Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome

Beilharz, Traude H.; Preiß, Thomas

doi:10.1261/rna.569407

Cited by 130 publications

(171 citation statements)

References 76 publications

(105 reference statements)

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“…This approach may elucidate some novel translational controls required for efficient translation of mRNAs encoding cell cycle regulators, which, as discussed above, in some cases require specialized translational initiation factors owing to their long and complex UTRs. Moreover, recent genome-wide profiling experiments of poly(A) tail lengths performed in transcriptionally active mitotically dividing cells have been a step forward in delineating the role of 3 0 UTRs in regulation of archetypal cell cycle progression [78,122,123]. This work suggests that polyadenylation status of mRNAs could be implicated in the regulation of archetypal cell cycle progression [78,122].…”

Section: Concluding Remarks and Future Perspectivesmentioning

confidence: 97%

Translational regulation of the cell cycle: when, where, how and why?

Kronja

Orr‐Weaver

2011

Phil. Trans. R. Soc. B

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Translational regulation contributes to the control of archetypal and specialized cell cycles, such as the meiotic and early embryonic cycles. Late meiosis and early embryogenesis unfold in the absence of transcription, so they particularly rely on translational repression and activation of stored maternal mRNAs. Here, we present examples of cell cycle regulators that are translationally controlled during different cell cycle and developmental transitions in model organisms ranging from yeast to mouse. Our focus also is on the RNA-binding proteins that affect cell cycle progression by recognizing special features in untranslated regions of mRNAs. Recent research highlights the significance of the cytoplasmic polyadenylation element-binding protein (CPEB). CPEB determines polyadenylation status, and consequently translational efficiency, of its target mRNAs in both transcriptionally active somatic cells as well as in transcriptionally silent mature Xenopus oocytes and early embryos. We discuss the role of CPEB in mediating the translational timing and in some cases spindle-localized translation of critical regulators of Xenopus oogenesis and early embryogenesis. We conclude by outlining potential directions and approaches that may provide further insights into the translational control of the cell cycle.

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Section: Concluding Remarks and Future Perspectivesmentioning

confidence: 97%

Translational regulation of the cell cycle: when, where, how and why?

Kronja

Orr‐Weaver

2011

Phil. Trans. R. Soc. B

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“…Microarray-based analyses of mRNA polyadenylation state uncovered widespread use of mRNA-specific poly(A) tail length control in the S. cerevisiae and Schizosaccharomyces pombe transcriptomes (Beilharz and Preiss 2007;Lackner et al 2007). Of note here, many mRNAs encoding cell cycle, cell polarity, and morphogenesis-related functions including septin assembly, were found to be present with mostly short oligo(A) tails in nonsynchronized, exponentially growing wild-type (wt) cell cultures.…”

mentioning

confidence: 90%

“…Of note here, many mRNAs encoding cell cycle, cell polarity, and morphogenesis-related functions including septin assembly, were found to be present with mostly short oligo(A) tails in nonsynchronized, exponentially growing wild-type (wt) cell cultures. These data suggested that rapid deadenylation by Ccr4-Pop2-NOT of such ''short-tailed'' mRNAs serves as a mechanism to restrict their translation to a tight time window during the cell cycle (Beilharz and Preiss 2007). Thus, even though the Ccr4-Pop2-NOT deadenylase shortens the poly(A) tails of virtually all mRNAs (Parker and Song 2004;Woolstencroft et al 2006;Beilharz and Preiss 2007;Goldstrohm and Wickens 2008), its effects on the group of ''short-tailed'' mRNAs are particularly critical for cell function, and their deregulation in deadenylase mutant cells is therefore likely to contribute to observable phenotypes.…”

mentioning

confidence: 97%

“…Our transcriptome-wide analysis had indicated that mRNAs that preferentially possess short poly(A) tails are enriched in gene ontology (GO) terms such as bud neck, cell cortex, establishment and maintenance of cell polarity, and cellular morphogenesis, and deadenylase mutant strains showed morphology defects (e.g., wide necks and elongated cells) that could result from problems in septin organization (Beilharz and Preiss 2007). We therefore decided to examine the role of the Ccr4-Pop2-NOT mRNA deadenylase in septin organization.…”

