Cited by 727RNA modifications and cancerRNA and protein synthesis mechanismsRNA regulation and disease

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Tuning the ribosome: The influence of rRNA modification on eukaryotic ribosome biogenesis and function

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Sloan, Katherine E., Warda, Ahmed S., Sharma, Sunny, Entian, Karl-Dieter, Lafontaine, Denis L. J., Bohnsack, Markus T.·2017·RNA Biology

DOI 10.1080/15476286.2016.1259781PMC PMC5699541

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Abstract

rRNAs are extensively modified during their transcription and subsequent maturation in the nucleolus, nucleus and cytoplasm. RNA modifications, which are installed either by snoRNA-guided or by stand-alone enzymes, generally stabilize the structure of the ribosome. However, they also cluster at functionally important sites of the ribosome, such as the peptidyltransferase center and the decoding site, where they facilitate efficient and accurate protein synthesis. The recent identification of sites of substoichiometric 2'-O-methylation and pseudouridylation has overturned the notion that all rRNA modifications are constitutively present on ribosomes, highlighting nucleotide modifications as an important source of ribosomal heterogeneity. While the mechanisms regulating partial modification and the functions of specialized ribosomes are largely unknown, changes in the rRNA modification pattern have been observed in response to environmental changes, during development, and in disease. This suggests that rRNA modifications may contribute to the translational control of gene expression.

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Figure 1. Structures of box C/D and box H/ACA sRNP complexes. (A) Structural model of an H/ACA box sRNP from Pyrococcus furiosus (PDB 3HAY)154 A surface view of the protein components is shown and sRNA and rRNA are indicated in dark gray and red, respectively. (B) Structural model of a Sulfolobus solfataricus box C/D sRNP (PDB 3PLA)155 is shown as in A. The modified nucleotide is shown in surface view. Note, that archaeal L7Ae is an ortholog of eukaryotic Snu13 and in eukaryotes, Nop56 and Nop58 are orthologous to archaeal Nop5.CC BY-NC-ND · PubMed Central

Figure 2. Base modifications in rRNA and the enzymes that install them. (A) Chemical structures of the 4 nucleotides and the modifications that are added in yeast rRNAs. The additional chemical groups are marked in red and the enzymes that introduce them in yeast are indicated above the arrow (yellow) and in humans below the arrow (green). (B) Three-step modification pathway for U1191 of the 18S rRNA in yeast.CC BY-NC-ND · PubMed Central

Figure 3. Distribution of rRNA modifications on the yeast ribosome. The S. cerevisiae 80S ribosome (PBD 4V88)6 is shown – 40S in teal and 60S in gray. The positions of 2′-O-methylations (purple), pseudouridines (blue) and base modification installed by stand-alone enzymes (orange) are indicated. Three functionally important regions of the ribosome, the peptidyltransferase center (PTC), the decoding site and the intersubunit bridge eB14, are also shown in a magnified view.CC BY-NC-ND · PubMed Central

