Participation of the adenosine salvage pathway and cyclic AMP modulation in oocyte energy metabolism

Richani, Dulama; Lavea, Cathy F.; Raji, K.; Riepsamen, Angelique H; Bertoldo, Michael J.; Bustamante, Salvador; Gilchrist, Robert B.

doi:10.1038/s41598-019-54693-y

Cited by 27 publications

(13 citation statements)

References 47 publications

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“…Hence, the study further corroborates the theory that cumulus cells provide metabolic support via gap junctional communication to maintain mitochondrial function and support oocyte meiotic progression and developmental competence. Consistent with our findings, Richani et al recently reported that the ATP levels increase in oocytes cultured with cumulus cells, and pharmacological inhibition of their gap-junction communication leads to a reduction of ATP levels in the oocytes [ 49 ]. These results demonstrate that the metabolic cooperativity between cumulus cells and oocytes mediated via gap junction communication directly affects intra-oocyte ATP levels.…”

Section: Discussionsupporting

confidence: 93%

Melatonin improves the quality of maternally aged oocytes by maintaining intercellular communication and antioxidant metabolite supply

Zhang

Wen

et al. 2022

Redox Biology

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In mammalian ovaries, oocytes are physically coupled to somatic granulosa cells, and this coupling is crucial for the growth and development of competent oocytes as it mediates the transfer of metabolic support molecules. However, aging-mediated dysregulation in communication between the oocytes and granulosa cells affects the oocyte quality. In the present study, we examined the defected germline-soma communication and reduced mRNA levels encoding key structural components of transzonal projections (TZPs) in maternally aged oocytes. Oral administration of melatonin to aged mice substantially increased TZPs and maintained the cumulus cells-oocyte communication, which played a central role in the production of adequate oocyte ATP levels and reducing the accumulation of reactive oxygen species (ROS), apoptosis, DNA damage, endoplasmic reticulum (ER) stress and spindle/chromosomal defects. This beneficial effect of melatonin was inhibited by carbenoxolone (CBX), a gap junctional uncoupler, which disrupts bidirectional communications between oocyte and somatic cells. Simultaneously, melatonin significantly increased the mRNA and protein levels corresponding to genes associated with TZPs and prevented TZP retraction in in vitro-cultured cumulus-oocyte complex (COCs). Furthermore, we infused melatonin and CBX into the COCs in vitro culture system and monitored the levels of nicotinamide adenine dinucleotide phosphate (NADPH) and glutathione (GSH) in cumulus cells and oocytes. Notably, COCs treated with melatonin demonstrated improved NADPH and GSH levels. Of note, CBX was capable of reducing NADPH and GSH levels, aggravated the ROS accumulation and ER stress. Collectively, our data demonstrate the role of melatonin in preventing age-associated germline-soma communication defects, aiding the relay of antioxidant metabolic molecules for the maintenance of oocyte quality from cumulus cells, which have important potential for improving deficient phenotypes of maternally aged oocytes and the treatment of woman infertility.

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Section: Discussionsupporting

confidence: 93%

Melatonin improves the quality of maternally aged oocytes by maintaining intercellular communication and antioxidant metabolite supply

Zhang

Wen

et al. 2022

Redox Biology

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“…This might be attributed to the significant capability of forskolin for increasing the expression of embryo quality genes such as Mvh , Gdf9 , Scp3 and Rec8 expressions related to the unsupplemented group (Bahmanpour et al., 2020). The feat of using forskolin/IBMX meaningfully improved embryo development and has been evidenced in different animals (Gilchrist et al., 2015; Richani et al., 2019). Supplementation with 5.0 μM forskolin (54.7%) to in vitro culture medium had higher blastocyst rate compared with control group (44.9%) (Meneghel et al., 2017).…”

Section: Impacts Of Forskolin On In Vitro Embryo Developmentmentioning

confidence: 99%

“…For this fact, many studies have used in culture media to decrease lipid content by chemical lipolysis, and enhance the cryotolerance and post‐vitrification quality of embryos (Bilodeau‐Goeseels, 2011; Paschoal et al., 2014, 2016; Zeng et al., 2014). Thus, forskolin increases the intracellular concentrations of cAMP, which inhibits the immediate resumption of meiosis and gives the oocyte more time to gain optimal developmental competence (Costa et al., 2019; Razza, 2018; Richani et al., 2019).…”