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confidence: 99%

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The Ccr4-Pop2-NOT mRNA Deadenylase Contributes to Septin Organization in Saccharomyces cerevisiae

Traven

Beilharz

et al. 2009

Genetics

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In yeast, assembly of the septins at the cell cortex is required for a series of key cell cycle events: bud-site selection, the morphogenesis and mitotic exit checkpoints, and cytokinesis. Here we establish that the Ccr4-Pop2-NOT mRNA deadenylase contributes to septin organization. mRNAs encoding regulators of septin assembly (Ccd42, Cdc24, Rga1, Rga2, Bem3, Gin4, Cla4, and Elm1) presented with short poly(A) tails at steady state in wild-type (wt) cells, suggesting their translation could be restricted by deadenylation. Deadenylation of septin regulators was dependent on the major cellular mRNA deadenylase Ccr4-Pop2-NOT, whereas the alternative deadenylase Pan2 played a minor role. Consistent with deadenylation of septin regulators being important for function, deletion of deadenylase subunits CCR4 or POP2, but not PAN2, resulted in septin morphology defects (e.g., ectopic bud-localized septin rings), particularly upon activation of the Cdc28-inhibitory kinase Swe1. Aberrant septin staining was also observed in the deadenylase-dead ccr4-1 mutant, demonstrating the deadenylase activity of Ccr4-Pop2 is required. Moreover, ccr4D, pop2D, and ccr4-1 mutants showed aberrant cell morphology previously observed in septin assembly mutants and exhibited genetic interactions with mutations that compromise septin assembly (shs1D, cla4D, elm1D, and gin4D). Mutations in the Not subunits of Ccr4-Pop2-NOT, which are thought to predominantly function in transcriptional control, also resulted in septin organization defects. Therefore, both mRNA deadenylase and transcriptional functions of Ccr4-Pop2-NOT contribute to septin organization in yeast.

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“…56 However, the fate of hyperadenylated transcripts is unclear. These hyperadenylated transcripts may simply be more abundant 57 and therefore translated more often, leading to elevated levels of their encoded proteins. Alternatively, hyperadenylated transcripts could be removed from cells via the RNA degradation machinery.…”

Section: Mutations In the Conserved Znf Pab Zc3h14 Are Linked To Nsmentioning

confidence: 99%

New kid on the ID block

Kelly¹,

Pak²,

Garshasbi³

et al. 2012

RNA Biology

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Polyadenosine RNA binding proteins (Pabs) play critical roles in regulating the polyadenylation, nuclear export, stability and translation of cellular RNAs. Although most Pabs are ubiquitously expressed and are thought to play general roles in post-transcriptional regulation, mutations in genes encoding these factors have been linked to tissue-specific diseases including muscular dystrophy and now intellectual disability (ID). Our recent work defined this connection to ID, as we showed that mutations in the gene encoding the ubiquitously expressed Cys 3 His tandem zinc-finger (ZnF) Pab, ZC3H14 (Zinc finger protein, CCCH-type, number 14) are associated with non-syndromic autosomal recessive intellectual disability (NS-ARID). This study provided a first link between defects in Pab function and a brain disorder, suggesting that ZC3H14 plays a required role in regulating RNAs in nervous system cells. Here we highlight key questions raised by our study of ZC3H14 and its ortholog in the fruit fly Drosophila melanogaster, dNab2 and comment on future approaches that could provide insights into the cellular and molecular roles of this class of zinc fingercontaining Pabs. We propose a summary model depicting how ZC3H14-type Pabs might play particularly important roles in neuronal RNA metabolism.

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Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome

Cited by 130 publications

References 76 publications

Translational regulation of the cell cycle: when, where, how and why?

Translational regulation of the cell cycle: when, where, how and why?

The Ccr4-Pop2-NOT mRNA Deadenylase Contributes to Septin Organization in Saccharomyces cerevisiae

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