Recruitment of the 40S ribosomal subunit to the 3'-untranslated region (UTR) of a viral mRNA, via the eIF4 complex, facilitates cap-independent translation

Journal of Biological Chemistry

Volumn 290, Issue 18, 2015, Pages 11268-11281

  Sharma, Sohani Das ^a   Kraft, Jelena J ^b   Miller, W Allen ^b   Goss, Dixie J ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MACROMOLECULES; VIRUSES;

BARLEY YELLOW DWARF VIRUS; CAP-INDEPENDENT TRANSLATION; FEED-BACK LOOP; RIBOSOMAL SUBUNITS; RNA VIRUS; UNTRANSLATED REGIONS;

NUCLEIC ACIDS;

ADENOSINE TRIPHOSPHATE; INITIATION FACTOR; INITIATION FACTOR 4A; INITIATION FACTOR 4B; INITIATION FACTOR 4F; INITIATION FACTOR 4G; MESSENGER RNA; RNA 40S; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CAPPED RNA; ISOPROTEIN; RNA HELICASE; VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANISOTROPY; ARTICLE; BASE PAIRING; BINDING AFFINITY; CONTROLLED STUDY; FLUORESCENCE ANISOTROPY; LUTEOVIRUS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA ANALYSIS; RNA BINDING; RNA STRUCTURE; RNA TRANSCRIPTION; SELECTIVE 2' HYDROXYL ACYLATION ANALYZED BY PRIMER EXTENSION ANALYSIS; TOEPRINTING; TRANSLATION INITIATION; TRANSLATIONAL ENHANCER ELEMENT; CHEMISTRY; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS; SMALL RIBOSOMAL SUBUNIT;

BARLEY YELLOW DWARF VIRUS; RNA VIRUSES;

3' UNTRANSLATED REGIONS; ADENOSINE TRIPHOSPHATE; BASE SEQUENCE; EUKARYOTIC INITIATION FACTOR-4F; LUTEOVIRUS; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA CAPS; RNA HELICASES; RNA, VIRAL;

EID: 84929492266     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.645002     Document Type: Article

References (65)

