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SL Trans-Splicing: Easy Come Or Easy Go?

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SL Trans-Splicing: Easy Come Or Easy Go? Review TRENDS in Genetics Vol.21 No.4 April 2005 SL trans-splicing: easy come or easy go? Kenneth E.M. Hastings Montreal Neurological Institute and Department of Biology, McGill University, 3801 University St, Montreal, Quebec, Canada H3A 2B4 Is spliced-leader (SL) trans-splicing an ancestral eukary- (i.e.joiningtwoseparateRNAmoleculestoforma otic characteristic that has been lost in multiple chimeric molecule). Two forms of spliceosomal trans- lineages, or did it arise independently in the various splicing occur naturally: (i) pre-mRNA donor trans- phyla in which it occurs? Recent studies have discovered splicing, in which a splice-donor site on one pre-mRNA SL trans-splicing in new metazoan phyla, including the molecule is joined to an acceptor site on another that is, in chordates. Its discovery in chordates identifies, for the most cases, transcribed from the same gene or genomic first time, a phylum that clearly contains both trans- region [12,13]; and (ii) SL trans-splicing. splicing and non-trans-splicing major groups, and In SL trans-splicing the donor is a specialized non- defines a limited and well-understood field in which to mRNA, the SL RNA, whose only known function is to study the evolutionary dynamics of SL trans-splicing. In donate a short (w15–50 nt) leader sequence that is this article, I summarize the evolutionarily relevant transferred to pre-mRNA splice-acceptor sites, and aspects of SL trans-splicing and consider the interplay which becomes the 50-end of the mature mRNA. Current among SL trans-splicing, pre-mRNA splice-signal syntax knowledge of the phylogenetic distribution of SL trans- and evolutionary genomics. splicing has emerged in two phases. SL trans-splicing was first discovered w20 years ago in kinetoplastids in the protist phylum Euglenozoa (reviewed in Ref. [14]) and, Introduction over the next several years, in two protostome bilaterian Spliced-leader (SL) trans-splicing is the spliceosomal metazoans, the nematode Caenorhabditis elegans [15] and transfer of a short RNA sequence, the spliced leader, the flatworm (Platyhelminthes) Schistosoma mansoni 0 from the 5 -end of a specialized non-mRNA molecule, the [16], and also in the protist Euglena gracilis (related to SL RNA (see Glossary), to unpaired splice-acceptor sites kinetoplastids) [17]. In the decade following these initial on pre-mRNA molecules. As a result, diverse mRNAs – findings, there were no reports of SL trans-splicing in ranging from a minority to 100% of the mRNA population additional phyla. However, during that time SL trans- 0 in different organisms – acquire a common 5 -sequence. splicing was discovered in additional species within the SL trans-splicing has a patchy phylogenetic distribution Euglenozoa, nematodes and flatworms, and extensive and enigmatic evolutionary origins [1]. The evolution- studies, particularly focused on kinetoplastids and ary relevance of SL trans-splicing has recently been broadened by a significant expansion of the known phylogenetic range to include the chordates [2,3]. Here, I Glossary provide an updated overview of evolutionary aspects of SL Appendicularian: (also called larvacean) a member of a planktonic tunicate trans-splicing, some of which were briefly reviewed by class in which the larval tail is maintained into adulthood. Ascidian: (also called sea squirt) a member of a sessile tunicate class featuring Nilsen in this journal in 2001 [1], and consider the possible a dramatic metamorphosis in which the larval tail is lost. genomic causes and consequences of the gain or loss of SL Kinetoplastid: trypanosome; a protist of the phylum Euglenozoa. 0 trans-splicing in an organismal lineage. See Refs [4,5] for Outron:the5-segment of a trans-spliced pre-mRNA upstream of the trans- splice-acceptor site. a review of the mechanism of trans-splicing and additional SL RNA: spliced-leader donor RNA. reviews considering the origin, function and phylogenetic Sm proteins: a class of related proteins that bind to a U-rich RNA motif and are found in snRNPs. distribution of SL trans-splicing [1,6,7] and its role in snRNP: small ribonucleoprotein particle consisting of snRNA complexed with polycistronic transcription [8]. specific proteins. Splice-acceptor site: the intron–exon junction at the 30-end of an intron. Splice-donor site: the exon–intron junction at the 30-end of an exon. 0 Eukaryotic pre-mRNA cis- and trans-splicing TMG: trimethyl guanosine (m3 2,2,7G), found in the 5 -cap structure of Spliceosomal pre-mRNA cis-splicing (i.e. intron removal) Sm-binding U snRNAs and in metazoan SL RNA. Tunicate: (also called urochordate) a member of a protochordate subphylum of is an ancient eukaryotic process [9] that is preserved in the chordates consisting of filter-feeding marine organisms having a leathery all or most lineages, albeit