Inactivation of protein kinase A is not required for c-mos translation during meiotic maturation of Xenopus oocytes

Faure, Sandrine; Morin, Nathalie; Dorée, Marcel

doi:10.1038/sj.onc.1202056

Cited by 24 publications

(27 citation statements)

References 27 publications

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“…The hormone, therefore, triggers cyclin B1 accumulation by acting through a decrease in PKA activity (Figure 10). This again differentiates cyclin B1 from Mos in terms of regulation, because it was recently shown that PKA does not exert any inhibitory effect on Mos translation induced by exogenous Mos injection (Faure et al, 1998). However, GVBD does not occur when exogenous Mos is injected in the presence of PKAc (Daar et al, 1993).…”

Section: Discussionmentioning

confidence: 99%

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

Frank-Vaillant

Jessus

Ozon

et al. 1999

MBoC

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Progesterone-induced meiotic maturation of Xenopus oocytes requires the synthesis of new proteins, such as Mos and cyclin B. Synthesis of Mos is thought to be necessary and sufficient for meiotic maturation; however, it has recently been proposed that newly synthesized proteins binding to p34 cdc2 could be involved in a signaling pathway that triggers the activation of maturation-promoting factor. We focused our attention on cyclin B proteins because they are synthesized in response to progesterone, they bind to p34 cdc2 , and their microinjection into resting oocytes induces meiotic maturation. We investigated cyclin B accumulation in response to progesterone in the absence of maturation-promoting factor-induced feedback. We report here that the cdk inhibitor p21 cip1 , when microinjected into immature Xenopus oocytes, blocks germinal vesicle breakdown induced by progesterone, by maturation-promoting factor transfer, or by injection of okadaic acid. After microinjection of p21 cip1 , progesterone fails to induce the activation of MAPK or p34 cdc2 , and Mos does not accumulate. In contrast, the level of cyclin B1 increases normally in a manner dependent on down-regulation of cAMP-dependent protein kinase but independent of cap-ribose methylation of mRNA.

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Section: Discussionmentioning

confidence: 99%

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

Frank-Vaillant

Jessus

Ozon

et al. 1999

MBoC

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“…Injection of the heat-stable PKA inhibitor PKI induces M-phase entry in the absence of progesterone. PKA inhibits both branches of the pathway: (i) PKA prevents synthesis of Mos and can block Mos-induced oocyte activation, and (ii) PKA blocks steps leading to activation of cdc25 (20)(21)(22)(23)(24)(25). However, no direct targets of PKA have been identified in this pathway.…”

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confidence: 99%

G ₂ arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A

Duckworth

Weaver

Ruderman

2002

Proc. Natl. Acad. Sci. U.S.A.

196

209

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Xenopus oocytes, which are arrested in G2 of meiosis I, contain complexes of cyclin B-cdc2 (M phase-promoting factor) that are kept repressed by inhibitory phosphorylations on cdc2 at Thr-14 and Tyr-15. Progesterone induces a cytoplasmic signaling pathway that leads to activation of cdc25, the phosphatase that removes these phosphorylations, catalyzing entry into M phase. It has been known for 25 years that high levels of cAMP and protein kinase A (PKA) are required to maintain the G 2 arrest and that a drop in PKA activity is required for M phase-promoting factor activation, but no physiological targets of PKA have been identified. We present evidence that cdc25 is a critical target of PKA. (i) In vitro, cdc25 Ser-287 serves as a major site of phosphorylation by PKA, resulting in sequestration by 14-3-3. (ii) Endogenous cdc25 is phosphorylated on Ser-287 in oocytes and dephosphorylated in response to progesterone just before cdc2 dephosphorylation and M-phase entry. (iii) High PKA activity maintains phosphorylation of Ser-287 in vivo, whereas inhibition of PKA by its heat-stable inhibitor (PKI) induces dephosphorylation of Ser-287. (iv) Overexpression of mutant cdc25 (S287A) bypasses the ability of PKA to maintain oocytes in G 2 arrest. These findings argue that cdc25 is a physiologically relevant target of PKA in oocytes. In the early embryonic cell cycles, Ser-287 is phosphorylated during interphase and dephosphorylated just before cdc2 activation and mitotic entry. Thus, in addition to its role in checkpoint arrest, cdc25 Ser-287 serves as a site for regulation during normal, unperturbed cell cycles.

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“…For example, purified bovine PKAc can inhibit the maturation induced by injection of Mos protein kinase (13) and also blocks Mos accumulation in response to progesterone (14). However, PKAc does not block the synthesis of endogenous Mos when mitogen-activated protein kinase (MAPK) is previously activated by injection of recombinant Mos protein (15), consistent with the observation that MAPK activity is required for full stimulation of Mos translation (16,17). Elevation of endogenous PKA activity by treatment of oocytes with 3-isobutyl-1-methylxanthine can also delay Cdc2͞cyclin B activation and germinal vesicle breakdown (GVBD) induced by injection of recombinant cyclin B or Cdc25A proteins (12).…”

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Inhibition of Xenopus oocyte meiotic maturation by catalytically inactive protein kinase A

Schmitt

Nebreda

2002

Proc. Natl. Acad. Sci. U.S.A.

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Progesterone induces G2-arrested Xenopus oocytes to develop into fertilizable eggs in a process called meiotic maturation. Protein kinase A (PKA), the cAMP-dependent protein kinase, has long been known to be a potent inhibitor of meiotic maturation, but little information is available on how PKA functions. We have cloned two Xenopus PKA catalytic subunit isoforms, XPKA␣ and XPKA␤. These proteins are 89% identical and both inhibit progesteroneinduced meiotic maturation when overexpressed at low levels, suggesting that PKA activity is tightly regulated in the oocyte. Unexpectedly, catalytically inactive XPKA mutants are able to block progesterone-induced maturation as efficiently as the wild-type active XPKA. These mutants also block meiotic maturation induced by Mos, but are less efficient at inhibiting Cdc25C-induced maturation. Our results indicate that PKA can inhibit meiotic maturation by a novel mechanism, which does not require its kinase activity and is also independent of binding to the PKA regulatory subunits.

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Inactivation of protein kinase A is not required for c-mos translation during meiotic maturation of Xenopus oocytes

Cited by 24 publications

References 27 publications

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

G ₂ arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A

Inhibition of Xenopus oocyte meiotic maturation by catalytically inactive protein kinase A

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Inactivation of protein kinase A is not required for c-mos translation during meiotic maturation of Xenopus oocytes

Cited by 24 publications

References 27 publications

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

Two Distinct Mechanisms Control the Accumulation of Cyclin B1 and Mos inXenopusOocytes in Response to Progesterone

G 2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A

Inhibition of Xenopus oocyte meiotic maturation by catalytically inactive protein kinase A

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G ₂ arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A