The DExH Box Protein Suv3p Is a Component of a Yeast Mitochondrial 3′-to-5′ Exoribonuclease That Suppresses Group I Intron Toxicity

Margossian, Steven; Li, Huilin; Zassenhaus, Hans Peter; Butow, Ronald A.

doi:10.1016/s0092-8674(00)80975-7

Cited by 117 publications

(91 citation statements)

References 40 publications

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“…Likewise, improperly processed rRNA species could compete for ribosomal proteins resulting in defects in mitochondrial ribosome assembly. In addition, it has been shown that the degradosome is required to "clear" the mitochondrion of excised group I introns that have been shown to catalyze an "exon-reopening" reaction on their processed, parent RNAs, thus rendering them non-functional (9,19). Here, we provide evidence for an additional function of the Fig.…”

Section: Discussionmentioning

confidence: 56%

“…Thus, upon completion of splicing, Mrs1p may remain bound to the excised RNA for a significantly long time, limiting its availability. In addition, the cofactor bound intron presumably retains activity and can catalyze an "exon-reopening" reaction on their processed, parent RNAs (9). Thus, the Suv3p-containing degradosome plays two essential, anti-toxicity roles in aI5␤ and bI3 intron biology: it replenishes splicing cofactor pools and removes the potentially dangerous catalytically active intron RNAs.…”

Section: Discussionmentioning

confidence: 99%

“…In this regard, a strain containing a mis-sense mutation in SUV3 (suv3-1) showed defects in 3Ј processing of mitochondrial mRNAs and increased stability of excised group I introns (9,18,19). In addition, inefficient splicing of aI5␤ and bI3, which are group I introns of COX1 and COB, respectively, was also observed.…”

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confidence: 99%

“…exon reopening reactions), which decreases expression (9). Degradation of excised group I introns is carried out by a two-protein complex called the mitochondrial degradosome or mtEXO (10,11).…”

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confidence: 99%

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Splicing of Yeast aI5β Group I Intron Requires SUV3 to Recycle MRS1 via Mitochondrial Degradosome-promoted Decay of Excised Intron Ribonucleoprotein (RNP)

Turk

Caprara

2010

Journal of Biological Chemistry

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Yeast Suv3p is a member of the DEXH/D box family of RNA helicases and is a critical component of the mitochondrial degradosome, which also includes a 3 3 5 exonuclease, Dss1p. Defects in the degradosome result in accumulation of aberrant transcripts, unprocessed transcripts, and excised group I introns. In addition, defects in SUV3 result in decreased splicing of the aI5␤ and bI3 group I introns. Whereas a role for Suv3p in RNA degradation is well established, the function of Suv3p in splicing of group I introns has remained elusive. It has been particularly challenging to determine if Suv3p effects group I intron splicing through RNA degradation as part of the degradosome, or has a direct role in splicing as a chaperone, because nearly all perturbations of SUV3 or DSS1 result in loss of the mitochondrial genome. Here we utilized the suv3-1 allele, which is defective in RNA metabolism and yet maintains a stable mitochondrial genome, to investigate the role of Suv3p in splicing of the aI5␤ group I intron. We provide genetic evidence that Mrs1p is a limiting cofactor for aI5␤ splicing, and this evidence also suggests that Suv3p activity is required to recycle the excised aI5␤ ribonucleoprotein. We also show that Suv3p acts indirectly as a component of the degradosome to promote aI5␤ splicing. We present a model whereby defects in Suv3p result in accumulation of stable, excised group I intron ribonucleoproteins, which result in sequestration of Mrs1p, and a concomitant reduction in splicing of aI5␤.Mitochondrial gene expression is largely controlled by posttranscriptional mechanisms because of the relatively simple nature of mitochondrial transcription (1-5). One critical control point is RNA degradation, which is involved in the extensive processing required of mitochondrial transcripts (6, 7). In Saccharomyces cerevisiae, intergenic regions are removed from polycistronic transcripts and in the case of two mRNAs, encoding the cytochrome oxidase I subunit (COX1) 2 and apocytochrome b subunit (COB), group I and group II catalytic introns are also removed. Splicing of these introns requires trans-acting factors to facilitate the RNA-catalyzed intron excision and ligation of flanking exons (8).Rapid turnover of excised group I introns is essential for mitochondrial gene expression because these RNAs act as endonucleases that cleave their parent, processed RNAs at the site of exon ligation (e.g. exon reopening reactions), which decreases expression (9). Degradation of excised group I introns is carried out by a two-protein complex called the mitochondrial degradosome or mtEXO (10, 11). The mitochondrial degradosome includes Dss1p, a 3Ј 3 5Ј single-stranded exonuclease, and Suv3p, a DEXH/D protein, one of the largest family of proteins that are involved in RNA metabolism (11-13). Indeed, some members show ATP-dependent unwinding of RNA helices. Suv3p is a member of the SKI2 subfamily, individuals of which are thought to couple ATP binding and hydrolysis cycles with translocation along an RNA single strand and disruption...

