The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast

Olivas, Wendy M.

doi:10.1093/emboj/19.23.6602

Cited by 262 publications

(335 citation statements)

References 50 publications

(86 reference statements)

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“…In either case, TOR signaling is likely to regulate poly(A) tail length directly, given that the ARO4 mRNA begins to be destabilized after only 10 min of rapamycin treatment. If TOR regulates deadenylation, then the major cytoplasmic deadenylation factors, Caf1p and Ccr4p , and the PUF proteins that have been found to control deadenylation in a mRNAspecific manner (Olivas and Parker, 2000) are potential targets of regulation. If TOR controls the length of the nascent poly(A) tail, any of the multitude of factors involved in polyadenylation could be regulated, however, two particularly good candidates are the PAN2/PAN3 nuclease, which is believed to trim new poly(A) tails in the nucleus to a mRNA-specific length (Brown and Sachs, 1998), and PBP1p, which is required for the addition of long poly(A) tails in vitro and is down-regulated at late log phase (Mangus et al, 1998).…”

Section: How Are Decapping and Poly(a) Tail Length Controlled By The mentioning

confidence: 99%

The Target of Rapamycin Signaling Pathway Regulates mRNA Turnover in the YeastSaccharomyces cerevisiae

Albig

Decker

2001

MBoC

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The target of rapamycin (TOR) signaling pathway is an important mechanism by which cell growth is regulated by nutrient availability in eukaryotes. We provide evidence that the TOR signaling pathway controls mRNA turnover in Saccharomyces cerevisiae. During nutrient limitation (diauxic shift) or after treatment with rapamycin (a specific inhibitor of TOR), multiple mRNAs were destabilized, whereas the decay of other mRNAs was unaffected. Our findings suggest that the regulation of mRNA decay by the TOR pathway may play a significant role in controlling gene expression in response to nutrient depletion. The inhibition of the TOR pathway accelerated the major mRNA decay mechanism in yeast, the deadenylation-dependent decapping pathway. Of the destabilized mRNAs, two different responses to rapamycin were observed. Some mRNAs were destabilized rapidly, while others were affected only after prolonged exposure. Our data suggest that the mRNAs that respond rapidly are destabilized because they have short poly(A) tails prematurely either as a result of rapid deadenylation or reduced polyadenylation. In contrast, the mRNAs that respond slowly are destabilized by rapid decapping. In summary, the control of mRNA turnover by the TOR pathway is complex in that it specifically regulates the decay of some mRNAs and not others and that it appears to control decay by multiple mechanisms. INTRODUCTIONIt is estimated that most of the microorganisms in the environment exist in conditions in which nutrients are limiting (Lewis and Gattie, 1991). Nutrient availability is very important in controlling cell division, growth, and physiology in microorganisms as well as in multicellular organisms. One critical response in yeast to glucose limitation is the switch from fermentation to respiration, which is termed the diauxic shift. At the diauxic shift, major changes in gene expression are induced (reviewed in Werner-Washburne et al., 1996) including a general repression of translation (Fuge et al., 1994) and extensive changes in the abundance of mRNAs (DeRisi et al., 1997). The target of rapamycin (TOR) signaling pathway senses external nutrient availability and is involved in mediating the changes in gene expression induced at the diauxic shift (reviewed in Cutler et al., 1999;Dennis et al., 1999;Thomas and Hall 1999;Cardenas et al., 1999). Rapamycin artificially induces a starvation-like state in yeast (Barbet et al., 1996) by first forming a complex with the yeast FK506 binding protein, FKBP. This complex then binds to and represses the activity of the TOR1 and TOR2proteins (Heitman et al., 1991). The TOR signaling transduction pathway is conserved among yeast, flies, and mammals. In mammalian cells, the TOR protein homolog mTOR/ FRAP/RAFT1 also coordinates nutrient and mitogenic signals to control cell growth and cell-cycle progression (reviewed in Cutler et al., 1999;Thomas and Hall, 1999). The Drosophila TOR homolog dTOR also senses nutrient availability (Oldham et al., 2000;Zhang et al., 2000). The TOR proteins are protein kinases...

