Open Access
Proceedings of the National Academy of Sciences of the United States of America, volume 111, issue 51, pages E5518-E5526
Structural and functional studies of Bud23–Trm112 reveal 18S rRNAN7-G1575 methylation occurs on late 40S precursor ribosomes
Létoquart Juliette
1
,
Huvelle Emmeline
2
,
Wacheul Ludivine
3
,
Bourgeois Gabrielle
1
,
Zorbas Christiane
3
,
Graille Marc
1
,
Heurgué Hamard Valérie
2
,
Lafontaine Denis L J
3, 4
1
Laboratoire de Biochimie, CNRS UMR 7654, Ecole Polytechnique, F-91128 Palaiseau Cedex, France;
|
2
CNRS FRE3630 (affiliated with Université Paris Diderot, Sorbonne Paris Cité), Institut de Biologie Physico-Chimique, Paris F-75005, France;
|
3
Center for Microscopy and Molecular Imaging, B-6041 Charleroi-Gosselies, Belgium; and
|
Publication type: Journal Article
Publication date: 2014-12-08
Quartile SCImago
Q1
Quartile WOS
Q1
Impact factor: 11.1
ISSN: 00278424, 10916490
PubMed ID:
25489090
Multidisciplinary
Abstract
Significance Ribosomes are essential cellular nanomachines responsible for all protein synthesis in vivo. Efficient and faithful ribosome biogenesis requires a plethora of assembly factors whose precise role and timing of action remains to be established. Here we determined the crystal structure of Bud23–Trm112, which is required for efficient pre-rRNA processing steps leading to 18S rRNA synthesis and methylation of 18S rRNA at position G1575. For the first time, to our knowledge, we identified where on Bud23–Trm112 the contacts with precursor ribosomes occur. We further report that the essential helicase Dhr1 interacts directly with Bud23–Trm112, proposing a concerted action of these proteins in ribosome assembly. Finally, we reveal that the methyltransferase activity of Bud23–Trm112 and its requirement for pre-rRNA processing are disconnected in time. The eukaryotic small ribosomal subunit carries only four ribosomal (r) RNA methylated bases, all close to important functional sites. N7-methylguanosine (m7G) introduced at position 1575 on 18S rRNA by Bud23–Trm112 is at a ridge forming a steric block between P- and E-site tRNAs. Here we report atomic resolution structures of Bud23–Trm112 in the apo and S-adenosyl-l-methionine (SAM)-bound forms. Bud23 and Trm112 interact through formation of a β-zipper involving main-chain atoms, burying an important hydrophobic surface and stabilizing the complex. The structures revealed that the coactivator Trm112 undergoes an induced fit to accommodate its methyltransferase (MTase) partner. We report important structural similarity between the active sites of Bud23 and Coffea canephora xanthosine MTase, leading us to propose and validate experimentally a model for G1575 coordination. We identify Bud23 residues important for Bud23–Trm112 complex formation and recruitment to pre-ribosomes. We report that though Bud23–Trm112 binds precursor ribosomes at an early nucleolar stage, m7G methylation occurs at a late step of small subunit biogenesis, implying specifically delayed catalytic activation. Finally, we show that Bud23–Trm112 interacts directly with the box C/D snoRNA U3-associated DEAH RNA helicase Dhr1 supposedly involved in central pseudoknot formation; this suggests that Bud23–Trm112 might also contribute to controlling formation of this irreversible and dramatic structural reorganization essential to overall folding of small subunit rRNA. Our study contributes important new elements to our understanding of key molecular aspects of human ribosomopathy syndromes associated with WBSCR22 (human Bud23) malfunction.
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- We do not take into account publications that without a DOI.
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- Statistics recalculated weekly.
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Létoquart J. et al. Structural and functional studies of Bud23–Trm112 reveal 18S rRNAN7-G1575 methylation occurs on late 40S precursor ribosomes // Proceedings of the National Academy of Sciences of the United States of America. 2014. Vol. 111. No. 51. p. E5518-E5526.
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Létoquart J., Huvelle E., Wacheul L., Bourgeois G., Zorbas C., Graille M., Heurgué Hamard V., Lafontaine D. L. J. Structural and functional studies of Bud23–Trm112 reveal 18S rRNAN7-G1575 methylation occurs on late 40S precursor ribosomes // Proceedings of the National Academy of Sciences of the United States of America. 2014. Vol. 111. No. 51. p. E5518-E5526.
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RIS
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TY - JOUR
DO - 10.1073/pnas.1413089111
UR - https://doi.org/10.1073%2Fpnas.1413089111
TI - Structural and functional studies of Bud23–Trm112 reveal 18S rRNAN7-G1575 methylation occurs on late 40S precursor ribosomes
T2 - Proceedings of the National Academy of Sciences of the United States of America
AU - Létoquart, Juliette
AU - Huvelle, Emmeline
AU - Wacheul, Ludivine
AU - Bourgeois, Gabrielle
AU - Zorbas, Christiane
AU - Graille, Marc
AU - Heurgué Hamard, Valérie
AU - Lafontaine, Denis L J
PY - 2014
DA - 2014/12/08 00:00:00
PB - Proceedings of the National Academy of Sciences (PNAS)
SP - E5518-E5526
IS - 51
VL - 111
PMID - 25489090
SN - 0027-8424
SN - 1091-6490
ER -
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@article{2014_Létoquart,
author = {Juliette Létoquart and Emmeline Huvelle and Ludivine Wacheul and Gabrielle Bourgeois and Christiane Zorbas and Marc Graille and Valérie Heurgué Hamard and Denis L J Lafontaine},
title = {Structural and functional studies of Bud23–Trm112 reveal 18S rRNAN7-G1575 methylation occurs on late 40S precursor ribosomes},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
year = {2014},
volume = {111},
publisher = {Proceedings of the National Academy of Sciences (PNAS)},
month = {dec},
url = {https://doi.org/10.1073%2Fpnas.1413089111},
number = {51},
pages = {E5518--E5526},
doi = {10.1073/pnas.1413089111}
}
Cite this
MLA
Copy
Létoquart, Juliette, et al. “Structural and functional studies of Bud23–Trm112 reveal 18S rRNAN7-G1575 methylation occurs on late 40S precursor ribosomes.” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 51, Dec. 2014, pp. E5518-E5526. https://doi.org/10.1073%2Fpnas.1413089111.