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Chapter 11 : Posttranscriptional Modifications in the U Small Nuclear RNAs

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Abstract:

This chapter deals with the posttranscriptional modifications of metabolically stable small nuclear RNAs (snRNAs) and the possible link to the function of these molecules. A study of the posttranscriptional modifications in the AT-AC specific spliceosomal snRNAs was started, and the results obtained are described in this chapter. The identity and location of all the detected posttranscriptional modifications are shown in the chapter. Interestingly, the sequence involved in where this pseudoknot structure is located contains posttranscriptional modifications: two 2’-O methylations and three pseudouridines. Posttranscriptional modifications may be required for stabilization of the pseudoknot structure. The importance of the posttranscriptional modifications of the human U2 snRNA for spliceosome activity was clearly demonstrated by reconstitution of the spliceosome with HeLa cell nuclear extracts depleted of U2 snRNA and complemented with in vitro transcribed U2 snRNA. It has now been clearly demonstrated that 5’-terminal posttranscriptional modifications play an essential role for the biogenesis of the spliceosomal U snRNPs in eukaryotes, and this is probably also the case for the U snRNAs involved in the recently discovered minor splicing machinery of vertebrates. The various recent experiments that are previously summarized in the chapter are strongly in favor of a direct functional role of U snRNA posttranscriptional modifications in spliceosome assembly and splicing.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11

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Figures

Image of Figure 1
Figure 1

The two chemical steps of nuclear pre-mRNA splicing. The highly conserved nucleotides and structures of the intermediates and products are shown ( ).

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 2
Figure 2

Steps of spliceosome assembly in the vertebrates. Substrate (pre-mRNA), intermediate (lariat-intron-exon2), and products (exonl, mRNA and lariat intron) of the reaction are indicated as well as the order of assembly of the snRNP components. First and second steps are the same as first and second steps in Fig. 1. (For references, see text.)

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 3
Figure 3

The various 5′-cap structures of U snoRNAs and spliceosomal U snRNAs. The mG cap of the RNA polymerase ii transcripts ( ); N,N,7-trimethylguanosine cap structure (in square brackets) of the spliceosomal U1, U2, U4, U5, U1 1, U12, and U4atac snRNAs ( ) and of the vertebrate U3, U8 and U13 snoRNAs ( ); and γ-methyl phosphate guanosine cap structure of U6 snRNA, U6atac snRNA ( ), and plant U3 snoRNA ( ) are shown.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 4
Figure 4

Rat U3B snoRNA. On the left, the possible secondary structure of the rat U3B snoRNA, based on the secondary structure experimentally established for the HeLa cell U3 snoRNA ( ). The primary sequence was from . The two pseudouridines identified in the rat hepatoma U3 snoRNA are shown (squared in black). The evolutionarily conserved sequences denoted Box A ( ), A′ ( ), ( ), C ( ), C′ ( ) and D ( ) are indicated. One the right, interaction of U3 snoRNA with 18S pre-rRNA, as proposed by (helices I, II, and III) and , (helix IV). In the table at the bottom, phylogenetic conservation of the heterologous helices, I, II, III and IV between U3 snoRNA and 18S rRNA sequences according to , and is shown. The 5′ domains of U3 snoRNAs from a wide range of organisms (top) are aligned to the complementary sequences in the respective SSU (small subunit) rRNA (bottom). The sequences are derived from the following GenEMBL database files, in order of listing in the table: U3 snoRNAs, M14061, K00780, X07318, X14411, M26649, X63788, and S74818; SSU rRNAs, X03205, V01270, XLRN01, X51576, J01353, M10932, and 152676. The putative extension of helix III in lower eukaryotes and the putative helix IV are in grey boxes.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 5
Figure 5

Secondary structure proposed for mouse U8 snoRNA. The sequence was from Kato and Harada (1984), and the structure was proposed by . The evolutionarily conserved sequences denoted Box C and D are indicated, as well as the identified posttranscriptional modifications. The interaction of U8 snoRNA with 28S rRNA, as proposed by , is shown. The posttranscriptional modifications are squared in black.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 6
Figure 6

