The Mos Pathway Regulates Cytoplasmic Polyadenylation in <i>Xenopus</i> Oocytes

Moor, Cornelia H. de; Richter, Joel D.

doi:10.1128/mcb.17.11.6419

Cited by 138 publications

(172 citation statements)

References 33 publications

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“…In Xenopus, Aurora A (Eg2) was one of several mRNAs identified initially as undergoing polyadenylation during the transition from an (immature) oocyte to an egg (Paris et al 1988). Many CPE-containing mRNAs, with mos being a notable exclusion, undergo polyadenylation-induced translation after MPF activation, when it is necessary to partially destroy CPEB (de Moor and Richter 1997;Mendez et al 2002). The 3Ј UTR of Aurora A mRNA contains putative CPEs, and these might drive polyadenylation and translation subsequent to MPF activation.…”

Section: Discussionmentioning

confidence: 99%

“…Xenopus laevis females were injected with pregnant mare serum gonadotropin (50 IU); 4 to 7 d later, ovarian lobes were removed and treated with collagenase and dispase (de Moor and Richter 1997), and stage VI oocytes were selected and cultured in Barth's medium for all procedures. Oocytes were injected with 30 nL of the indicated in vitro transcribed radiolabeled or radioinert mRNA suspended in water at a concentration of 0.1 to 0.5 µM.…”

Section: Oocyte Preparation and Injectionsmentioning

confidence: 99%

“…Kinase assays for CPEB phos-phorylation were performed in a total volume of 40 µL containing 20 µL of kinase buffer [10 mM MgCl 2 , 1 mM dithiothreitol, 20 mM HEPES pH 7.7, 50 mM KCl, and 30 µM (␥-32 P) ATP (0.16 mCi mL −1 )], 10 µL of CPEB substrate (0.5 µg), and 10 µL of extracts prepared from mock, progesterone-, or insulin-stimulated oocyte extracts. Kinase assays for MPF activity was conducted as in de Moor and Richter (1997). Reaction mixtures were incubated for 15 min at 30°C followed by 2D phosphopeptide mapping (Boyle at al.…”

Section: Kinase Assaysmentioning

confidence: 99%

“…To assay polyadenylation of injected radiolabeled CPE containing or lacking RNA (de Moor et al 1997), total RNA was isolated from oocytes that had been injected with radiolabeled RNA by the p-aminosalicylic acid-sodium dodecyl sulfate (SDS) method (de Moor and Richter 1997). The RNA was analyzed by electrophoresis on a 6% polyacrylamide gel containing 50% urea and 1X Tris-borate-EDTA buffer and phosphorimaging.…”

Section: Polyadenylation and Western Proceduresmentioning

confidence: 99%

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Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3

Sarkissian¹,

Méndez²,

Richter³

2004

Genes Dev.

115

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Progesterone stimulation of Xenopus oocyte maturation requires the cytoplasmic polyadenylation-induced translation of mos and cyclin B mRNAs. One cis element that drives polyadenylation is the CPE, which is bound by the protein CPEB. Polyadenylation is stimulated by Aurora A (Eg2)-catalyzed CPEB serine 174 phosphorylation, which occurs soon after oocytes are exposed to progesterone. Here, we show that insulin also stimulates Aurora A-catalyzed CPEB S174 phosphorylation, cytoplasmic polyadenylation, translation, and oocyte maturation. However, these insulin-induced events are uniquely controlled by PI3 kinase and PKC-, which act upstream of Aurora A. The intersection of the progesterone and insulin signaling pathways occurs at glycogen synthase kinase 3 (GSK-3), which regulates the activity of Aurora A. GSK-3 and Aurora A interact in vivo, and overexpressed GSK-3 inhibits Aurora A-catalyzed CPEB phosphorylation. In vitro, GSK-3 phosphorylates Aurora A on S290/291, the result of which is an autophosphorylation of serine 349. GSK-3 phosphorylated Aurora A, or Aurora A proteins with S290/291D or S349D mutations, have reduced or no capacity to phosphorylate CPEB. Conversely, Aurora A proteins with S290/291A or S349A mutations are constitutively active. These results suggest that the progesterone and insulin stimulate maturation by inhibiting GSK-3, which allows Aurora A activation and CPEB-mediated translation.[Keywords: Insulin; GSK-3; Xenopus oocytes; Aurora A; cytoplasmic polyadenylation; CPEB] Fully grown Xenopus oocytes arrested at the end of prophase I are stimulated to re-enter into the meiotic divisions (oocyte maturation) by progesterone. Although the initial signaling event that is propagated by progesterone is unclear, it involves an immediate but transient decrease in cyclic AMP (cAMP; Sadler and Maller 1989; for review, see Ferrell 1999) and the activation of Aurora A (Eg2), a member of the Aurora family of protein kinases (Andresson and Ruderman 1998). The most proximal known substrate of Aurora A is CPEB, a sequence-specific RNA binding protein that stimulates cytoplasmic polyadenylation and translational activation (Hake and Richter 1994;Mendez et al. 2000a). CPEB interacts with the cytoplasmic polyadenylation element (CPE), a cis element present in the 3Ј untranslated regions (UTRs) of several mRNAs including those that encode mos and cyclin B. The translation of mos mRNA is necessary to induce the MAP kinase cascade that indirectly activates M-phase promoting factor (MPF), a heterodimer of cyclin B and cdc2. MPF is responsible for many manifestations of oocyte maturation such as germinal vesicle breakdown (GVBD). Aurora phosphorylation of CPEB serine 174 enhances the association of CPEB with CPSF (cleavage and polyadenylation specificity factor), possibly helping to stabilize this group of proteins on the AAUAAA hexanucleotide, a second cis element essential for polyadenylation (Mendez et al. 2000a,b). CPSF is probably responsible for recruiting poly(A) polymerase to the end of the mRNA.Polyadenylat...

