Lipid Signaling During Gamete Maturation

Mostafa, Sherif; Nader, Nancy; Machaca, Khaled

doi:10.3389/fcell.2022.814876

Cited by 8 publications

(4 citation statements)

References 196 publications

(300 reference statements)

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“…The requirement for the lipase domain within ABHD2 for P4-dependent oocyte maturation suggests a potential role for lipid messengers downstream of P4 to release oocyte meiotic arrest. There is support for this idea in the literature from several early studies implicating lipid messengers in oocyte maturation, although there has been little consensus regarding specific pathways, lipases, or lipid mediators (32). To globally assess oocyte lipid profiles in response to P4, we performed unbiased mass-spectrometry based lipidomics and metabolomics (using the Metabolon CLP and HD4 platforms) at two time points after P4: 5 min to assess rapid changes in lipid abundances, and 30 min, a ‘point of no return’ where the majority of oocytes in the population commit to maturation (22).…”

Section: Resultsmentioning

confidence: 99%

“…The role of lipid signaling in oocyte maturation remains poorly defined, partly due to technical limitations in early studies, but also as a result of the complexity and transient nature of lipid signals (32). An additional confounding factor in oocyte lipidomics is that oocytes in the population mature in an asynchronous fashion in response to P4.…”

Section: Lipidomics During Oocyte Maturationmentioning

confidence: 99%

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Progesterone induces meiosis through two obligate co-receptors with PLA2 activity

Nader,

Assaf,

Zarif

et al. 2023

Preprint

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The steroid hormone progesterone (P4) regulates multiple aspects of reproductive and metabolic physiology. Classical P4 signaling operates through nuclear receptors that regulate transcription of target genes. In addition, P4 signals through membrane P4 receptors (mPRs) in a rapid nongenomic modality. Despite the established physiological importance of P4 nongenomic signaling, its detailed signal transduction remains elusive. Here, usingXenopusoocyte maturation as a well-established physiological readout of nongenomic P4 signaling, we identify the lipid hydrolase ABHD2 (α/β hydrolase domain-containing protein 2) as an essential mPRβ co-receptor to trigger meiosis. We show using functional assays coupled to unbiased and targeted cell-based lipidomics that ABHD2 possesses a phospholipase A2 (PLA2) activity that requires both P4 and mPRβ. This PLA2 activity bifurcates P4 signaling by inducing mPRβ clathrin-dependent endocytosis and producing lipid messengers that are G-protein coupled receptors agonists. Therefore, P4 drives meiosis by inducing the ABHD2 PLA2 activity that requires both mPRβ and ABHD2 as obligate co-receptors.Significance StatementNongenomic progesterone signaling is important for many physiological functions yet its detailed early signaling steps remain elusive. Here we show that progesterone induces rapid signaling to driveXenopusoocyte meiosis. Progesterone requires two cell membrane receptor to work in unison to signal. The co-receptor complex possesses lipase activity that produces lipid messenger and changes cell membrane structure. This leads to receptor endocytosis and activation of additional pathway to trigger meiosis. Nongenomic progesterone signaling operates in every tissue and regulates reproductive and metabolic physiology. Therefore, our findings have broad implications on our understanding of nongenomic progesterone signaling.

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Section: Resultsmentioning

confidence: 99%

Section: Lipidomics During Oocyte Maturationmentioning

confidence: 99%

Progesterone induces meiosis through two obligate co-receptors with PLA2 activity

Nader,

Assaf,

Zarif

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

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“…Sperm were previously thought to contribute very little beyond haploid DNA content to the zygote, much less any “experience” of the parental condition. Sperm contain proteins, lipids, and RNA that can influence gene expression in a developing embryo [ 130 , 158 , 217 , 218 ]. The fundamental steps of spermatogenesis begin with germ cell differentiation into spermatocytes via mitotic division and the production of haploid spermatids from the tetraploid primary spermatocytes via meiotic division.…”

Section: Examples Of Epigenetic Inheritance Induced By Biotic and Abi...mentioning

confidence: 99%

Inheritance of Stress Responses via Small Non-Coding RNAs in Invertebrates and Mammals

