publication . Article . 2014

Initiation of Translation by Cricket Paralysis Virus IRES Requires Its Translocation in the Ribosome

Fernandez, Israel S.; Bai, Xiao-Chen; Murshudov, Garib; Scheres, Sjors H. W.; Ramakrishnan, V.;
Open Access
  • Published: 01 May 2014 Journal: Cell, volume 157, issue 4, pages 823-831 (issn: 0092-8674, Copyright policy)
  • Publisher: Elsevier BV
Abstract
Summary The cricket paralysis virus internal ribosome entry site (CrPV-IRES) is a folded structure in a viral mRNA that allows initiation of translation in the absence of any host initiation factors. By using recent advances in single-particle electron cryomicroscopy, we have solved the structure of CrPV-IRES bound to the ribosome of the yeast Kluyveromyces lactis in both the canonical and rotated states at overall resolutions of 3.7 and 3.8 Å, respectively. In both states, the pseudoknot PKI of the CrPV-IRES mimics a tRNA/mRNA interaction in the decoding center of the A site of the 40S ribosomal subunit. The structure and accompanying factor-binding data show t...
Subjects
Medical Subject Headings: fungi
free text keywords: Biochemistry, Genetics and Molecular Biology(all), Article, General Biochemistry, Genetics and Molecular Biology, Biology, Eukaryotic initiation factor, Genetics, Ribosomal binding site, Translation (biology), Initiation factor, T arm, Molecular biology, Eukaryotic Ribosome, Internal ribosome entry site, Ribosome profiling
Related Organizations
Funded by
RCUK| Visualising proteins in health and disease
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: MC_UP_A025_1013
  • Funding stream: MRC
,
WT| Structure and function of ribosomes.
Project
  • Funder: Wellcome Trust (WT)
  • Project Code: 096570
  • Funding stream: Cellular and Molecular Neuroscience
,
RCUK| Structure and function of the translational machinery
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: MC_U105184332
  • Funding stream: MRC
47 references, page 1 of 4

Agirrezabala, X., Lei, J., Brunelle, J.L., Ortiz-Meoz, R.F., Green, R., Frank, J.. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell. 2008; 32: 190-197 [OpenAIRE] [PubMed]

Aitken, C.E., Lorsch, J.R.. A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol.. 2012; 19: 568-576 [OpenAIRE] [PubMed]

Amunts, A., Brown, A., Bai, X.-C., Llácer, J.L., Hussain, T., Emsley, P., Long, F., Murshudov, G., Scheres, S.H.W., Ramakrishnan, V.. Structure of the yeast mitochondrial large ribosomal subunit. Science. 2014; 343: 1485-1489 [OpenAIRE] [PubMed]

Bai, X.C., Fernandez, I.S., McMullan, G., Scheres, S.H.. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. Elife. 2013; 2: e00461 [OpenAIRE] [PubMed]

Ben-Shem, A., Garreau de Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G., Yusupov, M.. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science. 2011; 334: 1524-1529 [OpenAIRE] [PubMed]

Blanchard, S.C., Kim, H.D., Gonzalez, R.L., Puglisi, J.D., Chu, S.. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA. 2004; 101: 12893-12898 [OpenAIRE] [PubMed]

Costantino, D.A., Pfingsten, J.S., Rambo, R.P., Kieft, J.S.. tRNA-mRNA mimicry drives translation initiation from a viral IRES. Nat. Struct. Mol. Biol.. 2008; 15: 57-64 [OpenAIRE] [PubMed]

Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K.. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr.. 2010; 66: 486-501 [OpenAIRE] [PubMed]

Fei, J., Kosuri, P., MacDougall, D.D., Gonzalez, R.L.J.. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell. 2008; 30: 348-359 [PubMed]

Filbin, M.E., Kieft, J.S.. Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol.. 2009; 19: 267-276 [OpenAIRE] [PubMed]

Galej, W.P., Oubridge, C., Newman, A.J., Nagai, K.. Crystal structure of Prp8 reveals active site cavity of the spliceosome. Nature. 2013; 493: 638-643 [OpenAIRE] [PubMed]

Gao, Y.G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C., Ramakrishnan, V.. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science. 2009; 326: 694-699 [OpenAIRE] [PubMed]

Goddard, T.D., Huang, C.C., Ferrin, T.E.. Visualizing density maps with UCSF Chimera. J. Struct. Biol.. 2007; 157: 281-287 [PubMed]

Jackson, R.J., Hellen, C.U., Pestova, T.V.. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol.. 2010; 11: 113-127 [OpenAIRE] [PubMed]

