Translation Termination Is Involved in Histone mRNA Degradation when DNA Replication Is Inhibited

Kaygun, Handan; Marzluff, William F.

doi:10.1128/mcb.25.16.6879-6888.2005

Cited by 65 publications

(61 citation statements)

References 49 publications

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“…In addition to SLBP, this rapid turnover requires active translation and the nonsense-mediated decay factor Upf1 (Kaygun and Marzluff 2005a). The function of SLBP in regulated mRNA decay requires that it be positioned within a narrow window with respect to both the stop codon and the 3Ј end of the transcript (Kaygun and Marzluff 2005b). The primary candidate for the nuclease responsible for regulated histone mRNA decay is a 3Ј-to-5Ј exonuclease, termed 3Ј hExo .…”

Section: A Need For Precision and Uniformitymentioning

confidence: 99%

“…Most importantly, SLBP serves as the key modulator of the rapid, coordinate degradation of histone mRNA in response to both the end of S phase and the inhibition of DNA synthesis. In addition to SLBP, this rapid turnover requires active translation and the nonsense-mediated decay factor Upf1 (Kaygun and Marzluff 2005a). The function of SLBP in regulated mRNA decay requires that it be positioned within a narrow window with respect to both the stop codon and the 3Ј end of the transcript (Kaygun and Marzluff 2005b).…”

Section: A Need For Precision and Uniformitymentioning

confidence: 99%

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Eukaryotic mRNA 3′ processing: a common means to different ends: Figure 1.

Gilmartin¹

2005

Genes Dev.

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In principle, the formation of the 3Ј end of a eukaryotic mRNA is a simple process. At a minimum, it involves the hydrolysis of a single phosphodiester bond in the nascent transcript. For one unique class of mRNAs, transcripts of the metazoan replication-dependent histone genes, this is indeed the only requirement. All other eukaryotic mRNAs require both cleavage and subsequent poly(A) addition to the newly generated 3Ј hydroxyl. Despite this apparent simplicity, and more than two decades of work, basic questions concerning the mechanisms of 3Ј-end formation for both classes of transcripts persist. The accumulated evidence indicates that the mechanisms by which the ends of histone and polyadenylated mRNA are formed are fundamentally distinct, both in the factors responsible for processing and the RNA sequence elements that direct their action (for review, see Marzluff 2005;Zhao et al. 1999a). The 3Ј processing of polyadenylated mRNAs requires a complex of over a dozen proteins, nearly all of which are conserved from yeast to humans. In contrast, the formation of the 3Ј ends of the metazoan replication-dependent histone transcripts not only requires a unique set of proteins, but an essential snRNA component as well. In both cases, the identity of the endonuclease has remained largely a matter of speculation.Two reports-one from Kolev and Steitz (2005) in this issue of Genes & Development, and the second from Dominski et al. (2005a) have revealed that the mechanisms of poly(A) site processing and histone 3Ј processing are not quite as unique as they appear. Surprisingly, the two processing machines share a common core of proteins that almost certainly includes the endonuclease. The most exciting aspect of these reports, however, is that they provide a fresh insight into the evolution of what had seemed to be needlessly redundant mechanisms for generating mRNA 3Ј ends. In essence, these reports indicate that the enzymatic machinery responsible for cleaving all nascent pre-mRNAs is likely to be identical; the differences lie in the elaborate mechanisms that have evolved to recruit this machinery to the two classes of transcripts. The driving forces responsible for the evolution of two distinct 3Ј processing complexes are likely to involve the conflicting pressures of posttranscriptional regulation: coordinate cell cycle control of the replication-dependent histone mRNAs versus the developmental and cell-type-specific regulation of alternative poly(A) site selection. Similarities among contrastsThe RNA sequence elements that direct the 3Ј processing of histone and polyadenylated mRNAs could hardly be more different (Fig. 1A). Three elements contribute to mammalian poly(A) site recognition, each of which is recognized by a distinct protein complex (Zhao et al. 1999a). The most well conserved element is the AAUAAA hexamer that generally resides between 10 and 30 nucleotides (nt) upstream of the cleavage site. This element is recognized by a five-subunit complex termed cleavage and polyadenylation specificity factor (CP...

