RNA structure and the regulation of gene expression

Klaff, Petra; Riesner, Detlev; Steger, Gerhard

doi:10.1007/bf00039379

Cited by 53 publications

(30 citation statements)

References 146 publications

(136 reference statements)

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“…Formation of this hairpin structure could affect transcription efficiency or the stability of the transcript, although this topic, while analyzed in the past in bacterial and viral systems (Simoes and Sarnow, 1991;Emory et al, 1992;Hellendoorn et al, 1997), has not received much attention in plants (Klaff et al, 1996). Pyrimidine-rich elements in the 5# UTR of plants are known to have positive effects on transcription (Bolle et al, 1994), and they appear to be functionally conserved in diverse gene families across the plant kingdom.…”

Section: Differences Between the Thellungiella Species And Arabidopsismentioning

confidence: 99%

Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis

Dassanayake

et al. 2010

Plant Physiology

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The genome of Thellungiella parvula, a halophytic relative of Arabidopsis (Arabidopsis thaliana), is being assembled using Roche-454 sequencing. Analyses of a 10-Mb scaffold revealed synteny with Arabidopsis, with recombination and inversion and an uneven distribution of repeat sequences. T. parvula genome structure and DNA sequences were compared with orthologous regions from Arabidopsis and publicly available bacterial artificial chromosome sequences from Thellungiella salsuginea (previously Thellungiella halophila). The three-way comparison of sequences, from one abiotic stress-sensitive species and two tolerant species, revealed extensive sequence conservation and microcolinearity, but grouping Thellungiella species separately from Arabidopsis. However, the T. parvula segments are distinguished from their T. salsuginea counterparts by a pronounced paucity of repeat sequences, resulting in a 30% shorter DNA segment with essentially the same gene content in T. parvula. Among the genes is SALT OVERLY SENSITIVE1 (SOS1), a sodium/proton antiporter, which represents an essential component of plant salinity stress tolerance. Although the SOS1 coding region is highly conserved among all three species, the promoter regions show conservation only between the two Thellungiella species. Comparative transcript analyses revealed higher levels of basal as well as salt-induced SOS1 expression in both Thellungiella species as compared with Arabidopsis. The Thellungiella species and other halophytes share conserved pyrimidine-rich 5# untranslated region proximal regions of SOS1 that are missing in Arabidopsis. Completion of the genome structure of T. parvula is expected to highlight distinctive genetic elements underlying the extremophile lifestyle of this species.

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Section: Differences Between the Thellungiella Species And Arabidopsismentioning

confidence: 99%

Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis

Dassanayake

et al. 2010

Plant Physiology

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“…Two properties of RNA molecules cannot be denied: their natural tendency to form highly stable secondary and tertiary structures in vitro and in vivo (9,27,39) and the observation that alterations in these structures represent a well-known regulatory mechanism for many RNA cellular processes (60).…”

Section: Do Pre-mrnas Present Secondary Structure In Vivo?mentioning

confidence: 99%

“…Clearly, considering the enormously diverse sequences of all processed pre-mRNAs, it would be quite over the line to propose the presence of highly stable secondary structures (Fig. 1b) that resemble those of the highly conserved tRNAs, rRNAs, IRES, or other stability-, replication-, and localization-controlling elements present in several 3ЈUTRs of prokaryotic and eukaryotic mRNAs, in which proteins may also play a key role in stabilizing the structure (60). However, in between these two extremes there may exist a third possibility, represented by the existence of a loose amount of RNA-specific secondary structures which might, under normal conditions, influence the splicing machinery (Fig.…”