1. Flint, S. J., Enquist, L. W., Racaniello, V. R., and Skalka, A. M. (eds) (2009) Principles of Virology, 3rd Ed., pp. 156-170, ASM Press, Washington, D. C.
2. Reineke, L. C., and Lloyd, R.E.(2011) Animal virus schemes for translation dominance. Curr. Opin. Virol. 1, 363-372
3. Firth, A. E., and Brierley, I. (2012) Non-canonical translation in RNA viruses. J. Gen. Virol. 93, 1385-1409
4. Sweeney, T. R., Abaeva, I. S., Pestova, T. V., and Hellen, C. U. (2014) The mechanism of translation initiation on Type 1 picornavirus IRESs. EMBO. J. 33, 76-92
5. Fernandez, N, Garćia-Sacristan, A., Ramajo, J., Briones, C, and Martínez-Salas, E. (2011) Structural analysis provides insights into the modular organization of picornavirus IRES. Virology 409, 251-261
6. Fraser, C. S., and Doudna, J. A. (2007) Structural and mechanistic insights into hepatitis C viral translation initiation. Nat Rev. Microbiol. 5, 29-38
7. Hashem, Y., des Georges, A., Dhote, V., Langlois, R., Liao, H.Y., Grassucci, R. A., Pestova, T. V., Hellen, C. U., and Frank, J. (2013) Hepatitis-C-viruslike internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 503, 539-543
8. Costantino, D. A., Pfingsten, J. S., Rambo, R. P., and Kieft, J. S. (2008) tRNA-mRNA mimicry drives translation initiation from a viral IRES. Nat Struct. Mol. Biol. 15, 57-64
9. Simon, A. E., and Miller, W. A. (2013) 3' cap-independent translation enhancers of plant viruses. Annu. Rev. Microbiol. 67, 21-42
10. Pelletier, J., and Sonenberg, N. (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334, 320-325
11. Hellen, C. U., and Sarnow, P. (2001) Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15, 1593-1612
12. Jackson, R. J., Hellen, C. U., and Pestova, T. V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev. Mol. Cell Biol. 11, 113-127
13. Otto, G. A., and Puglisi, J. D. (2004) The pathway of HCV IRES-mediated translation initiation. Cell 119, 369-380
14. Kieft, J. S., Zhou, K., Jubin, R., Murray, M. G., Lau, J. Y., and Doudna, J. A. (1999) The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J. Mol. Biol. 292, 513-529
15. Pestova, T. V., Hellen, C. U., and Shatsky, I. N. (1996) Canonical eukaryotic initiation factors determine initiation of translation by internal ribo-somal entry. Mol. Cell Biol. 16, 6859-6869
16. Pestova, T. V., Shatsky, I. N, Fletcher, S. P., Jackson, R. J., and Hellen, C. U. (1998) A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 12, 67-83
17. Pfingsten, J. S., Costantino, D. A., and Kieft, J. S. (2006) Structural basis for ribosome recruitment and manipulation by a viral IRES RNA. Science 314, 1450-1454
18. Hertz, M. I., and Thompson, S. R. (2011) Mechanism of translation initiation by Dicistroviridae IGR IRESs. Virology 411, 355-361
19. Khan, M. A., Miyoshi, H, Gallie, D. R., and Goss, D. J. (2008) Potyvirus genome-linked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J. Biol. Chem. 283, 1340-1349
20. Gallie, D. R. (2001) Cap-independent translation conferred by the 5' leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. J. Virol. 75, 12141-12152
21. Khan, M. A., and Goss, D. J. (2012) Poly(A)-binding protein increases the binding affinity and kinetic rates of interaction of viral protein linked to genome with translation initiation factors eIFiso4F and eIFiso4F.4B complex. Biochemistry 51, 1388-1395
22. Guo, L., Allen, E. M., and Miller, W. A. (2001) Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA.Mol. Cell7, 1103-1109
23. Rakotondrafara, A. M., Polacek, C, Harris, E., and Miller, W. A. (2006) Oscillating kissing stem-loop interactions mediate 5' scanning-dependent translation by a viral 3'-cap-independent translation element. RNA 12, 1893-1906
24. Treder, K., Kneller, E. L., Allen, E. M., Wang, Z., Browning, K. S., and Miller, W. A. (2008) The 3' cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 14, 134-147
25. Miller, W. A., and White, K. A. (2006) Long-distance RNA-RNA interactions in plant virus gene expression and replication. Annu. Rev. Phyto-pathol. 44, 447-467
26. Nicholson, B. L., Wu, B., Chevtchenko, I., and White, K. A. (2010) Tom-busvirus recruitment of host translational machinery via the 3' UTR.RNA 16, 1402-1419
