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Chapter 17 : Nucleotide Modifications of Eukaryotic rRNAs: the World of Small Nucleolar RNA Guides Revisited

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Abstract:

Breakthroughs in the field of small nucleolar RNAs (snoRNAs) have illuminated the process of selection of the nucleotides to be ribose methylated and pseudouridylated in eukaryotic rRNA, opening new prospects for elucidating the role of these modifications in the assembly and function of the eukaryotic ribosome. This chapter summarizes our present knowledge of snoRNA guide function, which in both cases involves formation of a specific RNA duplex at each rRNA modification site, and focuses on recent progress and issues in this area. A putative box C/D antisense snoRNA that should direct the ribose methylation of A53 in human U6 has also been detected. These developments might have far-reaching implications in the field of mRNA biogenesis in eukaryotes, particularly since the crucial importance of snRNA nucleotide modifications for pre-mRNA splicing has just been established in the case of U2 snRNA. Archaebacterial rRNAs have recently been found to contain a large number of ribose methylations, amounting to 67 per ribosome in , i.e., a number very similar to that of eukaryotes and quite different from the very simple eubacterial pattern. The genomic organizations and modes of expression of both families of guide snoRNAs exhibit great diversity, with, in addition to intronic snoRNAs, snoRNAs encoded by independent genes and processed by a splicing-independent mechanism. Progress has been made in understanding how the sites of ribose methylations and pseudouridines are selected within the sequences of eukaryotic rRNAs.

Citation: Bachellerie J, Cavaillé J, Qu L. 2000. Nucleotide Modifications of Eukaryotic rRNAs: the World of Small Nucleolar RNA Guides Revisited, p 191-204. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch17

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Figure 1

Generic structure of the two major snoRNA families and corresponding guide RNA duplexes at rRNA modification sites. (a) Box C/D antisense snoRNAs. (Top) Locations of the two box motifs (and less conserved copies C′ and D′) and of the antisense elements (thick lines), present either as a single copy or as a pair. (Bottom) Canonical structure of the RNA duplex formed at each ribose-methylated site in rRNA. (b) H/ACA snoRNAs. (Top) Schematized conserved secondary structure. The total number of nucleotides within each of the long helical domains I and II may vary substantially among the different snoRNAs, with the variations affecting both the stem and loop regions. The pair of 4- to 8-nt-long complementarities to rRNA present within the long internal loop in domain I or II (or in both) is depicted by a thicker line. (Bottom) Canonical structure of the RNA duplex formed at each pseudouridylation site in rRNA.

Citation: Bachellerie J, Cavaillé J, Qu L. 2000. Nucleotide Modifications of Eukaryotic rRNAs: the World of Small Nucleolar RNA Guides Revisited, p 191-204. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch17
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Figure 2

In vivo dissection of the methylation guide RNA duplex by cotransfection of artificial guide snoRNA and RNA substrate in mammalian cells. (a) Construct expressing an artificial intron-encoded guide snoRNA under the control of the strong cytomegalovirus (CMV) promoter. (b) rRNA minigene construct expressing, under the control of RNA polymerase I, an RNA substrate (sequence shown) carrying the appropriate complementarity (underlined) to the artificial guide snoRNA. The detection of ribose methylation was based on the selection of a guanosine as the target nucleotide in the RNA substrate. The guanosine was placed in a sequence devoid of any proximal upstream guanosine. Two long oligonucleotides (horizontal arrows) generated by RNase T1 digestion reflect the degree of ribose methylation at the targeted guanosine (below circle; the two proximal upstream and downstream guanosines are shaded). P, oligonucleotide P (see below). (c) Schematized structure of the guide RNA duplex. Positions where a 1-nt bulge is strongly inhibitory for the targeted methylation are denoted by ovals. (d) Northern assay of the ribose methylation at the targeted guanosine. T1 RNase digests of total RNA from cells cotransfected with the guide (g.) snoRNA and its cognate RNA substrate were probed with oligonucleotide P, shown in panel b. +, present; –, absent.

Citation: Bachellerie J, Cavaillé J, Qu L. 2000. Nucleotide Modifications of Eukaryotic rRNAs: the World of Small Nucleolar RNA Guides Revisited, p 191-204. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch17
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Figure 3

Efficient methylation of an RNA polymerase II transcript addressed to the nucleolus. (a) Structure of the construct expressing the RNA polymerase II transcript, showing the guanosine targeted for methylation (vertical arrow) in the sequence (shaded) complementary to the antisense element of the cotransfected artificial guide snoRNA (not shown). The RNA substrate sequence was inserted in an intron, flanked by sequence elements able to form the typical stem-box terminal structure of box C/D snoRNAs. P, oligonucleotide P. (b) The level of targeted-ribose methylation was determined after RNase T1 digestion by Northern blotting with the oligonucleotide probe (P) delineated in panel a. Accumulation of the RNA substrate processed at the borders of the stem-box structure and expression of the cognate artificial guide snoRNA were both assessed on intact cellular RNA. Lanes 1, transfection with the RNA substrate alone. Lanes 2, cotransfection of the RNA substrate and the guide snoRNA.

Citation: Bachellerie J, Cavaillé J, Qu L. 2000. Nucleotide Modifications of Eukaryotic rRNAs: the World of Small Nucleolar RNA Guides Revisited, p 191-204. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch17
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Figure 4

Diversity of guide snoRNA biosynthetic pathways.

Citation: Bachellerie J, Cavaillé J, Qu L. 2000. Nucleotide Modifications of Eukaryotic rRNAs: the World of Small Nucleolar RNA Guides Revisited, p 191-204. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch17
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