Section: Do Pre-mrnas Present Secondary Structure In Vivo?mentioning

confidence: 99%

Influence of RNA Secondary Structure on the Pre-mRNA Splicing Process

Buratti

Baralle

2004

Molecular and Cellular Biology

376

302

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Pre-mRNA splicing in eukaryotes requires joining together the nucleotides of the various mRNA-coding regions (exons) after recognizing them from the normally vastly superior number of non-mRNA-coding sequences (introns). For three excellent reviews on general splicing and its regulation, refer to references 14, 62, and 70. In eukaryotes, the vast majority of splicing processes are catalyzed by the spliceosome, a very complex RNA-protein aggregate which has been estimated to contain several hundred different proteins in addition to five spliceosomal snRNAs (1,54,62,63,81,109). These factors are responsible for the accurate positioning of the spliceosome on the 5Ј and 3Ј splice site sequences. The reason why so many factors are needed reflects the observation that exon recognition can be affected by many pre-mRNA features such as exon length (5, 97), the presence of enhancer and silencer elements (8, 62), the strength of splicing signals (45), the promoter architecture (29,55), and the rate of RNA processivity (86). In addition, the general cellular environment also exerts an effect, as recent observations suggest the existence of extensive coupling between splicing and many other gene expression steps (69) and even its modification by external stimuli (96).In the midst of all this complexity, it has also been proposed that pre-mRNA secondary structures can potentially influence splicing activity. However, despite a steady increase of reports invoking their effects on splicing regulation, the last specific review on this subject is now more than 10 years old (3). Here, we propose to address again this specific issue in the current perspective of the general field. Before we do this, however, we have to answer a basic question. DO PRE-mRNAS PRESENT SECONDARY STRUCTURE IN VIVO?Two properties of RNA molecules cannot be denied: their natural tendency to form highly stable secondary and tertiary structures in vitro and in vivo (9, 27, 39) and the observation that alterations in these structures represent a well-known regulatory mechanism for many RNA cellular processes (60).In this particular respect, however, a question that still remains to be addressed conclusively regards the presence of secondary structures in pre-mRNAs in vivo. That this existence may not simply be taken for granted comes from early experimental evidence. In fact, it was suggested that in vitro evidence regarding the possible influence of RNA structure on splicing (94) could not be accurately reproduced in vivo (95). The reason why this should be so goes back to the classical concept that RNA is coated in vivo by proteins. In fact, heterogeneous ribonucleoprotein particles have been known since early studies and the major protein family involved, the hnRNP proteins, are very abundant in mammalian cells. These RNAprotein interactions may well prevent mRNAs from folding in stable secondary structures (34) (Fig. 1a). For this reason, it was hypothesized that, following transcription, pre-mRNA may be allowed only a very limited timespan to fold (36)....

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“…Comparative study of functional sequences through evolution has been a very useful tool with which to understand mechanisms and structures that otherwise elude interpretation (25,36). Recently, this approach has yielded important information regarding the evolution of the FGF-R2 gene through alternative splicing of the mutually exclusive IIIb and IIIc units (49).…”

mentioning

confidence: 99%

RNA Folding Affects the Recruitment of SR Proteins by Mouse and Human Polypurinic Enhancer Elements in the Fibronectin EDA Exon

Buratti

Muro

Giombi

et al. 2004

Molecular and Cellular Biology

110

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In humans, inclusion or exclusion of the fibronectin EDA exon is mainly regulated by a polypurinic enhancer element (exonic splicing enhancer [ESE]) and a nearby silencer element (exonic splicing silencer [ESS]).While human and mouse ESEs behave identically, mutations introduced into the homologous mouse ESS sequence result either in no change in splicing efficiency or in complete exclusion of the exon. Here, we show that this apparently contradictory behavior cannot be simply accounted for by a localized sequence variation between the two species. Rather, the nucleotide differences as a whole determine several changes in the respective RNA secondary structures. By comparing how the two different structures respond to homologous deletions in their putative ESS sequences, we show that changes in splicing behavior can be accounted for by a differential ESE display in the two RNAs. This is confirmed by RNA-protein interaction analysis of levels of SR protein binding to each exon. The immunoprecipitation patterns show the presence of complex multi-SR protein-RNA interactions that are lost with secondary-structure variations after the introduction of ESE and ESS variations. Taken together, our results demonstrate that the sequence context, in addition to the primary sequence identity, can heavily contribute to the making of functional units capable of influencing pre-mRNA splicing.The splicing process is a very flexible and critical step in gene expression. In fact, selected removal or inclusion of individual exons from nascent mRNA molecules allows a single gene to generate multiple proteins with different primary structures; in these cases, the process is known as alternative splicing (1, 38). Constitutive and alternative splicing processes are catalyzed by the spliceosome, a very complex RNA-protein aggregate that has been recently estimated to contain approximately 145 different proteins in addition to the five spliceosomal snRNAs (1,38,41,68). These factors are responsible for accurate positioning of the spliceosome on the 5Ј and 3Ј splice sequences that define the exon. However, correct positioning of the spliceosome is a very complex process owing to the degeneracy of the splice site consensus sequences, the presence of cryptic splice sites in large introns, and the fact that most pre-mRNAs contain multiple introns (26). Therefore, the action of several different proteins is required to achieve accurate positioning of the spliceosome on the splice site. Not surprisingly, alterations in the splicing process have been increasingly reported as being involved in many genetic diseases (5,8,13,23,58). Among the well-known factors that may heavily influence the identification of intron-exon boundaries by the spliceosome are the exon length (3, 65), the presence of splicing enhancer and silencer elements (5, 38), the strength of splicing signals (26), and the promoter architecture (19,33). In addition to these factors, it has been proposed that the natural tendency of RNAs to fold in highly stable secondary and tertia...

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RNA structure and the regulation of gene expression

Cited by 53 publications

References 146 publications

Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis

Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis

Influence of RNA Secondary Structure on the Pre-mRNA Splicing Process

RNA Folding Affects the Recruitment of SR Proteins by Mouse and Human Polypurinic Enhancer Elements in the Fibronectin EDA Exon

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