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Additional file 8 of Multiple links between 5-methylcytosine content of mRNA and translation
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Additional file 12 of Hypoxia induces alterations in tRNA modifications involved in translational control
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Additional file 13 of Hypoxia induces alterations in tRNA modifications involved in translational control
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Additional file 16 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135177
Additional file 12 of Multiple links between 5-methylcytosine content of mRNA and translation
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Additional file 1 of The nucleolar protein NOL12 is required for processing of large ribosomal subunit rRNA precursors in Arabidopsis
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Additional file 3 of m7GDisAI: N7-methylguanosine (m7G) sites and diseases associations inference based on heterogeneous network
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Additional file 11 of Hypoxia induces alterations in tRNA modifications involved in translational control
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Additional file 6 of Multiple links between 5-methylcytosine content of mRNA and translation
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Additional file 14 of Multiple links between 5-methylcytosine content of mRNA and translation
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Additional file 18 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135192
Additional file 19 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135201
Additional file 10 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135135
Additional file 3 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135213
Additional file 6 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
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Additional file 8 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600414
Additional file 8 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
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Additional file 7 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600411
Additional file 7 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135231
Additional file 5 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
Meng, Z., Li, X., Lu, S., Hua, Y., Yin, B., Qian, B., Li, Z., Zhou, Y., Sergeeva, I., Fu, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26733280
Additional file 13 of Multiple links between 5-methylcytosine content of mRNA and translation
Schumann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135153
Additional file 3 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
Meng, Z., Li, X., Lu, S., Hua, Y., Yin, B., Qian, B., Li, Z., Zhou, Y., Sergeeva, I., Fu, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26733274
Additional file 2 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600387
Additional file 4 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600396
Additional file 6 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600405
Additional file 5 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600402
Additional file 3 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600390
Additional file 15 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135171
Additional file 9 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135237
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Ma, C., Tu, D., Xu, Q., Wu, Y., Song, X., Guo, Z., & Zhao, X. (2023) · Figshare · doi:10.6084/m9.figshare.22611895
Additional file 9 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600417
Additional file 2 of The nucleolar protein NOL12 is required for processing of large ribosomal subunit rRNA precursors in Arabidopsis
Zakrzewska‐Placzek, M., Golisz, A., Krzysztoń, M., Piotrowska, J., Lichocka, M., & Kufel, J. (2024) · Figshare · doi:10.6084/m9.figshare.24494518
Additional file 17 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135186
Additional file 1 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135204
Additional file 11 of Multiple links between 5-methylcytosine content of mRNA and translation
Schümann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135144
Additional file 1 of Hypoxia induces alterations in tRNA modifications involved in translational control
Guo, H., Xia, L., Wang, W., Xu, W., Shen, X., Wu, X., He, T., Jiang, X., Xu, Y., Zhao, P., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22600378
Additional file 2 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
Meng, Z., Li, X., Lu, S., Hua, Y., Yin, B., Qian, B., Li, Z., Zhou, Y., Sergeeva, I., Fu, Y., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26027733
Additional file 4 of Multiple links between 5-methylcytosine content of mRNA and translation
Schumann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135216
Additional file 5 of Multiple links between 5-methylcytosine content of mRNA and translation
Schumann, U., Zhang, H.-N., Sibbritt, T., Pan, A., Horváth, A., Gross, S., Clark, S. J., Yang, L., & Preiß, T. (2020) · Figshare · doi:10.6084/m9.figshare.12135222
Additional file 2 of Multiple links between 5-methylcytosine content of mRNA and translation
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Additional file 1 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
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Additional file 7 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
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Additional file 4 of A comprehensive analysis of m6A/m7G/m5C/m1A-related gene expression and immune infiltration in liver ischemia–reperfusion injury by integrating bioinformatics and machine learning algorithms
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Authors: Sloan, K. E., Warda, A. S., Sharma, S., Entian, K.-D., Lafontaine, D. L. J., & Bohnsack, M. T.
Affiliations: Universitätsmedizin Göttingen (DE)
Université Libre de Bruxelles (BE)
Goethe University Frankfurt (DE)
Corresponding author: Bohnsack, Markus T.
ORCID: Sharma, Sunny
Lafontaine, Denis L. J.
Bohnsack, Markus T.
Venue: RNA Biology
Publisher: Informa UK Limited
Published: 2016-12-18
Volume: 14
Issue: 9
Pages: 1138-1152
ISSN: 1547-6286 (ISSN-L)
1555-8584
DOI: 10.1080/15476286.2016.1259781
PMC: PMC5699541
OpenAlex: W2557904026
Cited by: 707
References: 155
Citations by year: 2026: 63 · 2025: 64 · 2024: 81 · 2023: 101 · 2022: 90 · 2021: 90 · 2020: 96 · 2019: 57 · 2018: 47 · 2017: 15
FWCI: 3.62
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/4.0/ (vor)
Locations: RNA Biology (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion, other-oa)
GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
Keywords: rRNA modification, ribosome biogenesis, 80S ribosome, 2'-O-methylation, pseudouridylation, peptidyl transferase center, decoding site, translational regulation, ribosome structure, nucleolus
MeSH terms: Acetylation, Animals, Disease Susceptibility, Eukaryotic Cells, Humans, Methylation, Ribosomes, RNA, Ribosomal, Structure-Activity Relationship, RNA, Small Nucleolar

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Tuning the ribosome: The influence of rRNA modification on eukaryotic ribosome biogenesis and function

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