Expression of the essential mRNA export factor Yra1p is autoregulated by a splicing-dependent mechanism

Preker, Pascal J.; Kim, Karen S.; Guthrie, Christine

doi:10.1017/s1355838202020046

Cited by 48 publications

(70 citation statements)

References 40 publications

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“…Additionally, some of our predictions were previously reported as alternative 39ss (Davis et al 2000;Yassour et al 2009;Gahura et al 2011), which adds support to our proposed model, where premRNA secondary structure aids 39ss selection. Nonetheless, most of the splicing variation reported so far in yeast (Davis et al 2000;Preker et al 2002;Juneau et al 2007Juneau et al , 2009Pleiss et al 2007;Yassour et al 2009;Bergkessel et al 2011;Hossain et al 2011) corresponds to intron retention events and not to alternative 39ss selection and, hence, could not be recapitulated using our model. Using various yeast strains and conditions, we are able to experimentally validate a number of candidate alternative 39ss, further supporting our predictive model and confirming the existence of alternative 39ss selection in yeast.…”

Section: Discussionmentioning

confidence: 92%

“…S3). To the best of our knowledge, these two cases of alternative splicing have not been reported before in previous analyses of splicing variation in yeast (Davis et al 2000;Preker et al 2002;Juneau et al 2007Juneau et al , 2009Pleiss et al 2007;Yassour et al 2009;Bergkessel et al 2011;Hossain et al 2011). Some of the negative cases were shown before to have splicing variation different from alternative 39ss selection: HMF1 and REC102 Each predicted AG is given as the intron coordinates (chromosome, start, end, strand), the gene name, and the distance to the BS (calculated as explained in Materials and Methods).…”

Section: Validation Of Predicted Alternative 39ssmentioning

confidence: 85%

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RNA secondary structure mediates alternative 3′ss selection in Saccharomyces cerevisiae

Plass¹,

Codony-Servat²,

Ferreira³

et al. 2012

RNA

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Alternative splicing is the mechanism by which different combinations of exons in the pre-mRNA give rise to distinct mature mRNAs. This process is mediated by splicing factors that bind the pre-mRNA and affect the recognition of its splicing signals. Saccharomyces species lack many of the regulatory factors present in metazoans. Accordingly, it is generally assumed that the amount of alternative splicing is limited. However, there is recent compelling evidence that yeast have functional alternative splicing, mainly in response to environmental conditions. We have previously shown that sequence and structure properties of the pre-mRNA could explain the selection of 39 splice sites (ss) in Saccharomyces cerevisiae. In this work, we extend our previous observations to build a computational classifier that explains most of the annotated 39ss in the CDS and 59 UTR of this organism. Moreover, we show that the same rules can explain the selection of alternative 39ss. Experimental validation of a number of predicted alternative 39ss shows that their usage is low compared to annotated 39ss. The majority of these alternative 39ss introduce premature termination codons (PTCs), suggesting a role in expression regulation. Furthermore, a genome-wide analysis of the effect of temperature, followed by experimental validation, yields only a small number of changes, indicating that this type of regulation is not widespread. Our results are consistent with the presence of alternative 39ss selection in yeast mediated by the pre-mRNA structure, which can be responsive to external cues, like temperature, and is possibly related to the control of gene expression.

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Section: Discussionmentioning

confidence: 92%

Section: Validation Of Predicted Alternative 39ssmentioning

confidence: 85%

RNA secondary structure mediates alternative 3′ss selection in Saccharomyces cerevisiae

Plass¹,

Codony-Servat²,

Ferreira³

et al. 2012

RNA

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“…Indeed, introns have been shown to increase the fitness of yeast in two ways: (1) regulated splicing posttranscriptionally regulates gene expression (Engebrecht et al 1991;Li et al 1996;Nakagawa and Ogawa 1999;Preker et al 2002;Juneau et al 2007;Parenteau et al 2008) and (2) introns can function to enhance the transcriptional and translational output of the genes they occupy ( Juneau et al 2006). Here we provide compelling evidence that introns also improve the fitness of yeast by increasing protein diversity through alternative splicing.…”