Section: Introductionmentioning

confidence: 99%

The role of forskolin as a lipolytic stimulator during in vitro oocyte maturation and the in vitro embryo production of livestock

Raza

El-Aziz

Abdelnour

et al. 2021

Reprod Domestic Animals

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Cryopreservation is a modern technique which assists in the preservation of genetic material from oocytes and embryos for a long time. However, elevated vulnerability to cryopreservation due to the large accumulation of intracellular lipids within oocytes or embryos avoids success of this method. These lipids remain the main crucial factor limiting survival rates of oocytes and embryos after thawing. Lipid ingathering in the oocyte cytoplasm augments lipid peroxidation (LPO) and oxidative stress increases the apoptosis process, declines the viability after thawing, declines cytoskeleton actin filament injuries, lowers the blastocyst rates and reduces cryotolerance in the early stages of embryo development. There have been several attempts to reduce the ingathering of intracellular lipids in oocytes or embryos during the cryopreservation process, in that way enhancing the competence of cryopreserved oocytes or embryos and increasing their viability. One of the most applied agents for chemical delipidation is forskolin. Forskolin exhibited a possible part in improving the oocytes cryopreservation through stimulating cyclic adenosine monophosphate (cAMP) production. The main purpose of cAMP modulation is to provide energy to sustain the mammalian oocytes´ meiotic arrest. The purpose of the existing article is to assess and offer more evidence concerning the forskolin utilization as a modulator of cAMP during the cryopreservation of oocytes and its influence on meiosis completion and the reorganization of cytoplasm, which are prerequisites for the development of oocytes in addition to the contribution to fertilization and subsequently, the development of embryos.

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“…The ADO salvage pathway involves two steps: First, AMP is phosphorylated to ADP and then ADP to ATP, this might be an alternative pathway for ATP production to satisfy the energetic demands in the meiotic maturation of the oocyte, therefore the ADO salvage pathway has to be active in order to take advantage of the large amount of AMP generated by phosphodiesterase breakdown of cAMP [ 81 , 82 ]. In fact, it has been found that ATP is generated from AMP through the adenosine salvage pathway in mouse oocytes, and that the increment in the cAMP levels modifies adenine nucleotide metabolism, providing the AMP required for energy production through this salvage pathway [ 83 ].…”

Section: Ado Metabolismmentioning

confidence: 99%

Structure–activity features of purines and their receptors: implications in cell physiopathology

2022

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The purine molecular structure consists of fused pyrimidine and imidazole rings. Purines are main pieces that conform the structure of nucleic acids which rule the inheritance processes. Purines also work as metabolic intermediates in different cell functions and as messengers in the signaling pathways throughout cellular communication. Purines, mainly ATP and adenosine (ADO), perform their functional and pharmacological properties because of their structural/chemical characteristics that make them either targets of mutagenesis, mother frameworks for designing molecules with controlled effects (e.g. anti-cancer), or chemical donors (e.g., of methyl groups, which represent a potential chemoprotective action against cancer). Purines functions also come from their effect on specific receptors, channel-linked and G-protein coupled for ATP, and exclusively G-coupled receptors for ADO (also known as ADORAs), which are involved in cell signaling pathways, there, purines work as chemical messengers with autocrine, paracrine, and endocrine actions that regulate cell metabolism and immune response in tumor progression which depends on the receptor types involved in these signals. Purines also have antioxidant and anti-inflammatory properties and participate in the cell energy homeostasis. Therefore, purine physiology is important for a variety of functions relevant to cellular health; thus, when these molecules present a homeostatic imbalance, the stability and survival of the cellular systems become compromised.

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Participation of the adenosine salvage pathway and cyclic AMP modulation in oocyte energy metabolism

Cited by 27 publications

References 47 publications

Melatonin improves the quality of maternally aged oocytes by maintaining intercellular communication and antioxidant metabolite supply

Melatonin improves the quality of maternally aged oocytes by maintaining intercellular communication and antioxidant metabolite supply

The role of forskolin as a lipolytic stimulator during in vitro oocyte maturation and the in vitro embryo production of livestock

Structure–activity features of purines and their receptors: implications in cell physiopathology

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