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Mos in the oocyte: how to use MAPK independently of growth factors and transcription to control meiotic divisions.

Dupré A, Haccard O, Jessus C - J Signal Transduct (2010)

Bottom Line: In one specific cell type however, the female germ cell, MAPK does not follow this canonical scheme.Which unique functions could explain the evolutionary cost to have selected one gene to only serve for few hours in one very specific cell type?This review discusses the original features of MAPK activation by Mos and the roles of this module in oocytes.

View Article: PubMed Central - PubMed

Affiliation: CNRS, UMR 7622-Biologie du Développement, 9 Quai Saint-Bernard, 75005 Paris, France.

ABSTRACT
In many cell types, the mitogen-activated protein kinase (MAPK) also named extracellular signal-regulated kinase (ERK) is activated in response to a variety of extracellular growth factor-receptor interactions and leads to the transcriptional activation of immediate early genes, hereby influencing a number of tissue-specific biological activities, as cell proliferation, survival and differentiation. In one specific cell type however, the female germ cell, MAPK does not follow this canonical scheme. In oocytes, MAPK is activated independently of growth factors and tyrosine kinase receptors, acts independently of transcriptional regulation, plays a crucial role in controlling meiotic divisions, and is under the control of a peculiar upstream regulator, the kinase Mos. Mos was originally identified as the transforming gene of Moloney murine sarcoma virus and its cellular homologue was the first proto-oncogene to be molecularly cloned. What could be the specific roles of Mos that render it necessary for meiosis? Which unique functions could explain the evolutionary cost to have selected one gene to only serve for few hours in one very specific cell type? This review discusses the original features of MAPK activation by Mos and the roles of this module in oocytes.

No MeSH data available.


Related in: MedlinePlus

Patterns of Mos expression and MPF activity during oocyte meiotic maturation and at fertilization in Xenopus, mouse, and starfish. Prophase I-arrested oocytes require a physiological stimulus to undergo meiotic maturation: progesterone in frogs, release from the follicle in mammals, and 1-methyl-adenine in starfish. Once activated, MPF promotes entry into the first meiotic division: breakdown of the nuclear envelope (GVBD for germinal vesicle breakdown) and formation of the metaphase I spindle (MI). MPF activity falls due to partial cyclin degradation at meiosis I/meiosis II transition or interkinesis (IK), during which chromosomes remain condensed without nuclear membranes and in the absence of DNA replication. MPF rises again leading to entry into meiosis II. In vertebrates, oocytes arrest at metaphase II (MII), while in echinoderms, oocytes complete the second meiotic division and arrest at the G1 phase. Mos translational timing is different among species, occurring before MPF activation in Xenopus (however, Mos protein is unstable until GVBD and MAPK activity is detected only at time of MPF activation, not illustrated) and during metaphase I in other species.
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fig2: Patterns of Mos expression and MPF activity during oocyte meiotic maturation and at fertilization in Xenopus, mouse, and starfish. Prophase I-arrested oocytes require a physiological stimulus to undergo meiotic maturation: progesterone in frogs, release from the follicle in mammals, and 1-methyl-adenine in starfish. Once activated, MPF promotes entry into the first meiotic division: breakdown of the nuclear envelope (GVBD for germinal vesicle breakdown) and formation of the metaphase I spindle (MI). MPF activity falls due to partial cyclin degradation at meiosis I/meiosis II transition or interkinesis (IK), during which chromosomes remain condensed without nuclear membranes and in the absence of DNA replication. MPF rises again leading to entry into meiosis II. In vertebrates, oocytes arrest at metaphase II (MII), while in echinoderms, oocytes complete the second meiotic division and arrest at the G1 phase. Mos translational timing is different among species, occurring before MPF activation in Xenopus (however, Mos protein is unstable until GVBD and MAPK activity is detected only at time of MPF activation, not illustrated) and during metaphase I in other species.

