Abstract
No-go decay and nonstop decay are mRNA surveillance pathways that detect translational stalling and degrade the underlying mRNA, allowing the correct translation of the genetic code. In eukaryotes, the protein complex of Pelota (yeast Dom34) and Hbs1 translational GTPase recognizes the stalled ribosome containing the defective mRNA. Recently, we found that archaeal Pelota (aPelota) associates with archaeal elongation factor 1α (aEF1α) to act in the mRNA surveillance pathway, which accounts for the lack of an Hbs1 ortholog in archaea. Here we present the complex structure of aPelota and GTP-bound aEF1α determined at 2.3-Å resolution. The structure reveals how GTP-bound aEF1α recognizes aPelota and how aPelota in turn stabilizes the GTP form of aEF1α. Combined with the functional analysis in yeast, the present results provide structural insights into the molecular interaction between eukaryotic Pelota and Hbs1. Strikingly, the aPelota·aEF1α complex structurally resembles the tRNA·EF-Tu complex bound to the ribosome. Our findings suggest that the molecular mimicry of tRNA in the distorted “A/T state” conformation by Pelota enables the complex to efficiently detect and enter the empty A site of the stalled ribosome.
References
31
Referenced
98
-
MK Doma, R Parker, RNA quality control in eukaryotes. Cell 131, 660–668 (2007).
(
10.1016/j.cell.2007.10.041
) / Cell / RNA quality control in eukaryotes by Doma MK (2007) -
O Isken, LE Maquat, Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function. Genes Dev 21, 1833–1856 (2007).
(
10.1101/gad.1566807
) / Genes Dev / Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function by Isken O (2007) -
LE Maquat, Nonsense-mediated mRNA decay: Splicing, translation and mRNP dynamics. Nat Rev Mol Cell Bio 5, 89–99 (2004).
(
10.1038/nrm1310
) / Nat Rev Mol Cell Bio / Nonsense-mediated mRNA decay: Splicing, translation and mRNP dynamics by Maquat LE (2004) -
PA Frischmeyer, et al., An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295, 2258–2261 (2002).
(
10.1126/science.1067338
) / Science / An mRNA surveillance mechanism that eliminates transcripts lacking termination codons by Frischmeyer PA (2002) -
A van Hoof, PA Frischmeyer, HC Dietz, R Parker, Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295, 2262–2264 (2002).
(
10.1126/science.1067272
) / Science / Exosome-mediated recognition and degradation of mRNAs lacking a termination codon by van Hoof A (2002) -
MK Doma, R Parker, Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440, 561–564 (2006).
(
10.1038/nature04530
) / Nature / Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation by Doma MK (2006) -
DO Passos, et al., Analysis of Dom34 and its function in no-go decay. Mol Biol Cell 20, 3025–3032 (2009).
(
10.1091/mbc.e09-01-0028
) / Mol Biol Cell / Analysis of Dom34 and its function in no-go decay by Passos DO (2009) -
Y Inagaki, C Blouin, E Susko, AJ Roger, Assessing functional divergence in EF-1 alpha and its paralogs in eukaryotes and archaebacteria. Nucleic Acids Res 31, 4227–4237 (2003).
(
10.1093/nar/gkg440
) / Nucleic Acids Res / Assessing functional divergence in EF-1 alpha and its paralogs in eukaryotes and archaebacteria by Inagaki Y (2003) -
B Riis, SIS Rattan, BFC Clark, WC Merrick, Eukaryotic protein elongation-factors. Trends Biochem Sci 15, 420–424 (1990).
(
10.1016/0968-0004(90)90279-K
) / Trends Biochem Sci / Eukaryotic protein elongation-factors by Riis B (1990) - L Frolova, et al., Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase. RNA 2, 334–341 (1996). / RNA / Eukaryotic polypeptide chain release factor eRF3 is an eRF1- and ribosome-dependent guanosine triphosphatase by Frolova L (1996)
-
A Carr-Schmid, C Pfund, EA Craig, TG Kinzy, Novel G-protein complex whose requirement is linked to the translational status of the cell. Mol Cell Biol 22, 2564–2574 (2002).
(
10.1128/MCB.22.8.2564-2574.2002
) / Mol Cell Biol / Novel G-protein complex whose requirement is linked to the translational status of the cell by Carr-Schmid A (2002) -
HH Lee, et al., Structural and functional insights into Dom34, a key component of no-go mRNA decay. Mol Cell 27, 938–950 (2007).
(
10.1016/j.molcel.2007.07.019
) / Mol Cell / Structural and functional insights into Dom34, a key component of no-go mRNA decay by Lee HH (2007) - M Graille, M Chaillet, H van Tilbeurgh, Structure of yeast Dom34—A protein related to translation termination factor eRF1 and involved in no-go decay. J Biol Chem 283, 7145–7154 (2008). / J Biol Chem / Structure of yeast Dom34—A protein related to translation termination factor eRF1 and involved in no-go decay by Graille M (2008)
-
HW Song, et al., The crystal structure of human eukaryotic release factor eRF1—Mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100, 311–321 (2000).
(
10.1016/S0092-8674(00)80667-4
) / Cell / The crystal structure of human eukaryotic release factor eRF1—Mechanism of stop codon recognition and peptidyl-tRNA hydrolysis by Song HW (2000) -
Z Cheng, et al., Structural insights into eRF3 and stop codon recognition by eRF1. Genes Dev 23, 1106–1118 (2009).
(
10.1101/gad.1770109
) / Genes Dev / Structural insights into eRF3 and stop codon recognition by eRF1 by Cheng Z (2009) -
P Khusial, R Plaag, GW Zieve, LSm proteins form heptameric rings that bind to RNA via repeating motifs. Trends Biochem Sci 30, 522–528 (2005).