Jan, E., Sarnow, P.. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol.. 2002; 324: 889-902 [OpenAIRE] [PubMed]

47 references, page 1 of 4
Abstract
Summary The cricket paralysis virus internal ribosome entry site (CrPV-IRES) is a folded structure in a viral mRNA that allows initiation of translation in the absence of any host initiation factors. By using recent advances in single-particle electron cryomicroscopy, we have solved the structure of CrPV-IRES bound to the ribosome of the yeast Kluyveromyces lactis in both the canonical and rotated states at overall resolutions of 3.7 and 3.8 Å, respectively. In both states, the pseudoknot PKI of the CrPV-IRES mimics a tRNA/mRNA interaction in the decoding center of the A site of the 40S ribosomal subunit. The structure and accompanying factor-binding data show t...
Subjects
Medical Subject Headings: fungi
free text keywords: Biochemistry, Genetics and Molecular Biology(all), Article, General Biochemistry, Genetics and Molecular Biology, Biology, Eukaryotic initiation factor, Genetics, Ribosomal binding site, Translation (biology), Initiation factor, T arm, Molecular biology, Eukaryotic Ribosome, Internal ribosome entry site, Ribosome profiling
Related Organizations
Funded by
RCUK| Visualising proteins in health and disease
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: MC_UP_A025_1013
  • Funding stream: MRC
,
WT| Structure and function of ribosomes.
Project
  • Funder: Wellcome Trust (WT)
  • Project Code: 096570
  • Funding stream: Cellular and Molecular Neuroscience
,
RCUK| Structure and function of the translational machinery
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: MC_U105184332
  • Funding stream: MRC
47 references, page 1 of 4

Agirrezabala, X., Lei, J., Brunelle, J.L., Ortiz-Meoz, R.F., Green, R., Frank, J.. Visualization of the hybrid state of tRNA binding promoted by spontaneous ratcheting of the ribosome. Mol. Cell. 2008; 32: 190-197 [OpenAIRE] [PubMed]

Aitken, C.E., Lorsch, J.R.. A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol.. 2012; 19: 568-576 [OpenAIRE] [PubMed]

Amunts, A., Brown, A., Bai, X.-C., Llácer, J.L., Hussain, T., Emsley, P., Long, F., Murshudov, G., Scheres, S.H.W., Ramakrishnan, V.. Structure of the yeast mitochondrial large ribosomal subunit. Science. 2014; 343: 1485-1489 [OpenAIRE] [PubMed]

Bai, X.C., Fernandez, I.S., McMullan, G., Scheres, S.H.. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. Elife. 2013; 2: e00461 [OpenAIRE] [PubMed]

Ben-Shem, A., Garreau de Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G., Yusupov, M.. The structure of the eukaryotic ribosome at 3.0 Å resolution. Science. 2011; 334: 1524-1529 [OpenAIRE] [PubMed]

Blanchard, S.C., Kim, H.D., Gonzalez, R.L., Puglisi, J.D., Chu, S.. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. USA. 2004; 101: 12893-12898 [OpenAIRE] [PubMed]

Costantino, D.A., Pfingsten, J.S., Rambo, R.P., Kieft, J.S.. tRNA-mRNA mimicry drives translation initiation from a viral IRES. Nat. Struct. Mol. Biol.. 2008; 15: 57-64 [OpenAIRE] [PubMed]

Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K.. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr.. 2010; 66: 486-501 [OpenAIRE] [PubMed]

Fei, J., Kosuri, P., MacDougall, D.D., Gonzalez, R.L.J.. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell. 2008; 30: 348-359 [PubMed]

Filbin, M.E., Kieft, J.S.. Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol.. 2009; 19: 267-276 [OpenAIRE] [PubMed]

Galej, W.P., Oubridge, C., Newman, A.J., Nagai, K.. Crystal structure of Prp8 reveals active site cavity of the spliceosome. Nature. 2013; 493: 638-643 [OpenAIRE] [PubMed]

Gao, Y.G., Selmer, M., Dunham, C.M., Weixlbaumer, A., Kelley, A.C., Ramakrishnan, V.. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science. 2009; 326: 694-699 [OpenAIRE] [PubMed]

Goddard, T.D., Huang, C.C., Ferrin, T.E.. Visualizing density maps with UCSF Chimera. J. Struct. Biol.. 2007; 157: 281-287 [PubMed]

Jackson, R.J., Hellen, C.U., Pestova, T.V.. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol.. 2010; 11: 113-127 [OpenAIRE] [PubMed]

Jan, E., Sarnow, P.. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol.. 2002; 324: 889-902 [OpenAIRE] [PubMed]

47 references, page 1 of 4
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