ARPP19 phosphorylation site evolution and the switch in cAMP control of oocyte maturation in vertebrates.

IF 3.7 2区 生物学 Q1 DEVELOPMENTAL BIOLOGY Development Pub Date : 2024-11-22 DOI:10.1242/dev.202655
Ferdinand Meneau, Pascal Lapébie, Enrico Maria Daldello, Tran Le, Sandra Chevalier, Sarah Assaf, Evelyn Houliston, Catherine Jessus, Marika Miot
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Abstract

cAMP-PKA signaling initiates the critical process of oocyte meiotic maturation in many animals, but inhibits it in vertebrates. To address this "cAMP paradox", we exchanged the key PKA substrate, ARPP19, between representative species, the vertebrate Xenopus and the cnidarian Clytia, comparing its phosphorylation and function. We found that as in Xenopus, Clytia maturing oocytes undergo ARPP19 phosphorylation on a highly conserved Gwl site, which inhibits PP2A and promotes M-phase entry. In contrast, despite a PKA phosphorylation signature motif recognisable across most animals, Clytia ARPP19 was only poorly phosphorylated by PKA in vitro and in vivo. Furthermore, unlike Xenopus ARPP19, exogenous Clytia ARPP19 did not delay Xenopus oocyte maturation. We conclude that in Clytia ARPP19 does not intervene in oocyte maturation initiation because of both poor recognition by PKA and the absence of effectors that mediate vertebrate oocyte prophase arrest. We propose that ancestral ARPP19 phosphorylated by Gwl has retained a key role in M-phase across eukaryotes and it has acquired new functions during animal evolution mediated by enhanced PKA phosphorylation, allowing co-option into oocyte maturation regulation in the vertebrate lineage.

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ARPP19磷酸化位点进化与脊椎动物卵母细胞成熟的 cAMP 控制转换
cAMP-PKA信号在许多动物中启动了卵母细胞减数分裂成熟的关键过程,但在脊椎动物中却抑制了这一过程。为了解决这个 "cAMP 悖论",我们在脊椎动物章鱼和刺胞动物克莱提亚之间交换了关键的 PKA 底物 ARPP19,比较其磷酸化和功能。我们发现,与爪蟾一样,Clytia 成熟卵母细胞也会在一个高度保守的 Gwl 位点上发生 ARPP19 磷酸化,从而抑制 PP2A 并促进进入 M 期。与此相反,尽管大多数动物都能识别 PKA 磷酸化特征点,但 Clytia ARPP19 在体外和体内被 PKA 磷酸化的程度很低。此外,与爪蟾 ARPP19 不同,外源 Clytia ARPP19 不会延迟爪蟾卵母细胞的成熟。我们的结论是,Clytia ARPP19 不干预卵母细胞成熟的启动,因为 PKA 的识别能力很差,而且缺乏介导脊椎动物卵母细胞前期停滞的效应物。我们认为,被 Gwl 磷酸化的祖先 ARPP19 在真核生物的 M 期保留了关键作用,它在动物进化过程中通过增强 PKA 磷酸化获得了新的功能,从而在脊椎动物系中共同参与卵母细胞成熟调控。
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来源期刊
Development
Development 生物-发育生物学
CiteScore
6.70
自引率
4.30%
发文量
433
审稿时长
3 months
期刊介绍: Development’s scope covers all aspects of plant and animal development, including stem cell biology and regeneration. The single most important criterion for acceptance in Development is scientific excellence. Research papers (articles and reports) should therefore pose and test a significant hypothesis or address a significant question, and should provide novel perspectives that advance our understanding of development. We also encourage submission of papers that use computational methods or mathematical models to obtain significant new insights into developmental biology topics. Manuscripts that are descriptive in nature will be considered only when they lay important groundwork for a field and/or provide novel resources for understanding developmental processes of broad interest to the community. Development includes a Techniques and Resources section for the publication of new methods, datasets, and other types of resources. Papers describing new techniques should include a proof-of-principle demonstration that the technique is valuable to the developmental biology community; they need not include in-depth follow-up analysis. The technique must be described in sufficient detail to be easily replicated by other investigators. Development will also consider protocol-type papers of exceptional interest to the community. We welcome submission of Resource papers, for example those reporting new databases, systems-level datasets, or genetic resources of major value to the developmental biology community. For all papers, the data or resource described must be made available to the community with minimal restrictions upon publication. To aid navigability, Development has dedicated sections of the journal to stem cells & regeneration and to human development. The criteria for acceptance into these sections is identical to those outlined above. Authors and editors are encouraged to nominate appropriate manuscripts for inclusion in one of these sections.
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