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Section: Discussionmentioning

confidence: 99%

Section: Oocyte Preparation and Injectionsmentioning

confidence: 99%

Section: Kinase Assaysmentioning

confidence: 99%

Section: Polyadenylation and Western Proceduresmentioning

confidence: 99%

See 2 more Smart Citations

Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3

Sarkissian¹,

Méndez²,

Richter³

2004

Genes Dev.

115

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“…Second, the injection of a CPEB antibody into oocytes prevents polyadenylation in vivo (40). CPEB, which is also conserved among several invertebrates (3,20,43), is phosphorylated during maturation (12,30), although the extent to which this is important for activity of the protein is unclear (5). The specificity of the interaction of CPEB for RNA resides in three parts of the protein: the two RRMs and a cysteine-histidine region that coordinates a metal ion (15).…”

Section: Discussionmentioning

confidence: 99%

The 36-Kilodalton Embryonic-Type Cytoplasmic Polyadenylation Element-Binding Protein in Xenopus laevis Is ElrA, a Member of the ELAV Family of RNA-Binding Proteins

Good

Richter

1997

Molecular and Cellular Biology

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The translational activation of several maternal mRNAs in Xenopus laevis is dependent on cytoplasmic poly(A) elongation. Messages harboring the UUUUUAU-type cytoplasmic polyadenylation element (CPE) in their 3 untranslated regions (UTRs) undergo polyadenylation and translation during oocyte maturation. This CPE is bound by the protein CPEB, which is essential for polyadenylation. mRNAs that have the poly(U) 12-27 embryonic-type CPE (eCPE) in their 3 UTRs undergo polyadenylation and translation during the early cleavage and blastula stages. A 36-kDa eCPE-binding protein in oocytes and embryos has been identified by UV cross-linking. We now report that this 36-kDa protein is ElrA, a member of the ELAV family of RNA-binding proteins. The proteins are identical in size, antibody directed against ElrA immunoprecipitates the 36-kDa protein, and the two proteins have the same RNA binding specificity in vitro. Cl2 and activin receptor mRNAs, both of which contain eCPEs, are detected in immunoprecipitated ElrA-mRNP complexes from eggs and embryos. In addition, this in vivo interaction requires the eCPE. Although a number of experiments failed to define a role for ElrA in cytoplasmic polyadenylation, the expression of a dominant negative ElrA protein in embryos results in an exogastrulation phenotype. The possible functions of ElrA in gastrulation are discussed.Early development in many animals is programmed by mRNAs inherited by the egg at the time of fertilization. While many of these mRNAs are translationally dormant in oocytes, they become activated in a sequence-specific manner at subsequent developmental periods. Several mechanisms are likely to control the translation of these messages, but one that has been studied extensively in Xenopus laevis is poly(A) elongation (31). Some mRNAs, which encode such proteins as c-Mos, cyclin B1, cyclin-dependent kinase 2 (Cdk2), and the earlydevelopment-specific histone B4, are polyadenylated and translated during oocyte maturation (27-29, 33, 39). Other mRNAs, however, undergo these processes sometime after fertilization; they encode such proteins as polypeptide chain release factor (Cl1), Cl2 (function unknown), and activin receptor (28,(34)(35)(36).Both groups of mRNAs contain two cis-acting elements located in their 3Ј untranslated regions (UTRs) that are required for cytoplasmic polyadenylation. One is the virtually ubiquitous hexanucleotide AAUAAA, which is also important for nuclear pre-mRNA cleavage and polyadenylation. The second, called the cytoplasmic polyadenylation element (CPE), is a U-rich sequence located upstream of the hexanucleotide. The exact sequence of CPE differs between the two groups of mRNAs mentioned. The maturation-type CPE is UUUUUAU (consensus), whereas the embryonic CPE (eCPE) is oligo (U) 12-27 (reviewed in reference 31). At least two mRNAs that are polyadenylated in embryos also contain a third cis-acting sequence in the 3Ј UTR: the masking element that prevents precocious polyadenylation during maturation (34, 35). Because deletion of the maskin...

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Function of the Mos/MAPK pathway during oocyte maturation in the Japanese brown frogRana japonica

2000

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The Mos Pathway Regulates Cytoplasmic Polyadenylation in Xenopus Oocytes

Cited by 138 publications

References 33 publications

Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3

Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3

The 36-Kilodalton Embryonic-Type Cytoplasmic Polyadenylation Element-Binding Protein in Xenopus laevis Is ElrA, a Member of the ELAV Family of RNA-Binding Proteins

Function of the Mos/MAPK pathway during oocyte maturation in the Japanese brown frogRana japonica

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