The histone 3'-terminal stem-loop is necessary for translation in Chinese hamster ovary cells

Gallie, Daniel; Lewis, Nancy Jo; Marzluff, William F.

doi:10.1093/nar/24.10.1954

Cited by 87 publications

(80 citation statements)

References 48 publications

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“…The 39 end of histone mRNA and its bound SLBP play a critical role in multiple aspects of histone mRNA metabolism, including pre-mRNA processing (Dominski et al+, 1995;Wang et al+, 1996c;Martin et al+, 1997), export (Eckner et al+, 1991;Williams et al+, 1994), translation (Sun et al+, 1992;Gallie et al+, 1996), and mRNA stability (Pandey & Marzluff, 1987;Williams et al+, 1994)+ The frog oocyte is a convenient experimental system to study the many aspects of RNA metabolism because one can express or inject both specific RNAs and proteins and follow their subsequent metabolism+…”

Section: Resultsmentioning

confidence: 99%

Dual role for the RNA-binding domain of Xenopus laevis SLBP1 in histone pre-mRNA processing

Ingledue

Domiński

Sánchez

et al. 2000

RNA

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Section: Resultsmentioning

confidence: 99%

Dual role for the RNA-binding domain of Xenopus laevis SLBP1 in histone pre-mRNA processing

Ingledue

Domiński

Sánchez

et al. 2000

RNA

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“…SLBP is required for the translation of stem-loop histone mRNAs (Sun et al, 1992;Gallie et al, 1996), and we have recently shown that SLBP stimulates translation of histone mRNA in vivo and in vitro (Sanchez and Marzluff, 2002). The SLBP that accumulates during maturation may play a role in activating translation of histone mRNA during oocyte maturation and after fertilization, thus providing the histone proteins necessary both for repackaging the sperm chromatin and for synthesis of histone proteins for the first S-phase.…”

Section: Discussionmentioning

confidence: 99%

Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo

Allard

Champigny

Skoggard

et al. 2002

Journal of Cell Science

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The stem-loop binding protein (SLBP) binds to the 3′ end of histone mRNA and participates in 3′-processing of the newly synthesized transcripts, which protects them from degradation, and probably also promotes their translation. In proliferating cells, translation of SLBP mRNA begins at G1/S and the protein is degraded following DNA replication. These post-transcriptional mechanisms closely couple SLBP expression to S-phase of the cell cycle, and play a key role in restricting synthesis of replication-dependent histones to S-phase. In contrast to somatic cells,replication-dependent histone mRNAs accumulate and are translated independently of DNA replication in oocytes and early embryos. We report here that SLBP expression and activity also differ in mouse oocytes and early embryos compared with somatic cells. SLBP is present in oocytes that are arrested at prophase of G2/M, where it is concentrated in the nucleus. Upon entry into M-phase of meiotic maturation, SLBP begins to accumulate rapidly,reaching a very high level in mature oocytes arrested at metaphase II. Following fertilization, SLBP remains abundant in the nucleus and the cytoplasm throughout the first cell cycle, including both G1 and G2 phases. It declines during the second and third cell cycles, reaching a relatively low level by the late 4-cell stage. SLBP can bind the histone mRNA-stem-loop at all stages of the cell cycle in oocytes and early embryos, and it is the only stem-loop binding activity detectable in these cells. We also report that SLBP becomes phosphorylated rapidly following entry into M-phase of meiotic maturation through a mechanism that is sensitive to roscovitine, an inhibitor of cyclin-dependent kinases. SLBP is rapidly dephosphorylated following fertilization or parthenogenetic activation, and becomes newly phosphorylated at M-phase of mitosis. Phosphorylation does not affect its stem-loop binding activity. These results establish that, in contrast to Xenopus, mouse oocytes and embryos contain a single SLBP. Expression of SLBP is uncoupled from S-phase in oocytes and early embryos, which indicates that the mechanisms that impose cell-cycle-regulated expression of SLBP in somatic cells do not operate in oocytes or during the first embryonic cell cycle. This distinctive pattern of SLBP expression may be required for accumulation of histone proteins required for sperm chromatin remodelling and assembly of newly synthesized embryonic DNA into chromatin.

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“…An enhancing effect by the 3Ј-UTR has been observed for nonpolyadenylated histone mRNAs, the 3Ј stem-loop of which mimics a poly(A) tail (31), and for amyloid precursor protein and lipoprotein lipase mRNAs, which interestingly contain two alternative poly(A) sites (27,28). A few 3Ј translational enhancers have also been characterized in uncapped and/or unpolyadenylated viruses.…”

Section: Figmentioning

confidence: 99%

Alternative Translation Initiation of Human Fibroblast Growth Factor 2 mRNA Controlled by Its 3′-Untranslated Region Involves a Poly(A) Switch and a Translational Enhancer

Touriol

Roussigné

Gensac

et al. 2000

Journal of Biological Chemistry

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Five fibroblast growth factor 2 (FGF-2) isoforms are synthesized from human FGF-2 mRNA by a process of alternative initiation of translation. The regulation of FGF-2 isoform expression by the mRNA 5823-nucleotidelong 3-untranslated region containing eight alternative polyadenylation sites was examined. Because previous studies had shown that FGF-2 expression was regulated in primary cells but not in transformed cells, primary human skin fibroblasts were used in this study. Using an approach of cell transfection with synthetic reporter mRNAs, a novel translational enhancer (3-TE) was identified in the 1370-nucleotide mRNA segment located upstream from the eighth poly(A) site. Deletion mutagenesis showed that the 3-TE was composed of two domains with additive effects. The 3-TE exhibited the unique feature of modulating the use of FGF-2 alternative initiation codons, which favored the relative expression of CUG-initiated isoforms. Interestingly, the use of an alternative polydenylation site removing the 3-TE was detected in skin fibroblasts in response to heat shock and cell density variations. At high cell densities, 3-TE removal was correlated with a loss of CUG-initiated FGF-2 expression. These data show that the FGF-2 mRNA 3-untranslated region is able to modulate FGF-2 isoform expression by the coupled processes of translation activation and alternative polyadenylation.

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The histone 3'-terminal stem-loop is necessary for translation in Chinese hamster ovary cells

Cited by 87 publications

References 48 publications

Dual role for the RNA-binding domain of Xenopus laevis SLBP1 in histone pre-mRNA processing

Dual role for the RNA-binding domain of Xenopus laevis SLBP1 in histone pre-mRNA processing

Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo

Alternative Translation Initiation of Human Fibroblast Growth Factor 2 mRNA Controlled by Its 3′-Untranslated Region Involves a Poly(A) Switch and a Translational Enhancer

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