A model for the nuclear transport cycle of the spliceosomal U snRNPs. In the nucleus, newly transcribed snRNA (U1 as an example) binds the CBC-importin- complex, and the Ran/TC4 guanosine triphosphatase in its GTP-associated form (Ran GTP). This complex is exported to the cytoplasm through the nuclear pore complex (NPC). Importin- () interacts with the pore proteins Nup1p and Nup2p. In the cytoplasm, GTP is hydrolyzed in the presence of Ran GAP1, association of importin- promotes the liberation of the mG U snRNA, and the protein complex (Ran; importins CBC) is allowed to move back to the nucleus. The m7G U snRNAs associate with the Sm proteins in a sequential pathway, and hypermethylation of the cap structure occurs. Both events provide the bipartite nuclear localization signal (NLS), recognized by a cytosolic factor (snuportin) which drives the core snRNP back to the nucleus, where specific proteins can associate. (For references, see the text.)

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 7
Figure 7

A comparison of modified nucleotides in U5 snRNAs from different species. Only the stem-loop structure 1 that contains modified nucleotides is shown. The nucleotide sequences are from HeLa cells ( ), ( ), Pea ( ), ( ), ( ), ( ), ( ), ( ) and ( ). The posttranscriptional modifications are squared in black.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 8
Figure 8

Secondary structures of rat spliceosomal U1 and U2 snRNAs. The secondary structures are from and (U1) and and (U2). For the U2 snRNA structure, the sequences implicated in the proposed pseudoknot ( ) are overlined and joined by a double arrow. The Sm binding sites are boxed. The 3′ extremity is not shown. The posttranscriptional modifications are squared in black.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 9
Figure 9

Secondary structures of rat spliceosomal U4 and U6 snRNAs and U4-U6 and U4atac-U6atac snRNA interactions in vertebrates. (A) The secondary structures are from and Myslinski and Branlant (1991) (U4) and Mougin et al. (unpublished results) (U6). (B) U4-U6 snRNA duplex. The nucleotide sequences shown are from rat ( ). The heterologous stems I and II are as proposed by , and the additional stem III is as proposed by . (C) U4atac-U6atac snRNA duplex. The nucleotide sequences are from HeLa cells as determined by . The heterologous stems I and II were proposed by based on the model proposed by . An additional potential stem III is shown as proposed by . Pseudouridines were investigated in both RNAs; only one residue (pseudouridine 14 in U4atac) was detected ( ). The posttranscriptional modifications are squared in black.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 10
Figure 10

The 5′ and 3′ splice sites and branch-site consensus sequences of HeLa cells and introns and their interactions with the spliceosomal U snRNAs. (A) Consensus sequences of the major introns from vertebrates; (B) consensus sequences of the yeast introns; (C) consensus sequences of the minor introns from vertebrates. The complementary sequences of U1 and U11 for 5′ splice sites and U2 and U12 for the branch-point sequences (BP) are shown.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Image of Figure 11
Figure 11

U snRNA-U snRNA and U snRNA-pre-mRNA interactions at the catalytic center of the spliceosomes. (A) Major spliceosome of vertebrates; (B) yeast spliceosome. In panel A, the nucleotide sequences are from rat. The heterologous helices I, II, and III between U2 and U6 snRNAs are shown, as well as the base-pairing interaction between U2 snRNA and the branch-point sequence, and the interaction between U6 snRNA and the sequence close to the 5′-splice site. Interactions between the terminal loop of U5 snRNA and the exon extremities are also represented ( ). (C) Minor spliceosome of vertebrates. The nucleotide sequences are from HeLa cells ( ). The predicted interactions ( ) between U12 and U6atac snRNAs are shown. Potential interactions deduced from comparisons with the major spliceosome are also shown: the potential interaction between U6atac snRNA and the sequence at the 5′ end of the intron and the potential interaction of U5 snRNA with the exon extremities are shown. The posttranscriptional modifications are shown in black squares.

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
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Tables

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Table 1

Distribution of intramolecular nucleotide modifications in analyzed spliceosomal U snRNAs and U snoRNAs

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11
Generic image for table
Table 2

Internal posttranscriptional modifications in analyzed U snRNAs and spliceosomal U snRNAs

Citation: Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional Modifications in the U Small Nuclear RNAs, p 201-227. In Grosjean H, Benne R (ed), Modification and Editing of RNA. ASM Press, Washington, DC. doi: 10.1128/9781555818296.ch11

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