much reduced in some groups outer covering or tunic and a larval stage marked by a tail including dorsal nerve (e.g. kinetoplastids [10] and yeast [11]). In addition to cis- cord, notochord and flanking muscle cells. U snRNAs: a U-rich class of small nuclear RNAs, including spliceosomal splicing, the spliceosome is capable of trans-splicing snRNAs. Unpaired splice acceptor: a splice-acceptor site for which there is no Corresponding author: Hastings, K.E.M. ([email protected]). corresponding upstream splice-donor site. www.sciencedirect.com 0168-9525/$ - see front matter Q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.tig.2005.02.005 Review TRENDS in Genetics Vol.21 No.4 April 2005 241 nematodes, revealed functional and mechanistic features SL RNA intron-like moiety). SL RNAs are associated with of SL trans-splicing, as briefly summarized in the Sm proteins [21,22] and specific non-Sm proteins that following paragraphs. interact in vivo with other splicing components [23] in snRNPs. Whether the U snRNP-like nature of the SL SL RNAs snRNA and its unique base-pairing interaction with the Each SL trans-splicing organism has one, or a few, SL catalytically central U6 snRNA of nematodes [4] are simply RNA species. SL RNAs are transcribed by RNA polymer- a means for invading the spliceosome to gain effective access ase II (Pol II) from intronless genes that reside on short to pre-mRNA splice-acceptor sites, or whether the SL (from less than one kilobase to several kilobases) tandemly snRNP also makes a non-substrate contribution to the repeated DNA sequences that, in some organisms, also spliceosomal catalytic mechanism, is unknown. SL RNAs include 5S rRNA genes [4,18,19]. The presence or absence from different metazoan phyla have diverse nucleotide of the 5S RNA gene in the SL repeat is evolutionarily sequences. Apart from the presence of the unpaired splice- highly plastic and is not an informative long-range donor site, which is often involved in a predicted intra- phylogenetic signal [18].SLRNAsareshortRNAs molecular duplex secondary structure [7], they do not share (w45–140 nt) that contain a splice-donor site but no features beyond those also shared with the U snRNAs. acceptor site, and a hypermodified 50-cap structure containing 2,2,7-trimethylG (TMG) (in metazoa) [4] or Functions of SL trans-splicing monomethyl m7G in a hypermethylated ‘cap4’ structure SL trans-splicing has several distinct roles in mRNA (in kinetoplastids) [20]. The splice-donor site functionally function, including: (i) providing a 50-cap structure for divides the molecule into two segments (Figure 1). During protein-coding RNAs transcribed by the rRNA polymer- splicing, the 50-segment (i.e. the leader sequence) behaves ase, Pol I (uniquely in kinetoplastids [24,25]; Figure 1a); like the first exon in a conventionally-expressed gene, and (ii) resolving polycistronic Pol II transcripts into indivi- the 30-segment behaves like the 50-part of a conventional dual capped, monocistronic mRNAs by SL trans-splicing intron. to unpaired acceptor sites that are located upstream of Although they have no significant sequence identity, SL each open reading frame (ORF) (in kinetoplastids [19], RNAs have a striking overall similarity to Sm-class U-rich nematodes [26] and flatworms [27]; Figure 1b); and small nuclear RNAs (snRNAs) (i.e. U1, U2, U4 and U5), (iii) enhancing mRNA translational efficiency through which are present in spliceosomal small ribonucleopro- the hypermodified cap structure and/or leader sequence teins (snRNPs) and participate in the splicing mechanism (in kinetoplastids [28] and nematodes [29,30]; Figure 1d). (reviewed in Refs [1,4]). Shared features include a small An additional but less well-understood role for SL size, TMG cap and a U-rich Sm-protein-binding site (in the trans-splicing is that of trimming and sanitizing the (i) Capping pol I transcript ppp AG AUG SL RNA Protein-coding ORF Splice donor site m*Gppp AUG (ii) Resolving polycistronic m*Gppp GU Sm site pre-mRNA UAA AG AUG Leader Intron-like moiety Upstream ORF Protein-coding ORF m*Gppp AUG (iii) Sanitizing 5'-UTR m7Gppp AUG AG AUG Protein-coding ORF m*Gppp AUG (iv)SL-enhanced translation m7Gppp AG AUG Protein-coding ORF m*Gppp AUG m*Gppp AUG TRENDS in Genetics Figure 1. An overview of the biological functions of SL trans-splicing. On the left, the SL RNA is shown with its hypermodified cap structure and leader segment (red), and splice-donor site (indicated by GU) and intron-like moiety with a binding site for Sm proteins (black). The SL RNA cap depiction, m*Gppp, represents either the TMG-containing cap of metazoan SL RNA or the m7G-containing, but otherwise hypermodified, cap4 structure found in kinetoplastid SL RNA. Red arrows indicate trans- splicing events that transfer the SL RNA leader segment to unpaired splice-acceptor sites (indicated by AG) in several types of target pre-mRNA (on which the AUG translation start codons are shown).
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