Mentions: In the animal kingdom, the oocytes growing in the ovaries are arrested at prophase of the first meiotic division that resembles a G2-phase of the cell cycle. These immature oocytes require a physiological stimulus to undergo meiotic maturation: the progression through the meiotic divisions that converts them into fertilizable oocytes, again arrested at various stages of meiosis and awaiting fertilization (Figure 1). Indeed, the embryonic development cannot begin until completion of the female germ cell meiotic divisions. This temporal coupling is ensured by the arrest of meiotic divisions of the oocyte that depends on a biological activity called CSF (for cytostatic factor) [43, 44]. The CSF arrest is released by fertilization. Oocytes arrest at metaphase I in insects, molluscs and ascidians and at metaphase II in vertebrates. In echinoderms and cnidarians, oocytes complete meiosis and arrest in G1 (and are then called “eggs” in these species, as they completed meiotic divisions). In different species including the nematode Caenorhabditis elegans, fertilization occurs at prophase I and corresponds to the stimulus promoting meiotic maturation. Except for this last case, the stimuli for maturation are provided at ovulation by the follicular cells surrounding the oocyte. The signals are very different from species to species: steroid hormones in frogs and fishes, modified purines in starfish, removal of a follicular inhibitor in mammals, but all activate signaling pathways that converge to the same target, independently of transcription: the activation of the universal eukaryotic inducer of M-phase, MPF, a complex formed of the Cdk1 kinase, and Cyclin B. Once activated, MPF promotes entry into the first meiotic division: breakdown of the nuclear envelope (known as GVBD for germinal vesicle breakdown) and formation of the metaphase I spindle (Figures 1 and 2). MPF activity falls during anaphase I, due to partial cyclin B degradation, and rises again leading to entry into meiosis II. Importantly for the generation of proper haploid gametes, DNA replication does not occur between both meiotic divisions. The need for the Mos/MAPK cascade during oocyte meiotic maturation has been debated for decades (Figure 1). First, Mos has often been implicated in the initial step of MPF activation during reinitiation of meiotic division, especially in the frog oocyte. Second, Mos has been shown to be required during the metaphase I to metaphase II transition for the suppression of S-phase and for the reactivation of MPF after meiosis I, thus enabling the oocyte to enter meiosis II. Third, a universal role of Mos is to prevent parthenogenesis by arresting oocyte maturation at the various stages depicted in Figure 1, allowing them to await fertilization. Mos is therefore a key regulator of meiosis in the animal kingdom.


Mos in the oocyte: how to use MAPK independently of growth factors and transcription to control meiotic divisions.

Dupré A, Haccard O, Jessus C - J Signal Transduct (2010)

Patterns of Mos expression and MPF activity during oocyte meiotic maturation and at fertilization in Xenopus, mouse, and starfish. Prophase I-arrested oocytes require a physiological stimulus to undergo meiotic maturation: progesterone in frogs, release from the follicle in mammals, and 1-methyl-adenine in starfish. Once activated, MPF promotes entry into the first meiotic division: breakdown of the nuclear envelope (GVBD for germinal vesicle breakdown) and formation of the metaphase I spindle (MI). MPF activity falls due to partial cyclin degradation at meiosis I/meiosis II transition or interkinesis (IK), during which chromosomes remain condensed without nuclear membranes and in the absence of DNA replication. MPF rises again leading to entry into meiosis II. In vertebrates, oocytes arrest at metaphase II (MII), while in echinoderms, oocytes complete the second meiotic division and arrest at the G1 phase. Mos translational timing is different among species, occurring before MPF activation in Xenopus (however, Mos protein is unstable until GVBD and MAPK activity is detected only at time of MPF activation, not illustrated) and during metaphase I in other species.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3101788&req=5