Section: Discussionmentioning

confidence: 99%

“…Consequently, all 13 meiosis-specific introncontaining genes are regulated post-transcriptionally with splicing repressed during vegetative growth and induced during sporulation (Engebrecht et al 1991;Nakagawa and Ogawa 1999;Juneau et al 2007). Other examples of regulated splicing include YRA1 and MTR2 (RNA export) (Preker et al 2002;Parenteau et al 2008) and RPL30 (ribosomal) (Li et al 1996).…”

Section: Introductionmentioning

confidence: 99%

Alternative Splicing of PTC7 inSaccharomyces cerevisiaeDetermines Protein Localization

2009

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It is well established that higher eukaryotes use alternative splicing to increase proteome complexity. In contrast, Saccharomyces cerevisiae, a single-cell eukaryote, conducts predominantly regulated splicing through retention of nonfunctional introns. In this article we describe our discovery of a functional intron in the PTC7 (YHR076W) gene that can be alternatively spliced to create two mRNAs that code for distinct proteins. These two proteins localize to different cellular compartments and have distinct cellular roles. The protein translated from the spliced mRNA localizes to the mitochondria and its expression is carbon-source dependent. In comparison, the protein translated from the unspliced mRNA contains a transmembrane domain, localizes to the nuclear envelope, and mediates the toxic effects of Latrunculin A exposure. In conclusion, we identified a definitive example of functional alternative splicing in S. cerevisiae that confers a measurable fitness benefit. I N higher eukaryotes alternative splicing is pervasive; in humans the majority of genes are alternatively spliced to form multiple proteins (Modrek et al. 2001;Johnson et al. 2003). In contrast, only 5% of the genes in Saccharomyces cerevisiae contain introns and .95% of those intron-containing genes possess only a single intron (Nash et al. 2007). The simple architecture of the yeast genome constrains its ability to utilize alternative splicing and has encouraged the view that alternative splicing is absent in S. cerevisiae. Currently no conclusive examples of functional alternative splicing exist; most confirmed instances of alternative splicing in yeast downregulate gene expression, a process that is often referred to as ''regulated splicing.'' In this process, nonfunctional introns are not spliced out of the transcript and premature stop codons are included in the fully processed mRNA. The stop codons activate the nonsense-mediated decay (NMD) pathway and the mRNA is degraded before it can be translated (Gonzalez et al. 2001).The transition from vegetative growth to meiosis illustrates how regulated splicing improves yeast fitness. DNA breakage and recombination could be toxic during vegetative growth, and therefore entrance into meiosis is tightly controlled. Consequently, all 13 meiosis-specific introncontaining genes are regulated post-transcriptionally with splicing repressed during vegetative growth and induced during sporulation (Engebrecht et al. 1991;Nakagawa and Ogawa 1999;Juneau et al. 2007). Other examples of regulated splicing include YRA1 and MTR2 (RNA export) (Preker et al. 2002;Parenteau et al. 2008) and RPL30 (ribosomal) (Li et al. 1996).In contrast to regulated splicing, there is only one example in S. cerevisiae where splicing results in the expression of multiple proteins, SRC1 (Grund et al. 2008). SRC1 contains a single intron located at the 39 end of the pre-mRNA. The intron has two alternative 59-splice sites (Rodriguez-Navarro et al. 2002). Splicing at the most highly conserved 59-splice site (Bon et al. 2003) ...

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“…Yra1p was originally isolated in a screen for yeast genes that cause overexpressionmediated growth arrest (Espinet et al 1995), and was also shown to possess RNA-RNA annealing activity (Portman et al 1997). The level of Yra1p is tightly regulated by a negative feedback mechanism that involves splicing of its unusual intron (Preker et al 2002). Depletion of Yra1p results in nuclear accumulation of poly(A) + RNA, supporting its direct role in mRNA export in yeast (Strasser and Hurt 2000;Stutz et al 2000).…”

Section: Introductionmentioning

confidence: 95%

The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans

Longman¹,

Johnstone²,

Cáceres³

2003

RNA

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Expression of the essential mRNA export factor Yra1p is autoregulated by a splicing-dependent mechanism

Cited by 48 publications

References 40 publications

RNA secondary structure mediates alternative 3′ss selection in Saccharomyces cerevisiae

RNA secondary structure mediates alternative 3′ss selection in Saccharomyces cerevisiae

Alternative Splicing of PTC7 inSaccharomyces cerevisiaeDetermines Protein Localization

The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans

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