The Stem-Loop Binding Protein Is Required for Efficient Translation of Histone mRNA In Vivo and In Vitro

Sánchez, Ricardo Mondragón; Marzluff, William F.

doi:10.1128/mcb.22.20.7093-7104.2002

Cited by 120 publications

(192 citation statements)

References 78 publications

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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: 97%

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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Section: Discussionmentioning

confidence: 97%

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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“…Under in vivo conditions, SLBP is likely to be an essential factor in processing of all histone pre-mRNAs regardless of the HDE sequence and the extent of base pairing to the U7 snRNA (Pandey et al, 1994). Following processing, SLBP remains associated with the stem-loop at the 3' end and accompanies the mature histone mRNA to the cytoplasm (Dominski et al, 1995;Erkmann et al, 2005;Whitfield et al, 2004), where it stimulates its translation into histone proteins (Gorgoni et al, 2005;Sanchez and Marzluff, 2002).…”

Section: Stem-loop Binding Protein (Slbp)mentioning

confidence: 99%

“…During 3' end processing the HDE interacts with the U7 snRNP and the stem-loop is recognized by a protein termed the stem-loop binding protein (SLBP) . After completion of processing, SLBP remains associated with the stem-loop at the end of mature histone mRNAs and stimulates their translation into histone proteins in the cytoplasm (Gorgoni et al, 2005;Sanchez and Marzluff, 2002). The intracellular concentration of SLBP reaches the highest level during S phase and rapidly declines during the S/G2 transition due to proteasome degradation (Whitfield et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

Formation of the 3′ end of histone mRNA: Getting closer to the end

Domiński

Marzluff

2007

Gene

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Nearly all eukaryotic mRNAs end with a poly (A) tail that is added to their 3' end by the ubiquitous cleavage/polyadenylation machinery. The only known exception to this rule are metazoan replication dependent histone mRNAs, which end with a highly conserved stem-loop structure. This distinct 3' end is generated by specialized 3'end processing machinery that cleaves histone pre-mRNAs 4-5 nucleotides downstream of the stem-loop and consists of the U7 small nuclear RNP (snRNP) and number of protein factors. Recently, the U7 snRNP has been shown to contain a unique Sm core that differs from that of the spliceosomal snRNPs, and an essential heat labile processing factor has been identified as symplekin. In addition, cross-linking studies have pinpointed CPSF-73 as the endonuclease, which catalyzes the cleavage reaction. Thus, many of the critical components of the 3' end processing machinery are now identified. Strikingly, this machinery is not as unique as initially thought but contains a number of factors involved in cleavage/polyadenylation, suggesting that the two mechanisms have a common evolutionary origin. The greatest challenge that lies ahead is to determine how all these factors interact with each other to form a catalytically competent processing complex capable of cleaving histone pre-mRNAs.

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“…This complex mediates histonespecific mRNA processing that results in mature mRNAs that do not contain a poly(A) tail but end in the stem-loop structure. The stem-loop and SLBP are also involved in translation of histone mRNAs (Gallie et al 1996;Ling et al 2002;Sanchez and Marzluff 2002). SLBP is associated with polyribosomes, dependent on the presence of intact histone mRNA (Whitfield et al 2004;S.…”

Section: Introductionmentioning

confidence: 99%

The stem–loop binding protein stimulates histone translation at an early step in the initiation pathway

Gorgoni

Andrews

Schaller³

et al. 2005

RNA

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Metazoan replication-dependent histone mRNAs do not have a poly(A) tail but end instead in a conserved stem-loop structure. Efficient translation of these mRNAs is dependent on the stem-loop binding protein (SLBP). Here we explore the mechanism by which SLBP stimulates translation in vertebrate cells, using the tethered function assay and analyzing protein-protein interactions. We show for the first time that translational stimulation by SLBP increases during oocyte maturation and that SLBP stimulates translation at the level of initiation. We demonstrate that SLBP can interact directly with subunit h of eIF3 and with Paip1; however, neither of these interactions is sufficient to mediate its effects on translation. We find that Xenopus SLBP1 functions primarily at an early stage in the cap-dependent initiation pathway, targeting small ribosomal subunit recruitment. Analysis of IRES-driven translation in Xenopus oocytes suggests that SLBP activity requires eIF4E. We propose a model in which a novel factor contacts eIF4E bound to the 5 0 cap and SLBP bound to the 3 0 end simultaneously, mediating formation of an alternative end-to-end complex.

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The Stem-Loop Binding Protein Is Required for Efficient Translation of Histone mRNA In Vivo and In Vitro

Cited by 120 publications

References 78 publications

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

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

Formation of the 3′ end of histone mRNA: Getting closer to the end

The stem–loop binding protein stimulates histone translation at an early step in the initiation pathway

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