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Section: How Are Decapping and Poly(a) Tail Length Controlled By The mentioning

confidence: 99%

The Target of Rapamycin Signaling Pathway Regulates mRNA Turnover in the YeastSaccharomyces cerevisiae

Albig

Decker

2001

MBoC

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“…Such small differences would not have been detected in our microarray analysis, which had a cut-off of two-fold. The effects are also the opposite to those expected, since Puf-domain proteins have hitherto universally been described as enhancing mRNA degradation or inhibiting translation [2][3][4]6].…”

Section: Discussionmentioning

confidence: 99%

“…So far, therefore, there is no convincing evidence that PUF1 is essential for growth of trypanosomes under normal culture conditions. Notably, S. cerevisiae lacking all five PUF proteins are viable [6] although they show changes in the abundance of at least 168 different transcripts (out of 2500 detected) [6]. In contrast, alterations in a single S. cerevisiae PUF protein may result in subtle changes which are seen only under particular conditions.…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, alterations in a single S. cerevisiae PUF protein may result in subtle changes which are seen only under particular conditions. Thus, Puf3p binds the COX17 3 -UTR and promotes rapid deadenylation and decay of the transcript [6], but the effects are only seen under certain nutritional conditions [35]. Similarly, Puf4p appears to destabilise mRNAs only under conditions of transcriptional arrest [35].…”

Section: Discussionmentioning

confidence: 99%

“…In Drosophila, Pumilio protein is known to bind the 3 -untranslated region (3 -UTR) of hunchback mRNA, leading to an increase in the rate of deadenylation and repression of translation of this mRNA [2,3], while in C. elegans, FBF protein binds the 3 -UTR of fem-3 mRNA and leads to repression of translation [4]. PUF proteins in yeast and slime moulds also repress expression of target mRNAs by binding to sequences in the 3 -UTR [5][6][7]. PUF proteins are characterized by the presence of eight consecutive repeats (Puf repeats), each consisting of approximately 40 amino acids.…”

Section: Introductionmentioning

confidence: 99%

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Functional analysis of Trypanosoma brucei PUF1

Luu

Brems

Hoheisel

et al. 2006

Molecular and Biochemical Parasitology

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The genomes of Trypanosoma brucei, Leishmania major and Trypanosoma cruzi each encode 10 proteins with PUF domains. PUF domain proteins from yeast and metazoa have been shown to bind RNA and to regulate mRNA stability and translation. Phylogenetic analysis suggested that the PUF proteins were duplicated and diverged early in evolution, and that most PUF proteins were lost during the evolution of mammals. Depletion of any of the first nine T. brucei PUF protein mRNAs by RNA interference had no effect on cell growth; combined depletion of PUF1 and PUF3, PUF3 and PUF4, and PUF1 and PUF4 mRNAs also had no effect. In conflict with a previous report, procyclic trypanosomes lacking PUF1 genes grew normally and we could find no evidence that PUF1 is required for growth of trypanosomes in culture. Depletion or elimination of PUF1 mRNA did not affect the abundances of any other mRNAs, as detected in microarray analysis, and also had minimal effects on the proteome. (In control experiments, treatment of bloodstream and procyclic cells with 100 ng/ml tetracycline also had no detectable effects on the transcriptome and proteome.) PUF1 preferentially bound to retroposon RNAs and was not associated with polysomes. We suggest that, as in yeast, there may be functional redundancy among the Kinetoplastid PUF proteins, or they may be involved in fine-tuning gene expression together with other proteins. Alternatively, PUF proteins may be needed in differentiating trypanosomes or in non-culturable life-cycle stages.

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Yeast Puf3p‐mediated mRNA decay is regulated by carbon source‐specific differential interaction of Puf3p with Pop2p and Yak1p

et al. 2023

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Puf3p regulates the stability of nuclear-encoded mRNAs acting in mitochondrial biogenesis and function in Saccharomyces cerevisiae. This work identifies the phosphorylation of Pop2p, a component of the deadenylase complex, as being critical for adapting Puf3p-mediated mRNA decay upon carbon source alterations. We demonstrate that the Puf3p-Pop2p association diminishes in mitochondria-reliant conditions and establish Yak1p, a kinase that phosphorylates Pop2p at threonine 97, as a new player in Puf3p-mediated regulation of mRNA decay. Yak1p deletion alters the half-life of Puf3p target mRNAs. Our findings outline a metabolism-driven regulatory switch, whereby, in mitochondria-independent conditions, Puf3p recruits Pop2p and the decay machinery to bound mRNAs for rapid decay. Conversely, in mitochondria-reliant conditions, the association of Puf3p with Yak1p increases, placing Yak1p proximal to neighboring Pop2p. Subsequent Pop2p phosphorylation reduces the Puf3p-Pop2p interaction and stabilizes Puf3p target mRNAs.

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The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast

Cited by 262 publications

References 50 publications

The Target of Rapamycin Signaling Pathway Regulates mRNA Turnover in the YeastSaccharomyces cerevisiae

The Target of Rapamycin Signaling Pathway Regulates mRNA Turnover in the YeastSaccharomyces cerevisiae

Functional analysis of Trypanosoma brucei PUF1

Yeast Puf3p‐mediated mRNA decay is regulated by carbon source‐specific differential interaction of Puf3p with Pop2p and Yak1p

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