Ow,

Hall

2023

Epigenomes

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While reports on the generational inheritance of a parental response to stress have been widely reported in animals, the molecular mechanisms behind this phenomenon have only recently emerged. The booming interest in epigenetic inheritance has been facilitated in part by the discovery that small non-coding RNAs are one of its principal conduits. Discovered 30 years ago in the Caenorhabditis elegans nematode, these small molecules have since cemented their critical roles in regulating virtually all aspects of eukaryotic development. Here, we provide an overview on the current understanding of epigenetic inheritance in animals, including mice and C. elegans, as it pertains to stresses such as temperature, nutritional, and pathogenic encounters. We focus on C. elegans to address the mechanistic complexity of how small RNAs target their cohort mRNAs to effect gene expression and how they govern the propagation or termination of generational perdurance in epigenetic inheritance. Presently, while a great amount has been learned regarding the heritability of gene expression states, many more questions remain unanswered and warrant further investigation.

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“…In most vertebrates, oocytes primarily arrested in prophase of meiosis I, resume meiosis and undergo germinal vesicle breakdown to produce mature oocytes that arrest at metaphase of the second meiotic division until fertilization (Von Stetina & Orr-Weaver, 2011;Nader et al, 2013). Meiotic arrest and resumption are controlled by specific molecular events (Machaca, 2007;Santella et al, 2020;Hatirnaz et al, 2022;Mostafa et al, 2022), and are driven by a complex cascade of hormonal signaling (Abbara et al, 2018;Stewart & Davis, 2019). Despite the complexity and diversity of these molecular and physiological events, they converge on Ca 2+ as a key orchestrator of these developmental events (Figure 1).…”

Section: Neuronal Signaling and Calcium Regulation During Oocyte Matu...mentioning

confidence: 99%

Neurotransmitters, neuropeptides and calcium in oocyte maturation and early development

Alhajeri

Alkhanjari

Hodeify

et al. 2022

Front. Cell Dev. Biol.

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A primary reason behind the high level of complexity we embody as multicellular organisms is a highly complex intracellular and intercellular communication system. As a result, the activities of multiple cell types and tissues can be modulated resulting in a specific physiological function. One of the key players in this communication process is extracellular signaling molecules that can act in autocrine, paracrine, and endocrine fashion to regulate distinct physiological responses. Neurotransmitters and neuropeptides are signaling molecules that renders long-range communication possible. In normal conditions, neurotransmitters are involved in normal responses such as development and normal physiological aspects; however, the dysregulation of neurotransmitters mediated signaling has been associated with several pathologies such as neurodegenerative, neurological, psychiatric disorders, and other pathologies. One of the interesting topics that is not yet fully explored is the connection between neuronal signaling and physiological changes during oocyte maturation and fertilization. Knowing the importance of Ca2+ signaling in these reproductive processes, our objective in this review is to highlight the link between the neuronal signals and the intracellular changes in calcium during oocyte maturation and embryogenesis. Calcium (Ca2+) is a ubiquitous intracellular mediator involved in various cellular functions such as releasing neurotransmitters from neurons, contraction of muscle cells, fertilization, and cell differentiation and morphogenesis. The multiple roles played by this ion in mediating signals can be primarily explained by its spatiotemporal dynamics that are kept tightly checked by mechanisms that control its entry through plasma membrane and its storage on intracellular stores. Given the large electrochemical gradient of the ion across the plasma membrane and intracellular stores, signals that can modulate Ca2+ entry channels or Ca2+ receptors in the stores will cause Ca2+ to be elevated in the cytosol and consequently activating downstream Ca2+-responsive proteins resulting in specific cellular responses. This review aims to provide an overview of the reported neurotransmitters and neuropeptides that participate in early stages of development and their association with Ca2+ signaling.

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Lipid Signaling During Gamete Maturation

Cited by 8 publications

References 196 publications

Progesterone induces meiosis through two obligate co-receptors with PLA2 activity

Progesterone induces meiosis through two obligate co-receptors with PLA2 activity

Inheritance of Stress Responses via Small Non-Coding RNAs in Invertebrates and Mammals

Neurotransmitters, neuropeptides and calcium in oocyte maturation and early development

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