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Section: Discussionmentioning

confidence: 56%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Splicing of Yeast aI5β Group I Intron Requires SUV3 to Recycle MRS1 via Mitochondrial Degradosome-promoted Decay of Excised Intron Ribonucleoprotein (RNP)

Turk

Caprara

2010

Journal of Biological Chemistry

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“…The Saccharomyces cerevisiae nuclear genome encodes three DExH͞D-box proteins (Suv3p, Mrh4p, and Mss116p) that function in mitochondria (9)(10)(11). Of these, Mss116p is the most closely related to CYT-19.…”

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confidence: 99%

The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function

Huang

Rowe

Mohr

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

155

223

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Group I and II introns self-splice in vitro, but require proteins for efficient splicing in vivo, to stabilize the catalytically active RNA structure. Recent studies showed that the splicing of some Neurospora crassa mitochondrial group I introns additionally requires a DEAD-box protein, CYT-19, which acts as an RNA chaperone to resolve nonnative structures formed during RNA folding. Here we show that, in Saccharomyces cerevisiae mitochondria, a related DEAD-box protein, Mss116p, is required for the efficient splicing of all group I and II introns, some RNA end-processing reactions, and translation of a subset of mRNAs, and that all these defects can be partially or completely suppressed by the expression of CYT-19. Results for the aI2 group II intron indicate that Mss116p is needed after binding the intron-encoded maturase, likely for the disruption of stable but inactive RNA structures. Our results suggest that both group I and II introns are prone to kinetic traps in RNA folding in vivo and that the splicing of both types of introns may require DEAD-box proteins that function as RNA chaperones.bakers' yeast ͉ mitochondria ͉ splicing factor D ExH͞D-box proteins are a large, ubiquitous protein family, whose members use the energy of ATP hydrolysis to mediate RNA structural rearrangements in a variety of cellular processes (1, 2). These proteins have a core region containing nine conserved motifs flanked by unique N-and͞or C-terminal extensions, which in some cases target the proteins to their sites of action by specific RNA or protein interactions. The proteins are named for the amino acid sequence of motif II, which in different subfamilies is DEAD, DEAH, or some variant thereof. Experiments with model substrates show that DExH͞D-box proteins can act as RNA helicases (3) or can disrupt ribonucleoprotein (RNP) complexes independently of their helicase activity (4). However, how these proteins function on their natural substrates has remained largely unknown.Group I and II introns self-splice in vitro but require proteins for efficient splicing in vivo to help fold the intron RNA into the catalytically active structure (5). In the fungus Neurospora crassa, the splicing of a subset of mitochondrial (mt) group I introns depends on two proteins encoded by nuclear genes, the mt tyrosyl-tRNA synthetase (CYT-18 protein), which stabilizes the catalytically active RNA structure, and the DEAD-box protein 7). Recently, CYT-19 was shown to function as an ATP-dependent RNA chaperone to destabilize nonnative structures that constitute kinetic traps in the CYT-18-assisted RNA folding pathway (7). A mutation in the cyt-19 gene did not affect the splicing of non-CYT-18-dependent group I introns or a group II intron, but did inhibit some 5Ј and 3Ј end processing reactions and, possibly, mt translation (7,8).The Saccharomyces cerevisiae nuclear genome encodes three DExH͞D-box proteins (Suv3p, Mrh4p, and Mss116p) that function in mitochondria (9-11). Of these, Mss116p is the most closely related to CYT-19. The two proteins have 32...

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Degradation of mRNA in bacteria: emergence of ubiquitous features

2000

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The DExH Box Protein Suv3p Is a Component of a Yeast Mitochondrial 3′-to-5′ Exoribonuclease That Suppresses Group I Intron Toxicity

Cited by 117 publications

References 40 publications

Splicing of Yeast aI5β Group I Intron Requires SUV3 to Recycle MRS1 via Mitochondrial Degradosome-promoted Decay of Excised Intron Ribonucleoprotein (RNP)

Splicing of Yeast aI5β Group I Intron Requires SUV3 to Recycle MRS1 via Mitochondrial Degradosome-promoted Decay of Excised Intron Ribonucleoprotein (RNP)

The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function

Degradation of mRNA in bacteria: emergence of ubiquitous features

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