Two RNA-binding motifs in eIF3 direct HCV IRES-dependent translation

Nucleic Acids Research

Volumn 41, Issue 15, 2013, Pages 7512-7521

  Sun, Chaomin ^a   Querol Audí, Jordi ^a   Mortimer, Stefanie A ^a   Arias Palomo, Ernesto ^a   Doudna, Jennifer A ^a,b   Nogales, Eva ^a,b   Cate, Jamie H D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR; INITIATION FACTOR 3; INITIATION FACTOR 3A; INITIATION FACTOR 3C; INITIATION FACTOR 5B; UNCLASSIFIED DRUG; VIRUS RNA;

40S RIBOSOME SUBUNIT; ARTICLE; BINDING SITE; BIOINFORMATICS; CONTROLLED STUDY; ELECTRON MICROSCOPY; HEPATITIS C VIRUS; INTERNAL RIBOSOME ENTRY SITE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; RIBOSOME SUBUNIT; RNA BINDING; RNA STRUCTURE; RNA TRANSLATION; START CODON; TRANSLATION INITIATION; VIRUS TRANSCRIPTION;

BINDING SITES; CODON, INITIATOR; EUKARYOTIC INITIATION FACTOR-3; HELIX-LOOP-HELIX MOTIFS; HEPACIVIRUS; HUMANS; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN INTERACTION MAPPING; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RIBOSOMES; RNA, VIRAL;

EID: 84883477130     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt510     Document Type: Article

References (52)