fig2: Patterns of Mos expression and MPF activity during oocyte meiotic maturation and at fertilization in Xenopus, mouse, and starfish. Prophase I-arrested oocytes require a physiological stimulus to undergo meiotic maturation: progesterone in frogs, release from the follicle in mammals, and 1-methyl-adenine in starfish. Once activated, MPF promotes entry into the first meiotic division: breakdown of the nuclear envelope (GVBD for germinal vesicle breakdown) and formation of the metaphase I spindle (MI). MPF activity falls due to partial cyclin degradation at meiosis I/meiosis II transition or interkinesis (IK), during which chromosomes remain condensed without nuclear membranes and in the absence of DNA replication. MPF rises again leading to entry into meiosis II. In vertebrates, oocytes arrest at metaphase II (MII), while in echinoderms, oocytes complete the second meiotic division and arrest at the G1 phase. Mos translational timing is different among species, occurring before MPF activation in Xenopus (however, Mos protein is unstable until GVBD and MAPK activity is detected only at time of MPF activation, not illustrated) and during metaphase I in other species.
Mentions: In the animal kingdom, the oocytes growing in the ovaries are arrested at prophase of the first meiotic division that resembles a G2-phase of the cell cycle. These immature oocytes require a physiological stimulus to undergo meiotic maturation: the progression through the meiotic divisions that converts them into fertilizable oocytes, again arrested at various stages of meiosis and awaiting fertilization (Figure 1). Indeed, the embryonic development cannot begin until completion of the female germ cell meiotic divisions. This temporal coupling is ensured by the arrest of meiotic divisions of the oocyte that depends on a biological activity called CSF (for cytostatic factor) [43, 44]. The CSF arrest is released by fertilization. Oocytes arrest at metaphase I in insects, molluscs and ascidians and at metaphase II in vertebrates. In echinoderms and cnidarians, oocytes complete meiosis and arrest in G1 (and are then called “eggs” in these species, as they completed meiotic divisions). In different species including the nematode Caenorhabditis elegans, fertilization occurs at prophase I and corresponds to the stimulus promoting meiotic maturation. Except for this last case, the stimuli for maturation are provided at ovulation by the follicular cells surrounding the oocyte. The signals are very different from species to species: steroid hormones in frogs and fishes, modified purines in starfish, removal of a follicular inhibitor in mammals, but all activate signaling pathways that converge to the same target, independently of transcription: the activation of the universal eukaryotic inducer of M-phase, MPF, a complex formed of the Cdk1 kinase, and Cyclin B. Once activated, MPF promotes entry into the first meiotic division: breakdown of the nuclear envelope (known as GVBD for germinal vesicle breakdown) and formation of the metaphase I spindle (Figures 1 and 2). MPF activity falls during anaphase I, due to partial cyclin B degradation, and rises again leading to entry into meiosis II. Importantly for the generation of proper haploid gametes, DNA replication does not occur between both meiotic divisions. The need for the Mos/MAPK cascade during oocyte meiotic maturation has been debated for decades (Figure 1). First, Mos has often been implicated in the initial step of MPF activation during reinitiation of meiotic division, especially in the frog oocyte. Second, Mos has been shown to be required during the metaphase I to metaphase II transition for the suppression of S-phase and for the reactivation of MPF after meiosis I, thus enabling the oocyte to enter meiosis II. Third, a universal role of Mos is to prevent parthenogenesis by arresting oocyte maturation at the various stages depicted in Figure 1, allowing them to await fertilization. Mos is therefore a key regulator of meiosis in the animal kingdom.

Bottom Line: In one specific cell type however, the female germ cell, MAPK does not follow this canonical scheme.Which unique functions could explain the evolutionary cost to have selected one gene to only serve for few hours in one very specific cell type?This review discusses the original features of MAPK activation by Mos and the roles of this module in oocytes.

View Article: PubMed Central - PubMed

Affiliation: CNRS, UMR 7622-Biologie du Développement, 9 Quai Saint-Bernard, 75005 Paris, France.

ABSTRACT
In many cell types, the mitogen-activated protein kinase (MAPK) also named extracellular signal-regulated kinase (ERK) is activated in response to a variety of extracellular growth factor-receptor interactions and leads to the transcriptional activation of immediate early genes, hereby influencing a number of tissue-specific biological activities, as cell proliferation, survival and differentiation. In one specific cell type however, the female germ cell, MAPK does not follow this canonical scheme. In oocytes, MAPK is activated independently of growth factors and tyrosine kinase receptors, acts independently of transcriptional regulation, plays a crucial role in controlling meiotic divisions, and is under the control of a peculiar upstream regulator, the kinase Mos. Mos was originally identified as the transforming gene of Moloney murine sarcoma virus and its cellular homologue was the first proto-oncogene to be molecularly cloned. What could be the specific roles of Mos that render it necessary for meiosis? Which unique functions could explain the evolutionary cost to have selected one gene to only serve for few hours in one very specific cell type? This review discusses the original features of MAPK activation by Mos and the roles of this module in oocytes.

No MeSH data available.


Related in: MedlinePlus