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Chapter 13 : Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs

Authors: Jean-Pierre Bachellerie1, Jérôme Cavaillé1
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Affiliations: 1: Laboratoire de Biologie Moléculaire Eucaryote du CNRS, Université Paul-Sabatier, 118, route de Narbonne, 31062 Toulouse Cédex, France
Content Type: Monograph
Publication Year: 1998

Category: Microbial Genetics and Molecular Biology

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Abstract:

This chapter provides a progress report on developments that should set the stage for dissecting the rRNA-ribose methylation machinery and for deciphering the role of these modifications in ribosome assembly and function. Interestingly, ribose methylations are far from being uniformly distributed within the universally conserved domains of eukaryotic rRNAs. The finding that small RNA guides specify the sites of ribose methylation in eukaryotic rRNAs raises the issue that RNA cofactors also could be involved in prokaryotes. Prokaryotic rRNAs have considerably fewer ribose methylations than eukaryotic rRNAs, with only 4 sites in . Two prokaryotic rRNA ribose methylases have been characterized so far that are each specific for a single site in rRNA. The presence of a complex repertoire of site-specific, -acting snoRNA guides sufficient to precisely target the modification through the formation of a common canonical duplex structure with the rRNA substrate strongly suggests that the enzymology of the reaction is quite simple, at least as to the variety of protein enzymes involved. snoRNA-guided ribose methylation of rRNA involves the formation of scores of 10-21 bp long intermolecular RNA duplexes along the elongating pre-rRNA transcript in eukaryotes. Analyzing the structure of the methylase(s) and pseudouridine synthase(s) involved in the modification of eukaryotic rRNAs, with particular reference to RNA editing enzymes, also recognizing double-stranded RNA structures could be illuminating.

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
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Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs
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Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
/content/10.1128/9781555818296.chap13.fig13-1
Figure 1

Clustering of ribose methylation sites in eukaryotic 28S rRNA secondary structure. Only the universally conserved domains of the rRNA molecule are represented (the evolutionarily variable D domains are indicated by dots; the junction between the 5′ and 3′ halves of the molecule is schematized by a broken line). Ribose methylated sites are shown by filled circles (sites that are still presumptive are denoted by question marks). (A) Sites conserved between the yeast and vertebrates (the two arrows point to sites conserved in 23 S rRNA). (B) Ribose methylated sites specific to vertebrates.

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Figure 1

Clustering of ribose methylation sites in eukaryotic 28S rRNA secondary structure. Only the universally conserved domains of the rRNA molecule are represented (the evolutionarily variable D domains are indicated by dots; the junction between the 5′ and 3′ halves of the molecule is schematized by a broken line). Ribose methylated sites are shown by filled circles (sites that are still presumptive are denoted by question marks). (A) Sites conserved between the yeast and vertebrates (the two arrows point to sites conserved in 23 S rRNA). (B) Ribose methylated sites specific to vertebrates.

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
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Figure 2

Ribose methylated nucleotides involved in tertiary interactions in 28S rRNA structure. Among the few tertiary interactions by canonical base pairing which are supported by comparative sequence analysis ( ), only the ones involving ribose methylated nucleotides are shown here (dotted lines). In each case the precise nucleotide positions involved are indicated for human 28S rRNA (the corresponding 23S rRNA coordinates are also given in parentheses).

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10.1128/9781555818296/fig13-2.gif
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Figure 2

Ribose methylated nucleotides involved in tertiary interactions in 28S rRNA structure. Among the few tertiary interactions by canonical base pairing which are supported by comparative sequence analysis ( ), only the ones involving ribose methylated nucleotides are shown here (dotted lines). In each case the precise nucleotide positions involved are indicated for human 28S rRNA (the corresponding 23S rRNA coordinates are also given in parentheses).

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
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Figure 3

Generic structure of snoRNAs belonging to the box C/D antisense family. Most snoRNAs contain a single antisense element (filled bar), located either immediately upstream from box D (top) or in the 5′ half, immediately upstream from another copy of box D, box D′ (middle). A few snoRNAs (U24, U32, U36, U45 and U50) contain two different antisense elements (bottom). The 5′-3′ terminal stem-box structure shared by most members of the family is schematized on the right.

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Image of Figure 3
Figure 3

Generic structure of snoRNAs belonging to the box C/D antisense family. Most snoRNAs contain a single antisense element (filled bar), located either immediately upstream from box D (top) or in the 5′ half, immediately upstream from another copy of box D, box D′ (middle). A few snoRNAs (U24, U32, U36, U45 and U50) contain two different antisense elements (bottom). The 5′-3′ terminal stem-box structure shared by most members of the family is schematized on the right.

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
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Figure 4

The snoRNA/rRNA guide duplex at ribose methylation sites. (A) Structure of the canonical base pairing (dots denote base pairs not present in all duplexes). (B) Representation of the RNA duplex as an Α-form helix, in the case of the U24-25S rRNA interaction. The nucleotides shown are written in the upper part and the site of ribose methylation is denoted by an arrow. (Panel Β is reproduced with permission from )

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10.1128/9781555818296/fig13-4.gif
Image of Figure 4
Figure 4

The snoRNA/rRNA guide duplex at ribose methylation sites. (A) Structure of the canonical base pairing (dots denote base pairs not present in all duplexes). (B) Representation of the RNA duplex as an Α-form helix, in the case of the U24-25S rRNA interaction. The nucleotides shown are written in the upper part and the site of ribose methylation is denoted by an arrow. (Panel Β is reproduced with permission from )

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
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Figure 5

Mutually exclusive snoRNA/rRNA duplexes at adjacent ribose methylation sites. The two sites of ribose methylation in the 18S rRNA sequence (middle line) are boxed. Arrowheads point to the fifth nucleotide upstream from box D in each cognate guide snoRNAs, U32 and U33 ( ).

10.1128/9781555818296/fig13-5_thmb.gif
10.1128/9781555818296/fig13-5.gif
Image of Figure 5
Figure 5

Mutually exclusive snoRNA/rRNA duplexes at adjacent ribose methylation sites. The two sites of ribose methylation in the 18S rRNA sequence (middle line) are boxed. Arrowheads point to the fifth nucleotide upstream from box D in each cognate guide snoRNAs, U32 and U33 ( ).

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
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Tables

Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs
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Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
/content/10.1128/9781555818296.chap13.tab13-1
Table 1

Numbers of modified nucleotides detected in rRNAs of representative species

10.1128/9781555818296/tab13-1_thmb.gif
10.1128/9781555818296/tab13-1.gif
Generic image for table
Table 1

Numbers of modified nucleotides detected in rRNAs of representative species

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13
/content/10.1128/9781555818296.chap13.tab13-2
Table 2

Ribose-methylated sites in eukaryotic rRNAs associated with a known snoRNA guide

10.1128/9781555818296/tab13-2_thmb.gif
10.1128/9781555818296/tab13-2.gif
Generic image for table
Table 2

Ribose-methylated sites in eukaryotic rRNAs associated with a known snoRNA guide

Citation: Bachellerie J, Cavaillé J. 1998. Small Nucleolar RNAs Guide the Ribose Methylations of Eukaryotic rRNAs, p 255-272. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch13

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