, Agranovsky AA, Morozov SY, Efimov VA, Casper R, Atabekov JG. Complete nucleotide sequence and genome organization of a tobamovirus infecting cruciferae plants. FEBS Lett 1994, 350:5-8. 10.1016/0014-5793(94)00721-7, 7545946.
33. Leathers V, Tanguay R, Kobayashi M, Gallie DR. A phylogenetically conserved sequence within viral 3′ untranslated RNA pseudoknots regulates translation. Mol Cell Biol 1993, 13:5331-5347. 360232, 8355685.
34. Wu B, White KA. A primary determinant of cap-independent translation is located in the 3′-proximal region of the tomato bushy stunt virus genome. J Virol 1999, 73:8982-8988. 112930, 10516004.
35. Wang S, Guo L, Allen E, Miller WA. A potential mechanism for selective control of cap-independent translation by a viral RNA sequence in cis and in trans. RNA 1999, 5:728-738. 10.1017/S1355838299981979, 1369800, 10376873.
36. Leclerc GJ, Leclerc GM, Barredo JC. Real-time RT-PCR analysis of mRNA decay: half-life of Beta-actin mRNA in human leukemia CCRF-CEM and Nalm-6 cell lines. Cancer Cell Int 2002, 2:1. 116431, 11988110.
37. Douthwaite JA, Lees DM, Corder R. A role for increased mRNA stability in the induction of endothelin-1 synthesis by lipopolysaccharide. Biochem Pharmacol 2003, 66:589-594. 10.1016/S0006-2952(03)00336-8, 12906923.
38. Bung C, Bochkaeva Z, Terenin I, Zinovkin R, Shatsky IN, Niepmann M. Influence of the hepatitis C virus 3′-untranslated region on IRES-dependent and cap-dependent translation initiation. FEBS Lett 2010, 584:837-842. 10.1016/j.febslet.2010.01.015, 20079737.
39. Gallie DR. The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res 2002, 30:3401-3411. 10.1093/nar/gkf457, 137081, 12140325.
40. Wang Z, Treder K, Miller WA. Structure of a viral cap-independent translation element that functions via high affinity binding to the eIF4E subunit of eIF4F. J Biol Chem 2009, 284:14189-14202. 10.1074/jbc.M808841200, 2682867, 19276085.
41. Madin K, Sawasaki T, Ogasawara T, Endo Y. A highly efficient and robust cell-free protein synthesis system prepared from wheat embryos: plants apparently contain a suicide system directed at ribosomes. Proc Natl Acad Sci USA 2000, 97:559-564. 10.1073/pnas.97.2.559, 15369, 10639118.
42. Makino S, Goren MA, Fox BG, Markley JL. Cell-free protein synthesis technology in NMR high-throughput structure determination. Methods Mol Biol 2010, 607:127-147. 10.1007/978-1-60327-331-2_12, 20204854.
43. Vinarov DA, Newman CL, Tyler EM, Markley JL, Shahan MN. Wheat germ cell-free expression system for protein production. Curr Protoc Protein Sci 2006, Chapter 5:18. Unit 5.
44. Marillonnet S, Thoeringer C, Kandzia R, Klimyuk V, Gleba Y. Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nat Biotechnol 2005, 23:718-723. 10.1038/nbt1094, 15883585.
45. Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol Bioeng 2009, 103:706-714. 10.1002/bit.22299, 2704498, 19309755.
46. Daniell H, Singh ND, Mason H, Streatfield SJ. Plant-made vaccine antigens and biopharmaceuticals. Trends Plant Sci 2009, 14:669-679. 10.1016/j.tplants.2009.09.009, 2787751, 19836291.
47. Wang S, Browning KS, Miller WA. A viral sequence in the 3′-untranslated region mimics a 5′ cap in facilitating translation of uncapped mRNA. EMBO J 1997, 16:4107-4116. 10.1093/emboj/16.13.4107, 1170033, 9233819.
48. Mukherjee AK, Sollod BL, Wikel SK, King GF. Orally active acaricidal peptide toxins from spider venom. Toxicon 2006, 47:182-187. 10.1016/j.toxicon.2005.10.011, 16330063.
49. Peden K, Symons R. Cucumber mosaic virus contains a functionally divided genome. Virology 1973, 53:487-492. 10.1016/0042-6822(73)90232-8, 4576349.
50. Scholthof HB, Scholthof KBG, Jackson AO. Identification of tomato bushy stunt virus host-specific symptom determinants by expression of individual genes from a potato virus X vector. Plant Cell 1995, 7:1157-1172. 160941, 7549478.
51. Allen E, Wang S, Miller WA. Barley yellow dwarf virus RNA requires a cap-independent translation sequence because it lacks a 5′ cap. Virology 1999, 253:139-144. 10.1006/viro.1998.9507, 9918872.
52. Rakotondrafara AM, Jackson J, Pettit Kneller EJ, Miller WA. Preparation and electroporation of oat protoplasts from cell suspension culture. Current Protocols in Microbiology 2007, John Wiley & Sons, New York, Coico R, Towalik T, Quaries J, Stevenson B, Taylor R, 16D.13.11-16D.13.12.