27. Gazo, B. M., Murphy, P., Gatchel, J. R., and Browning, K. S. (2004) A novel interaction of Cap-binding protein complexes eukaryotic initiation factor (eIF) 4F and eIF(iso)4F with a region in the 3'-untrans-lated region of satellite tobacco necrosis virus. J. Biol. Chem. 279, 13584-13592
28. Truniger, V., Nieto, C, Gonzalez-Ibeas, D., and Aranda, M. (2008) Mechanism of plant eIF4E-mediated resistance against a Carmovirus (Tombus-viridae): cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant J. 56, 716-727
29. Stupina, V. A., Meskauskas, A., McCormack, J. C, Yingling, Y. G., Shapiro, B. A., Dinman, J. D., and Simon, A. E. (2008) The 3' proximal translational enhancer of Turnip crinkle virus binds to 60S ribosomal subunits. RNA 14, 2379-2393
30. Miras, M., Sempere, R. N, Kraft, J. J., Miller, W. A., Aranda, M. A., and Truniger, V. (2014) Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking. New Phytol. 202, 233-246
31. Wang, S., Browning, K. S., and Miller, W. A. (1997) A viral sequence in the 3'-untranslated region mimics a 5' cap in facilitating translation of uncapped mRNA. EMBOJ. 16, 4107-4116
32. Banerjee, B., and Goss, D. J. (2014) Eukaryotic initiation factor (eIF) 4F binding to barley yellow dwarf virus (BYDV) 3'-untranslated region correlates with translation efficiency. J. Biol. Chem. 289, 4286-4294
33. Kraft, J. J., Treder, K., Peterson, M. S., and Miller, W. A. (2013) Cation-dependent folding of 3' cap-independent translation elements facilitates interaction of a 17-nucleotide conserved sequence with eIF4G. Nucleic Acids Res. 41, 3398-3413
34. Kneller, E. L., Rakotondrafara, A. M., and Miller, W. A. (2006) Cap-independent translation of plant viral RNAs. Virus Res. 119, 63-75
35. Wang, Z., Kraft, J. J., Hui, A. Y., and Miller, W. A. (2010) Structural plasticity of Barley yellow dwarf virus-like cap-independent translation elements in four genera of plant viral RNAs. Virology 402, 177-186
36. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415
37. Goss, D. J., and Rounds, D.J. (1988) A kinetic light-scattering study of the binding of wheat germ protein synthesis initiation factor 3 to 40S ribosomal subunits and 80S ribosomes. Biochemistry 27, 3610-3613
38. Spremulli, L. L., Walthall, B. J., Lax, S. R., and Ravel, J. M. (1977) Purification and properties of a Met-tRNAf binding factor from wheat germ. Arch. Biochem. Biophys. 178, 565-575
39. McCormack, J. C, Yuan, X., Yingling, Y. G., Kasprzak, W., Zamora, R. E., Shapiro, B. A., and Simon, A. E. (2008) Structural domains within the 3' untranslated region of Turnip crinkle virus. J. Virol. 82, 8706-8720
40. Acker, M. G., Kolitz, S. E., Mitchell, S. F., Nanda, J. S., and Lorsch, J. R. (2007) Reconstitution of yeast translation initiation. Methods Enzymol. 430, 111-145
41. Stupina, V. A., Yuan, X., Meskauskas, A., Dinman, J. D., and Simon, A. E. (2011) Ribosome binding to a 5' translational enhancer is altered in the presence of the 3' untranslated region in cap-independent translation of turnip crinkle virus. J. Virol. 85, 4638-4653
42. van Heerden, A., and Browning, K. S. (1994) Expression in Escherichia coli of the two subunits of the isozyme form of wheat germ protein synthesis initiation factor 4F: purification of the subunits and formation of an enzy-matically active complex. J. Biol. Chem. 269, 17454-17457
43. Mayberry, L. K., Dennis, M. D., Leah Allen, M., Ruud Nitka, K., Murphy, P. A., Campbell, L., and Browning, K. S. (2007) Expression and purification of recombinant wheat translation initiation factors eIF1, eIF1A, eIF4A, eIF4B, eIF4F, eIF(iso)4F, and eIF5. Methods Enzymol. 430, 397-408
44. Rozen, F., Edery, I., Meerovitch, K., Dever, T. E., Merrick, W. C, and Sonenberg, N. (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell Biol. 10, 1134-1144
45. Wilkinson, K. A., Merino, E. J., and Weeks, K. M. (2006) Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nat. Protoc. 1, 1610-1616
46. Merino, E. J., Wilkinson, K. A., Coughlan, J. L., and Weeks, K. M. (2005) RNA structure analysis at single nucleotide resolution by selective 2'-hydroxyl acylation and primer extension (SHAPE).J. Am. Chem. Soc. 127, 4223-4231