1. Hinnebusch,A.G. (2011) Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev., 75, 434-467, first page of table of contents
2. Hinnebusch,A.G. and Lorsch,J.R. (2012) The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb. Perspect. Biol., 4, pii: a011544
3. 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
4. Fraser,C.S. and Doudna,J.A. (2007) Structural and mechanistic insights into hepatitis C viral translation initiation. Nat. Rev. Microbiol., 5, 29-38
5. Sokabe,M., Fraser,C.S. and Hershey,J.W. (2012) The human translation initiation multi-factor complex promotes methionyltRNAi binding to the 40S ribosomal subunit. Nucleic Acids Res., 40, 905-913
6. Pisarev,A.V., Kolupaeva,V.G., Yusupov,M.M., Hellen,C.U. and Pestova,T.V. (2008) Ribosomal position and contacts of mRNA in eukaryotic translation initiation complexes. EMBO J., 27, 1609-1621
7. Silvera,D., Formenti,S.C. and Schneider,R.J. (2010) Translational control in cancer. Nat. Rev. Cancer, 10, 254-266
8. 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
9. Kieft,J.S., Zhou,K., Jubin,R. and Doudna,J.A. (2001) Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA, 7, 194-206
10. Sizova,D.V., Kolupaeva,V.G., Pestova,T.V., Shatsky,I.N. and Hellen,C.U. (1998) Specific interaction of eukaryotic translation initiation factor 3 with the 5' nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J. Virol., 72, 4775-4782
11. 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 RNAinduced changes in the conformation of the 40s ribosomal subunit. Science, 291, 1959-1962
12. 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
13. Tsukiyama-Kohara,K., Iizuka,N., Kohara,M. and Nomoto,A. (1992) Internal ribosome entry site within hepatitis C virus RNA. J. Virol., 66, 1476-1483
14. Siridechadilok,B., Fraser,C.S., Hall,R.J., Doudna,J.A. and Nogales,E. (2005) Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science, 310, 1513-1515
15. Damoc,E., Fraser,C.S., Zhou,M., Videler,H., Mayeur,G.L., Hershey,J.W., Doudna,J.A., Robinson,C.V. and Leary,J.A. (2007) Structural characterization of the human eukaryotic initiation factor 3 protein complex by mass spectrometry. Mol. Cell. Proteomics, 6, 1135-1146
16. Sun,C., Todorovic,A., Querol-Audi,J., Bai,Y., Villa,N., Snyder,M., Ashchyan,J., Lewis,C.S., Hartland,A., Gradia,S. et al. (2011) Functional reconstitution of human eukaryotic translation initiation factor 3 (eIF3). Proc. Natl Acad. Sci. USA, 108, 20473-20478
17. Buratti,E., Tisminetzky,S., Zotti,M. and Baralle,F.E. (1998) Functional analysis of the interaction between HCV 5'UTR and putative subunits of eukaryotic translation initiation factor eIF3. Nucleic Acids Res., 26, 3179-3187
18. Cai,Q., Todorovic,A., Andaya,A., Gao,J., Leary,J.A. and Cate,J.H. (2010) Distinct regions of human eIF3 are sufficient for binding to the HCV IRES and the 40S ribosomal subunit. J. Mol. Biol., 403, 185-196
19. Mortimer,S.A. and Weeks,K.M. (2009) Time-resolved RNA SHAPE chemistry: quantitative RNA structure analysis in onesecond snapshots and at single-nucleotide resolution. Nat. Protoc., 4, 1413-1421
20. Mortimer,S.A. and Weeks,K.M. (2007) A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J. Am. Chem. Soc., 129, 4144-4145
21. Barbu,V. and Dautry,F. (1989) Northern blot normalization with a 28S rRNA oligonucleotide probe. Nucleic Acids Res., 17, 7115
22. Lander,G.C., Stagg,S.M., Voss,N.R., Cheng,A., Fellmann,D., Pulokas,J., Yoshioka,C., Irving,C., Mulder,A., Lau,P.W. et al. (2009) Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol., 166, 95-102
23. van Heel,M., Harauz,G., Orlova,E.V., Schmidt,R. and Schatz,M. (1996) A new generation of the IMAGIC image processing system. J. Struct. Biol., 116, 17-24
24. Ludtke,S.J., Baldwin,P.R. and Chiu,W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol., 128, 82-97
25. Tang,G., Peng,L., Baldwin,P.R., Mann,D.S., Jiang,W., Rees,I. and Ludtke,S.J. (2007) EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol., 157, 38-46
26. Scheres,S.H., Nunez-Ramirez,R., Gomez-Llorente,Y., San Martin,C., Eggermont,P.P. and Carazo,J.M. (2007) Modeling experimental image formation for likelihood-based classification of electron microscopy data. Structure, 15, 1167-1177
27. Sorzano,C.O., Marabini,R., Velazquez-Muriel,J., Bilbao-Castro,J.R., Scheres,S.H., Carazo,J.M. and Pascual-Montano,A. (2004) XMIPP: a new generation of an open-source image processing package for electron microscopy. J. Struct. Biol., 148, 194-204
28. Querol-Audi,J., Sun,C., Vogan,M.J., Smith,M.D., Gu,Y., Cate,J.H. and Nogales,E. (2013) Architecture of human translation initiation factor 3. Structure, 21, 920-928
29. Wang,L. and Brown,S.J. (2006) BindN: a web-based tool for efficient prediction of DNA and RNA binding sites in amino acid sequences. Nucleic Acids Res., 34, W243-W248
30. Kelley,L.A. and Sternberg,M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc., 4, 363-371
31. Crooks,G.E., Hon,G., Chandonia,J.M. and Brenner,S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190
32. Dmitriev,S.E., Pisarev,A.V., Rubtsova,M.P., Dunaevsky,Y.E. and Shatsky,I.N. (2003) Conversion of 48S translation preinitiation complexes into 80S initiation complexes as revealed by toeprinting. FEBS Lett., 533, 99-104
33. Pestova,T.V., Lomakin,I.B., Lee,J.H., Choi,S.K., Dever,T.E. and Hellen,C.U. (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature, 403, 332-335
34. Lee,J.H., Pestova,T.V., Shin,B.S., Cao,C., Choi,S.K. and Dever,T.E. (2002) Initiation factor eIF5B catalyzes second GTPdependent step in eukaryotic translation initiation. Proc. Natl Acad. Sci. USA, 99, 16689-16694
35. Pestova,T.V. and Kolupaeva,V.G. (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev., 16, 2906-2922
36. Terenin,I.M., Dmitriev,S.E., Andreev,D.E. and Shatsky,I.N. (2008) Eukaryotic translation initiation machinery can operate in a bacterial-like mode without eIF2. Nat. Struct. Mol. Biol., 15, 836-841
37. Shin,B.S., Maag,D., Roll-Mecak,A., Arefin,M.S., Burley,S.K., Lorsch,J.R. and Dever,T.E. (2002) Uncoupling of initiation factor eIF5B/IF2 GTPase and translational activities by mutations that lower ribosome affinity. Cell, 111, 1015-1025
38. Lander,G.C., Estrin,E., Matyskiela,M.E., Bashore,C., Nogales,E. and Martin,A. (2012) Complete subunit architecture of the proteasome regulatory particle. Nature, 482, 186-191
39. Passmore,L.A., Schmeing,T.M., Maag,D., Applefield,D.J., Acker,M.G., Algire,M.A., Lorsch,J.R. and Ramakrishnan,V. (2007) The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol. Cell, 26, 41-50
40. Locker,N., Easton,L.E. and Lukavsky,P.J. (2007) HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J., 26, 795-805
41. Valasek,L., Mathew,A.A., Shin,B.S., Nielsen,K.H., Szamecz,B. and Hinnebusch,A.G. (2003) The yeast eIF3 subunits TIF32/a, NIP1/c, and eIF5 make critical connections with the 40S ribosome in vivo. Genes Dev., 17, 786-799
42. Altschul,S.F., Madden,T.L., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402
43. Punta,M., Coggill,P.C., Eberhardt,R.Y., Mistry,J., Tate,J., Boursnell,C., Pang,N., Forslund,K., Ceric,G., Clements,J. et al. (2012) The Pfam protein families database. Nucleic Acids Res., 40, D290-D301
44. Papadopoulos,J.S. and Agarwala,R. (2007) COBALT: constraintbased alignment tool for multiple protein sequences. Bioinformatics, 23, 1073-1079
45. Di Tommaso,P., Moretti,S., Xenarios,I., Orobitg,M., Montanyola,A., Chang,J.M., Taly,J.F. and Notredame,C. (2011) T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res., 39, W13-W17
46. Berry,K.E., Waghray,S., Mortimer,S.A., Bai,Y. and Doudna,J.A. (2011) Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure, 19, 1456-1466
47. Vasa,S.M., Guex,N., Wilkinson,K.A., Weeks,K.M. and Giddings,M.C. (2008) ShapeFinder: a software system for highthroughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis. RNA, 14, 1979-1990
48. Suloway,C., Pulokas,J., Fellmann,D., Cheng,A., Guerra,F., Quispe,J., Stagg,S., Potter,C.S. and Carragher,B. (2005) Automated molecular microscopy: the new Leginon system. J. Struct. Biol., 151, 41-60
49. Voss,N.R., Yoshioka,C.K., Radermacher,M., Potter,C.S. and Carragher,B. (2009) DoG Picker and TiltPicker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol., 166, 205-213
50. Mindell,J.A. and Grigorieff,N. (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol., 142, 334-347
51. Scheres,S.H., Nunez-Ramirez,R., Sorzano,C.O., Carazo,J.M. and Marabini,R. (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc., 3, 977-990
52. Scheres,S.H., Gao,H., Valle,M., Herman,G.T., Eggermont,P.P., Frank,J. and Carazo,J.M. (2007) Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat. Methods, 4, 27-29.