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Section: A Need For Precision and Uniformitymentioning

confidence: 99%

Section: A Need For Precision and Uniformitymentioning

confidence: 99%

Eukaryotic mRNA 3′ processing: a common means to different ends: Figure 1.

Gilmartin¹

2005

Genes Dev.

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“…Since histone mRNA degradation requires that the histone mRNA be translated (Graves et al 1987;Kaygun and Marzluff 2005b), it is likely that SLBP is associated with the histone mRNP when degradation is initiated. Consistent with this possibility, we detected the association of SLBP with both Upf1 and Lsm1 after treatment of cells with inhibitors of DNA replication (Kaygun and Marzluff 2005a;Mullen and Marzluff 2008), suggesting that the oligo(U) tail is added to the histone mRNA while it is still associated with polyribosomes.…”

Section: Introductionmentioning

confidence: 99%

The C-terminal extension of Lsm4 interacts directly with the 3′ end of the histone mRNP and is required for efficient histone mRNA degradation

Lyons

Ricciardi

Guo

et al. 2013

RNA

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Metazoan replication-dependent histone mRNAs are the only known eukaryotic mRNAs that lack a poly(A) tail, ending instead in a conserved stem-loop sequence, which is bound to the stem-loop binding protein (SLBP) on the histone mRNP. Histone mRNAs are rapidly degraded when DNA synthesis is inhibited in S phase in mammalian cells. Rapid degradation of histone mRNAs is initiated by oligouridylation of the 3 ′ end of histone mRNAs and requires the cytoplasmic Lsm1-7 complex, which can bind to the oligo(U) tail. An exonuclease, 3′ hExo, forms a ternary complex with SLBP and the stem-loop and is required for the initiation of histone mRNA degradation. The Lsm1-7 complex is also involved in degradation of polyadenylated mRNAs. It binds to the oligo(A) tail remaining after deadenylation, inhibiting translation and recruiting the enzymes required for decapping. Whether the Lsm1-7 complex interacts directly with other components of the mRNP is not known. We report here that the C-terminal extension of Lsm4 interacts directly with the histone mRNP, contacting both SLBP and 3 ′ hExo. Mutants in the C-terminal tail of Lsm4 that prevent SLBP and 3 ′ hExo binding reduce the rate of histone mRNA degradation when DNA synthesis is inhibited.

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“…ABCE1 function in translation termination is also likely to regulate histone mRNA stability, which is controlled by Upf1-mediated decay mechanism coupled to translation and normally triggered when DNA replication is inhibited. 86,87 Inefficient termination is proposed to determine histone mRNA degradation 92,93 and thus could account for the reduced histone mRNA levels observed in ABCE1-depleted cells (Fig. 3C).…”

Section: Discussionmentioning

confidence: 99%

ABCE1 is essential for S phase progression in human cells

et al. 2016

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ABCE1 is a highly conserved protein universally present in eukaryotes and archaea, which is crucial for the viability of different organisms. First identified as RNase L inhibitor, ABCE1 is currently recognized as an essential translation factor involved in several stages of eukaryotic translation and ribosome biogenesis. The nature of vital functions of ABCE1, however, remains unexplained. Here, we study the role of ABCE1 in human cell proliferation and its possible connection to translation. We show that ABCE1 depletion by siRNA results in a decreased rate of cell growth due to accumulation of cells in S phase, which is accompanied by inefficient DNA synthesis and reduced histone mRNA and protein levels. We infer that in addition to the role in general translation, ABCE1 is involved in histone biosynthesis and DNA replication and therefore is essential for normal S phase progression. In addition, we analyze whether ABCE1 is implicated in transcript-specific translation via its association with the eIF3 complex subunits known to control the synthesis of cell proliferation-related proteins. The expression levels of a few such targets regulated by eIF3A, however, were not consistently affected by ABCE1 depletion.

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Translation Termination Is Involved in Histone mRNA Degradation when DNA Replication Is Inhibited

Cited by 65 publications

References 49 publications

Eukaryotic mRNA 3′ processing: a common means to different ends: Figure 1.

Eukaryotic mRNA 3′ processing: a common means to different ends: Figure 1.

The C-terminal extension of Lsm4 interacts directly with the 3′ end of the histone mRNP and is required for efficient histone mRNA degradation

ABCE1 is essential for S phase progression in human cells

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