47. Jaramillo, M., Dever, T. E., Merrick, W. C, and Sonenberg, N. (1991) RNA unwinding in translation: assembly of helicase complex intermediates comprising eukaryotic initiation factors eIF-4F and eIF-4B. Mol. Cell Biol. 11, 5992-5997
48. Sachs, M. S., Wang, Z., Gaba, A., Fang, P., Belk, J., Ganesan, R., Amrani, N., and Jacobson, A. (2002) Toeprint analysis of the positioning of translation apparatus components at initiation and termination codons of fungal mRNAs. Methods 26, 105-114
49. Yu, Y., Marintchev, A., Kolupaeva, V. G., Unbehaun, A., Veryasova, T., Lai, S. C, Hong, P., Wagner, G., Hellen, C. U., and Pestova, T. V. (2009) Position of eukaryotic translation initiation factor eIF1A on the 40S ribosomal subunit mapped by directed hydroxyl radical probing. Nucleic Acids Res. 37, 5167-5182
50. Das, R., Laederach, A., Pearlman, S. M., Herschlag, D., and Altman, R. B. (2005) SAFA: semi-automated footprinting analysis software for high-throughput quantification of nucleic acid footprinting experiments. RNA 11, 344-354
51. Laederach, A., Das, R., Vicens, Q., Pearlman, S. M., Brenowitz, M., Herschlag, D., and Altman, R. B. (2008) Semiautomated and rapid quantification of nucleic acid footprinting and structure mapping experiments. Nat Protoc. 3, 1395-1401
52. Filbin, M. E., Vollmar, B. S., Shi, D., Gonen, T., and Kieft, J. S. (2013) HCV IRES manipulates the ribosome to promote the switch from translation initiation to elongation. Nat Struct. Mol. Biol. 20, 150-158
53. Luo, Y., and Goss, D. J. (2001) Homeostasis in mRNA initiation: wheat germ poly(A)-binding protein lowers the activation energy barrier to initiation complex formation. J. Biol. Chem. 276, 43083-43086
54. Khan, M. A., and Goss, D. J. (2005) Translation initiation factor (eIF) 4B affects the rates of binding of the mRNA m7G cap analogue to wheat germ eIFiso4F and eIFiso4F.PABP. Biochemistry 44, 4510-4516
55. Firpo, M. A., Connelly, M. B., Goss, D. J., and Dahlberg, A. E. (1996) Mutations at two invariant nucleotides in the 3'-minor domain of Escherichia coli 16 S rRNA affecting translational initiation and initiation factor 3 function. J. Biol. Chem. 271, 4693-4698
56. Ray, S., Yumak, H., Domashevskiy, A., Khan, M. A., Gallie, D. R., and Goss, D. J. (2006) Tobacco etch virus mRNA preferentially binds wheat germ eukaryotic initiation factor (eIF) 4G rather than eIFiso4G.J. Biol. Chem. 281, 35826-35834
57. Yumak, H., Khan, M. A., and Goss, D. J. (2010) Poly(A) tail affects equilibrium and thermodynamic behavior of tobacco etch virus mRNA with translation initiation factors eIF4F, eIF4B and PABP. Biochim. Biophys. Acta 1799, 653-658
58. Maag, D., Fekete, C. A., Gryczynski, Z., and Lorsch, J. R. (2005) A conformational change in the eukaryotic translation preinitiation complex and release of eIF1 signal recognition of the start codon. Mol. Cell 17, 265-275
59. Pestova, T. V., Kolupaeva, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I., and Hellen, C. U. (2001) Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. U.S.A. 98, 7029-7036
60. Spahn, C. M., Kieft, J. S., Grassucci, R. A., Penczek, P. A., Zhou, K., Doudna, J. A., and Frank, J. (2001) Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291, 1959-1962
61. Guo, L., Allen, E., and Miller, W. A. (2000) Structure and function of a cap-independent translation element that functions in either the 3' or the 5' untranslated region. RNA 6, 1808-1820
62. Gao, F., Kasprzak, W., Stupina, V. A., Shapiro, B. A., and Simon, A. E. (2012) A ribosome-binding, 3' translational enhancer has a T-shaped structure and engages in a long-distance RNA-RNA interaction. J. Virol. 86, 9828-9842
63. Wang, Z., Parisien, M., Scheets, K., and Miller, W. A. (2011) The cap-binding translation initiation factor, eIF4E, binds a pseudoknot in a viral cap-independent translation element. Structure 19, 868-880
64. Bai, Y., Zhou, K., and Doudna, J. A. (2013) Hepatitis C virus 3'UTR regulates viral translation through direct interactions with the host translation machinery. Nucleic Acids Res. 41, 7861-7874
65. Barry, J. K., and Miller, W. A. (2002) A-1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proc. Natl. Acad. Sci. U.S.A. 99, 11133-11138