(
10.1016/j.tibs.2005.07.006
) / Trends Biochem Sci / LSm proteins form heptameric rings that bind to RNA via repeating motifs by Khusial P (2005) - TM Link, P Valentin-Hansen, RG Brennan, Structure of Escherichia coli Hfq bound to polyriboadenylate RNA. Proc Natl Acad Sci USA 106, 19286–19291 (2009). / Proc Natl Acad Sci USA / Structure of Escherichia coli Hfq bound to polyriboadenylate RNA by Link TM (2009)
-
MA Schumacher, RF Pearson, T Moller, P Valentin-Hansen, RG Brennan, Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: A bacterial Sm-like protein. EMBO J 21, 3546–3556 (2002).
(
10.1093/emboj/cdf322
) / EMBO J / Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: A bacterial Sm-like protein by Schumacher MA (2002) -
MA Ragan, JM Logsdon, CW Sensen, RL Charlebois, WF Doolittle, An archaebacterial homolog of pelota, a meiotic cell division protein in eukaryotes. FEMS Microbiol Lett 144, 151–155 (1996).
(
10.1111/j.1574-6968.1996.tb08522.x
) / FEMS Microbiol Lett / An archaebacterial homolog of pelota, a meiotic cell division protein in eukaryotes by Ragan MA (1996) - K Saito, et al., An omnipotent role of archaeal EF1α in translation elongation, termination and quality control of protein synthesis. Proc Natl Acad Sci USA, in press. (2010). / Proc Natl Acad Sci USA / An omnipotent role of archaeal EF1α in translation elongation, termination and quality control of protein synthesis by Saito K (2010)
-
H Berchtold, et al., Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature 365, 126–132 (1993).
(
10.1038/365126a0
) / Nature / Crystal structure of active elongation factor Tu reveals major domain rearrangements by Berchtold H (1993) -
M Kjeldgaard, P Nissen, S Thirup, J Nyborg, The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure 1, 35–50 (1993).
(
10.1016/0969-2126(93)90007-4
) / Structure / The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation by Kjeldgaard M (1993) -
L Vitagliano, M Masullo, F Sica, A Zagari, V Bocchini, The crystal structure of Sulfolobus solfataricus elongation factor 1 alpha in complex with GDP reveals novel features in nucleotide binding and exchange. EMBO J 20, 5305–5311 (2001).
(
10.1093/emboj/20.19.5305
) / EMBO J / The crystal structure of Sulfolobus solfataricus elongation factor 1 alpha in complex with GDP reveals novel features in nucleotide binding and exchange by Vitagliano L (2001) -
TM Schmeing, et al., The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326, 688–694 (2009).
(
10.1126/science.1179700
) / Science / The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA by Schmeing TM (2009) -
P Nissen, et al., Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog. Science 270, 1464–1472 (1995).
(
10.1126/science.270.5241.1464
) / Science / Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu, and a GTP analog by Nissen P (1995) -
LY Frolova, et al., Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis. RNA 5, 1014–1020 (1999).
(
10.1017/S135583829999043X
) / RNA / Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis by Frolova LY (1999) -
CMT Spahn, et al., Structure of the 80S ribosome from Saccharomyces cerevisiae—tRNA-ribosome and subunit-subunit interactions. Cell 107, 373–386 (2001).
(
10.1016/S0092-8674(01)00539-6
) / Cell / Structure of the 80S ribosome from Saccharomyces cerevisiae—tRNA-ribosome and subunit-subunit interactions by Spahn CMT (2001) -
DJ Taylor, et al., Comprehensive molecular structure of the eukaryotic ribosome. Structure 17, 1591–1604 (2009).
(
10.1016/j.str.2009.09.015
) / Structure / Comprehensive molecular structure of the eukaryotic ribosome by Taylor DJ (2009) -
LN Dimitrova, K Kuroha, T Tatematsu, T Inada, Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J Biol Chem 284, 10343–10352 (2009).
(
10.1074/jbc.M808840200
) / J Biol Chem / Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome by Dimitrova LN (2009) - E Krissinel, K Henrick, Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D60, 2256–2268 (2004). / Acta Crystallogr / Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions by Krissinel E (2004)
-
NA Baker, D Sept, S Joseph, MJ Holst, JA McCammon, Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci USA 98, 10037–10041 (2001).
(
10.1073/pnas.181342398
) / Proc Natl Acad Sci USA / Electrostatics of nanosystems: Application to microtubules and the ribosome by Baker NA (2001)
Dates
Type | When |
---|---|
Created | 14 years, 11 months ago (Sept. 28, 2010, 12:45 a.m.) |
Deposited | 3 years, 2 months ago (June 7, 2022, 3:12 a.m.) |
Indexed | 4 months ago (April 26, 2025, 2:21 a.m.) |
Issued | 14 years, 11 months ago (Sept. 27, 2010) |
Published | 14 years, 11 months ago (Sept. 27, 2010) |
Published Online | 14 years, 11 months ago (Sept. 27, 2010) |
Published Print | 14 years, 10 months ago (Oct. 12, 2010) |
@article{Kobayashi_2010, title={Structural basis for mRNA surveillance by archaeal Pelota and GTP-bound EF1α complex}, volume={107}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1009598107}, DOI={10.1073/pnas.1009598107}, number={41}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Kobayashi, Kan and Kikuno, Izumi and Kuroha, Kazushige and Saito, Kazuki and Ito, Koichi and Ishitani, Ryuichiro and Inada, Toshifumi and Nureki, Osamu}, year={2010}, month=sep, pages={17575–17579} }